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BREEDING AND MOLT IN THE WHITE (GYGIS ALBA) ON CHRISTMAS ISLAND,PACIFIC OCEAN

N. PHILIP ASHMOLE Peabody Museum of Natural History Yale University New Haven, Connecticut 06520

INTRODUCTION AND METHODS Within this, an effort was made to locate all active nests; the nests were marked with red paint and Christmas Island lies in the Central Equa- numbered with aluminum garden labels, and the torial Pacific at 2” N, 157” W, about 1209 activity (if any) at all known sites was recorded at miles south of . I made a series of least once on each visit to the island. As many adults visits to the island during the period March as possible were caught and banded during incubation as they left their , while a few more were caught 1963 to February 1964, and one later visit while brooding or about to feed chicks. With few in June 1964. The primary purpose of the exceptions, adults were banded only if they were visits was to study the sexual cycles of the known to have an or chick. At a later stage in on the island. The results of the the study a special effort was made to recapture banded birds. This was achieved generally when they work on one , the ( were roosting or were involved in a subsequent breed- fuscutu), have already been published (Ash- ing attempt. The restriction of banding to adults that mole 1965), while the feeding ecology of the could be associated with known active nests meant that only a relativelv small number (248) could be various species and the marine environment banded.- Many individuals could not be‘ caught with of the island’ have been treated elsewhere a hand net, and the alternative method, of catching (Ashmole and Ashmole 1967). The present incubating birds at night using a headlamp, was employed only when it was particularly important to paper gives results of work on the White or recapture a previously banded , since it can result Gygis a&a, whose breeding and in the accidental loss of the egg as the adult leaves molt cycles proved, like those of Stermz fus- the nest in a hurry. On the other hand, every bird banded provided valuable information if it was re- cab, to be of special interest. captured, and no time was wasted in catching banded birds of unknown breeding history. In this paper the term sexual cycle is used to indicate the whole series of events from the laying of the first On the routine visits to sites in the study area all (or only) egg by the bird or its mate in one breeding chicks found were measured (wing length and ex- period until the laying of the first egg in the next posed cuhnen length) and weighed- when they were breeding period. Stonehouse ( 1962a) reasonably con- first seen, and were also banded. Chicks whose date sidered the sexual cycle to run from the beginning of hatching was known ( & one day) were measured of courtship in one breeding cycle to the same point and weighed whenever they were visited. These in the next. I have used the laying of the first egg measurements and weights were plotted against age only because it is a definite occurrence that is easier in to produce graphs that were used in estimat- to record. The breeding period (of an individual) is ing the hatching dates of chicks whose ages were not considered as the time period during which an indi- known precisely. From these data, approximate lay- vidual is involved more or less continuously in breed- ing dates were calculated by assuming an incubation ing activities, without a pause for a complete post- period of 36 days. This estimate is based on the breeding molt (= postnuptial or prebasic molt-see experience of Dorward ( 1963) on , Amadon 1966). supported by personal observations. Because of the Gygk was studied mainly on Cook Island, an islet long incubation period there was little chance of fail- about one mile long that lies in the center of the ing to record breeding activity at a site, in spite of entrance to the main lagoon of Christmas Island. The the rather long intervals between visits, nrovided that first visit to Cook Island was from 2 to 9 March 1963, the egg survived to hatching. However, some eggs after which there was an interval of seven weeks. must have been laid and lost between visits, and so Subsequently, no interval was longer than five weeks, were not recorded. and many were much shorter. The original plan During the study 387 examinations were made of called for observations to be continued for at least the molt of 235 adult Gygis; 97 birds were examined 13 months, but unfortunately the regular observations more than once, and 29 more than twice. On each had to be terminated on 8 February 1964; however, occasion the condition of each of the primaries and a final three-week visit to Christmas Island in June rectrices was recorded, and at the same time all the 1964 included two weeks on Cook Island. In- all, primaries and rectrices on the left side were given 101 days were scent working on Cook Island. Because a nick with a small-diameter nanernunch near the tin the observations were carried out over a relatively of the outer vane. It was thnspo&ible to determine short period, and were not continuous, the data are at a subsequent examination exactly which incomplete and difficult to analyze. However, the had been replaced in the interval. A rapid check was main features of the breeding and molt regime of this also made for the presence of growing feathers in population of Gygis were established. various parts of the body, and the state of the brood A segment of Cook Island comprising about one patches was recorded. In a sample of the birds, the tenth of its total area was chosen as a study area. secondaries in one wing were also examined.

1351 The Condor, 70:35-55, 1968 36 N. PHILIP ASHMOLE

Although breeding Gygis may be found on Cook Island at all times of vear. individuals that have finished breeding seem -to leave the island imme- diately, at about the same time that they start their molt. They are not seen again until they have almost completed their molt, when they return to start court- ship for their next breeding period. As a result, the details of the middle part of the molt could not be observed directly, but the general plan became clear from records of the start and finish of molt, and of the retention or loss of punched feathers during the period when the birds were absent. In recording the state of the individual flight feathers, the numerical method detailed by Ashmole ( 1962) was utilized (see also table 2). On this system each growing is assigned a score, according to its growth stage, of 1 (empty socket or’ pm feather), 2, 3, or 4. Full-grown new feathers FIGURE 1. Monthly numbers of eggs of Gygis alba score 5, so that in birds in which a molt wave pro- laid in study area on Cook Island (Christmas Island) gresses steadily through a feather series, the position in 1963 and 1964. For explanation see text. of the wave can be recorded simply by scoring 5 for each feather that has already been replaced, and adding the appropriate lower figures for growing feathers. In the case of Gygis and other species in months, the egg was assigned half to one which two or more molt waves are active at the same month and half to the other. The months in time in the same feather series, it is necessary for some purposes to record the positions of the separate which diagonal lines have been added on top waves, while for others it is more useful to consider of the columns are those in which the timing the total effect of the progress in all the waves in a of the visits made it certain that many eggs given time period. Each procedure can easily be laid were not recorded. followed by using the scoring system in an appropriate Figure 1 shows that in the first year during manner. For instance in the present paper the “pri- mary molt score” used to indicate the molt stage which I made regular observations there was reached by an individual is computed by scoring five much more laying in the period April through points for all primaries replaced since the last breed- August than during the rest of the year, but ing period, and adding appropriate scores for all the even the months with least laying (November partly grown feathers present in any of the molt waves. A completed molt scores 100 if both wings 1963 and January 1964) had well over one are considered, or 50 in a single wing. Individual quarter as many layings as occurred in the primaries are referred to by using a letter L or R (left month with greatest activity (April 1963). or right) and a number representing the position of However, in May of 1964 there was a peak of the feather in the primary series: thus “L and R 1” identifies the innermost (proximal) primaries in the laying much higher than any in the previous two wings. year. In conjunction with the observations of Gallagher (1960) the data suggest that BREEDING laying may generally be heaviest during April THE TEMPORAL DISTRIBUTION OF BREEDING through August, but it is clear that a sub- The most striking feature of the breeding of stantial amount of breeding takes place at all Gygis on Christmas Island is that eggs and times of year. chicks can be found at all times of year. SUCCESS OF BREEDING AT DIFFERENT TIMES Figure 1 shows the temporal distribution of laying, each column representing the eggs The available data on the success of breeding laid in one month. The solid black histogram in relation to the time of laying of the egg are includes data on 228 eggs for which the month presented in table 1. However, because of of laying was definitely known or could be the irregularity of my visits to the island, and reliably calculated from measurements of the the different amounts of time spent searching chick. However, an additional 232 eggs for juveniles after they had learned to fly, the known to have been laid were either lost as figures for the different periods are not fully eggs or the chicks disappeared before they comparable; in all cases they are minima. The were measured. The laying dates for these results are presented solely to show that eggs are less precisely known, but have been throughout the period for which I have data, incorporated as the stippled portion of the a fair proportion of the eggs laid produced histogram in figure 1, by assigning them to flying young. the most likely month, on the basis of the On Christmas Island some chicks from nests in small record of visits to the site concerned. When trees flutter from their nest sites when alarmed even before they are six weeks old, and many do so by the possible time of laying of an egg spanned the time they are seven weeks old, when they can 10 or more days of each of two adjacent barely fly. In contrast, on Ascension Island, although BREEDING AND MOLT IN THE 37

TABLE 1. Breeding success of Gygis dba on Christ- high survival to independence, since six of mas Island, 1963. these old chicks caught between the last week of December 1963 and the first week of Febru- Number of chicks known Number to have survived to ary 1964 were found to be strikingly thin and Estimated known Laying number of to have 6 9 12 weak. It seems clear from these records that period eggs laid* hatched week@ weeks weeks there must have been a food shortage in the Dec. 1962- last part of December 1963 and in January Jan. 1963 >5 (5) ’ (4) (3) (3P 1964, but it cannot have been severe since Feb.-Mar. young chicks were not noticeably affected. 1963 >23 15 11 1 0 It may well be that chicks much more than Apr.-May 12 weeks old would normally have started 1963 79 35 17 8 3 fishing for themselves, but that under slightly Jun.-Jul. abnormal conditions the transition to indepen- 78% 37 20 18 12” 1963 dent life-and perhaps the time of departure Aug.-Sept. from the island-was delayed. It is of interest 1963 66% 28 22 14 7” that three birds caught when between 16 and Oct.-Nov. 19 weeks old and obviously much too weak to 1963 31 11 (8) (5) ’ (I) for themselves were nevertheless stronger a Data from figure 1. b Chicks generally become able to fly when between six and (and in at least one case heavier) a few days seven weeks old. After this they cannot always be found at later, evidently having been fed in the in- their nest sites, even if alive. c Data for chicks from eggs laid in December 196~January terval, although they were so old. The food 1963 are placed in parentheses because observations started situation clearly improved in the first week of only in March 1963, and those for October-November 1963 because the last regular visit finished on 8 February 1964. February 1964, since many large regurgita- d Two of these birds were weak when last seen, apparently tions (of small squid) were obtained from from lack of food. e Three of these birds were weak when last seen. roosting Gyg& at this time (Ashmole and r One of these birds was weak when last seen. Ashmole 1967).

SEXUAL CYCLES OF INDIVIDUAL BIRDS the wings of the chicks grow at about the same rate, the chicks mostly begin to fly-from ledges on steep On Ascension Island Dorward (1963) found cliffs-only when they are between 60 and 75 days that almost all egg-laying by Gygis occurred old ( Dorward 1963). On Christmas Island (and in the period November through March, many other Pacific Islands) the nests of this species are on blocks or bushes close to the ground, and although the length of the sexual cycles of it is generally possible for the chicks to return to their individual pairs varied from 8 to 14 months, nest sites-where they are exclusively fed-even if and most of the cycles were of 11 or 12 they cannot fly. The new information from Christmas months. (However, Dorward assumed that Island thus supports the suggestion of Dorward and Ashmole (1963) that young of spp. and of eggs laid in precisely the same site in two Gygis that are not old enough to be able to fly successive seasons belonged to the same pair. properly are more ready to leave their nest sites to On Christmas Island, where good potential avoid potential predators in colonies where the nests sites were scarcer, a number of especially are close to alternative perching sites than they are in those that are in precipitous places. attractive sites were used by more than one Smith (1966) showed experimentally that chicks pair.) On Christmas Island, where laying of Lams gluucoides, L. hypmboreus, and L. argen- occurred in all months, an attempt was made tatus, tested on cliff ledges when 8-9 or 13-14 days to determine the relation between the length old, were much more likely to jump from the ledges when alarmed if they had been raised in nests on the of the sexual cycle and the success or lack of ground than if they had been raised on cliff ledges. success in the included breeding period. It is very possible that the observed differences in Because the main study could not be con- behavior of chicks of Gygis in different colonies also tinued for more than 11 months, relatively depend on experience after hatching, rather than on genetic differences. few banded individuals finished a breeding period and the subsequent molt, and returned Between the ages of 7 and 12 weeks the chicks to breed again, during the period of observa- were seen near their nest sites less and less tion. However, some more birds were recap- frequently; several were caught when more tured during the visit in June 1964, and 31 than 12 weeks old, but it is likely that some birds were caught during two, successive leave the island during their fourth month breeding periods. A number of other birds from hatching. Young from eggs laid in the were recaptured when in the final stages of two periods June-July and August-September the molt following the breeding period in lQ63 were seen in relatively large numbers which they were banded, but had not started when more than 12 weeks old (table 1) , but breeding when I left the island. The sexes this may have indicated a low rather than a are externally indistinguishable in Gygis, so I 38 N. PHILIP ASHMOLE have no information on possible differences Since successful breeding can take place at in the relations between breeding and molt in any time of year, one might expect successful males and females. However, pair-bonds nor- birds to start breeding about a month earlier mally persist from one breeding period to the each year. However, in about half of the next, so that the length of the sexual cycle is breeding attempts the egg is lost or the chick the same in the two members of each pair. disappears while very young, and the adults The data on the sexual cycles of individuals generally lay a replacement egg. Thus a bird are not given in full because of their com- that is successful at its second attempt in a plexity, but are considered to justify the fol- given breeding period will not be ready to lowing general statements, which are accom- breed again until about a year after its first panied by specific examples. attempt. The rearing of a chick occupies about five Some of the birds that are unsuccessful in months, not counting the preliminaries to a given breeding period are finished with laying but including just over one month for breeding activities sooner than successful incubation and about four months during birds. After spending the same time over which the chick is dependent. The latter molt as the successful birds, these individuals estimate is based on one normal chick that return to breed again after about 8 to 10 was seen to be fed when just over four months months. old, plus the three chicks mentioned in the An example of a short cycle of this kind is provided last section that were evidently fed-during bv a bird that was banded when incubating on 10 a period of food shortage-when more than August 1963, the egg having been laid during July or four months old. However, it is possible that early August. By 18 August there was only an empty chicks sometimes become independent when shell below the nest. The adult was next seen on a new-hatched chick on 2 June 1964, indicating laying only about three months old (cf. Dorward about 27 April. The interval between layings was 1963). thus about 8% to 9% months. Another example is Molt occupies almost the entire period be- that of a pair that was banded while incubating an tween successive breeding periods, and lasts egg laid between 6 April and 3 May 1963. By 18 June the egg had gone; and there was no chick. The about 5% to 7 months. For a few weeks at next eaa was laid about 24 December. 8 or 8% the beginning molt may overlap with the end months--after the previous one. Both adults were of the period of dependence of the chick, caught during the first 10 days of incubation, and while molt is generally completed during the had completed their molt. As in the previous example, it is possible that in the first breeding period an egg courtship period shortly before the laying of was laid and lost before the one I saw, but even in the egg. (Molt and its relations with breeding this case the overall sexual cycle would have been are fully discussed later.) much less than a year in length. Another interesting As might be expected from the above, no pair hatched a chick about l-June 1963, but it died shortlv before 3 Tub. No egg had been laid bv this sexual cycle in which a chick was raised pair by the time “of *my dep&re from the island on (which will be referred to as a “successful” 8 February 1964, but both birds were roosting by the cycle) is known to have been completed in nest site, with their molt virtually completed, and less than 10% months. an egg may well have been laid during late February. This would have been about 10 months after the An example of a successful cycle is provided by a bird previous laying. that was banded on 10 August 1963 when incubating The cycles cited above are among the shorter an egg subsequently calculated to have been laid about 19 July. The chick was last seen on 17 Novem- ones recorded for both successful and unsuc- ber, when it was about 12 weeks old. The adult was cessful breeders. There were a number of recaptured on the same day and found not to have cases in which successful breeders appeared started the molt of its flight feathers. On 14 June to have sexual cycles longer than one year, or I964 it was caught again, incubating an egg laid since 2 June. This bird had completed a successful in which unsuccessful breeders were found on cycle of breeding and molt in just under 11 months. eggs laid 11 or 12 months after the previous Similarlv. a uair in which both adults were banded laying. It is probable that in some of these hatchedan’ egg on 6 March 1963, the third day of cases the first egg laid in the second breeding my first visit to the island. The chick was well and could fly on 3 May, when it was 58 days old, and period was never seen, and a replacement egg probably survived to independence. On 31 December was the one recorded. I.963 one of the adults was found at the same site incubating an egg that must have been laid in the An extreme case that will serve to illustrate this previous -WO weeks. Unfortunately the egg fell off possibility is of a bird caught on an egg on 1 May the site on 20 Tanuarv, nrobablv dislodged by the i963, but whose egg was broken by 3 May, no re- other member of-the pair as I tried-unsuccessfully- ulacement being seen. On 6 February 1964, two days to catch it. A replacement egg was laid in the first before I left the island for nearly four months, the week of February, and the second adult was caught bird was found incubating an egg, laid about nine incubating. This pair thus had an almost certainly months after the previous one. But on 5 June 1964 successful sexual cycle that lasted 10% to 11 months. the same bird was found incubating again, without BREEDING AND MOLT IN THE WHITE TERN 39 having molted any flight feathers in the interval. If Stresemann and Stresemann 1966). Further- I had left Cook Island two days earlier in February, more, Stresemann has pointed out that in the this bird would have been recorded, with misgivings, (Sterna albifmm) three genera- as having an unsuccessful sexual cycle lasting 13 months. In fact, the cycle was much less than a tions of feathers are present in the wings of year, and the June I964 egg was probably the third breeding birds, because a third molt wave laid in that breeding period. starts at about the time that the first wave It is noteworthy that in this bird (and some others) reaches the tip of the wing. Stresemann the interval between the laying of the last observed egg in the first breeding period and the last observed believes that in the White-winged egg in the next was a little more than a year, as a (Chlidonias Ieucoptemcs) all the primaries result of the loss of an egg or eggs early in the second are replaced twice, and the inner ones a third breeding period, followed by the laying of replace- time, before breeding starts. ment eggs and consequent long involvement in breed- Stresemann ( 1965 ) and Stresemann and ing activities. Another example will serve to illustrate how long this involvement may sometimes be. An Stresemann (1966) use the term “die period- adult was banded when incubating an egg that was ische Staffelmauser” to describe the type of laid about 13 Aueust 1963. but in which the chick molt in which one or more new cycles of molt died after pipping- A second egg was present in the of the primaries begin before the preceding site on 3 November, but had gone by 19 November. Although neither parent was caught while incubating one is completed, but in which molt starts this egg, it seems highly likely that one was the again after breeding only with the first pri- banded bird, since it was caught while roosting on mary. They differentiate “die cyclische Staf- I7 November and was found to have fully developed felmauser” ( 1965) or “die kontinuierliche brood oatches. On 20 Tanuarv 1964 it was found on the same site incubating a third egg, laid about 31 Staffelmauser” (1966) as a molt pattern in December, which hatched about 5 February. Thus which there is again a series of successive this bird-and presumably also its unbanded mate- molt waves moving simultaneously out through was involved in breeding activities for nearly six the primaries, but in which the process does months before it finally hatched an egg successfully. Because I left the island soon after the egg hatched, not stop before the breeding period, but I do not know what happened to the chick; however, continues all the time. These terms could be if it was successfully reared, being dependent for rendered “periodic stepwise molt” and “con- about four months, the breeding period of the adult tinual (or cyclic) stepwise molt,” respectively, must have occupied nine to 10 months. The molt program of this bird (864 in table 2) was of special but in the present paper I have generally interest, and is discussed in the section on the relations found it more convenient to employ informal between breeding and molt; however, it may be said descriptions, using the term “molt wave” to here that since molt takes about six months, and indicate a single sequence of molt travelling overlaps only to a small extent with breeding activ- ities. the whole sexual cycle of this individual must along a feather series. have taken much longer than a year, if its chick was One problem of terminology that arises successfully reared. immediately is that Stresemann and Strese- mamr include the boobies (Sulu spp.) in the MOLT group having “continual stepwise molt,” but INTRODUCTION Dorward (1962) has shown that in Sulk dac- In his study on Ascension Island Dorward tylutra there is a tendency for molt to be (1963) discovered that a molting Gygis nor- temporarily arrested during the breeding mally has, at a given time, growing primaries period, continuing afterward from the points at either two or three separate points in each where it stopped. A pause in molt during wing. The present work was planned to breeding probably also occurs in other birds clarify, mainly by the use of punchmarks to in this group, for instance in members of the identify old feathers, some of the problems Phaethon (personal observations). raised in Dorwards’ study. The results con- Thus the Stresemanns ’ “continual stepwise firm that the sequence of molt in the wings molt” is a slightly heterogeneous category. of adult Gygis is unusual in that two or three In some species each molt wave does progress waves of molt start simultaneously after continuously until it reaches the tip of the breeding and progress outward through the wing, but in others each molt wave pauses feather series one behind the other, in the during the breeding period, and resumes its same way as in boobies, SuZu spp. (Dorward progress afterward from the point where it 1962). left off. However, it does seem useful to main- In many other species of a second tain the distinction that the Stresemanns have wave of molt starts from the first primary emphasized between this category and the before the first wave reaches the tenth pri- other. The important consideration is that in mary, so that about half of the primaries are “periodic stepwise molt” all the molt waves replaced twice between successive breeding stop before breeding, and never continue, periods (Stresemann 1963; Ashmole 1963a; since after breeding a new wave starts from 40 N. PHILIP ASHMOLE the first primary and is followed later by one the two wings. For example, in bird 785 or two additional waves, also starting from primary R 6 was the first to be molted, fol- the first primary. In “continual stepwise lowed by L 2, 6, and 9; presumably molt molt,” on the other hand, each molt wave does waves also started soon with primaries R 2 eventually reach the tip of the wing, whether and 9. or not there is a pause in molt for breeding. Dorward (1963) found that molt started Stresemann and Stresemann (KM), on the after breeding (and also finished) at different basis of the information on Gygis published points in different individuals. This finding by Dorward ( 1963 ) , and the examination of is confirmed by the present data. The nine museum specimens, came to the conclusion birds referred to above actually provide ex- “ . . . dass Gygi.s, genau so wie Sterna albifrom amples of molt waves starting after breeding und Chlidmim leucoptera, die Handschwin- with every primary except numbers 1 and 10, gen periodisch in drei Staffeln emeuert.” This whose lack of representation may well be due implies that after breeding molt would start to chance. In fact, a later examination of one only with the first primary, and that the triple- of these birds (859) strongly suggested that wave system would be reestablished only as molt waves did start with the tenth primaries. the first molt wave progressed out through the Similarly, molt waves may stop before breed- primary series and second and third waves ing at different points in the primary series started successively from the first primary. In in different birds. There is a suggestion from fact, however, my field data on the molt of the data that waves may stop most frequently Gygis, based on repeated examination of after the growth of primaries 4, 8, and of marked birds with punched feathers, show course 10. This may imply that they most that after breeding each molt wave starts often start with number 1, 5, and 9. However, again from the point that it had reached at other patterns of molt are also common. the time when breeding started’ and the molt From each of the starting points a molt was inhibited. Gygi.s thus has an interrupted wave progresses outward, eventually reaching “continual stepwise molt” of a kind that has the next more distal starting point, or the not previously been recorded for any species outermost feather (number 10). At this stage of tern. In the Christmas Island population all the feathers have been replaced. The I found that one complete replacement nor- available evidence indicates that each molt mally occurs between successive breeding wave normally stops when it reaches the point periods, and it appears that the unusual where a more distal one started at the begin- sequence of the molt is an adaptation per- ning of the molt. For example, in bird 801 mitting rapid replacement of the feathers with a molt wave was just starting with L 7 on 18 minimal impairment of flying ability. November 1963, while on 6 June 1964 molt It should be mentioned that one other spe- was apparently stopping, and L 6 had just cies of tropical tern, the Black-naped tern completed’ its growth. Furthermore, it seems (Sterna sumatranu), probably has a molt that after breeding each molt wave generally similar to that of Gygi.s (Ashmole unpub- or always starts with the molt of the feather lished) . As in Gygis, growing feathers may be immediately distal to the last one replaced in found at two or three widely separated points that wave before breeding. The most certain in each wing, but without field data it is examples are birds 945 and 508. In the latter difficult to be sure that molt starts after breed- case R 8 was the last primary to be replaced ing at the several points at which it stopped. in two successive molts, and in each it was In the following pages all references to still growing after the laying of the egg. The specific birds, using band numbers, imply that beginning of a third molt was observed, and the available records on the primary molt of as predicted a molt wave started with pri- these individuals may be found in table 2. maries L 9 and then R 9; another wave com- menced with L 5 and R 4, indicating that MOLT OF THE PRIMARIES the asymmetry observed in the previous two On Christmas Island nine Gygis were exam- cycles was being maintained, and would ined when they were just starting a molt after doubtless result in R 8 again being the last a breeding period, and the results show that feather replaced. The history of this bird thus molt starts from several points in each wing, provides good evidence that the pattern of at more or less the same time. Examples are primary molt is normally the same in succes- provided by birds 508 and 785 (table 2). sive cycles, and involves one complete replace- However, it is clear that molt does not usually ment of the feathers. begin at precisely the same date at the dif- Dorward ( 1963), in his work on the Ascen- ferent starting points in a single wing, or in sion Island population, did not find an obvious BREEDING AND MOLT IN THE WHITE TERN 41

TABLE 2. Examples of molt patterns in the primaries of Gygis aZbaon Christmas Island.”

Primary number

Bird Date, breeding status, molt status 1 2 3 4 5 6 7 8 9 10

508 4 Mar. 63, egg, L. molt ending: score 99. R. i 20 Jan. 64, egg, L. N N N N N N N 4 N N molt ending: score 94. R. 4 1 2 Jun. 64, not breeding. L. P P P P 4 P P P 3 P molt starting: score 12. R. 3 2 556 30 Apr. 63, egg, L. no molt. R. * 20 Jan. 64, not breeding. L. N 5 N N 1 N N 2 N molt near end: score 86. R. 4 9 1 3 6 Feb. 64, not breeding. L. P P P P P 2 P P 4 P molt ending( ?) : score 92. R. 2 4 15 Jun. 64, egg, L. P P N P P P P P P N no molt. R. 785 17 Sep. 63, second egg, L. no molt. R. 4 Nov. 63, second egg lost, L. P 1 P P P 1 P P 1 P molt starting: score 5. R. 2 801 9 Aug. 63, egg, L. no molt. R. 18 Nov. 63, not breeding, L. P 5 P P P P 1 P P P molt starting: score 3 or 8. R. 2 6 Jun. 64, not breeding, L. N N N N N 5 N N N 4 molt ending: score 99. R. 816 10 Aug. 63, L. 4 molt ending: score 98. R. 4 2 Jan. 64, L. P P P 1 P P P P /P” P” molt starting: score 2. R. 1 /O 0 856 18 Sept. 63, chick( ?), L. 3 molt ending?: score 98( ?). R. 6 Feb. 64, not breeding, L. N N 3 N N 1 N N N N molt near end: score 96. R. 4 3 4 4 Jun. 64, chick, L. P P P P P N P P N P no molt. R. 859 18 Sep. 63, egg, L. no molt. R. 19 Jan. 64, old chick( ?), L. P P P P P P P P P /P” molt starting: score 1. R. 1 /O 6 Jun. 64, not breeding, L. N 2 N N 4 N N N 2 N molt ending: score 87. R. 3 4 2 864 19 Sep. 63, dead “holed” egg, L. /O no molt. R. /o 17 Nov. 63, 2nd egg lost( ?), L. P P P /P” P P P 4 P P molting. R. 4 18 Jan. 64, egg (prob. 3rd), L. P P P N /P P P N /P” P” no molt. R. N /. N /O 0 0 945 foJzi$4, egg, L. /O 0 R. 10 0 0 1 Jun. 64, not breeding, L. 3 N N 2 N N N 1 N N molt ending: score 84. R. N N 2 N N N 2 N N 4

a Explanation of symbols: L., R., left, right; /, discontinuity between feathers of very different age; N, feather full-grown, but either obviously new or known by the absence of a punch mark to have been molted since previous examination (feathers at stages 1 or 2 could not be punched, and so normally appear as N at the next examination); ., feather of indeterminate age; 0, feather con- spicuously old, but without a punch mark; P, feather shows punch mark made at previous examination, and thus is known not to have been molted in the interval; P”, feather conspicuously old, and has a punch mark; 1, empty socket or pin feather; 2, growing feather with vane up to one-third grown; 3, growing feather with vane between one-third and two-thirds grown; 4, growing feather with vane more than two-thirds grown but not full length; 5, feather full length, but still with blood in calamus. 42 N. PHILIP ASHMOLE relationship between the place where molt hapsL and R 1, may have been replacedtwice within finished before breeding and the place where a singlecYc1e. Dorward ( 1963:372, and personal communication) it started afterward, such as might have been recorded an individual on Ascension Island that had expected from the above. However, this can a chick able to fly in February, and that was starting probably be explained by the frequent lack molt in mid-March, with primaries R 7 and R 10 of complete synchrony between the start (and (and also L 4) at stage 1; in mid-September it was near the end of its molt, with primaries R 7 and finish) of the

- Overal I mean interval 18.5

6 16 20 30 40 Proximal Distal Score of outer molt wave

FIGURE 2. Relative positions of molt waves in wings of Gygis alba in which two or three waves were found in progress at the same time. For explanation see text. Symbols: a used in plotting the relative positions of the two most proximal (or the only two) molt waves in a wing; x used in plotting the relative positions of the two most distal molt waves, when three waves were present; o used in plotting the relative positions of the only two molt waves in wings of two birds in which an intermediate wave had probably just become inactive.

of the series implies that they catch up with RATE OF PRIMARY MOLT each other as they move outward; this is The rate of primary molt is a function of the readily explained by the greater length of the linear growth rate and length of the feathers, outer feathers, which doubtless take longer to and of the number of feathers that are grow- complete their growth. However, there is also ing at any one time. Although there are no a tendency for the successive waves to be very data on the rates of growth of different pri- close together when the score of the outer maries in Gygis, the inner primaries are so one is lower than 30. The four birds respon- much shorter than the outer ones that it seems sible for the six records of closely spaced certain that the former take less time to com- proximal waves (556,856, 859, and 945) were plete their growth. (For a discussion of rates all just completing their molt, suggesting that of growth of different primaries in other late in the molt new waves may start at the species see Ashmole 1962. ) I have only a first primary when the preceding wave has little information on the total time taken to barely reached primary four ( score about 15). replace particular primaries. In one bird This could result in certain inner primaries primary L 3 was molted and the new feather being replaced twice within a single molt, as completed its growth in less than 46 days, already indicated. The absence of such closely while in another bird (864) the much longer spaced’ waves in the middle of the primary feathers L 8 and R 7 molted and reached series must imply that when the next cycle stage 4 in less than 59 days. These and a few of molt starts after breeding, a wave that had other records, together with some information previously reached only the first, second, or on the rate of progress of single waves of third primary may not always become active molt over a long period (e.g., bird 859 in again until some time after the more distal table 2), indicate that each of the innermost waves, or may be abandoned altogether and (shortest) primaries is replaced in little more be overrun by a new wave starting with the than a month, and that the longest ones take first primary. 1% to 2 months. 44 N. PHILIP ASHMOLE

Molting Gygis have a high average number and the data support this expectation. In one of primaries growing at any one time. In most Gygis seen close to the start and to the end of the (and other birds) a single of a primary replacement (bird 859), a score wave of molt travels out along the primary change of 86 was achieved in.?39 days, a series, so that normally one finds growing rate of 0.62 per cent per day. Another bird feathers at only one point in each wing. How- (856) achieved an even higher rate, with a ever, at this point there are often two feathers score change of 90 in 141 days (not counting growing simultaneously, since each primary the completion of growth of the last feather is normally molted well before its proximal in the previous cycle of replacement), a rate neighbor has completed its growth. (There of 0.64 per cent per day. A third individual is much variation in the degree of overlap, probably achieved an equally high rate, since both at different stages in the molt and in it had a score of 94 six months (183 days) different species.) In Gygis the growth of after being caught while incubating. Molt each primary is almost or quite completed probably did not start until some time later. before the adjacent one is molted. Thus on These rates are equal to the highest observed Christmas Island I found only two birds with among A. tenuirostris on Ascension Island, two adjacent feathers in one wing actively and imply that a molt may sometimes be com- growing at the same time (e.g., 508); in two pleted in less than 6 months. However, one other birds (e.g., 556) primaries were virtually other bird ( 801) seen when just starting a full length, but perhaps just still growing, molt had still not quite completed it 6% after the shedding of their distal neighbors. months later, so that it is clear that molt some- However, in this species the rarity with times takes as long as 7 months. which adjacent feathers are growing simul- In this context it should be mentioned that taneously is more than counterbalanced by in one case where both members of a pair the presence of several molt waves, so that were banded, it was found that although both molting birds normally have two or three finished with breeding activities on the same widely spaced growing feathers in each wing. day (when their chick died), one finished its Thus the nine birds examined when their molt several weeks before the other. Clearly, primary molt score was between 77 and 9.1 molt must either have started at different had a mean of 2.39 growing primaries per times in the two birds or have taken longer wing. Near the end of the primary replace- to complete in one than in another. ment the different molt waves naturally do SYMMETRY OF THE MOLT not stop at precisely the same time, so that OF THE PRIMARIES rather fewer feathers are found growing together. The 31 birds examined when their Of 50 individuals in which primaries were primary score was between 92 and 99 had a seen growing and the symmetry of the molt mean of 1.26 growing feathers per wing. in the two wings could be judged, 13 showed A useful comparison may be made with no appreciable asymmetry, in that equivalent Anous tenuirostris, a species that is closely growing feathers in the two wings were given related to Gygis and is similar in size. It the same score of 1, 2, 3, or 4. Twenty-six has only one molt wave in each wing, but others showed minor divergences from com- adjacent feathers are frequently found grow- plete symmetry, ranging from probably merely ing at the same time. On Ascension Island transient ones (e.g., a feather recently shed in A. tenuirostris with primary molt scores be- one wing, but not yet in the other) to score tween 71 and 91 had a mean of I.72 growing differences of 2 or 3 between the wings. The feathers per wing, while beyond a score of remaining 11 birds had more important asym- 91 they averaged only 1.15 feathers per wing metries. (As might be expected, divergences (Ashmole 1962: table 5). I have no data for from symmetry in favor of the left and right the middle of the molt of Gygis, but the wings occurred in roughly equal numbers). scanty records for the early part of the molt Of these 11 birds, eight showed differences of show that it is normal for there to be two or about one feather (a score difference of 5), three growing feathers per wing at this time, two a little less, and one apparently of two whereas in A. tenuirostris there was generally feathers. Among these birds no symmetrical only one. molt waves were seen, and one bird (945) This comparison suggests that the time showed asymmetry at four separate points in needed for replacement of all the primaries the wings at the same time. Several of these should be shorter in Gygis than in A. tenuiros- birds were also examined when breeding, and t&v (assuming that the linear growth rate of showed discontinuities at different positions the feathers is comparable in the two species), in the two wings, indicating that molt had BREEDING AND MOLT IN THE WHITE TERN 45 stopped asymmetrically (e.g., 945). Bird 598, TABLE 3. Relationship of molt of secondaries in already mentioned as an individual that Gygis a.Zbawith breeding and with molt of the pri- maries. showed asymmetry in three successive molts, also demonstrated that molt may start asym- Numbers of birds metrically. On 2 June 1964 the difference Breeding ’ Not breedingb between the two wings was more than one Molt of No molt Molt of No molt feather at the proximal wave-front, but much secondaries in sec- secondaries in sec- less at the distal one. Since the wave starting in moeress ondariesc in moeress ondaries with primary R 4 had five long feathers to Molt of primaries replace, it is clear that R 8 would again be in progress, molted very late, or be retained through a score l-12 0 0 1 1 breeding period. Molt of primaries in progress, MOLT OF THE SECONDARIES score 77-99 0 3 18 3 No molt in Because examination of the secondaries is very primaries time-consuming, details of the state of molt (score 100/O) 1 17 1 2 of the secondaries were obtained at only about a Incubation was in progress, or there was a dependent chick. 56 examinations. These records are sufficient b These birds did not have eggs or chicks, and their brood to show that the sequence of secondary re- patches were not fully naked. c In some cases the secondaries were examined on only one placement in Gygis does not follow the rela- side. tively simple pattern exemplified by Anous tenuiro&+.s (Ashmole 1962). In the latter 1962). In the latter case it was shown that species the proximal feathers are molted first, these middle feathers, which would normally followed closely by the most distal feathers, have been replaced last, were molted either and a wave of molt then progresses from each during breeding or shortly after the start of end of the series toward the middle. The data the next molt. suggest that secondary molt in Gygis also Table 3 gives the available information on generally progresses from both ends of the the timing of secondary molt in relation to series toward the middle; but one frequently the molt of the primaries. Birds that had finds a number of separated feathers growing nearly completed molt of their primaries were at the same time, indicating that the replace- usually also molting secondaries, and birds ment of the secondaries, like that of the pri- that were not molting primaries were gener- maries, involves more than one molt wave ally not molting secondaries either. The data progressing in a given direction simulta- are not sufficient to show whether secondary neously. For example, one bird examined molt occurs mainly near the end of the pri- when its primary molt score was 84 was grow- mary molt, as it does in other terns. ing in the left wing secondaries 3, 6, 13, and 16. Furthermore, among birds whose primary MOLT OF THE RECTRICES molt was at least four-fifths completed, but The molt of the rectrices of Gygis on Christ- still progressing, there were individuals grow- mas Island occurs largely during the period ing each one of the secondaries from number 2 when the primaries are molting, which is through number 17; even the lack of birds generally when the birds are not breeding growing the outermost and innermost second- (see table 4 and later discussion); however, aries could have been due to chance. growing rectrices may occasionally be found Although the data do not permit full anal- at any stage in the sexual cycle. ysis of this complex system of secondary molt, Most of my observations of molting birds it is clear from examinations of wings of were made during the later stages of the breeding birds that all the secondaries are primary replacement (scores between 77 and normally replaced between successive breed- 99). At this time any of the rectrices could ing periods. The one exception involved a be found growing, but the center ones less bird that, while it was incubating, had one frequently and the outer ones more frequently conspicuously old secondary, which had evi- than the rest. My records are as follows (each dently not been replaced between breeding growing rectrix counted separately) : ls’ ( cen- periods. It is of interest that this feather was ter feathers) 6 records; 2s’ 17; 3s’ 11; 4s’ 18; the twelfth secondary (counting from the 5s’ 16; 6s’ 26. This result suggests that a basic most distal feather inwards), since similar sequence of molt in the tail, which might be retention of middle secondaries-most often obvious in young birds undergoing their first 11 and E-was sometimes found in Anous molt, has become largely obscured during the tenuirotiris on Ascension Island (Ashmole lives of the individual birds. A similar sugges- 46 N. PHILIP ASHMOLE

TABLE 4. Molt of primaries and rectrices of GygZs estimated ages of their chicks were 66, 78, 80, &a at different stages of the sexual cycle. Numerals 84, 85, and 127 days. In the last of these in parentheses indicate the numbers of birds in each cases there was evidence that the chick had in which molt of the rectrices was in progress. finally left the nest site and gone to sea within Numbers of birds the previous five days, but the adult was With de- Unknown Not found in the nest-tree at night carrying a fish Incu- P$z;t breeding breed- presumably intended for the departed chick. bating statusa ingb This adult had still not started molt of its Molt of primaries flight feathers or tail, although the primaries in progress, were badly abraded. Of the three birds that score 1-12 0 I(0)’ 3 (0) 4 (2) were molting, one was an exceptional indi- Molt of primaries in progress, vidual that was growing certain feathers both score 77-99 ll(2) 0 6 (3) 26 (23) while incubating and when it had a chick, Molt of primaries while the other two had just started their in progress, score molt. One of them (859) had a primary molt indeterminate 5 (I) 2 (0) 2(I) 0 score of 1 at the time when its chick should No molt in have been about 99 days old (it had last been primaries caught 15 days earlier); the other had a score (score 100/O) 221 (9) 54 (6) 47 (6) 5 (3) of 5 when its chick was 89 days old. Totals 237 57 58 35 Although breeding and molt occurred 8 This category includes birds known to have recently lost separately in a large majority of the birds eggs, but which still had naked incubation patches and may studied, a few were molting some primaries have re-laid, as well as other birds whose breeding status was uncertain. or rectrices, or both, while incubating or b These birds did not have eggs or chicks, and their incuba- tion patches were not fully naked. caring for small chicks (table 4). In this e Chick was 89 days old. respect the Christmas Island population con- trasts with the population of the same species tion was made, with a little more evidence, in on Ascension Island, where Dorward ( 1963 ) the case of Anous tenuirostti on Ascension found no birds molting primaries or rectrices Island. A basic sequence would also imply a while they had eggs or small chicks. basic symmetry, but this is not detectable in Examination of the 25 records of birds that were the majority of the adults. incubating while growing flight feathers ( 13 primaries Rectrices are normally all replaced between only, 9 rectrices only, 3 both) showed that in about successive breeding periods, but I have no I9 of them the observed situation could reasonably be explained in terms of breeding having started evidence as to whether any are replaced twice. shortly before molt was completed, in contrast to the normal situation in which breeding starts RELATIONSHIPS OF BREEDING shortly after the end of the molt. It is of interest ACTIVITIES AND MOLT that two birds (one is 508 in table 2) account for four of the records, each having been found incubat- Individual Gygis on Christmas Island were ing while still growing flight feathers on two separate generally not molting when they were in- occasions, in each case about 10 months apart. This volved in breeding activities (table 4). Thus, finding implies that certain individuals have a per- in 237 examinations of incubating birds, 212 sistent tendency to start breeding before molt is completed. showed no molt in the primaries or tail, while In the other six birds which were growing primaries in 57 examinations of birds that had depen- or rectrices while incubating, it was not clear that dent chicks 48 showed no molt. In contrast, molt was just finishing; in some of them feathers had in 35 checks on birds that were not involved obviously been shed after the laying of the egg, and not all could reasonably be explained as accidental in breeding, 33 showed some molt in the feather losses. Two of these birds are of special primaries or tail. Similarly, most birds had interest, since it was almost certain that each had had few or no growing body feathers while they at least- one earlier egg in the same breeding period, were incubating or had young chicks (see and so had already been involved in breeding for rather a long time. -One of them molted one primary below, and table 5). just before the laying of the replacement egg, and The records of birds examined while they another primary and a rectrix before its chick was had chicks show that a new molt of the flight two months old. The other replaced two primaries in each wing, as if in the start of a normal molt, dur- feathers does not normally start until the ing the incubation of its replacement egg and the chick is three or four months old and nearly early life of the resulting chick. However, molt or quite independent. Of the nine adults appeared to be stopping at the time when the chick examined when they had chicks more than was five weeks old. Although it was not actually seen molting during nine weeks old and well able to fly, six still its breeding period, it is worth considering here bird had complete primaries and rectrices. The 864 (table 2)) already discussed as an example of BREEDING AND MOLT IN THE WHITE TERN 47 an individual that was involved in breeding activities TABLE 5. Body molt of Gygis &a at different stages for nearly six months before it hatched its egg success- of the sexual cycle. fully. When first caught on 19 September 1963, incubating a pipped but dead egg, it had one con- Numbers of birds spicuously old primary in each wing. On 17 Novem- ber, when its second egg had probably just been lost, Incubating With dependent chick it had nearly completed the growth of new feathers Less More replacing the two old ones. These feathers, clearly “m”,4;’ NO Molt of than two than two Not cate- molt in primaries in months months breed- representing the most distal wave-fronts in the wings, gory= pIiIllalieS progress old old ing were probably shed soon after the loss of the first egg. On 18 January 1964 the bird was incubating 1 144 4 34 again, was not molting, but had replaced two more 2 53 8 9 : z primaries, this time in the proximal molt waves. (My 3 6 1 0 0 27 data suggest that, in this species, once a feather has TotalP 203 13 43 10 34 been shed the growth of its successor always continues to completion, even if the bird becomes involved in * Category 1 indicates that no growing feathers, or only one or two, were seen in a rapid check of various parts of the body; breeding early in its growth.- , and further molt is category 2 indicates that growing feathers were seen only in inhibited. ) small numbers, or that they were largely restricted to one part Five additional birds, examined when they had of the body; category 3 indicates the presence of many growing chicks less than two months old. had erowine flight feathers. b1 have no information on the body molt of the 28 birds feathers; three had single growing re&ices, o\e had with known breeding status that are not represented in this no less than four growing rectrices, while the other table but do appear in table 3. had evidently molted one primary in each wing just before its chick hatched, and subsequently shed a rectrix when the chick was about five weeks old. This Similarly, although a large majority of in- last bird was not known to have had and lost another cubating birds were not molting body feathers egg previously, but the possibility cannot be excluded. (and hardly any were in heavy body molt), Thus there is some evidence that in birds lay- those individuals that were molting primaries ing two or three eggs within one breeding while incubating showed a highly significant period (because of the loss of the first ones), tendency also to be involved in body molt. molt may be initiated at the positions of the This is in accord with the evidence discussed wave-fronts at the time, only to stop again as above, that birds involved in a series of breeding activities continue. This could be unsuccessful breeding attempts sometimes the explanation of the curious sequence of molt a few flight feathers during their ex- records from bird 556 (table 2), since the egg tended breeding period, and it suggests a found in June 1964 was almost certainly not temporary relaxation (presumably during the the first laid in that breeding period, and intervals between successive breeding at- although all the primaries had been replaced tempts) of the inhibition of molt activity that by February 1964, and molt was apparently normally operated during a breeding period. stopping, two primaries in the left wing (and In conclusion, it may therefore be said that probably two in the right wing) had been molted again by June. whereas breeding and molt in this population of Gygis are very largely mutually exclusive, Although attention was concentrated mainly on investigation of the molt of the flight they may overlap in three distinct situations. feathers, nearly all the birds handled were First, some birds start breeding (in the sense examined rapidly for growing feathers in the of having an egg) before completion of the main regions of the body; subsequently, each growth of those flight feathers that were she.d record was assigned to one of three body molt last. Second, an unknown proportion of suc- categories representing negligible, light, and cessful breeders start their normal molt some heavy molt. In spite of the subjectivity of this weeks before their chick becomes indepen- method, the results show striking differences dent. Finally, some birds that lose one or in the proportion of birds in each of the three more eggs in a breeding period may undergo categories at different stages in the sexual some molt before finishing their last breeding cycle (table 5). Birds examined when they attempts. When they are not breeding, the were not breeding were nearly all in heavy birds are clearly involved in molt for virtually body molt. Of the 10 birds examined when all the time. They are not seen on the island they had chicks more than two months old, between the very early stages of the molt and nine were involved in body molt. Most birds the time when all or nearly all of the old with chicks less than two months old were flight feathers have been shed, but the growth not molting body feathers, but the nine indi- of the last feathers to be shed is normally viduals that did show some body molt in- completed during the courtship period, when cluded the only two birds that were molting the pair are spending much time together primaries when they had chicks of this age. near the nest site. 48 N. PHILIP ASHMOLE

DISCUSSION longer period than those that lose their eggs, ADAPTATIONS OF THE BREEDING or their chicks when they are small. Thus, AND MOLT CYCLES assuming that the molt takes a roughly con- The outstanding feature of the biology of the stant period, the total time required for a Christmas Island population of Gygis is that successful breeder to complete breeding breeding occurs at all times of the year. The and then molt will be considerably longer fact that in both 1933-59 (Gallagher 1966) than the time required by an unsuccessful and 1963-64 there was a substantial peak in bird (see, for example, Stonehouse 19621,). laying in the northern summer cannot be Since, as already mentioned, nearly all bird interpreted without further data. It is pos- species have evolved cycles in which success- sible, for instance, that Gygis in the Christmas ful individuals can complete their breeding Island population retain a degree of the re- and molt within a year, and so be ready again sponsiveness to environmental proximate fac- at the optimum time in the next season, it tors, which forms part of the adaptation sys- follows that unsuccessful individuals will have tem for the timing of breeding in colonies some “surplus” time. where seasonal changes in the environment This surplus time, inevitably wasted in make it advantageous to breed at a particular annually breeding populations, can be used’ time of year. Alternatively, it may be that in environments that permit the species to peaks of breeding on Christmas Island occur breed at any time of year. In a population at different times in different years, and are colonizing a constant environment from a produced solely by fluctuations in the num- seasonal one, an individual that completes one bers of birds that are finished with molt and unsuccessful breeding attempt and the sub- are ready to breed; these fluctuations could sequent molt in less than a year will be be related to such factors as the success in favored by selection if it starts breeding again breeding in the preceding months and the at once, since it will on the average produce number of young birds settling to breed for more young than birds that do not. Thus in the first time. constant environments one can expect to find Although it is unfortunate that the reasons that birds are no longer dependent on environ- for the observed peaks in laying are not under- mental proximate stimuli to initiate breeding, stood, the facts remain that a substantial pro- but that they are brought back into breeding portion of the population may be found condition as soon as possible by an intrinsic breeding at any time and that individual cyclical tendency, sometimes supplemented by members of the population are not tied to an response to social stimulation. Breeding and annual breeding schedule. These observations molt should alternate with each other con- are critical in that they show that this popula- tinuously, and the molt should be as rapid tion of Gygis is exposed to a type of selection as possible. very different from that operating on annual- However, it must be borne in mind that breeding populations of this or any other it is not necessary or likely that any environ- species. ment has an entirely constant suitability for breeding throughout the year. If one season The vast majority of all birds have evolved in environments in which there are well- is on the average only slightly better for breeding than others, it will still be selectively developed annual cycles that make breeding advantageous for a bird that is ready to breed much more likely to succeed at one season at another time to attempt to ,do so rather than at others. In such environments all but than waiting, if there is a reasonable chance a few birds have evolved sexual cycles that of being successful. For any species in a given last one year, the exceptions being those large environment, the breeding regime that is species in which successful breeding occupies evolved will be determined by the probabilities more than a year. Thus in most bird popula- of successful breeding at different seasonsand tions individuals that attempt to breed at the lengths of the unsuccessful and successful times other than the normal breeding season sexual cycles. It may also be influenced by are subject to strong counter-selection, and the extent to which the species, in other parts those birds are favored that respond promptly of its range, is dependent on social stimulation and accurately to the external stimuli used in in timing its breeding activities. For instance, timing the normal breeding season. the extremely social nature of Sternu fumztu However, in sea birds and other species may be one of the reasons why breeding of with long incubation and fledging periods, this species is closely synchronized even on individuals that raise chicks successfully are Ascension Island and Christmas Island, al- involved in breeding activities for a much though it is not restricted to one particular BREEDING AND MOLT IN THE WHITE TERN 49 season. Since species living together in a favor of making repeated attempts to breed, given environment exploit it in different ways, if the first is unsuccessful, before abandoning it is not surprising to find that in certain the chance of successful breeding in that environments where seasonal influences are breeding period and starting postbreeding slight, some species have retained annual molt. breeding while in others nonannual regimes Thus the record of a Gygis on Christmas have been evolved. The sea birds of Ascen- Island that was incubating an egg in early sion Island provide one good example (see February and another in early June of the papers in Ibis, 103b, 1962-63), while on same year, without having undergone an Christmas Island dramatic contrasts are found intervening molt, is not unexpected, in spite even within the terns. Anous tenuirostris and of the fact that if it raised a chick from the Procelsternu cerulea maintain annual breed- last egg its sexual cycle would have lasted ing schedules, Sterna fuscata breed at six- or longer than a year. Another record of a bird 12-month intervals according to their breeding that had an equally long (4% month) interval success (Ashmole lQ65), and Gygis show between the laying of its first and last egg, great variety in the length of their sexual but which did molt a few flight feathers dur- cycles. ing this .period, has already been detailed. Since Gygi.s breed on Christmas Island at In an environment that shows strong sea- all times of year, and individuals can com- sonal variation in the availability of food, no plete unsuccessful-and sometimes successful bird can afford to spend so long in late at- -cycles in less than a year, we may assume tempts to breed in one season that it is not that the observed sexual cycles have been ready to breed at the optimum time in the subject to selection of the kind discussed next year. But in Gygis on Christmas Island, above, so that molt should be as rapid as which has a good chance of breeding success- possible, and there should be no “wasted” fully in any month, it may be that the only time. In fact, as already shown, birds in this factor limiting the time that may be spent in population spend virtually all their time either breeding attempts in one breeding period is breeding or molting, and there is sometimes the need to replace the before it a little overlap between the two. No data are becomes grossly inefficient. Possibly there is available on the length of time occupied by also a limit to the time for which the gonads the molt in annual-breeding populations of can remain active, but present evidence sug- Gygis, but this might be expected to be as gests that this factor is readily modified by long or longer than on Christmas Island, and selection (e.g., Miller 1959); indeed, the ex- might also show less tendency to overlap with ample, just mentioned, of a bird whose last the earliest and latest stages of breeding activ- (probably third) egg in one breeding’ period ity. On the other hand, the length of time was laid four and a half months after the first for which birds are involved in breeding is impressive evidence of such modification, activities need not be shortened by the type when it is compared with the situation found of selection operating on Christmas Island. in most tern populations. In successful breeders the length of this period It may thus be concluded that the environ- is determined mainly by the growth rate of ment of Christmas Island is such that Gygi.s the chick, and there is circumstantial evidence can breed at any time, and that the species that in sea birds that lay a clutch of one egg has evolved a flexible breeding schedule that this has evolved primarily in relation to the virtually eliminates “wasted” time, when the rate at which parents can collect food during bird is not either breeding or undergoing the breeding period (Ashmole lQ63b). For feather replacement at the maximum rate. In birds that lose an egg or small chick one or comparison with other sea birds the most more times during a breeding period, selection conspicuous feature of the ecology of this for the laying of replacement eggs will be population is the frequent completion of critically dependent on the length of the sexual cycles in less than 12 months, thus period suitable for breeding. In most strongly giving those adults successful in one breeding seasonal environments this period will gener- period a chance to raise two chicks in less ally be short, and the laying of replacement than two years. However, the occasional eggs-inevitably much later than the~optimum occurrence of very long sexual cycles, in time, if the first egg was laid close to it-will which pairs spend more than one year over a be relatively uneconomic since it will rarely breeding period and the subsequent molt, is lead to the successful rearing of a chick. But also dependent on the seasonless environment in environments in which breeding is possible and the flexibility of the breeding regime. at any time of year, there will be selection in The molt sequence shown by Gygi.s appears 50 N. PHILIP ASHMOLE to be an exceptionally efficient one for birds except the part nearest to the shaft, are white. that depend critically throughout the year on In the spread wing viewed from below, the their agility in flight. In most tern species white part of each primary largely obscures two or more adjacent primaries may be found the dark pigment in its proximal neighbor, growing at the same time. Thus the aero- but at the same time is itself physically sup- dynamic characteristics of the wing must be ported by its neighbor, and so does not be- very different when the bird has a complete come abraded quickly. The fact that Gygis set of remiges and when it is at various stages (and Sterna sumutrana) have not evolved of the molt. In Gygis this effect is minimized, these arrangements implies that the trans- since one primary normally completes its lucence (as well as the whiteness), which is growth before the next is shed, and the slot a most conspicuous feature of their plumage, left by the molt of one feather is partly is advantageous to them and outweighs the covered by the adjacent feathers. By having disadvantage of having primaries more subject two or three widely spaced growing feathers to abrasion. The possibility that the advantage in the wing at the same time, molt can be lies in reduced conspicuousness to their prey completed rapidly, but the effective shape of is discussed in another paper (Ashmole and the wing is very similar at all times. Ashmole 1967). It is doubtless significant that Although the present description of the molt Sterna sumatranu, which is the only tern apart of Gygis relates to the Christmas Island pop- from Gygis to have unpigmented primaries ulation, it is known that two or more molt (except in juveniles), is also the only other waves can be fourrd progressing simulta- tern thought to replace its primaries by an neously through the primary series in indi- interrupted “continual stepwise molt” (Ash- viduals from other populations. It has been mole, unpublished). shown that primaries are normally replaced only once between successive breeding periods CONTROL OF MOLT OF THE REMIGES on Christmas Island, but it is possible that The pattern of molt of Gygis brings into focus in populations in which breeding occurs at the largely unsolved problem of how a pro- strictly annual intervals unsuccessful breeders tracted sequential molt of the flight feathers, may continue molt after the first replacement which is of common occurrence among birds, has been completed, until it is time for breed- is controlled physiologically. Although experi- ing. If so, the molt sequence found in this mental work has clarified some aspects of the species would be especially advantageous, endocrine control of molt, most of it has been since it would allow extra replacement of old concerned primarily with demonstrating what outer primaries, which are most subject to substances or procedures can stimulate or abrasion, as well as of inner ones, which inhibit “a molt” in , and has thus been suffer less wear. In contrast, in those Pale- only marginally relevant to the problem of arctic terns in which primary molt continues the control of a complex molt that may last after all the feathers have been replaced once, for more than six months, or almost all the it is only the inner feathers that are replaced time that a bird is not breeding. The present again, and all the outer ones are relatively data on the molt of Gygis do not provide a old when breeding starts. complete solution to this problem, but they The of a different sequence by do indicate some of the facts that satisfactory Gygis could be made especially advantageous theories must explain. Some preliminary alter- by the fact that its feathers are entirely un- native hypotheses have been presented here pigmented. Since feathers with melanin are in the hope that they may help in the planning in general much more resistant to abrasion of future experiments. Only the molt of the than those without, it would be especially flight feathers-and mainly of the primaries- disadvantageous for Gygis to start breeding is considered in this discussion. Once the with old outer primaries. It is worth mention- mechanisms involved in the control of molt ing in this context that many other species of of the primaries are understood, it will prob- terns have evolved pale-colored-but not ably be easy to interpret the molt of the translucent-wings by means of two comple- secondaries. The control of molt of the body mentary mechanisms. First, they have a super- feathers is a rather separate problem, and the ficial “frosting” or “silvering” on the wing present study did not provide much critical feathers, “due to elongated, curved and frilled information about it. barbules on the distal sides of the barbs” The most general fact requiring explanation ( Dwight 1901), which largely obscures the is that the pattern of molt of the remiges in dark pigment below when the feather is new. most species of birds involves a definite Second, the inner webs of the primaries, sequence of molt that is adhered to rather BREEDING AND MOLT IN THE WHITE TERN 51 precisely. Whether the molt lasts for six species in which several waves of molt travel weeks or six months, it is unusual for a feather simultaneously through the feather series, but to be molted out of the normal sequence. For in which the waves start after breeding at instance in the Christmas Island population of different points in different individuals. Two Gygis every molt wave for which adequate examples of such species are Gygi.s and Sula information is available travelled out through dactylatru ( Dorward 1962); in both, molt the primary series in exact sequence from starts after breeding from the points where it proximal to distal feathers. The more prox- stopped at the start of breeding, and not from imal of two adjacent feathers never molted genetically fixed positions. after the more distal, and each feather was The second general hypothesis is that of a invariably nearly or completely grown before gradient and threshold system, in which it is its distal neighbor was shed. assumed that a general molting stimulus in- Two general hypotheses seem possible at creases gradually in intensity, and that each first sight. First, one can suppose that the follicle in a feather series has a slightly differ- physiological state of the bird becomes suit- ent threshold of response, so that an orderly able for molt at a definite time in relation to molt is achieved. It is necessary and reason- breeding activities, that molt starts at certain able to assume that a follicle that has just points in the feather series that are genetically produced a feather is refractory to further determined, and that the sequence of molt stimulation during the rest of that molt, so thereafter is determined by the reactions of that it does not molt again in spite of the the different feather follicles to the general (assumed) steadily increasing molt stimulus. physiological state, and by interactions among This mechanism is a very likely one for the follicles. It is not necessary in this case controlling the molt of the many species in to postulate that the intensity of any systemic which a single molt wave progresses rapidly molt stimulus changes during the course of through a feather series, and in which the the molt. One version of this hypothesis was length of the molt may be measured in weeks proposed by Miller ( 1941) in a paper on the rather than months. However, it seems rather molt centers in the secondaries of the Fal- improbable in species in which molt is almost coniformes. He suggested that given a general continuous between one breeding season and internal stimulation of molt, and a relatively the next that a general molt stimulus should high threshold for response to this stimulation increase in strength throughout this period. in the follicle, the follicles with the best blood Furthermore, this hypothesis appears defi- supply might initially be the only ones to nitely not to be sufficient to explain the molt react. Then, if the shedding of these feathers of species like Gygis, in which molt starts after improved the blood supply to the adjacent breeding with different feathers in different follicles, one would expect to find an orderly individuals, and probably sometimes with dif- molt sequence of the kind that in fact occurs. ferent feathers in a single individual in differ- Another version of the same general hypoth- ent years. Difficulties also arise in applying esis would be that after molt started at it to species (including many terns-Strese- genetically determined points, the growth of mann 1963; Stresemann and Stresemann 1966) these first feathers would stimulate the molt in which a new molt wave starts with the molt of the adjacent ones. Molt would then con- of the innermost primaries before the previous tinue, each growing feather stimulating its molt wave has reached the outermost ones. neighbor, until the end of the feather series Before attempting to explain the observed was reached. To explain the fact that in some features of the molt of Gygis, I shall consider species several adjacent feathers may be briefly the molt of some species of Palearctic growing at the same time, while in others a terns that show interesting differences from feather is molted only as its neighbor com- Gygi.s. Although my most nearly complete pletes its growth, one has only to postulate data are for the Black Tern (Chlidonius minor differences between species in the niger), the molt of the (Sterna stimulus-response mechanism between one hirmdo) and many other species (but not the follicle and its neighbor. However, this hy- , S. paradisaea) is apparently sim- pothesis is less satisfactory when applied to ilar (Stresemann 1963; Stresemann and Strese- feather series in which the molt is irregular, mann 1966; Ashmole, unpublished). The nor- or in which the molt sequence does not cor- mal pattern is for primary molt to start near respond with the linear arrangement of the the end of the breeding period (at least some- feathers. Both these situations arise in the times pausing during southward migration) rectrices of various species. Furthermore, this and to proceed continuously until the start of type of hypothesis cannot easily be applied to the northward migration in the following 52 N. PHILIP ASHMOLE spring. A molt wave starts with the innermost refractory period, during which they do not primaries and progresses outward until it initiate another molt wave, even though the reaches the outermost ones. But shortly before general physiological state of the bird permits the first molt wave reaches the outermost the first wave to continue its progress out primaries, a new wave starts with a second through the primary series. The length of this replacement of the innermost feathers. This refractory period, and the rate of progress of wave progresses usually as far as the fourth, the first molt wave, will determine the extent fifth, or sixth primary (sometimes replacing of overlap between the two successive molt one more primary in one wing than another) waves in the primaries. This postulate also before it stops at about the time of the north- provides an explanation of the sequence of ward migration. Breeding birds thus have a molt in juvenile Palearctic terns; it is known sharp discontinuity at some point in the pri- for a number of species that the second com- mary series, with new feathers proximal to it plete replacement of the primaries of young and older ones distal to it. After breeding, birds, starting with the innermost feathers, is molt starts again with the innermost primary, initiated before the first cycle of replacement not at the discontinuity. The outer primaries has been completed by the molt of the outer- are therefore replaced once each year, but most ones ( Stresemann 1963; Stresemann and the inner ones twice. Stresemann 1966; Ashmole, unpublished). If It seems useful to present a preliminary the initiation of the first molt with the shed- hypothesis as to the kind of mechanism con- ding of the innermost primary is controlled by trolling this molt sequence in Palearctic terns, an age-dependent change in the general hor- and to suggest a way in which the mechanism monal balance in the young bird, and sub- could have been modified during evolution to sequent progress of the molt wave is at least give rise to the molt pattern found in Gygis. partly locally controlled, the start of the next First, it must be emphasized that in most molt wave (and of subsequent ones) can be species of Palearctic terns, as in Gygis, molt explained as depending solely on the comple- of the primaries is continuous except when tion of the refractory period of the follicle of the birds are breeding or migrating. This the innermost primary. Each molt wave will implies that the normal physiological state of then continue its progress out through the the adult bird is one that permits molt of the primary series, and be regularly succeeded by flight feathers, molt being inhibited only new waves, until a general inhibition of molt under certain specific circumstances. In most takes place, as in breeding. tern species the postbreeding molt starts with Although the ontogeny of the molt pattern the shedding of the innermost primaries, even of Gygis is not yet known, Dorward (1962) though these are not the oldest primaries has given an account of molt in young S&z present. It therefore appears that there is a ductyiiztm, another (unrelated) species in genetically determined tendency for molt of which adults have two or three simultaneous the primaries to start with the innermost waves of molt in the primaries. In this species feathers. This might be mediated by their the juvenile primaries are replaced by a wave having an especially low threshold to stimula- of molt progressing from the innermost pri- tion, so that as the hormonal inhibition of molt maries outward, but another wave is initiated that is generally associated with breeding with the innermost feathers when the first has gradually dissipated, they would be the first reached primary 6 or 7; from that time onward to respond. After the molt of the innermost new waves start regularly at the innermost feathers, molt progresses outward in a single primary, so that for the rest of their lives the wave, although some outer primaries are older birds have several molt waves in each wing, than the inner ones and there is an age dis- though these are generally inactive when the continuity in the middle of the series. If it is birds are breeding (Dorward 1962). It seems assumed that an active follicle provides a extremely likely that the ontogeny of the molt stimulus for the onset of activity in its distal pattern in Gygis is similar to that in Sulk neighbor, the precision of the progress of molt ductylutra, and thus essentially the same as in out through the heterogeneous feather series other juvenile terns. In this case there is no can be explained by its being under local need to postulate a different physiological rather than systemic control. control mechanism. To account for the fact that a second cycle The critical difference between adult Gygis of primary replacement starts in most tern and S. dactylutra on the one hand and adult species before the first one is completed, one Palearctic terns on the other is that after may postulate that the innermost primaries breeding’ is finished molt in the former species (and presumably also the others) have a continues from the several points at which it BREEDING AND MOLT IN THE WHITE TERN 53 stopped, while in the latter group it starts ally retained through the breeding period. again only from the innermost primaries. A They are then replaced early in the next molt. possible explanation of this is that a modifica- If the control system had involved fixed tion of the normal control mechanism has been thresholds and a graduated molt stimulus, evolved, such that in adult Gygis (and S. or if the molt of each feather (except those dactylatru) a feather follicle that has just pro- with which molt commences) was controlled duced a new feather has a very high threshold by stimuli from molting neighbors, one would to stimulation, but that this threshold declines have expected the retained feathers to be steadily with time, until eventually molt will replaced late in the next molt, rather than as occur even without stimulation by a molting it started. However, an experimental ap- neighbor. Thus when breeding stops, and the proach to the problem is clearly desirable. general hormonal balance of the bird again Although this is not the place for a review permits molt, the several oldest feathers in of the extensive data on the hormonal control each wing will be molted first, irrespective of of molts (Assenmacher 1958; Wagner 1962; their positions. This will, of course, result in Stresemann and Stresemann Elf%), it seems molt starting from all the discontinuities at relevant to mention that it cannot be con- which it stopped before breeding, and not sidered established that cyclical changes in necessarily with the innermost primary, unless thyroxine levels provide the main control of it happens to be one of the oldest primaries natural molt. Juhn (1963) argues that there left in the wing. is little evidence that under natural conditions This hypothesis leads to the view that in the thyroid shows special activity at the time Gygis and Sulk dactylatra-and perhaps also of initiation of the molt. Furthermore, she in some other birds-the molt should be points out that growing feathers, which in the considered not so much as a precisely pro- show a clear structural response to thy- grammed discrete event starting after breed- roxine administration at a level far below that ing, but as a continuous process initiated by stimulating molt, do not show these modifica- the shedding of the juvenile first primaries and tions when grown during the normal molt progressing in a single sequence throughout period. Juhn also investigated the mechanism the life of the bird, interrupted only by the of progesterone-induced molt in capons and inhibition imposed by breeding activities. found that feathers regenerating during treat- This view is in full accord with the observa- ment with progesterone were similar to those tions that a few individual Gygti (e.g., bird grown by untreated birds, but the feathers 8f34 in table 2) molted a few primaries-in grown by birds treated with enough thyroxine the normal sequence-after the failure of one to induce an equivalent amount of molt breeding attempt, but stopped molt again showed the usual structural response to this during another attempt a few weeks later. hormone. The implication is that molt-stim- The implication is merely that the hormonal ulation by progesterone does not act by stim- inhibition of molt was temporarily relaxed ulating thyroid output. Juhn (1963) provi- between breeding attempts, permitting the sionally concluded that “molt is essentially an shedding of the oldest feathers before the autonomous process, the primary seat of the resumption of breeding activities. cyclical renewals being the feather papilla If, in Gygis, the age of a feather is of critical proper.” importance in determining the timing of its Stresemann and Stresemann ( 1966: 14) molt, the period after a follicle has produced came to a similar conclusion. Commenting on a new feather should be viewed as a “prepara- the statement of Rawles (1960:230) that tory” rather than as a “refractory” period, “feather primordia in different positions on stimulation over a considerable period being the body exhibit orderly and characteristic a prerequisite to further response (at normal differences in threshold of reaction to known levels of stimulation). There are some indica- doses of hormones (thyroxine and estrogen),” tions that a “preparatory” process in the they say: “It seems to us that some peculiar- feather follicle may also be important in the ities of the sequence can be explained only by control of molt in certain species besides Gygis another hypothesis. This is that the different (and SuZa dactylatra). For instance, in Anozrs reaction of the feather germs to a known dose tenuirostti on Ascension Island (Ashmole of hormone depends not on the different 1962) it was shown that whereas all second- height of their thresholds but on the fact that aries are normally replaced during the later the feather papillae do not develop their stages of the primary molt, finishing with the sensitivity to this known‘ dose of hormone ’ middle ones shortly before breeding starts, simultaneously, but in a determined sequence some of these middle secondaries are occasion- of a plan.” 54 N. PHILIP ASHMOLE

Wagner ( 1962), on the basis of experi- further field evidence, and also experimental mental work on body molt in passerines, sug- work on a wider range of species than has gests that the sex hormones may have an hitherto been used. important regulating (Zeitgeber) effect in the SUMMARY natural molt cycle through their inhibition of Sexual and molt cycles of the White Tern molt. This suggests that in some other species, Gygis &a on Christmas Island (Pacific as in Gygti, molt may not depend on a special Ocean) were investigated by following the hormonal stimulus; rather, it should be viewed histories of banded birds with individually as a process occurring whenever the bird is marked primaries and rectrices, in a study area in a normal physiological state, provided that in which the events at all nest sites were it is not inhibited by the presence of hormones recorded. related to reproduction or migration, or by Breeding birds are found on the island at certain other circumstances. These latter cir- all times of year-though not always in the cumstances are not well understood, but it is same numbers-and successful breeding ap- possible that the inability of a bird to obtain parently occurs at all seasons.The sexual cycles adequate food acts directly as a proximate of individuals vary widely in length, lasting stimulus resulting in cessation or slowing at least lo?4 months in birds that rear a chick down of molt, or delaying its onset. Probable successfully, but often substantially less in cases of all these phenomena in a population unsuccessful breeders. Within these cycles, of Anous tenuirostriswere described by Ash- molt occurs almost entirely when the birds mole ( 1962). Conversely, a sudden improve- are not breeding, and occupies about 5% to 7 ment in the availability of certain foods may months; during most of this time the birds are stimulate molt. Wagner (1962) records that absent from the island. molt in some caged birds may be evoked at One complete replacement of the primaries unusual times by generous feeding with meal- and rectrices normally occurs between succes- worms or fresh ant eggs. Effects of nutrition sive breeding periods. The primaries are re- on molt presumably operate through changes placed by a series of simultaneous molt waves, in metabolic activity; however, the nature of each progressing steadily outward and sep- the changes and the role of the thyroid in arated by about four feathers from the adja- regulating them are not yet understood. In cent waves. Thus, although several feathers addition to the proximate effects of food grow simultaneously in each wing, there is supply on molt, the cycle of food availability minimal variation in aerodynamic character- in the environment is doubtless a major ulti- istics. mate cause of the type of molt cycle that is Gygis on Christmas Island are considered evolved in a bird population. to have adapted to an environment in which In birds in which molt can occur without seasonal changes are slight by evolving the a special internal stimulus, there must be a ability to start a new breeding period when- mechanism to ensure that it follows a definite ever their molt is completed. They also some- program and that feathers are not replaced times continue breeding efforts (i.e., lay re- unnecessarily often. As discussed above, the placement eggs) over an unusually long evidence suggests that in Gygti and certain period if the first attempt is unsuccessful. other species this mechanism involves time- Data on the unusual sequence of molt in dependent processes in the feather follicles, Gygis, and on the molt patterns of some such that after a follicle has produced a new Palearctic terns, are used in considering the feather it will not again become active until type of mechanism involved in the control of it has been exposed for a considerable time complex and lengthy natural molts. In Gygis to a physiological climate permitting molt. A and some other species an extended period mechanism of this kind could be sufficient to of exposure of the follicle to a physiological prevent further molt in the fall after the com- climate permitting molt may be a prerequisite plete postbreeding molt that occurs in most for the molt of each feather, so that when birds. molt starts after a pause, the oldest feathers In conclusion it is useful to emphasize the are shed first. It seems possible that in some need, when attempting to determine the bird species there is no special internal stimu- physiological control of molt, to remember lus for molt, but that old feathers are replaced that the evolution of different molt regimes whenever molt is not inhibited by hormonal in different bird species has necessarily been or other factors. accompanied by divergent adaptations of the control mechanisms. Full understanding of ACKNOWLEDGMENTS natural molt will therefore have to await This work was undertaken while the author BREEDING AND MOLT IN THE WHITE TERN 55 was the holder of a Yale University/Bishop Mary Juhn and Douglas F. Dorward kindly Museum (Hawaii) Fellowship. Grateful ac- read drafts of the manuscript, while Dr. Dor- knowledgment is made to H. Laurence Achil- ward also provided some unpublished in- les, S. Dillon Ripley, and Roland W. Force, formation from his study of Gygi.s on Ascen- who made this arrangement possible, and to sion Island. It is a pleasure also to thank the Royal Air Force and the members of the Charles G. Sibley and my wife, with whom R. A. F. Officers ’ Mess, Christmas Island, for I have had helpful discussions on several assistance and hospitality. aspects of the study.

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