Primary Molt of California Condors

The Condor 89:468-485 0 The Cooper Ornithological Society 1987

NOEL F. R. SNYDER* U.S. Fish and Wildlife Service,Condor Research Center, 2291A Portola Road, Ventura, CA 93003

ERIC V. JOHNSON BiologicalSciences Department, California PolytechnicState University, San Luis Obispo,CA 93407

DAVID A. CLEKDENEN CondorResearch Center, 22914 Portola Road, Ventura, CA 93003

Abstract. Primary molt of the California Condor (Gymnogypscalifornianus) was studied intensively from 1982 through 1985, using repeated flight photographs of the remaining individuals in the wild population as a basisfor most analyses.On the average,wild condors replaced 4.4 of the 8 emarginated primaries on each wing each year. The specific primaries molted were generallythe onesmissed in the previous year and were usuallywell-distributed among the eight possibilities, with a tendency for low-numbered primaries to molt earlier than high-numbered primaries. Within individuals, molt of one wing was commonly very different from that of the other wing. Primary molt of captive juveniles was similar to that of wild juveniles. The interval from loss to full replacement of individual primary feathers was normally 3% to 4 months, with the primaries closestto the leading edge of the wing growing most slowly. Most primaries were shed between 1 February and 1 September. Primaries lost in late fall and early winter were not replaceduntil the following summer, indicating interrupted molt over the winter. In general, primary molt of the condor differs from that of smaller cathartids in being highly seasonal, highly variable in sequence, highly asymmetric between wings, and in following a roughly 2-year cycle. Molt of the condor shows many similarities to that of the White Stork (Ciconia ciconia) and to that of large accipitrid vultures. Key words: California Condor;Gymnogyps californianus;primary molt; secondarymolt; rectrix molt.

INTRODUCTION on primary, secondary, and tail molt of captive In late 198 1 we began intensive efforts to pho- condors studied in 1984 and 1985. tograph wild California Condors (Gymnogyps californianus) in flight as a means of identifying METHODS individuals and censusing the remnant popula- California Condors in full feather have 8 emar- tion. The many differences in feather patterns, ginated primaries (numbers 3 through 10) and especially primary feather patterns, proved di- two secondary-like primaries (numbers 1 and 2) agnostic in differentiating individuals and led to on each wing (Fig. 1A). Because the emarginated minimum population counts of 2 1, 19, 15, and primaries overlap only minimally and can be 9 wild condors for 1982, 1983, 1984, and 1985, readily differentiated in flight photographs of wild respectively (Johnson 1985, Snyder and Johnson birds, it has been possible to obtain comprehen- 1985). Identifying individuals through time re- sive documentation of their patterns of molt quired an understanding of patterns and rates of through repeated photographs of individual con- primary molt. Here we present the results of pri- dors. To facilitate systematic studies, the thou- mary molt studies of wild individuals followed sands of condor flight photographs taken in the from 1982 through 1985, supplemented by data past few years were sorted into files for individual birds and arranged in temporal sequences within each year. For each individual, we first tabulated ’ ’ Received 1 April 1986. Final acceptance 18 Feb- ruary 1987. the status of all primaries 3 through 10 for each 2Present address:P.O. Box 105, Portal, AZ 85632. date. We then determined the sequences in which

[4681 CALIFORNIA CONDOR MOLT 469 feathers molted, the frequencies with which giv- browner and more frayed feathers of previous en primaries molted over the several-year peri- years, allowing determinations of overall annual od, and the maximum and minimum spans of molt patterns. time each molting primary took from loss to full However, annual inspections did not yield de- replacement. Maximum replacement period was tailed information on molt sequences within computed as the interval between the date an old years. Partial information on within-year se- primary was last photographed in place to the quencesof captives was obtained in 1985 by pe- date a replacement feather was first documented riodic collection of molted primaries in the cages photographically to be fully grown. Minimum of three 2-year-old individuals. Not all primaries period was computed as the interval between the were recovered, but enough were found to allow date a primary was first photographed missing some preliminary conclusions. and the last date its replacement was photographed in less than fully developed condition. RESULTS Normally there was no difficulty in determining the timing of lossof primaries, but we sometimes MOLT SEQUENCE AND FREQUENCY encountered problems determining when growth The primary molt sequencesof the 16 wild adults of a primary was finished. Judgments of the de- and seven wild immatures that were photo- greeof completion of growing featherswere made graphed during the 4-year period are presented by comparisonswith lengths of adjacent feathers, in Table 1. From the temporal spacing of pho- but suchjudgments were sometimes hindered by tographsand data on the time it takes individual problems with resolution of photographs,effects primaries to complete loss-replacement cycles, ofangular aspectin the photographs,the fact that we rated the molt data for each bird in each year adjacent feathers were also sometimes growing as complete (all molting primaries detected), simultaneously, and intrinsic variability in ap- probably complete, or probably incomplete. For pearance of feather lengths, apparently due to most of the analyses that follow, we used data momentary movements of feather tips in the only from birds and years for which we judged wind. Thus, some of the variability in docu- our information to be complete or probably commented replacement periods undoubtedly traced plete. to errors in judgment of completion dates. Some Although molt sequencestended to be highly feathers, when complete, were abnormally short variable, an underlying pattern of low-numbered relative to adjacent feathers, but this was easily primaries molting before high-numbered pri- detectedby looking at long seriesof photographs maries was discernible when the rank orders of of individual birds and did not cause general primary molt were averaged for all wild adults difficulties. and immatures (Table 2). In fact, the average Unfortunately, molt patterns of secondaries, rank orders show a perfect correlation with pri- rectrices, and primaries 1 and 2 could not be mary number by a Spearman’s rank correlation studied comprehensively by the photographic test (Y,= 1.O, P < 0.001). This same relationship method, mainly because these feathers overlap is apparent from an examination of the seasonal one another to such an extent that patterns of timing-of-loss distributions of the various pri- loss and regrowth of specific feathers could not maries (Fig. 2). be discerned clearly at the usual distances from Molt sequenceswere most regular in juveniles, which photographswere taken. Nevertheless, we which tended to replace primaries 1 through 5 gained limited information on molt of these in their first molting period, both in the wild and feathers from some of the better photographsof in captivity (seeTodd and Gale 1970). However, wild birds. In addition, we accumulated consid- several individuals did not progressas far as pri- erable data on molt of thesefeathers from annual mary 5, some progressedfarther, and in some, fall examinations of captive condors at the Los primary replacement did not proceedin a strictly Angeles and San Diego zoos. Captives were consecutive order up the sequence(Tables 1 and sometimes examined in the hand, but were more 3). At one extreme was a wild bird (PAX) trapped usually checkedwith binoculars while they were and examined in the hand in late 1982, that molt- in sunning postures.Viewed at closerange, feath- ed only primaries 1 and 2 on one wing and pri- ers of the year were characteristically black and maries 1 through 3 on the other wing in his first clean-edged,and were readily differentiated from molt. At the other extreme were two captives, 470 N. F. R. SNYDER, E. V. JOHNSON AND D. A. CLENDENEN CALIFORNIA CONDOR MOLT 471

FIGURE 1. A. An adult California Condor (CCF) in perfect feather on 24 January 1982. Numbers indicate the emarginated primaries followed intensively in this study. B. Photographof BOS toward the end of her first molting period on 2 September 1983, illustrating primary molt limited to lower-numbered primaries, and molt of innermost secondariesand rectrices.Note also secondary 1 on left wing clearly in molt and that sequenceof replacementof primaries is normal on right wing but partially reversedon left wing. C. PCA in extremely heavy primary and secondarymolt on 8 August 1983. Primaries in molt are L3, L6, L7, L9, LlO, R4, R6, R7, and R8.

Tecuya and Pit-u, that molted primaries 1 through course of events, although the degree to which 7 on each wing during their first molts. In part, various captives began secondmolt waves up the the number of primaries molted in the first molt sequence before they finished first waves was was related to hatching date (Fig. 3) with the variable. At one extreme, Sisquoc and Tecuya earliest-hatching birds molting the most prima- molted primaries 1 through 4 as well as high- ries in the following year (r, = -0.77, P < 0.01). numbered primaries on both wings in their sec- All three recent captives for which molted pri- ond molt periods. At the other extreme, Topa- maries were collected during their second molt topa, the captive studied by Todd and Gale (Almiyi, Tecuya, and Sisquoc) started their sec- (1970) limited primary replacement in his second molt by replacing primaries 1 through 3 for ond molt almost exclusively to high-numbered a secondtime. Partway through this processthey primaries and started a second molt wave only also began replacement of high-numbered pri- on one wing and only with primary 1. maries they had not molted (or presumably had Of the wild immatures, REC molted mainly not molted) in their first year. For example, Al- high-numbered primaries in his second year, almiyi, who had molted primaries 1 through 5 in though photographs are adequate to show that her first molt in 1984, again dropped primaries he also molted primary 2 on both wings. It seems 1 through 3 between February and April 1985, likely that he may also have molted primary 1 and in the same year also molted primaries 6 on both wings in this year, but this cannot be through 10, starting in April. The overall molting discernedclearly in the photographs.In his fourth patterns of Sespe, Cuyama, Cachuma, and To- year, REC again showed a molting pattern very patopa in their second years suggesteda similar similar to that of many captives in their second

474 N. F. R. SNYDER, E. V. JOHNSON AND D. A. CLENDENEN

Primary 3 TABLE 2. Rank orders of primary molt (see Table l).a 4 (Apr 1, 59.51 n n No. of lo- Primary 4 Pnmary no. instances Mean rank SD 5- (Apr 9.5. 53.51 3 71 1.52 1.03 4 68 2.02 1.22 lo- Primary 5 70 2.20 1.27 5- (Apr 23. 54.3) : 68 2.15 1.14 I 70 3.22 1.16 lO- Primary 6 8 55 3.31 1.10 5- (May 24.6. 37.6) 9 61 3.61 0.90 10 55 4.41 0.98

lo- Primary 7 * Only birds wth complete OT probably complete molt sequences considered. 5- (May 25. 46.61

was a tendency toward molting every other primary in one season’smolt, but in the caseswhere this pattern was approached most closely, it was not followed consistently through the years nor from one wing to the other. Usually the primaries molted in one year were not molted the next year and vice versa, so that all primaries tended to molt about once every 2 years. However, primaries sometimes molted twice in 2 years and occasionally failed to molt FIGURE 2. Timing of loss of various primaries. For even once in 2 years. For the 16 primaries num- each feather, timing is plotted as the midpoint of the bered 3 through 10, the average for both male interval between the last time the feather was photographed as still present and the first time it was pho- and female wild birds was 4.4 primaries molted tographed absent. Arrows indicate median loss dates per wing per year. The average for captives (Ta- for the various primaries. Median loss dates are also ble 3) was almost identical at 4.3 primaries per tabulated along with standarddeviations of loss dates. wing per year. When the same primary molted twice in 2 years (Table 1). Likewise, the pattern exhibited years, there was a strong tendency for the feather by IC 1, another wild bird, in his third and fourth to drop early in the first year and late in the molts was very similar to that of many captives in their first and second years. On the other hand, HIW, another wild bird, showed a very irregular and individual molting sequence in his second year. Although molt of HIW was not followed in his first year, the irregular second-year pattern 0 0 shown by this bird suggests that his first molt 0 0.0 0 may also have been quite irregular. The only other wild immature for which data exist in the late immature stageswas BFE, first studied in his fourth year. The molt of this bird showed some resemblance to that of ICI and REC in their fourth years, but by his sixth year, BFE’s I I I I I I I I molt (especially his left wing) had become essen- 10 20 30 to 20 30 9 19 April JUlltZ tially adult in pattern. May Hatching date In adults, molt was distributed relatively evenly FIGURE 3. Numbers of primaries molted per wing across the span from primary 3 through 10 in in first molting period as a function of hatching date any one year, although the exact patterns varied in previous year. Only birds with accurately known greatly from bird to bird. In some adults there hatching dates are considered.

416 N. F. R. SNYDER, E. V. JOHNSON AND D. A. CLENDENEN

TABLE 4. Frequency of primary molt of wild Cali- loo- fornia Condors in 2-year periods.”

90. No. of No. of No. of cases cases cases Pi;;? 80. %;;;:a Mean molting interval PIiItlaIy times in twice in no. 2 years 2 years Yearsb n lo- 3 57 20 1.64 21 4 63 15 1.60 28 5 65 13 1.76 26 @ 60. 6 67 10 1.74 30 8 s 7 61 16 1.71 28 g so- 8 72 6 1.82 21 c 9 76 2 1.93 27 6 40 10 14 1 2.09 20 r t a Only birds with completeor probablycomplete molt sequencesfol- 00 30 lowed in consecutiveyears considered. bCalculated as the elapsedtime betweenconsecutive drop dates or Between s completmndates for various feathers.To reducebias, no interval was individuals includedin the tabulationsif lessthat 2 yearsof data was available for z 20. the featherin questionfollowing the first drop date.

10 second year. In the first year, such feathers had i an average rank of 1.6, whereasthe rank average

in the second year was 3.6, a highly significant “fi Wlthl” individuals difference (z = -7.753, P < 0.001, Wilcoxon’s I I signed-ranks test). In addition, there was a gen- 0 11 12 ~3~4~5~6~78’ 9~10~11~12~13~14~’ eral trend for low-numbered primaries to be re- Numbers of dlscrepancles placed more frequently than high-numbered pri- FIGURE 4. Distribution of numbers of primary maries (Table 4). The average interval measured feather discrepanciesbetween and within individuals between consecutive molts was highly signifi- in consecutiveyears (1982 to 1985). Discrepanciesde- fined as feathers molting twice in 2 years or not at all cantly correlatedwith primary number (rS= 0.88, in 2 years. P = 0.005) and ranged from 1.60 years for primary 4 to 2.09 years for primary 10. Thus, the overall pattern was for birds to molt cantly different from the within-individual dis- primaries slightly faster than on a 2-year cycle, tribution by a median test (x2 = 4 1.92, P < 0.005). and this led to discrepanciesfrom a regular al- Thus, identification of individuals from year ternation of molt and nonmolt years for indi- to year can be determined quite reliably by vidual primaries. If discrepanciesare defined as matching birds with the fewestdiscrepancies. This caseswhere a primary molted twice in 2 years conclusion is not circular, becauseessentially all or not at all in 2 years, it is straightforward to birds studied have also been identifiable from examine the numbers of discrepancies per bird year to year by means other than feather dis- in year to year comparisons.The averagenumber crepancies-most importantly by peculiarities of of discrepancieswithin individuals was 1.8 (range feather damage, but also by other information 0 to 4) between 1982 and 1983, 2.4 (range 0 to such as patagial tags on some birds, head color 5) between 1983 and 1984, and 2.8 (range 0 to characteristicsin some birds, and behavioral pe- 5) between 1984 and 1985. The overall average culiarities, especially traditional use of certain was 2.2 (range 0 to 5). For each bird, discrep- nesting and roosting areas. The only individuals ancies were fewer, or at least no greater, with for which we were forced to rely entirely on dis- itself than with other individuals, and the overall crepancies in year to year identifications were distribution of between-individual discrepancies UN1 and BFE for 1983 to 1984. (Fig. 4) suggeststhat it is unusual to have three It is also possible to compare the molt pattern or fewer discrepancies (only 2.4% of the total of one wing of a bird with that of the other wing comparisons). On the average, there were 8.0 in the same year, defining discrepanciesas feath- discrepancies between individuals, and the be- ers that molt on one wing and not on the other tween-individual distribution is highly signifi- (Table 5). Right-left discrepanciestended to be CALIFORNIA CONDOR MOLT 477

TABLE 5. Between-wing primary feather discrep- Primary 3 ancies within individuals from 1982 through 1985.a v Min

No. of dwxepancies Max & Bird 1982 1983 1984 1985 (Yea6 Primary 4 SBM Ad. 3 1 3 3 Min SBF Ad. 5 5 5 5 1 r Max CVM Ad. 5 7 6 - CVF Ad. 6 5 6 - Primary 5 v PCA Ad. 5 5 4 3 li.A s ll&____. Min PCB Ad. 4 4 - - Max SMM 0 1 1 1 PPF 2:: 2 3 3 - CCF Ad. 0 - 2 1 CCM Ad. 3 3 2 - SSM Ad. 2 1 2 - SSF Ad. UN1 Ad. 23 2 2 : Min HIW 2-5 2 ; 4 4 Max REC 2-5 1 1 2 Primary 8 BFE 4-6 2 3 3 - v Min ICI 3-4 1 1 - - 17--‘ BOS 1 - 1 - - Max Mean change between years 0.0 +0.2 -0.2 Min - Featherdiscrepancies defined as feathersmolting on onewmg but not Max the other.Only birdswith completeor probablycomplete molt sequences considered. Primary 10 v Min I ‘ Max fewer among immatures than among adults, but this tendency did not reach statistical significance I I I I 100 110 120 130 by a median test (x2 = 2.04, P > 0.10). Among Days adults, the average number of right-left discrep- FIGURE 5. Minimium (above axis) and maximum ancies within individuals (3.1) was reasonably (below axis) periods from loss to full replacement for closeto the averagenumber between individuals given primaries. Arrows delineate averagereplacement (3.9) suggestinga high degree of independence periods, computed as means of the 10 highest mini- of molt between wings. Whether the adults show- mum values and 10 lowest maximum values for each primary. ing the most right-left discrepancieswere the old- est individuals is unknown. In the four years covered in Table 5, there was no overall trend and 10 largest minimum periods, ranged from toward increasing numbers of between-wing dis- about 3% to 4 months and varied systematically crepancies in individuals from one year to the with primary number. There was a bias toward next. lengthy loss-replacement periods for the primaries closest to the leading edge of the wing. A RATES OF PRIMARY GROWTH comparison of averageperiod lengthswith actual In Figure 5 we present the distributions of min- feather lengths of two representative individuals imum and maximum replacement intervals for and with feather weights of primaries collected the various primaries in the zone where these below roosts over the years (Fig. 6) shows that, values converge (approximately 100 to 125 days). while primary 10 is the shortestprimary in length In general, the rates of feather growth seen for and lightest in weight, its average loss-replace- the various primaries were quite uniform among ment period is longer than those of primaries 3, different individuals in the population, judging 4, and 5. Why primaries at the leading edge of from the small amount of overlap in maximum the wing have relatively sluggishreplacement pe- and minimum periods for most primaries. Av- riods is unknown, but this appearsto be a regular erage molt period, defined for each primary as feature of molt in other families of birds as well the mean of the 10 smallest maximum periods (e.g., Newton 1967, 1969). 478 N. F. R. SNYDER, E. V. JOHNSON AND D. A. CLENDENEN

grown primaries) up to 9 or 10 (occasionally 11) months out of the year. Individuals were most likely to show no evidence of molt from Novem- ber through February. In addition to the steady seasonalprogression of median drop dates for individual primaries (Fig. 2) there was a significant reduction in variance of drop dates as one moves up the primary sequence (Y, = -0.79, P < 0.025). Thus primaries 3 and 4 were quite likely to drop at any time during the molting season,while primaries 9 and 10 were quite consistently shedin the latter part. At least in part, this reduction in variance is a reflection of the progressivereduction in the tendency for primaries to molt in consecutive years as one moves up the primary sequence(Ta- ble 4) as consecutive-year molting of primaries , normally entails early molt in one year and late ,’ molt in the next. ./’ Mundy (1982) found a marked depression in molting activity of older (presumably breeding) accipitrid vultures in Africa during the breeding season. In adult condors there was likewise a differencein the seasonaltiming of molt betweek 3 i 5 6 7 8 9 lb Primary number breeding and nonbreeding birds (Fig. 7). Breed- “lx, ers ofboth sexesshowed a clear tendency to begin “\ FIGURE 6. A. Measuredtotal primary featherlengths for two birds: BFE, an adult (Los Angeles County Mu- primary molt earlier and end it later than non- seum 102739) and ICI, a subadult (LACM 101811). breeders, presumably leading to a relatively B. Average weights of primaries (sample size given for greater retention of flying abilities for breeders each). C. Estimated average loss-replacementperiods during the middle portion of the breeding season. for various primaries from Figure 5. D. Calculated growth rates for various primaries based on A. and C. The occasionalfeathers lost in late fall or early E. Average growth rates for various primaries based winter had exceptionally long periods for re- on B. and C. placement, indicating a period of interrupted molt over the winter (Table 6). We excluded these feathers from the general calculations of rates of SEASONAL TIMING OF PRIMARY MOLT AND feather replacement (Fig. 5) becauseof their ob- INTERRUPTED OVERWINTER MOLT viously exceptional nature. In all of these cases Most primaries were shed between 1 February a protracted period of no-growth occurred prior and 1 September (Fig. 2). Since primaries shed to the initiation of visible growth of replacement at the end of this period tended to be the higher- feathers, and the birds exhibited feather gaps in numbered primaries and took close to 4 months their wings lasting in some casesover half a year. to replace, birds were commonly in some state For unknown reasons,all instances of long-last- of primary molt (either with missing or partly ing gaps involved primaries 5 through 7. There

TABLE 6. Casesof interrupted primary molt over the winter.

Minimum Maximum Date last Date first Date last Date first period period Bird Primary present missing short complete (days) (days)

CCF L-5 1l-2-82 11-24-82 5-27-83 6-13-83 184 223 PCA R-6 - 11-25-81 6-23-82 7-3 l-82 210 - PCA L-6 - 11-25-81 6-23-82 7-31-82 210 PCA L-6 9-23-84 1O-22-84 7-30-85 8-5-85 281 316 CVF L-7 10-27-82 12-26-82 5-29-83 6-30-83 154 246 CALIFORNIA CONDOR MOLT 479

Breeding males 3 4 5 6 7ag 10

Nonbreeding males n 5 347 69 6 10

Breeding females 3 4 5 67 89 10

Nonbreeding females 3 4 5 8 79106

r I I I I I I I I 1 pe;o 1 lhz,,o 30 10 20 30 10 20 30 10J2uo,30 10 20 30 10 20 APr May Jul Aug FIGURE 7. Median drop dates for primaries of breeding and nonbreedingadult California Condors. Primary number given for each median date. were no indications that these casesmight have sibly also his R9 and R16 secondaries)in his first involved feathers accidentally breaking off near molting period, a completely different pattern. their bases prior to molt. Furthermore, when tail molt commenced in To- patopa in his second molting period, the order MOLT OF SECONDARIES AND RECTRICES of replacement of rectrices (L4-LS, L3, L6, L2, In their 2-year molt study of Topatopa, a captive and Ll; and Rl, R6, R4, R2, R5, and R3) was bird obtained before its first molt, Todd and Gale quite different from that of BOS. (1970) reported no tail molt and essentially no Tail molt among recently-hatched captives secondary molt in the first molting period, then generally followed a pattern of no replacements complete and almost complete molt of these in the first year (seven birds examined in 1985) feather categories in the following year. While followed by partial replacements in the second the photographic method was not adequate to year (six birds examined in 1985). The most give detailed information on molt of these feath- common patterns in the second molting period ers in wild birds, it was informative enough to were replacement of two outer and two central confirm much of what Todd and Gale reported. rectrices (two individuals) and replacement of Although we saw limited signs of molt of rec- two outer and four central rectrices (two indi- trices and secondariesin some wild yearlings, the viduals). One bird replaced two outer and six generally smooth contours of these feathers in central rectrices and one molted 2, 3, and 6 on photographs of yearlings suggested minimal the right side and 1, 2, and 6 on the left, possibly molting as a rule. having molted Rl in its first year. However, a yearling female (BOS) that died Secondary molt of recently-hatched captives and was recovered shortly after completing her resembled the pattern exhibited by BOS, with all first molt in November 1983, had replaced 4 of birds examined in the first year (seven individ- her 12 rectrices (Ll, L2, Rl, and R3) and 3 of uals) molting secondary 1 on each side, some 22 secondarieson each wing (Ll, L19, and L22; birds also molting secondary2 on each side (two Rl, R15 or R16, and R21) (see Fig. 1B). Topa- individuals), and all birds molting a high-num- topa molted his Ll 1 and R17 secondaries(pos- bered secondaryor two closeto the body on both 480 N. F. R. SNYDER, E. V. JOHNSON AND D. A. CLENDENEN sides (mainly secondary 21 or 22). Secondary primary 10 before starting another molt wave of molt of the second year was much more exten- low-numbered primaries. Topatopa was also un- sive, generally involving about half of the sec- usual in molting all tail feathers and nearly all ondaries, and was extremely variable in detail secondariesin his secondyear. We are unable to but with a general tendency for most replace- account for these peculiarities. ments to occur near the body and among the In general, however, the patterns of molt doc- most distal secondaries.Molt in the secondyear umented in wild and captive juvenile condors did not result in replacement of all original sec- were quite similar, suggestingthat captivity was ondaries in the birds checkedclosely (except To- not producing great distortions in molting pat- patopa). Thus as a general rule, a large fraction terns. The numbers of primaries molted per year, of the original rectrices and secondaries lasted the sequencesfollowed, and the seasonaltiming without replacement into the third molting pe- of molt all appeared to reflect the same general riod (at least in captives). In contrast, essentially patterns, although there was considerable vari- none of the original primaries lasted this long, ability in detail in both wild and captive indi- although Cuyama apparently failed to molt pri- viduals. The clearest effect of captivity on molt maries 9 and 10 on the left wing in his first two was seen in HIW, UNI, and CCF, all of whom molts, and Cachuma apparently failed to molt were captured in the midst of the molting season primary 10 on the right wing during her first two in 1985, and all ofwhom exhibited some primary molts (Table 3). feathers that did not quite reach full length, apparently as a result of the stressof capture and DISCUSSION adjustment to captivity during the period of Among wild individuals, the most deviant molt- growth of these feathers. The failures of HIW to ing patterns were found in PCA and PAX. PCA molt primary RlO and of UN1 to molt primary (Fig. 1C) exhibited a consistent tendency to molt LlO in 1985 could also have been a result of more primary feathers than average and in one capture. year ( 198 5) actually replaced every primary from Although Miller (1937) reported a California 3 through 10 on his left wing (although one of Condor specimen with 13, rather than 12 rec- these primaries had dropped late in 1984). PCA n-ices, none of the wild or captive condors ob- also consistently exhibited the highest number served in this study, so far as could be deter- of primary feather discrepanciesof any wild bird mined, exhibited unusual numbers of flight from year to year. In addition, PCA accounted feathers.Mundy (1982) found low frequenciesof for more than half the instances documented in individuals (generally about 5%) with more or the wild population of birds dropping primaries fewer primaries and rectricesthan normal in five in the fall and not replacing them until the fol- speciesof African vultures. lowing summer. Remarkably, every such case with PCA involved a primary 6. No causesfor SEASONAL CONSIDERATIONS these peculiarities are known. The seasonal timing of primary molt docu- PAX in 1982 representedanother extreme, re- mented in this study (mainly March to October) placing only a single primary of the 16 possible matches that reported for condors by Wilbur between numbers 3 and 10 on his two wings. (1975). Wild California Condors most common- PAX’s molt also started very late in 1982 (late ly lay eggsin February or March, hatch eggsin July), and it is possible that this bird fledged April or May, and fledge young in September or extremely late in 198 1 or possibly even early in October. Young remain strongly dependent on 1982. However, the extremely abbreviated molt their parentsuntil the following spring,and adults of PAX in 1982 might alternatively have been commonly do not breed in years following suc- related to poor health or genetic problems. When cessful fledging of young (Koford 1953, Snyder this bird was trapped for the captive flock in late and Hamber 1985). Thus, primary molt in the 1982, it was quite light in weight and gaped with speciesnormally coincides with the egg-nestling- the slightest exertion. Chronic gaping is a trait early fledgling phasesof the breeding cycle, and PAX has retained as a captive to this day. the period of heaviest molt-midsummer- is Among captives, the most unusual molt was the season of heaviest food demands in repro- exhibited by Topatopa, who showeda strongten- duction, a period that is commonly avoided in dency to finish molting his first primaries through molt of other avian species(Payne 1972). How- CALIFORNIA CONDOR MOLT 481

ever, for the condor it appears that summer is the sense both of avoiding metabolic costs of also a period of reasonably good food availability molt and avoiding the penalties resulting from and consistently good foraging weather (Miller reduction of effective wing surface area. How- et al. 1965). ever, the delays in completing first molt of rec- Thus, the seasonaltiming of molt in condors trices and secondaries result in some of these may relate more to foraging opportunities than feathersbeing in service for 3 years, which poses to the reproductive cycle per se. The winter risks of excessive feather wear for parts of the months, December through March, are normally flight surface during the third year. the period of most frequent storm fronts in southern California, while from May through COMPARISONS WITH OTHER SPECIES October it is unusual to seemuch, if any, rainfall. Various features of primary molt of California During periods of heavy rainfall and low clouds, Condors find instructive parallels and contrasts condorsare unable to forageefficiently, and their in the molt of large accipitrid vultures in Africa. opportunities for finding food are often limited Mundy (1982) noted that all five specieshe stud- to brief l- or 2-day windows of good weather ied in southern Africa greatly reduced molt dur- between successivefronts. In addition, the rel- ing the winter months, a pattern similar to that atively short daylengths in the winter months of Gymnogyps.However, unlike the situation with automatically reduce the potential hours for for- Gymnogyps,the winter months for these species aging to a significant extent (see Johnson et al. are the dry seasonand are the central part of the 1983). Further, food needs in winter are rela- breeding season,when the birds are tending eggs tively high becauseof low temperatures, yet pe- and nestlings.This correspondencein season,but riods of cold weather can inhibit feeding by freez- not in weather or in stagesof the breeding cycle, ing carcasses,making them difficult for condors might be taken as evidence that the primary fac- to ingest. Thus, it may be critical that the birds tor controlling timing of molt in large vultures are in their most perfect plumage in winter so is daylength, perhaps through its influence on they can move about the foraging grounds with foraging opportunities. Apparently consistent maximal efficiency. with this possibility is the fact that Houston (197 5) While the abilities of condors to survive star- was unable to find much evidence for seasonal vation are undoubtedly well developed (we have change in molt of Gyps africanus and G. ruep- seen incubating birds sit as long as 10 days with- pellii in an equatorial region of central Africa out food), the capacities of the birds to attain with relatively uniform daylength throughout the good physical condition for the initiation of re- year. However, Mundy (1982) provided an al- production may depend on their abilities to cope temative explanation for relatively nonseasonal with limited foraging opportunities in winter and molt in this region, based on relatively low sea- on their avoidance of the metabolic costsof molt sonality in weather conditions. during this period. Furthermore, molt attempted The data of Mundy and Houston indicate that during periods of food deprivation in winter may juveniles of the African species,like those of the pose risks of the production of short or struc- California Condor, begin first molt of primaries turally weak feathers. The fact that molt nor- about 8 to 9 months after fledging and that pri- mally begins in the spring with low-numbered mary molt of juveniles proceedsquite regularly primaries, while high-numbered primaries, pos- up the sequence.Very little secondaryor tail molt sibly more critical to flight, are not shed until the was seen until about a year and a half after fledg- dry midsummer period, may minimize the pen- ing, also correspondingto the situation in Gym- alities of startingmolt before the winter and spring nogyps.Further, although the data of these au- storms are over. thors do not cover molting patternsand sequences The near absence of molt in secondariesand of adults in detail, their data for young birds rectrices,and the restriction of molt to low-num- suggestthat primary feathers may molt on a bered primaries in yearlings is of special interest. greater than l-year cycle, as in Gymnogyps. Becauseyearlings probably face the greatestmor- Commonly in these species, a second wave of tality rates of any age-classof free-flying condors molt started up the primary sequencebefore the as they develop abilities to forage on their own first wave carried through the higher-numbered and compete for food at carcasses,it seemsrea- primaries, again similar to Gymnogyps. sonable that these birds restrict molt greatly, in By repeatedmeasurements ofgrowing primary 482 N. F. R. SNYDER, E. V. JOHNSON AND D. A. CLENDENEN and secondary feathers of captive G. africanus, and it seems likely that such individuals suffer Houston (1975) calculated a very uniform rate considerable lossesin flying abilities. of feather elongation of 4.4 mm per day. Simi- Prevost (1983) suggestedthat there seem to be larly, Mundy (1982) found that primary growth limits to how fast developing flight feathers can of nestling G. africanusproceeded at 4.7 mm per elongate, basing this conclusion on a review of day. While we have not made the same sorts of literature on feather growth in many different measurements for Gymnogyps, we know the groups of birds. A number of authors have ar- lengths of the total periods from loss to full re- gued that the extended lengths of time it takes placement of the various primaries with some to grow the long primaries in large flying birds accuracy and calculate that averaged over the in effect force these birds into a molt dilemma entire period, rates of elongation for the various (Stresemann and Stresemann 1960, 1966; Stre- primaries range from 4.3 to 6.0 mm per day (Fig. semann 1963, 1967; Edelstam 1984). Either they 6). While growth of Gymnogyps ’ primaries ap- cannot replace the feathers frequently (e.g., an- pears to average somewhat faster than that of G. nually) or they must replace them to a greater or africanus, primaries of G. africanus are some- lesserextent on a simultaneous basis. However, what shorter than those of Gymnogvps, and if a number of primaries are in molt simulta- Houston’s estimated times for replacement of neously, it becomes disadvantageous to molt the various primaries of this species(95 to 124 them in the simple sequential order character- days) are strikingly similar to the replacement istic of most small birds becauselarge gapswould periods documented in this study. form in the airfoil. Although the replacement periods for individ- As discussedby the aboved authors, a number ual primaries may be quite similar in the two of apparent solutions to the above problem have species,it appearsthat the numbers of primaries evolved in different groups of relatively large in molt at the same time vary considerably, with birds. For example, falcons and parrots molt pri- the fewestnumber molting simultaneously in the maries in two directions simultaneously from a equatorial G. africanus studied by Houston central focus. Some cuckoos follow a pattern of (1975) considerably greater numbers found dur- molting every other primary in sequence, then ing the main molting season of G. africanus in molting the ones missed in a second round more southerly regions of Africa (Mundy 1982) through the sequence.Many large accipitrids and and even more primaries molting simultaneous- other groupsfollow a pattern that has been termed ly at the height of the molting season of Gym- a serial molt or “Staffelmauser” in which pri- nogyps.Houston rarely found more than two primaries molt in a sequential order but in which maries simultaneously in molt for juveniles or new waves of molt begin before old ones have more than four primaries simultaneously in molt finished. In young birds these waves tend to be for older birds, and he emphasizedthat primaries far apart in the primary span, but in older birds were characteristically not shed until the preced- several molt waves may be proceeding up the ing primaries in sequencewere fully grown, Mun- primary sequencesimultaneously in roughly par- dy found an average of 3.7 primaries simulta- allel fashion. Edelstam (1984) claimed that the neously in molt for juveniles and 4.3 primaries Staffelmauserpattern of molting is characteristic simultaneously in molt for adults during the sea- of all large cathartids, and it has also been re- son of heaviest molt (October through Decem- ported in their close relatives, the storks, by ber). In Gymnogyps,from July through Septem- Bloeschet al. (1977). Edelstam also commented, ber and considering only primaries 3 through 10, however, that as individuals of the largestspecies the average number of primaries in molt simul- age, inconsistenciesappear that disturb the pat- taneously for all birds was 5.1 (4.6 for immatures tern, and in “adult large vultures it may be dif- and 5.3 for adults). Correspondingly, the period ficult occasionally to trace any organized molting of molt appears to be most seasonally concen- pattern at all,” a conclusion earlier advanced by trated for Gymnogyps,less so for G. africanus in Stresemann and Stresemann (1960). southern Africa, and apparently least so for G. With the California Condor, it is possible to africanus in equatorial Africa. During the heavy interpret many of the molt patterns in Tables 1 molt period of Gymnogyps, individuals some- and 3, especially those of young birds, as being times have fewer than four of the emarginated consistent with a Staffelmauser arrangement. primaries on a wing fully operational (Fig. IC), However, a close examination of the data indi- CALIFORNIA CONDOR MOLT 483 cates fairly frequent distortions of the pattern, replacement at rough intervals of 2 years (Table especially in older birds, and it is questionable 4). An apparent molt wave could be a result of how useful it is to describe the molt pattern of factors such as these, rather than itself being a adults as a seriesof roughly parallel waves mov- “driving force” in determining the order in which ing up the sequence. For one thing, the waves primaries are replaced. one can trace in Table 1 are exceedingly variable In contrast to the complicated patterns of pri- in speed, sometimes covering a 3-primary span mary molt characteristicof adult California Con- (or more) in one year and sometimes taking 3 dors, wing molt of the smaller cathartids appears years to go the same distance. Such variability to be quite simple. Regular sequential molt of can sometimes be seen in different parts of the primaries has been especiallywell studied in cap- same wing of the same bird in the same years tive and wild Turkey and Black vultures (Cu- (e.g., SBM’s right wing from 1982 to 1984). thartes aura and Coragyps stratus) by Amadeo Moreover, waves appear to catch up with each Rea (unpubl.). In these species,primaries are re- other and die out on occasion. For example, two placed in an almost invariant 1 through 10 se- molt waves in SBM’s left wing in 1982-posi- quence, regardlessof age of the bird, although tioned at primaries 5 and 7-end up being a new molt cycles generally start in late summer single wave by 1984-primary 9, and then 10. before preceding cycles are completely finished, And on occasion, waves appear to originate in so that both low- and high-numbered primaries the middle of the primary span without any an- are commonly missing or growing simultaneous- tecedents(e.g., a wave starting at HIW’s left pri- ly at this time. Both C. aura and C. atrutus re- mary 7 in 1984). In itself, the Staffelmausercon- place all primaries on an annual basis, and de- cept does not explain why primary molt in spite the fact that both species occur in highly condors has a strong tendency to begin close to seasonal environments and breed on a highly the low end of the sequenceand end close to the seasonalbasis in North America (Jackson 1983) high end of the sequenceeach year (although this molt in both species is spread throughout the pattern is not necessarily inconsistent with the year so there is no period of true molt arrest in Staffelmauser concept). one season. Instead of describing molt of adult condors as Perhaps the most detailed published study of a series of roughly parallel waves, one could al- flight feather molt of a large soaring specieshas ternatively describeit as a pattern in which about been that of Bloesch et al. (1977) on the White half of the primaries molt each year, and al- Stork (Ciconia ciconia), and it is informative to though these can be almost any combination of compare their results with our own because of specific primaries, molt tends to move roughly the well-documented close taxonomic relation- as a single wave up the sequence,replacing feath- ship of storkswith cathartids (seeRea 1983, Sib- ers that had not molted in 2 years and skipping ley and Ahlquist 1986). Like the California Con- feathersthat molted the previous year, or at least dor, the White Stork molts about 55% of its late in the previous year. More specifically, feath- primaries each year, and although this species ers that are not molted in one year are almost has 11 functional primaries while the condor has always molted in order up the sequencethe next only 10 (primary 11 is vestigial in cathartids), year, although in the secondyear, birds also often other aspectsof molt in thesetwo speciesare also molt one or two feathersthat molted early in the quite similar. In both, low-numbered primaries previous year. These repeats tend to come late are replaced more frequently than high-num- in the molting period of the second year, but bered primaries. In the stork, average periodic- often occur intermixed in sequencewith molt of ities range from once every 1.2 years for primary feathers that did not molt in the first year. The 1 to once every 2.5 years for primary 11, values overall validity of this description is clear from very similar to those for the condor given in Tables 1 and 2 and Figure 2. Table 4. Further, in both speciesgrowth rates of As another alternative, it might be best not to the various primaries show a peak at about pri- talk about molt waves at all but instead to de- maries 5 and 6, with especially slow growth of scribe molt order as simply a consequence of the outermost primaries (10 or 11). In addition, different seasonal specificities of various pri- the seasonaltiming of molt is very similar (spring maries in timing of molt potential (Fig. 2) in to early fall) in both species,and coincides with interaction with a periodic factor driving feather the breeding seasonfor both species. 484 N. F. R. SNYDER, E. V. JOHNSON AND D. A. CLENDENEN

Principal differences in molt between the and Game; the Bureauof Land Management; the Con- species lie in the regularity of secondary molt dor Survival Fund; Hawk Mountain SanctuaryAsso- ciation; the Illinois Natural History Survey; the Los and in the rigor with which they approach a Staf- Angeles, Morro Coast, Kern, Santa Barbara, and Tu- felmauser molt pattern overall. Bloesch et al. lare County Audubon Societies;and Van Nuys Char- (1977) documented a quite consistent pattern of ities. We are especially grateful to the Santa Barbara secondarymolt starting with three foci-second- Museum of Natural History for use of their darkroom aries 1, 5, and 2 1 or 22-and presented data facilities and to Amadeo Rea and Walter Spofford for accessto their unpublished molt data. Critical com- indicating considerablesecondary molt in the first ments on the manuscriptby Peter Mundy, Ian Newton, molting period of most individuals. In the cap- Ralph Palmer, and Amadeo Rea were most helpful. tive condorswe have examined closely, there has Photographersproviding materialson which the study been a fairly consistentpattern for secondarymolt was based were L. Andaloro, A. Anderson, S. Ander- son, V. Apanius,M. J. Arnold, L. Aulman, D. B. Bar- to start with secondary 1 and either 21 or 22, bour. L. Beniamin. A. Blakeslev.P. Bloom. K. Brown. but we have seen no sign of a focus at secondary B. Bush, G.-Carpenter, B. Cicbna, D. Clendenen, C: 5 (although Rea [ 19831 reported such a focus for Cogan,C. Comeau, S. Ducummon, P. Ensley,D. Foote, Black and Turkey vultures). Instead, captive con- G. Fugle, J. Grantham, J. Grinnell, G. Guliasi, J. Ham- dors have exhibited a variable situation, with ber, H. Hamber, R. Hamber, N. Harris, P. Harvey, B. Hatfield, W. Hawk, L. Hecht, C. Heidsick, P. Hester, several internal foci developing in unpredictable P. Hicks, T. Hicks, A. Hogg, J. Ingram, W. Jacobi, E. positions in the secondaryspan after initial molt- V. Johnson, J. Johnson, V. Ketner, P. Kleintjes, S. ing of the most proximal and most distal sec- Kimple, D. Ledig, A. Leete, W. Lehman, C. Mc- ondaries, a pattern very similar to that reported Conathy, V. Meretsky, H. 0. Miller, K. Miner, L. Mor- for several speciesof African vultures by Mundy ton, K. Nelson, T. Nichols, R. Norris, J. C. Ogden, G. Perlmutter, B. Peterson, S. Pletschet, P. Principe, R. (1982), and to that reported for the Eurasian Ramey, D. Rimlinger, L. Riopelle, J. Roach, B. Rob- Sparrowhawk (Accipiter nisus) by Newton and erts, J. Roser, J. Russin, G. Sanders,J. Schmitt, J. M. Marquiss (1982). Furthermcre, unlike storks, Scott, H. Snyder, N. Snyder, M. Stein, D. Sterner, E. condors do not commonly molt more than sec- Strauss.T. Sturm, D. Thomuson. R. Thorstrom, T. Tomlin, M. Turansky, F. Viliablanca, L. Von Hendy, ondaries 1 and 2 and one or two feathers in the M. P. Wallace, D. Ward, A. Webster, G. Wegener, R. region of secondaries 19 through 22 in the first Wilson, E. Wise, M. Witt, N. Wood, and B. Woods. molting period. We are also gratefulto Eric L. Johnsonfor translating In general, the molt sequencesof several cap- the paper by Bloeschet al. (1977). tive juvenile storks (Bloesch et al. 1977) appeared to be much closer to an ideal Staffelmau- LITERATURE CITED ser pattern than we have found in the condor, BLOESCH,M., M. DIZERENS,AND E. SUTTER. 1977. although these authors too found some irregu- Die Mauser der Schwungfedernbeim Weisstork Ciconia ciconia. Omithol. Beob. 74:16 l-l 88. larities that were difficult to rationalize on the EDELSTAM,C. 1984. Patterns of moult in large birds basis of a strict Staffelmauser. of prey. Ann. Zool. Fenn. 211271-276. Thus, although flight feather molt of the White HOUSTON,D. C. 1975. The moult ofthe White-backed Stork showsmany similarities to the molt of the and Ruppell’s Griffon vultures Gypsafricanus and California Condor and this could be considered G. rueppellii. Ibis 117:474-488. JACKSON,J. A. 1983. Nesting phenology, nest site to provide further support for a close taxonomic selection, and reproductive successof Black and relationship between storksand cathartids, molt Turkey vultures, p. 245-270. In S. R. Wilbur and of the condor appears to be more similar to that J. A. Jackson[eds.], Vulture biology pnd manage- of some large accipitrids in certain respects. ment. Univ. of California Press, Berkeley. JOHNSON,E. V. 1985. Commentary, California Con- ACKNOWLEDGMENTS dor population estimates. Condor 87:446-447. JOHNSON,E. V., D. L. AULMAN,D. A. CLENDENEN,G. The resultsreported in this paper are derived from the GULIASI,L. M. MORTON,P. I. PRINCIPE,AND G. cooperative efforts of numerous organizationsand in- M. WEGENER.1983. California Condor: activity dividuals participatingin the condor conservationpro- patterns and age composition in a foraging area. gram. Of primary importance have been the contri- Am. Birds 37:941-945. butions of the U.S. Fish and Wildlife Service: the KOFORD.C. B. 1953. The California Condor. Natl. National Audubon Society;California Polytechnic&ate Audubon Sot. Res. Rep. 4. University, San Luis Obispo; the U.S. Forest Service; b MILLER,A. H., I. MCMILLAN,AND E. MCMILLAN. 1965. the SantaBarbara Museum ofNatural Historv: the San The current status and welfare of the California Diego and Los Angeles zoos; the Western Foundation Condor. Natl. Audubon Sot. Res. Rep. 6. of Vertebrate Zoology; the Santa Cruz Predatory Bird MILLER, L. 1937. Feather studies on the California Research Group; the California Department of Fish Condcr. Condor 39: 160-l 62. CALIFORNIA CONDOR MOLT 485

MUNDY, P. J. 1982. The comparative biology of ment-clutching and annual nesting of California southern African vultures. Vulture Study Group, Condors. Condor 87:374-378. Johannesburg. SNYDER,N.F.R., AND E. V. JOHNSON.1985. Photo- NEWTON,I. 1967. Feather growth and moult in some aranhic censusinp.of the 1982-1983 California captive finches. Bird Study 14:1 O-24. ??ondorpopulati&. Condor 87: 1-13. NEWTON,I. 1969. Moult and weightsof captive Red- STRESEMANN,E. 1963. Taxonomic significanceof wing polls Carduelisjlammea. J. Omithol. 110:53-61. molt. Proc. XIII Int. Omithol. Congr. (1962): 17 l- NEWTON,I., AND M. MARQUISS. 1982. Moult in the 175. Sparrowhawk.Ardea 70: 163-l 72. STRESEMANN,E. 1967. Inheritance and adaptation in PAYNE,R. B. 1972. Mechanisms and control ofmolt, moult. Proc. XIV Int. Omithol. Congr. (1966):75- p. 103-155. In D. S. Famer and J. R. King [eds.], 80. Avian biology. Vol. 2. Academic Press,New York. STRESEMANN,E., AND V. STRESEMANN.1966. Die PREVOST,Y. 1983. The moult of the Osprey Pandion Mauser der Vogel. J. Omithol. 107:1-488. haliaetus.Ardea 7 1:199-209. STRESEMANN,V., A&D E. STRESEMANN.1960. Die REA, A. M. 1983. Cathartid affinities: a brief over- Handschwingenmauserder Tagraubvogel.J. Or- view, p. 26-54. In S. R. Wilbur and J. A. Jackson nithol. 101:373-403. [eds.j,Vulture biology and management.Univ. of TODD, F. S., AND N. B. GALE. 1970. Further notes California Press, Berkeley. on the California Condor at Los AngelesZoo. Int. SIBLEY,C., AND J. AHLQUIST. 1986. Reconstructing Zoo Yearb. 10:15-17. bird phylogeny by comparing DNA’s. Sci. Am. WILBUR,S. R. 1975. California Condor plumage and 254182-92. molt as field study aids. Calif. Fish Game 6 1:144- SNYDER,N.F.R., ANDJ. A. HAMBER. 1985. Replace- 148.