Part Process Entailing Loss of Old Feathers
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THE MECHANISM OF FEATHER REPLACEMENT DURING NATURAL MOLT G•oxG• E. WATSON MOST ornithological reference books state that natural molt is a two- part processentailing loss of old feathers, "ecdysis," and subsequent growth of new feathers, "endysis" (Stresemann,1927; Mayaud, 1950; Wing, 1956; Van Tyne and Berger, 1959). Furthermore, investigators who have studiedmolt in penguins,cassowaries, and emusstate or imply that they are aberrant,since, in thesebirds, the old feathersare pushed out attachedto the tips of the feathersof the incominggeneration and are later abradedor are pulled off by the bird (Bartlett, 1879; Lowe, 1933; Friedmann, 1949; Rand, 1950). The evidenceto be presentedin this paper,very briefly reportedearlier by Watson (1963), indicates,however, that this latter mechanismof feather replacementis more widespread among birds than previouslybelieved and that natural molt is actively concernedonly with the incominggeneration. This finding is of signifi- cancefor relating molts to plumages,especially in view of the current con- troversy over their nomenclature(Humphrey and Parkes, 1959, 1963; Miller, 1961, 1962; Stresemann,1963). During the courseof early developmentin birds, the natal downsare carried out on the tips of the incomingjuvenal feathersin the first molt, but are soonabraded. For this reason,some authors have maintained that down should not be considereda separate generation,but merely the modifiedtips of the juvenal feathers (Jones,1907). Furthermore,pluck- ing a definitive feather usually stimulatesregeneration (Lillie and Juhn, 1932; but see Morton, 1962). The distal portion of the papilla is torn away in plucking but the papilla beginshealing over at once and usually an entire new feather is grown (Cohen and 'Espinasse,1961). The regen- eration of plucked feathershas receivedmuch attention, especiallyfrom developmentalbiologists interested in regulation and morphogenesis(see review by Lillie, 1942). Their findingshave been interpreted to reinforce the view that lossof feathersin molt stimulatesgrowth of the new feath- ers. The mechanismof replacementof feathersduring natural molt, how- ever, has been little investigated. MATERIALS AND METHODS Observationson molt in living birds were made on 6 hand-reared Rhode Island red chickens,20 Chukar Partridges (Al½½tori$½hukar), and 20 JapaneseQuail •a•oni½•). Most of these were incubator-hatched, but 7 chukars and $ quail were incubated by a domestic hen. The birds were kept in wire cagesand fed commercial chick starter (protein 25 per cent) supplementedwith fresh lettuce or grass; dry soil and eggshellswere available for dusting and grit. Until the birds were able to ther- tooregulate, they were brooded under a 100-watt incandescent bulb. Many of the 486 The Auk, 80: 456-495. October, Oct.1963 I W^rso>;,Feather Replacement 487 birds were handled daily and examinedfor molt while they were developing.All juvenal feathersdropped by one chukar were collectedevery other day. Nonliving material consistedof five birds. An adult male Chukar Partridge, which died while molting at the Highland Park Zoo in Pittsburgh, and an adult male House Sparrow (Passerdomesticus), picked up dead in Arlington, Virginia, were examined in the flesh. Flat skins of two molting Greater Scaup ducks (Aythya marila) were examinedimmediately after preparation. A wild Ruddy Sheld-Duck (Casarca ferrugi- nea), preservedin formalin in 1960, was studiedtwo years later. Molting feathers were examined and photographed,when possible,on the living bird. Others were plucked, and examinedor dissectedwhile fresh, under a binocular dissectingmicroscope. A few molting featherswere preservedin Bouin's or Carnoy's fluids and examined after fixation. In order to investigategrowth rate during the developmentof early feather gener- ations,Richard J. Hart, a studentat Yale University, made daily measurementsunder my direction on the innermostprimary (number I) in female "Hall Cross" Rhode Island red preservedembryos and living chicks. For each day of incubation (days II through 20) he measuredat least five specimens.Five chickswere raised for 32 days under the same conditions as the other live birds under observation. Measurements taken with caliperson the visible portion of the feather were recordedto the nearest 0.I mm in the embryos and 0.5 mm in the live chicks. ACKnOWLEDGMEnTS Most of the observationshere reported were made at the Peabody Museum of Nat- ural History while I was a resident graduate student in the Department of Zoology, Yale University. I thank S. D. Ripley, director of the museum, for providing me with space and cages; and E. J. Boell, chairman, for use of departmental incubator facilities and cagingmaterials. Among many personswho have contributed variously to this study, I am indebted to R. J. Andrew, A. Brewerton, J. Cohen, Mrs. Judith Lenz, L. L. Wolf, Mrs. Caroline Lutz, K. C. Parkes, P. Stettenheim, E. Stresemann, M. B. Trautman, J.P. Trinkaus, J. Weston, and my family. I am especiallygrateful to R. J. Hart for measuring chicks and to P. S. Humphrey for constructive criticism of the manuscript. OBSeRVAtiOnS A•D A Rhode Island red chick in its fifth week provided the first evidence that the two-step sequenceof molt might not be a reality. The bird had fully grown the inner juvenal primarieson both wings, but someof the more distal remigeswere still in growth. Becausethe primarieswere to be saved for work on pigmentation,they were pulled. When the innermost primary was plucked,the break camewell below the inferior umbilicusat the collar, that part of the papilla in which new growth was taking place. Firmly attached to the base of the calamusof the old feather was 10 mm of new feather sheath. The featherwas not easy to dislodgeand the force applied was considerable. The calamusof the juvenal primary is entirely keratinizedand contains a seriesof dry pulp caps. The outer wall of the new feather sheath ap- pears to be continuouswith the keratinized calamusof the old feather and 488 WATSO.%Feather Replacement [ Vol.Auk 80 there is no apparent constrictionat their juncture (Figure IA). Within the new sheath,barbs have begunto form but the vascularizedpulp still reachesalmost to the calamusof the old feather. The pulp capshave not dosed the inferior umbilicusas they do in later feathergenerations (Lil- Figure 1. A. Zone of juncture between base of calamus (light area) of juvena! innermost primary and tip of sheath (dark area) of first basic primary in five-week- old Rhode Island red chick. Total length of preservedspecimen, 18 mm. B. Juvenal flank feather (arrow) of living Chukar Partridge pushed out of follicle still attached to tip of incoming basic feather sheath. Other basic feathersalready breaking sheaths. Photographer'sfingers at bottom and left. C. Shed breast feather of adult Ruddy Sheld-Duck with broken-off cap of keratinized new feather sheath attached to base of calamus. lie, 1940). The new sheathhas not yet becomefully keratinizedand hard, even near its tip. Every molting bird subsequentlyinvestigated in detail has shown this samemode of feather replacementin all molts and in most feather tracts. The new feather sheath may push the base of the calamusof the old feather well beyond the end of the follicle so that the point of attachment of the two feather generationsis visible externally (Figure lB). Often there is a constrictionat the zone of juncture betweenthe two generations, but the outer layers of the calamusand sheathappear continuous.In the OCt.1963 ] WATSON,Feather Replacement 489 live bird, the calamusof the old featheris translucentand whitishbut the vascularizedpulp and barbsof the incomingfeather make the new sheath appeardull, dark purple. When the old feather,thus carriedout on the tip of the sheathof the incomingfeather, breaks off, part of the keratinizedtip of the newsheath comesaway attachedto the inferior umbilicusof the old feather (Figure 1C). This may help the sheathof the new feather to start breakingopen. Most of the attachedfeathers were foundduring the first prebasicmolt, but attachedfeathers were also presentin later molts. This phenomenon was observedin the hackles,wing coverts,and alulae of Rhode Island red cockerelsundergoing the subsequentmolt whenmore than six monthsold. A year-old Chukar Partridgeand an adult House Sparrowexamined soon after death showed several first basic feathers which had been carried out on the tips of sheathsduring the secondprebasic molt. Observationsby Dr. Milton B. Trautman (letter), on a captiveMottled Duck (Anas fulvigula) in 1953 suggestthat the sameprocess takes place in the wing quillsof year-oldducks: On June 18 at 11 a.m. "Fulvi" lost his first primary. That primary and all his other flight feathers were still firmly attached at 9 o'clock that same morning when I carefully jerked at some of the primaries. By 1 p.m. the next day (i.e. within 26 hours) he had lost all flight feathers. By early morning of the 19th, less than 24 hours after the first primary was dropped, some of the new primaries were one quarter inch out of the follicles.... When a feather was dropped, I could see the tip of the sheath of the new feather in the follicle. Definitive breast featherswere also found attachedto the tips of in- comingfeather sheaths in preservedflat skinsof wild Greater Scaupducks and in a wholespecimen of RuddySheld-Duck preserved in formalin.The connectionsbetween the two feather generationsin the skinsof the scaup had survivedmanual washingin detergentand benzeneand subsequent drying in sawdustand a forcedair stream.