Sensory control of clutch size in the Common SwiftApus apusSACHA HAYWOOD*†
Department of Zoology, Edward Grey Institute of Field Ornithology, Oxford, UK
Clutch size varies among individuals in most bird species. A widespread assumption isthat such variation results from variable timing in the disruption of ovarian folliculargrowth that brings, with a few days’ lag, egg-laying to an end. Currently, there is empiri-cal evidence that this is the case in Blue Tits Cyanistes caeruleus but not in Zebra FinchesTaeniopygia guttata, in which the timing of follicular disruption has been shown to beinvariant. Here, I investigate clutch size regulation of Common Swifts Apus apus. Usingexperimental egg removal, I show that, assuming the female gets enough egg contact,the determination of clutch size occurs at noon solar time on the day the first egg of aclutch is laid. In spite of individual variation in clutch size, there was no hint of any vari-ability in the timing of clutch-size determination. In this species therefore, the timing ofthe signal disrupting follicular growth appears invariant. The physiological mechanismthat controls clutch size is discussed, including the existence of an endogenous circadianclock and potential zeitgeber, the developmental range of clutch size for the species, thesensory nature of the input that triggers follicular disruption, and the stress of layingextra eggs.
Keywords: circadian clock, follicular disruption, solar time, tactile stimulus, ultraviolet light.
In most bird species, clutch size varies between aswell as within individuals. Physiological mecha-nisms underlying such variation remain controver-sial. There is strong evidence that Zebra FinchesTaeniopygia guttata release a signal 6 h after dawnon the third day of egg-laying to disrupt ovarianfollicular growth, regardless of the final clutch size(Haywood 1993a). However, an explanation ofclutch-size control in which the timing of thissignal is described as invariant has failed to winuniversal approval (Challenger et al. 2001, Wagner& Williams 2007, Williams 2012). There is a gen-erally held assumption that birds in general exhibitvariable timing of follicular disruption, despite anabsence of empirical data (Beukeboom et al. 1988,Meijer et al. 1990, Meijer 1995, Sockman et al.2000, 2006, Williams 2012).
The only species for which the existence of avariable timing has been established experimen-
tally is the Blue Tit Cyanistes caeruleus (Hay-wood 1993b). However, Blue Tits should beconsidered a special case. The rapid-growth phaseof yolk deposition, which conditions the scopefor clutch-size variation under invariant timing, isso short in Blue Tits (3 days, the shortest of anyknown bird species) and individual clutch-sizevariation so large (7–13 eggs, among the largestof any bird species) that the timing of folliculardisruption is bound to vary (Haywood 2007, inpress).
One of the key arguments advanced in sup-port of the assumption that most birds have avariable timing of follicular disruption is that thealternative mechanism could not account for therange of clutch size, from one to nine eggs,observed in the Zebra Finch (Williams 2012).Invariance in the release of a signal dedicated tothe disruption of follicular growth limits clutchsize to four-egg, five-egg and six-egg clutches inZebra Finches. That range, dubbed the develop-mental range of clutch size (Haywood 2007, inpress), represents 90% of all clutches laid in this
†Present address: 6 rue Christiani, 75018 Paris, France.
species (Haywood 1993a). Other clutches, thosethat deviate from the developmental range, maybe categorized as deficiency-carrying clutches(e.g. calcium supply is known to alleviate layingof such clutches; Haywood 1993a, Reynolds &Perrins 2010) or as ill-determined clutches, asthe input of sensory origin (contact with eggs inthe nest) is not always effective in controllingclutch size within the pre-programmed time-frame (Haywood 1993a). It is therefore possibleto explain the full range of clutch size laid byZebra Finches under the model of an invarianttiming.
To widen the basis of support for the invari-ance in timing of follicular disruption as a mecha-nism controlling clutch size in birds, there is needto investigate additional species. In the presentpaper, I document the sensory control of clutchsize in the Common Swift Apus apus through aseries of egg removal experiments. CommonSwifts represent a good model species for thistype of study because: (1) preliminary work hasestablished that females respond to experimentalegg removal by laying extra eggs; (2) egg manipu-lation has, at least as measured by the rate ofnest desertion, negligible impact on the nestingbirds; and (3) close monitoring of nestboxes canprovide useful information on behaviours at thenest throughout the egg-laying period and, inparticular, around the time of clutch-size determi-nation.
METHODS
From 1993 to 1995, I studied a colony of Com-mon Swifts breeding in the tower of the Museumof Natural History in Oxford. The colony hasbeen studied since 1948, when the ventilatorshafts of the tower were fitted with nesting boxes(Lack & Lack 1951). About 50 pairs of CommonSwifts were nesting in the tower at the time ofmy study.
Data collection and solar time
Nestboxes are spread over five different levels ofthe University Museum tower. Those at the fourhighest levels are equipped with a small windowand black curtain at the opposite end to the birds’entrance so that, when the curtain is lifted, behav-iour can be observed. Most of the Swifts in thetower showed little or no fear of observers. All my
observations involved a visit to the nest, usuallylasting a few seconds, performed through the rearwindow. Longer inspection visits (lasting a fewminutes or more) were carried out: (1) to weigh,measure and mark freshly laid eggs, an operationonly performed when parents were away from thebox or (2) to ascertain, through the rear window,when exactly the birds interrupted contact witheggs.
Nestboxes were inspected at least once a daythroughout the pre-laying, laying and early incu-bating periods. At each visit, I recorded the date,time, number of birds present in the nestbox andsitting on the nest and, whenever possible, thenumber of eggs in the nest (or outside it) beforeand after my visit and egg measurements. Eggtemperature (cold, slightly warm, warm) was alsorecorded during the egg-laying period, simply bytouch, to confirm behavioural observations indicat-ing whether adult Swifts seen on the nest had egg-to-skin contact or not. To minimize disturbanceand avoid as much as possible altering the amountof contact birds had with their eggs, no attemptwas made to open the box while birds were pres-ent. During incubation, I sometimes gently pushedaside the sitting bird to check the number of eggsin the nest.
To take into account seasonal changes in photo-period, I used solar time, that is, the time deter-mined from the actual position of the sun in thesky. Hence, solar noon (12:00 h) is the time whenthe sun is at its highest point in the sky. Solar time(tsol) was obtained from:
tsol ¼ tstd þ4� ðLstd � LlocÞ þ Et
60ð1Þ
where tstd is the local standard time (in hours) (forthe UK, clock time calibrated on Greenwich MeanTime (GMT) or clock time minus 1 h, due to Brit-ish Summer Time (BST)), Lstd is the standardmeridian for local time zone (in °W) (for the UK,the standard meridian is 0°W), Lloc the longitudeof the location (in °W) and Et is the Equation ofTime. Et represents the difference between truesolar time and mean solar time (as measured byclock time) in minutes. The equation corrects forthe eccentricity of the Earth’s orbit and the Earth’saxial tilt and was calculated according to the equa-tion from Duffie and Beckman (1980) as cited byRabl (1985) as
in degrees and D is the number of days since thebeginning of the year.
Experimental design
Eggs were removed continuously for 1 (Experi-ment 1) to 6 days (Experiment 6) starting on theday the first egg of a clutch was laid. Eggremoval was always carried out so as to leave thenest empty. The aim of each experiment was toreduce as much as possible, for periods lasting1–6 days, the contact of the female with hereggs. However, to minimize disturbance, each eggwas removed when parents were away from thenestbox, which means that they had someamount of egg contact each time an egg was laid.Because the proportion of three-egg clutchesdeclines with the season (Lack & Lack 1951,Lack 1956a), nests of early and late breederswere randomly assigned to the experimental orun-manipulated categories. Replacement clutcheswere treated in the same fashion as first clutches.After each manipulation, a full clutch of eithertwo or three eggs was given back to the parents,who usually sat on it at once.
It is popularly believed that nesting CommonSwifts are especially prone to desertion, perhapsbecause David Lack reported that adults takenout of the boxes to be ringed usually desert theiryoung (Lack & Lack 1951, Lack 1956b). How-ever, as he also observed, Swifts are remarkablytame and eggs and young can be handled whilethe parents are at the nest without causing deser-tion. To evaluate the desertion rate, some preli-minary egg removal experiments were carried outin 1993 (n = 9 experimental nests). Since noneof the birds whose eggs were removed desertedtheir nest, the bulk of egg manipulations wentahead as planned in 1994 and 1995. Desertioneventually occurred for two of a total of 85experimental nests (a rate of 2.4%). In bothcases, no adult Swifts returned to the box to startincubation after eggs were placed back into thenest.
Estimation of the developmental rangeof clutch size
There is only one method to determine the devel-opmental range of clutch size in birds. It entailscalculation of the developmental maximum(cmax)
cmax ¼ Int�� p
i
�� rmax
�þ Int
� t þ ii
�þ 1 ð4Þ
and minimum (cmin)
cmin ¼ Int�� p
i
�� rmin
�þ Int
� t þ ii
�þ 1 ð5Þ
clutch size, where Int (x) is the integer function, pis the phase (in days) of rapid growth of ovarianfollicles, i is the interval (in days) at which folliclesare recruited into rapid growth, rmax and rmin areratios of the maximum and minimum number,respectively, of pre-ovulatory follicles survivingfollicular disruption to the overall number ofcohorts undergoing rapid growth, and t is the time(in days) of disruption of follicular growth relativeto the time the first egg of a clutch is laid(Haywood 2007).
Two techniques are used to determine the timerequired to form an egg. The first requires count-ing the alternation of day and night deposition inyolk rings and, to date yolk rings, the use of lipo-philic Sudan dye (Warren & Conrad 1939). TheSudan dye treatment was not used for this study,as it would have required the capture of femaleCommon Swifts with subsequent force-feeding ofa dye capsule prior to or during the egg-layingperiod. This was considered too much of a disrup-tion. The follicle rapid-growth phase was thereforeestimated solely from naturally occurring yolk ringsthat can be distinguished by freezing, fixing informalin and staining with a potassium dichromatesolution (Grau 1976, 1984). In the absence of adate marker of yolk growth, the lag time, that is,the time between the end of the rapid-growthphase and oviposition, was not assessed experi-mentally. It was inferred from two other speciesknown to lay eggs on alternate days, the EurasianKestrel Falco tinnunculus (Beukeboom et al. 1988,Meijer et al. 1989) and the Barn Owl Tyto alba(Durant et al. 2004). Both species demonstratethat the mean lag time is equivalent to the meaninterval between successive ovipositions. I there-fore assumed that the lag time of Common Swiftslasts 2 days.
The second method relies upon the frequencydistribution of oviposition intervals. Successiveeggs are laid that belong to the same or differentclutches. When the transition from intra-clutch(shorter) intervals to re-laying (longer) intervalsoccurs, the frequency curve of oviposition intervalsceases to decline and, as the time required to forman egg is reached, begins to rise before starting todecline again. In theory, therefore, the lowestpoint between the two peaks coincides with theshortest re-laying interval, that is, the minimumperiod of egg formation. In this study, ovipositionintervals were calculated (in days) on the basis ofdaily visits to nests that were made mostlybetween 09:00 and 15:00 h local standard time(GMT). I systematically assumed that an egg waslaid in the morning, prior to my visit, unless I hadconclusive evidence that it was laid after my firstvisit the previous day.
Statistical analyses
Single-egg clutches, whether from manipulated orun-manipulated nests, as well as un-manipulatedfour-egg clutches, formed no part of the controland experimental groups as they may be catego-rized as either deficiency-carrying or ill-determinedclutches (see Results). Means are provided withthe standard error of the mean (sem). Statisticalcomparisons of means of clutch sizes or ovipositionintervals were made using Student’s t-test forunmatched pairs (Fowler & Cohen 1995).
RESULTS
Clutch size
Common Swifts nesting at Oxford usually lay two,sometimes three, and exceptionally one or foureggs. The frequency distribution of clutch sizeobserved in 1993–95 (un-manipulated nests: threeone-egg, 46 two-egg, 25 three-egg and two four-egg clutches) is not significantly different from thatrecorded by Lack (1956a) in 1947–55 (unknownnumber of one-egg, 78 two-egg, 54 three-egg andtwo four-egg clutches) mainly from the UniversityMuseum tower in Oxford, with some from twovillages near Oxford (Radley, Sotwell) and one inHertfordshire (Great Offley) (t = 1.139, df = 208,two-tailed P = 0.256).
During the study period, two four-egg clutcheswere laid in un-manipulated nests. In both cases,
the enlarged clutch resulted from the ejectionbehaviour of the parents. The four eggs wereejected from the box, one after the other, usuallywithin a few hours of egg-laying. More broadly,because of this odd but not uncommon behaviour,I cannot rule out that over the 3 years of my studya few eggs escaped detection. Single-egg clutches(un-manipulated: n = 3, experimental: n = 4) areconsidered incomplete (see below).
Occurrence and timing of stimulus
When eggs were removed as laid, starting with thefirst egg of the clutch, clutch size increased to foureggs in a significant proportion of females: 21 of53 that were subjected to egg removal for four tosix consecutive days (a rate of 39.6%). By compar-ison, among un-manipulated clutches (n = 76), asindicated above, only two clutches contained foureggs (a rate of 2.6%). No female subjected to eggremoval for up to three consecutive days laid foureggs.
The experimental increase in clutch sizeinduced by egg removal could be observed inthree-egg clutches as well, despite the fact that itwas not possible to separate individual femalesthat lay one extra egg from those that did not. Fig-ure 1b shows that regardless of the day on whichegg removal started, a significant number offemales laid a three-egg instead of a two-egg clutch(see Table 1 for overall statistical significance).
Experiment 1 showed that removal of eggs aslaid increased clutch size significantly from thefirst day of egg-laying (Table 1). The effect
Table 1. Mean clutch sizes � sem of control and experimentalclutches for Experiments 1–6.
Experiment Mean � sem n t-test (df)One-tailedP-value
measured on day 1 suggests that clutch size isdetermined on that day. To find out preciselywhen this event happens, I examined data fromfemales subjected to egg removal until day 4–6 oflaying. The focus is on females that responded bylaying either four (n = 21) or two eggs (n = 9),not three eggs (n = 23), because only the former
can demonstrate without ambiguity whether extraeggs had been laid or not. As shown in Figure 2,plotting solar time at which the first egg isremoved against final clutch size reveals the exactmoment of disruption of the growth of yolky folli-cles. Thus, in Common Swifts nesting at Oxford,assuming sufficient stimulation from the egg in thenest, the determination of clutch size occurs at12:09 h solar time, or between 11:51 and 12:17 hfor the females that were next-in-line on eitherside of the divide.
At three nests, four eggs were laid in spite ofthe fact that the first egg was experimentallyremoved after 12:09 h solar time (see Fig. 2). Inthese case, and in no others (n = 30), from themoment I arrived in the University Museum towerand until I had the opportunity to remove the eggin the nest, both parents were wrestling to gaincontrol over the nest, presumably competing to bein physical contact with the egg. Both sexes takepart in incubation. It was not possible to ascertain
(a)
(b)
(c)
Figure 1. Proportions of (a) two-egg, (b) three-egg and (c)four-egg clutches laid in response to egg removal. Eggs wereremoved as soon as possible after oviposition, leaving thenest empty. Egg removal took place during the first 1–6 daysof the laying period (Experiments 1–6, respectively).
Figure 2. Timing of determination of clutch size in the Com-mon Swift. Females were subjected to egg removal starting atdifferent times on the day the first egg was laid (day 1) andlasting at least until day 4 of laying (Experiments 4–6).Depending upon the onset time, they responded by layingeither four-egg clutches, i.e. extra eggs, or two-egg clutches,i.e. no extra egg. Three-egg clutches are not shown, as thosethat contain extra eggs and those that do not cannot be distin-guished. Eggs were removed either immediately after thebird(s) left the box (filled circles), in which case the end of thefemale’s contact with eggs is known, or some unknown periodof time after they vacated the box (open circles). Threefemales (crosses) failed to trigger an end to laying on day 1.Behaviour of the pair at the nest suggests that the female wasprevented from getting enough egg contact in time to lay anormal clutch size (see Results). The dotted line indicates thelimit between females that determined clutch size on day 1and those that did not; it stands at 12:09 h solar time.
whether it was the male or the female that was ontop of the egg, since the sexes are not dimorphic.The fact that the event was repeated three timesindependently, each time causing at least one extraegg to be laid, suggests that the male’s urge toincubate prevented the female from obtainingsufficient egg contact.
Under natural conditions, this behavioural quirkis of little consequence because had the first eggnot been removed, the female would havesucceeded, probably by the next morning at thelatest, in gaining enough contact with her egg tolay a normal clutch size.
Oviposition time of the first egg
This study was not designed to investigate oviposi-tion time so as not to increase disturbance; however,data were collected from 31 nests that show that87% of the time the first egg of a clutch was laidbefore 09:30 h local standard time, between 09:31and 10:30 h in 7% of all nests, between 10:31 and11:30 h in 3%, and between 11:31 and 12:55 h in3% of all nests. According to Lack (1956b), first andsubsequent eggs of Common Swifts nesting in theUniversity Museum tower are laid in the morning,between 06:00 and 09:00 h local standard time(07:00 and 10:00 h BST), with a few earlier and avery few later or in the afternoon.
Developmental range of clutch size
To calculate this range in the Common Swift, Iassumed, based on convergent data from otherindeterminate laying species (Gilbert et al. 1983,Haywood 1993a, Challenger et al. 2001), that theratios are 0.5 for rmax (i.e. all existing pre-ovulatoryfollicles survive the follicular disruption) and zerofor rmin (i.e. no pre-ovulatory follicles survive theevent). Every other ovarian parameter is known:t = 0.20 days, i = 2.0 days, estimated from themost common oviposition intervals in controlclutches (i.e. 77%, as opposed to 22% for 3-dayintervals and 1% for 4-day intervals, n = 96), andp = 5.0 days, derived from the time it takes toform an egg. The two methods used to estimatethis period give similar results. Of nine yolks exam-ined, all showed that females lay down betweenfive (n = 2) and six (n = 7) countable ring pairs,suggesting that, including the 48 h required to addalbumen, membranes and shell, Common Swifteggs are formed over 7–8 days. The frequencydistribution method of determining the duration ofegg formation from oviposition intervals (Fig. 3)revealed a first peak at the 2-day interval and asecond one at the 9-day interval and, in between, alow at the 7-day interval. This suggests a minimumperiod of 7 days for egg formation.
Calculation of the developmental minimum andmaximum clutch size gives two and three eggs.
Figure 3. Frequency distribution of oviposition intervals foreggs laid by both control and experimental females in 1993–95 (n = 287). Oviposition intervals within clutches, rangingover 2–6 days (filled bars), are distinguished from those thatseparate consecutive clutches, ranging over 7–15 days (openbars), on the basis of estimates for the time required to forman egg obtained by the method of yolk rings. The low reachedat 7 days corroborates the minimum estimate of the yolk-ringmethod.
Figure 4. Mean oviposition intervals (and sem) of control andexperimental groups for different clutch sizes: (C/2) two-egg and(C/3) three-egg control clutches, and (E/2) two-egg, (E/3) three-egg and (E/4) four-egg experimental clutches. Significant ovipo-sition intervals from two-tailed t-test for unmatched pairs areindicated with asterisks (** P < 0.01; NS, P > 0.05). None ofthe oviposition interval differences within the control or experi-mental groups was significant. For further details, see Results.
The values correspond to the normal functioningof the input-dependent mechanism that controlsclutch size in the Common Swift. This means thata clutch whose size is outside the developmentalrange may be considered deviant. Single-eggclutches may be incomplete due to the fact thatthey are deficiency-carrying clutches (Haywood1993a, Reynolds & Perrins 2010) or simply becauseother laid eggs within the same clutch remainedundetected (e.g. due to egg ejection behaviour)despite frequent visits to the nest. Likewise, four-egg clutches may be described as defective, orrather ill-determined clutches, insofar as the inputthat brings an end to egg-laying fails to act withinthe usual timeframe (see Clutch size).
Stress of laying extra eggs
Common Swift eggs are laid on alternate days.Longer oviposition intervals arise in slightly lessthan a quarter of cases and have been linked toadverse weather conditions (Lack & Lack 1951,Lack 1956a,b). Oviposition intervals might there-fore constitute a measure of the stress of layingextra eggs.
Results of comparisons between control andexperimental groups are shown in Figure 4. Fortwo-egg clutches, mean oviposition intervals of theexperimental group were longer than for thecontrol group, but the difference is not significant(2.471 � 0.151 days, n = 17, vs. 2.239 � 0.071,n = 46, t = 1.563, df = 61, two-tailed P > 0.05).For three-egg clutches, the difference betweenmean oviposition intervals of the experimentalgroup and the control group is positive and signifi-cant (2.705 � 0.118, n = 44, vs. 2.240 � 0.059,n = 25, t = 2.858, df = 67, two-tailed P < 0.01).Finally, the difference between mean ovipositionintervals of four-egg experimental and three-eggcontrol clutches was also positive and significant(2.603 � 0.091, n = 21, vs. 2.240 � 0.059,n = 25, t = 3.461, df = 44, two-tailed P < 0.01).
DISCUSSION
Clutch size and endogenous circadianclock
To my knowledge, this is the first experimentaldemonstration that there exists a brief moment intime, over the period of egg-laying, that is devotedto controlling clutch size in free-living birds.
Evidence gathered from Experiments 4–6 demon-strate that a species-specific timing occurs in theCommon Swift. Assuming the female can musterenough contact with the egg, clutch size is deter-mined at 12:09 h solar time, or between 11:51and 12:17 h for the individuals next-in-line oneither side of the divide, on the day the first egg ofa clutch is laid (Fig. 2). This suggests that thetiming of follicular disruption is tightly controlledby the operation of an internal circadian clock.
In birds, events leading to the disruption offollicular growth and hence to the cessation of egg-laying are still poorly understood. Prolactin, a hor-mone synthesized and released from the anteriorpituitary gland, has long been hypothesized to playa central role (Eisner 1958, 1960, Lea et al. 1981,Meijer et al. 1990) but experimental evidence infavour of its action remains weak (Haywood 1993c,Sockman et al. 2000, 2006). Another hypothesisattributes the control of avian clutch size to an inhi-bition of the release and synthesis of gonadotropins,follicle-stimulating hormone (FSH) and luteinizinghormone (LH), from the anterior pituitary glandthrough actions on the gonadotrophin-releasinghormone (GnRH) system and the anterior pituitarygland. Proposed some 20 years ago (Haywood1993c), this hypothesis has received little attentionto date. Yet, the discovery of gonadotrophin-inhibi-tory hormone (GnIH) in the Japanese Quail Cotur-nix japonica hypothalamus (Tsutsui et al. 2000) andadvances made in our knowledge regarding GnIHcapacity to act on GnRH neurons, reduce circulat-ing FSH and LH concentration, and inhibit gonadaldevelopment and maintenance (Ubuka et al. 2006,2008, Tsutsui et al. 2010, 2012) argue in favour ofthis alternative hypothesis. The present finding of aclose temporal regulation of the timing of folliculardisruption is also consistent with this hypothesis. Inmammals, the master circadian clock is located inneurons of the suprachiasmatic nucleus (SCN) ofthe anterior hypothalamus, which have beenshown to form close appositions (synapses) withcells synthesizing an RFamide (Arg-Phe-NH2)-related peptide (RFRP-3), i.e. a mammalian GnIHhomologue (Gibson et al. 2008).
Invariance in timing of folliculardisruption
Although it was not possible to subject the samefemales to egg-removal experiments starting atvarious times throughout the egg-laying period,
there are reasons to suggest that the timing of fol-licular disruption is invariant in this species. First,if the timing of follicular disruption had varied asa function of final clutch size, as it is the case inthe Blue Tit (Haywood 1993b), with a minimumoviposition interval of 48 h, females laying three-egg clutches under un-manipulated conditionsshould have shown notably later timing of follicu-lar disruption than those laying two-egg clutches.As demonstrated in Figure 2, this is not the case.The almost complete absence of overlap betweenfemales that triggered an end to egg-laying on thefirst day of laying and those that did not, arguesstrongly for a timing of events that is identical inall individuals.
Another reason to validate the hypothesis ofinvariance in timing of follicular disruption in theCommon Swift stems from the observation that allindividual variation in clutch size can be fullyexplained by the developmental range that aninvariant timing entails and outside it, by theoccurrence of deviants. Over 93% of all un-manipulated clutches (n = 76) fall within thedevelopmental range, which spans just two sizes,two-egg and three-egg clutches, while those out-side, single-egg and four-egg clutches, comply withthe definition of deviants from the developmentalrange (see Results and Fig. 5).
Invariance in timing of follicular disruption hasnow been established experimentally for onespecies of Passeriformes, the Zebra Finch (Hay-wood 1993a), one species of Apodiformes (thisstudy) and possibly two species of Charadriiformes,the Lesser Black-backed Gull Larus fuscus and theNorthern Lapwing Vanellus vanellus (Klomp 1951,Paludan 1951, Haywood in press). There is alsosome indirect evidence of invariance in timing offollicular disruption for another species of Char-adriiformes, the Eurasian Dotterel Charadrius mor-inellus (Haywood in press), three additional speciesof Passeriformes, the African Stonechat Saxicola tor-quatus, the European Stonechat Saxicola rubicolaand the House Sparrow Passer domesticus (Hay-wood in press) and one species of Gruiformes, theAmerican Coot Fulica americana (S. Haywoodunpubl. data). In contrast, only a single species, theBlue Tit, has been found to have a timing of follicu-lar disruption that varies with clutch size (Hay-wood 1993b). Although it may be reasonable tohypothesize that invariance in timing of folliculardisruption is the standard mechanism controllingclutch size in birds, more species that belong toother bird orders and families will have to be inves-tigated to validate this hypothesis.
Onset of competence
An interesting feature of the sensory control ofclutch size in Common Swifts is its occurrence onthe very first day of the laying period. In contrast,clutch size in the Zebra Finch is determined onthe 3rd day. Such an early timing for a determina-tion event that involves both a signal generated byeggs in the nest and the female’s newly acquiredcapacity to respond to it, a property that may betermed ‘competence’ (Waddington 1940, Gurdon1987, Grainger 1996, Haywood 2007), has impor-tant implications. Unlike the signal originatingfrom the egg in the nest that brings about disrup-tion of follicular growth (possibly via the hypothal-amus and the anterior pituitary gland),competence takes time to develop. This is unsur-prising because competence as the principle laiddown by Waddington (1940) entails gene expres-sion. In Zebra Finches, various egg removal oraddition experiments aiming to advance or delayexperimentally the egg stimulus (Haywood 1993a)have shown that the build-up of competencebegins on day 2 of laying, that is one full daybefore the complete acquisition of competence. In
Figure 5. Schematic representation of the determination of athree-egg clutch (developmental maximum) in the CommonSwift. Successive cohorts of pre-hierarchical follicles arerecruited into the 5-day phase of rapid growth on the alternateday. When, as a result of stimulation from the first egg in thenest, the disruption of follicular growth strikes (arrow), there isone ovum in the oviduct (second egg to be laid) and one pre-ovulatory follicle in the ovary (third egg to be laid). After theevent, all pre-hierarchical follicles undergo atresia.
Common Swifts, the issue is yet to be investigatedexperimentally but, assuming competence arises asin the Zebra Finch through egg stimulation, itwould have only 3–6 h to develop before becom-ing fully operational at around solar noon. This isinferred from the observation that most eggs arelaid between 6:00 and 9:00 h local standard time(Lack 1956b).
In fact, this putative period of egg contactrequired before the onset of competence may stillrepresent an overestimate, for two reasons: (1) thefirst egg of the clutch is sometimes laid after09:00 h local standard time (see Results) and (2)casual observations (S. Haywood pers. obs.)suggest that first eggs may be left unattended forup to 36 min before noon on day 1 (data fromtwo-egg clutches only, i.e. clutches for whichdetermination was known to have taken place onday 1). More research is needed to understandhow a state of competence arises for the determi-nation of clutch size in Common Swifts andindeed in indeterminate laying species in general.
Tactile stimulation as inductive signal
Competence plays a central role in the physiologi-cal mechanism controlling clutch size. However,as highlighted by the response of Common Swiftsto egg removal, it requires stimulation from theegg in the nest, or ‘induction’ (Spemann &Mangold 1924, Waddington 1940, Gurdon 1987,Grainger 1996, Haywood 2007), to successfullytrigger follicular disruption. The sensory nature ofthe inductive signal is yet to be determined andmay in theory be visual, tactile, olfactory or evenauditory. But, in the Common Swift, three linesof evidence point to the involvement of tactilestimulation. The first consists of an empirical rule.Current knowledge of the control of clutch size inbirds indicates that the type of induction underly-ing the disruption of follicular growth relates tothe manner in which eggs are incubated. Speciesthat rely upon their own body heat for incubationuse tactile stimulation of the brood patch, speciesthat are entirely dependent upon finding a suitablehost nest use visual cues, and species whose incu-bation strategy is to exploit solar energy, volcanicactivity or microbial decomposition as a heatsource rely on thermal cues (Chance 1940, Frith1959, Haywood 1993a,c). Therefore, accordingto this rule, Common Swifts would use tactilestimulation.
A second argument arises from the behaviour ofCommon Swifts at the nest on day 1 before solarnoon. If the nature of the induction was visual,one would first expect to observe female contactwith the egg to last only a few seconds or minutes,as is typical of species (obligate brood parasites)that rely upon a visual input to control clutch size(Chance 1940, Haywood 1993c, White et al.2009). I would also expect parents to leave thenest mostly unattended on the morning the firstegg is laid, as (1) this is a time of high energydemand for females, and (2) incubation startswhen the clutch is complete or sometimes, inthree-egg clutches, with the penultimate egg (Lack1956b). However, Common Swifts were oftenpresent in the box in the morning and particularlyon the day the first egg is laid.
One final argument in favour of tactile stimula-tion is the observation that, on the first day of egg-laying and hence between 1 and 5 days before theonset of incubation, Common Swifts are in closecontact with the egg. Temperature taken after thebird(s) left the box on day 1 of laying reveals thatin 100% of the cases (n = 36) the egg was eitherwarm or slightly warm. In conclusion, althoughtactile stimulation may not be the only cue usedby Common Swifts in controlling clutch size, italmost certainly is the most important one.
Zeitgeber
Having discussed the opening of a window of com-petence and the induction that puts an end to it,one may ask why the onset of competence occursso close to solar noon. Is it a reflection of a roleplayed by some environmental time-giving cue(Zeitgeber) to which the endogenous circadianclock that controls the onset of competence isentrained?
Given its widespread use by birds to control thetime of breeding and moult (Kumar et al. 2004),we might suppose that photoperiod or some otherparameter of day-length (e.g. twilight transitions)also serves as Zeitgeber in the present case. How-ever, because photoperiod changes throughout theseason, it is a poor indicator of solar noon. Analternative Zeitgeber for the onset of competencewould be the daily variation in ultraviolet (UV)light. UV radiation has a maximum for all latitudesat solar noon (Seckmeyer et al. 2008) and isreduced less by clouds than by total solar radia-tion (Calb�o et al. 2005). Consistent with the
hypothesis that UV light regulates the timing ofcompetence is the fact that birds possess a tetra-chromatic colour vision system. It is made up offour spectrally distinct types of cone, includingone that is sensitive to violet or UV wavelengths,depending on the taxon (Hart & Hunt 2007).Visual pigments have not been investigated in theApodidae, but Alpine Swifts Tachymarptis melbahave been shown to use UV signals to regulatefood provisioning to the young (Bize et al. 2006).With respect to UV radiation acting as Zeitgeber,there is some evidence in the Atlantic CanarySerinus canaria that UV light cycle can entrain thecircadian rhythms of perch-hopping and feedingactivity (Pohl 1992).
Egg removal as stress
While brood size manipulations by Perrins (1964)demonstrated that individuals laying a four-eggclutch would raise fewer offspring per brood thanthose laying a three-egg clutch, would feedingconditions at the time of laying also affect egg for-mation? In this aerial-feeding species, it is obvi-ously not easy to manipulate food supply.Alteration of oviposition intervals by egg removalmay be regarded as a measure of the stress andstrain of laying eggs. If this assumption is correct,females laying three-egg and four-egg clutchesappear more stressed than those laying two-eggclutches (Fig. 4). This might suggest that, whileproducing eggs, Common Swifts may be close tosome limit in terms of either foraging efficiencyand nutrient utilization or environmental carryingcapacity, or both. It is also possible that food isnot directly involved but instead, the physiologicalneed for egg contact increases as laying progressesso as to significantly impact oviposition intervals infemales laying three-egg and four-egg clutches.
I wish to thank Chris Perrins for granting me the oppor-tunity to carry out this study of the Common Swifts ofthe University Museum tower, and Colleen Downs forthoughtful comments on earlier drafts. Two anonymousreviewers provided valuable comments on the manu-script. Data were collected under English Nature li-cences No. SB:11:93, No. SB:24:94, No. SB:23:95 andNo. SB:37:96.
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