An analysis of the mechanism responsible for controlling clutch size was ... showed no significant variation between females (n = 12) in relation to clutch size.
The Auk 110(4):778-786, 1993
SENSORY
CONTROL
OF CLUTCH
SIZE IN
THE ZEBRA FINCH (TAENIOPYGIA GUTTATA) SACHA HAYWOOD
EdwardGreyInstituteof FieldOrnithology, Departmentof Zoology,
University of Oxford,SouthParksRoad,OxfordOX1 3PS,UnitedKingdom
A!tSTRACT.--Ananalysis of the mechanismresponsiblefor controlling clutch size was carried out in the Zebra Finch (Taeniopygia guttata)by manipulatingthe number of eggs present in the nest during laying. Sensorycuesinvolved were alsoinvestigated.Stimulation from the eggspresent in the nest during the secondand third day of the egg-layingperiod
determinedhow femalesceaseto lay in this species.Disruptionof ovarianfollicular growth wastriggeredon the third day of laying, 6 _+1 h after the onsetof light (14L:10D),by tactile stimulation. Contact with eggs also was required to induce the onset of sensitivity to the stimulusresponsiblefor ending laying. The hypothesisthat individual variationsin clutch size (four to six eggs)are causedby early disruptionof follicular growth for smallerclutches versus late disruption for larger clutches was tested. The timing of follicular disruption showedno significantvariation between females(n = 12) in relation to clutch size. There is good evidence that this result, establishedin domesticatedZebra Finches,holds true for wild Zebra Finches as well. Individual
variation
in clutch size resulted from the variable
number
of growing follicles that, oncefollicular disruptionhasbeen triggered,were able to complete the rapid-growthphaseand ovulate.Received 11 May 1992,accepted 30 October1992. CONSIDERABLE PROGRESShas been made in our
(1) whether the Zebra Finch is, like the few
understanding of the evolution of clutch size
sinceLack(1947)first attemptedto explainwhy birdslay the numberof eggsthey lay.Although it has been known for quite some time that clutch-sizecontrolmechanismsmay differ be-
passerine species studied so far (Haywood 1993a), an indeterminate layer; (2) if yes, the number of eggsand the duration of contactre-
quired to induce the female to ceaselaying; (3) the type of stimulusperceivedby the female tween species (Cole 1917), how birds control that might be visual, tactile, olfactory, or authe size of a clutch is still a very little known ditory; and (4) the timing of the stimulus reaspectof their breedingbiology.Somespecies, sponsiblefor the ending of laying. Given that classified as tactile indeterminate or semideterclutch size variesin this species,usuallyfrom minatelayers,havebeenshownto rely on eggs four to six eggs,an attempt hasalsobeen made presentin the nestduring the laying period to to uncover the mechanismresponsiblefor inceaselaying whereasothers,classifiedas deter- dividual variation in clutch size. If a contact minate layers,do not need suchstimulus(Hay- betweenthe femaleand her eggsis involved, wood 1993a). The role of a contact between the it may be hypothesizedthat in femaleslaying femaleand her eggsin stoppinglaying hasbeen smaller clutches laying might be inhibited substantiated, through egg-removal experi- soonerby the eggsalready presentin the nest ments, in a number of species,mostly nonpas- than in femaleslaying largerclutches.This hyserines(for a review, seeHaywood 1993a).Stud- pothesiswas testedby determiningfor eachof ies carried out in gulls have demonstratedthat a dozen femalesthe characteristic, averagesize the contactbetweenthe femaleand the firstegg of severalsuccessive clutchesand the precise of a clutchresultsin disruptionof ovarian fol- timing of disruption of ovarian follicular licular growth (growing follicles becoming growth. atretic instead of ovulating) and then, after a METHODS few days,cessationof egglaying (Paludan1951, Weidmann 1956).
Zebra Finchesbred in captivity for many genera-
The aim of my study was to analyzein the tions were kept in indoor cages(35 x 40 x 45 cm). Zebra Finch (Taeniopygia guttata)how females All pairs were maintained at about 20ø(/and under a control their clutch size by manipulating the photoperiod of 14L:10D; with light on at 0800. Pairs number of eggspresentin the nestduring lay- were providedwith freshwater,seeds,eggfood,grit, ing. Experiments were carried out to determine: 778
and cuttlebone ad libitum. In addition, salad leaves for
October1993]
Sensory Controlof ClutchSize
80
779
60 14L: 10D
50
c•
60
¸
c•
40
¸
E 20
•-• lO
2
3
4
5
6
7
8
9 101112131415161718192021222324
0
1
2
3
Time (hours)
4
5
Clutch
6
7
8
9
size
Fig. 1. Timing of egg laying in Zebra Finches Fig. 2. Clutch sizesin domesticatedZebra Finches maintained on lighting cycle of 14 h light and 10 h dark (14L:10D).Horizontal axis indicatesparticular (n = 140). time of day (e.g.8 indicates0800to 0859).Percentages represent hourly ratio between number of oviposi- Clutches greater than six eggs were also discounted tions witnessed (n = 21) and number of visits to a
nest box yielding a new egg (n = 360). green supplementand hay for nestingmaterial were given aboutoncea week. A single nestbox wasavailable to eachpair. The contentsof nestswere checked daily before 1300. Most eggswere laid before that time (Fig. 1), but if an egg was laid that day after my visit it was generally detected on the next visit be-
cause,in contrastto freshly laid eggswhich appear chalky, 24-h-old eggsoften are shiny due to repeated contactwith broodpatches.Pairswere constantlyinduced to lay a new clutch by removing the previous
(3.6% of all clutches) because there is some evidence
that, as a consequenceof removing clutches early during the incubation period, the natural tendency of males to incubate eggs during the laying of the following clutch was greatly enhanced. This alter-
ation in the male behaviorcaused,in a few pairs,the female to spend lesstime on her eggs early during laying, thus occasionallydelaying the cessationof egg laying. The following experimentswere conducted: Experiments 1-3.--In the first experiment,eachlaid egg was removed from the nest as soonas it was laid (this is noted as 0000...
on the basis of the number
of eggspresentdaily in the nest,after visit), until the one. Clutches were removed at the earliest on the female had laid at least six eggs. In the secondexfifth day of laying in order to preventadverseeffects periment, the first egg was left, but eachsubsequent on either ovipositionor ovarianfollicular growth (and, eggwasremoved(i.e. a singleeggwasleft throughout hence, on clutch size), but before the seventhday of the laying period; 1111 ...). In the third experiment, the laying period in order to limit the impactof in- five eggswere added to the clutch on the day the first cubation on relaying and generate the shortestrelay- egg was laid (6789 . . .). Experiments 4-7.--In the fourth experiment, in oring periods.All pairs were kept under constantconditions throughout the study,and no changein clutch der to prevent tactilestimulationof the female by the size was detected with its advancement. The same eggs and allow visual contact with a clutch of eggs females were used to produce both control and ex- throughout the egg-laying period, eggs were reperimental clutches. Control clutches were not intermoved as laid and a set of six eggs glued to one fered with exceptto weigh and measurethe female another was hung from the ceiling of the nest box, and the eggs,as was done for experimentalclutches. about 80 mm above the nest cup, on the first day of Clutches associatedwith the experiments 1-18 delaying until laying stopped(or was stopped).In the scribedbelow were producedat random. Overall, 25 fifth experiment,eachegg as it was laid was replaced pairswere involved in theseexperiments;not all pairs by a flat brownish button 10 mm in diameter. The aim was to provide the female with a tactile stimulus were used for each experiment. Clutch size rangedfrom one to nine eggs,but most but no visual, olfactory,and auditory stimuli similar clutchescomprisefour to six eggs(Fig. 2). Clutches to eggs. In the sixth experiment, in order to test smaller than four eggswere discounted(5.7% of all whether olfactory cues supplement tactile stimulus clutches) because some of these were related to calin cessationof egg laying, all eggslaid were replaced cium deficiency since some eggs were thin shelled by eggscoatedwith a plasticfilm (acrylic white paint, Liquitex), which prevented any possible olfactory and renewing the old cuttlebone resulted in the female resuming the production of larger clutches. stimulusfrom the egg. A similar seventhexperiment
780
s^c}• HAYWOOD
[Auk,Vol.110
had been reared (in a single batch) as part of a previous study (Haywood and Perrins 1992). Individual
•
estimates of clutchsizewere calculatedby takingthe meansizeof sevenclutchessuccessively laid by each femaleand controlledfor the effectof (early)age.To
60
relate these estimates of individual
•
clutch size to the
timing of follicular disruption,eachfemalewas subjectedto the following egg-removalexperiments.At differenttimeson the third day of the laying period, completesetsof eggswere removed from the nest in order to determine whether femaleswould lay in an indeterminatemanneror not; eggslaid on subsequent
40
20
5
6
7
8
9
Relaying intervals Fig. 3. Relaying periods in domesticatedZebra
Finches(n = 195)calculated by subtracting dateof removalof a clutchfromlayingdateof firsteggof following clutch.
days were also removed (before 1300) until at least six eggshad been laid. Setsof eggswere removed at 0800, 2200, and 1400, respectively.Femalessystem-
aticallyrespondedby indeterminatelayingwhen egg removalstartedat 0800,by determinatelaying when egg removal started at 2200, and by either indeterminate or determinatelaying when eggremovalstarted at 1400.Consequently,femalesthat respondedin an indeterminate manner at 1400 were subjectedto egg removal at 1500, whereas those that responded in a determinate manner at 1400 were subjectedto
was conducted to test the contribution of auditory cueswith eggscoatedwith a thin layer of transparent
eggremovalat 1300.The resultsobtainedin this way were confirmedby further egg-removalexperiments rubber(silasticelastomer,Dow Corning),which pre- carriedout at 1400(repeatexperiments)and 1200.The vented the female from hearing any normal sounds timing of these removal experimentswas such that and indeterminate reoriginating from contact between the birds' bill or in most cases determinate clawsand the eggs. sponsesalternated. The latest time at which the feExperiments 8-11.--In theseexperiments, thetiming male respondedin an indeterminatemanner and the of stimuluswasestablished by comparingvariouspe- earliesttime that brought about a clutch of four to riods during which eggswere left in the nest. In the six eggsgive, for each female, an estimate of the intest groups,eggswere removed (alwaysbefore 1300) tervalduringwhichthe disruptionof folliculargrowth from the secondday onwards.(experiment8:10000 occurs.Eachinterval was transformedinto a single ß..), the third day onwards(experiment9: 12000...), middle value, sothat the degreeto which the timing the fourth day onwards(experiment10:12300 ...), of follicular disruptioncoyarieswith meanindividual and the fifth dayof the layingperiod(experiment11: clutch size could be estimated. 12340...). Statistical analyses.--Foreachof the experiments1Experiments 12 14.--Here, the first egg to be laid 18,meansof clutchsizesof controland experimental was removed (experiment 12: 01234...), the first two
eggsto be laid were removed(experiment13:00123 ß..), and the first three eggsto be laid were removed (experiment 14:00012 ...). Experiments 15-18.--Eggswere put into the nestone
groups were tested for statisticaldifferences.In total for these experiments,239 control and 208 manipulated clutcheswere laid by 25 females.Since not all 25 femaleswere involved in eachof the experiments,
the meanclutchsizeof controlsis computedonly for day (experiment15:•234 ...), two days(experiment the femalesusedin a given experimentso asto form 16:n345 ...), three days (experiment17:•23456...), matchedpairs. When several,control or experimenand four days (experiment 18: •2•4567...) before the tal, clutcheswere obtainedfrom a single female,an firsteggof the clutchwaslaid (thedaysduringwhich averageclutch size for that female was kept in the eggswere addedbut no egg was laid are indicatedin
calculation
superscript).A rough idea of when to start adding eggswasprovidedby the consistency of relayingperiods, which are mostly of five days (Fig. 3). Each clutchwas attributeda posterJori to the experiments
experimentalgroups.Clutch size obtainedfor the experimental femalesand the correspondingcontrols were testedfor the similarity between means(twotailed t-test for matchedpairs;Sokaland Rohlf 1981).
described
of the mean clutch size of the control
or
above.
Experiment 19.--Among the 25 femalesusedduring this work only 12 were used to test the hypothesis
RESULTS
that folliculardisruptionmightbe triggeredsignifiQuantitativenature of stimulus.--Femalesleft cantlylaterin thosefemaleslayingthe largestclutches.All 12 femaleshad in commonthe factthat they with no eggin the nestduring the laying period
October 1993]
781
SensoryControlof ClutchSize
TABLE1. Mean clutchsize + SD of controland experimentalfemalesfor experiments1 to 18.
Experiment 1 Egg removed as laid (0000...) 2 Single egg left (1111...) 3 Five eggsadded (6789...)
Samplesizea
Control
Quantitative nature of 7 (63, 32) 7 (60, 14) 6 (60, 12)
stimulus 5.28 + 0.34 5.01 + 0.50 5.20 + 0.32
Qualitative nature of stimulus 4 (59, 5) 5.40 + 0.15 4 (48, 4) 5.42 + 0.16 5 No olfactory, auditory, or visual stimuli 4 (4, 4) 5.75 + 0.43 6 No olfactory stimulusb 4 (4, 4) 5.75 + 0.43 7 No auditory stimulusb 4 No tactile
stimulus
Experimental 13.43 + 4.37 5.00 + 0.60 5.03 + 0.48
t-test(df) 4.62 (6)** 0.07 (6) ns 0.75 (5) ns
9.50 5.75 5.75 5.75
+ + + +
1.50 0.43 0.43 0.43
4.55 (3)*** 2.29 (3) "3 0.00 (3) "s 0.00 (3) n•
7.38 9.42 4.74 4.83
+ + + +
2.00 1.81 0.54 0.62
2.74 (7)* 9.42 (17)*** 3.78 (19)** 1.16 (5) "s
Timing of stimulus 8 9 10 11
Egg removal from 2nd day (10000...) Egg removalfrom 3rd day (12000...) Egg removal from 4th day (12300...) Egg removal from 5th day (12340...)
8 (70, 8) 18 (197, 33) 20 (212, 39) 6 (51, 9)
Experimental delay of 12 Egg removal until 2nd day (01234...) 5 (47, 9) 13 Egg removal until 3rd day (00123...) 8 (68, 9) 14 Egg removal until 4th day (00012...) 9 (77, 13)
5.34 5.26 5.23 5.09
+ + + +
0.34 0.32 0.34 0.50
stimulus 5.39 + 0.26 5.32 + 0.34 5.34 + 0.31
Experimental advanceof stimulus 15 Egg addition one day in advance(•234...) 4 (46, 4) 5.47 + 0.11 16 Egg addition two daysin advance(•2345...) 5 (48, 5) 5.23 + 0.37 17 Eggadditionthreedaysin advance('23456. . .) 4 (35, 4) 5.43 + 0.18 18 Eggadditionfour daysin advance(m4567...) 3 (25, 5) 5.47 + 0.19
5.28 + 0.39 6.19 + 0.79 7.08 + 0.33
0.58 (4) "• 2.55 (7)* 12.60 (8)***
5.25 + 0.43 4.40 + 0.49 3.75 + 0.43
0.88 (3) n• 2.35 (4) "• 5.31 (3)**
2.78 + 0.31
8.64 (2)*
*, P < 0.05; **, P < 0.01; ***, P < 0.001; ", P > 0.05.
Number of controland experimentalfemales,with numbersof clutchesfor controlsand experimentals,respectively,in parentheses. Control was testgroup in experiment5.
laid on averagesignificantlymoreeggsthan the controls (Table 1, experiment 1). One female
laid a singleclutchof 39 eggs,with nine singleday gapsin the sequence.When, after the first
newly laid eggswere replaced by eggs coated with a plasticfilm or a thin layer of transparent rubber did not lay significantly larger clutches than birdswhoseeggswere replacedby buttons
egg, further eggs were not allowed to accu- (Table 1, experiments 6-7). Timingof stimulus.--When egg removal startmulate in the nest through the laying period, experimentalclutchsizeswere not significantly ed on the secondor third day of the laying differentfrom the controls(Table1, experiment period, femaleslaid significantlymore eggsper 2). When a full clutch(five eggs)was placedin clutch than the controls(Table 1, experiments the nest on the first day of laying, clutch sizes 8-9). When egg removal started on the fourth of experimental females also remained un- or fifth day of the laying period, however, fechanged (Table 1, experiment 3). malesdid not lay significantlymore eggsthan Qualitativenatureof stimulus.--Femalesthat the control (Table 1, experiments10-11). For were given the opportunity of prolongedvisual the 20 females where eggs were removed on contactwith a clutch during laying, but lacked the fourth day of the laying period, none laid tactile stimulationfrom eggs,laid significantly a clutch greater than six eggs. By contrast,the more eggs per clutch than the controls (Table proportionof females(n = 18) laying clutches 1, experiment 4). Femalesin contactwith but- greater than six eggswhen eggswere removed tons insteadof eggsduring the laying period on the third day of the laying periodwas 100%. had clutch sizes not different from the controls In experiments8-9, somefemalesinterrupted (Table 1, experiment 5). Somefemaleslaid extra laying altogether as a result of the start of egg eggs,but they were not taken into accountbe- removal instead of continuing laying beyond causethesebirds, or their mates,systematically their normal clutch size.Among all 81 clutches ejectedthe buttonsfrom the nest.Femaleswhose manipulatedbeforethe third day of the laying
782
SACHA HAYWOOD
period, 9.9%were smaller than seveneggs(n = 21 females),whereasamong217 control clutch-
[Auk,Vol. 110 DISCUSSION
es of the same 21 females, 96.8% were smaller
Resultspresented here show that female Zebra Finches require contact with at least one manipulated clutchessmaller than seven eggs egg during laying to lay a normal clutch (four was greater when egg removal started on the to six eggs). A single egg actually is sufficient secondday of the laying period, by comparison to trigger the cessationof egg laying although, with clutcheswhere egg removal startedon the under natural conditions, most females have first or third day, this difference is not signifi- already laid three eggswhen the egg stimulus cant (X 2 = 4.49, 2 df, P = 0.106). ending laying occurs.Clearly, suchstimulusreSlightly smaller clutchesthan expectedwere ceived by the female is independent of the on average laid by females manipulated on the number of eggsin the nestsincefive eggsadded fourth day of egg laying (Table 1). Lack of con- on the first day of laying doesnot lead to smaller tact with eggs at this stage sometimes prevents clutch size. When eggsare removed as they are the last large yolky follicle from completing the laid, close visual contact with a clutch is not rapid-growth phaseand ovulating. Hence, this sufficientto stopfemalesfromlayingeggs.When causes a reduction in clutch size in the Zebra I replaced eggs as they were laid with buttons Finch. (in order to provide the female with a tactile Experimentaldelay of stimulus.--Femalesfor stimulus but no visual, olfactory, and auditory which only the first egg laid was removed did stimuli similarto eggs),experimentalclutchsizes not lay significantly more or fewer eggs per did not differ from the controls (Table 1). Thus, clutch than the controls (Table 1, experiment only tactile stimulus is required to induce fe12). Females in which the first two eggs were malesto stop laying. This finding is confirmed removed did significantly increasetheir clutch by experiments involving eggs coated with size (Table 1, experiment 13), although not as plastic to prevent egglike olfactory stimulus or much as females in which the first three eggs coatedwith rubberto prevent egglikeauditory were removed (Table 1, experiment 14). Re- stimulus, which suggestthat neither olfactory moval of the first two eggs induced the female nor auditory factors are involved in synergy to lay an average of one extra egg, whereas with tactile stimulus in ending laying in this removal of the first three eggs induced the fe- species.To sum up, following the classification of clutch-sizecontrol mechanismsproposedfor male to lay an averageof two extra eggs. Experimentaladvanceof stimulus.--Eggsadded the birdsinvestigatedto date (Haywood 1993a), one or two days before females started laying the Zebra Finch is a tactile indeterminate layer did not significantly affect the clutch size laid of type S. It has often been speculated that in species by experimental females(Table 1, experiments 15-16), whereaseggsadded three or four days responding to egg removal, females may be usbefore females started laying did (Table 1, ex- ing a visual stimulusfrom the eggs(alone or in periments 17-18). Resultsin Table 1 show that connection with tactile stimulus) to trigger addition of eggs two, three, and four days be- cessationof egg laying (Lack 1947, Chappell fore the first was laid induced females to lay 1948, Jones 1969, Steen and Parker 1981, Lea et on average one, two, and three fewer eggs,re- al. 1981, Kennedy 1991). Until now, however, spectively, than the controls. only Steen and Parker (1981) have attempted to Individualvariationin clutchsize.--Among the test the involvement of visual cues.They sub12 females tested, the timing of disruption of stantiated their view that such cues are in use ovarian follicular growth was restrictedto an in bantamhens (Gallusgallus)by putting a wire interval starting 5 h (1300) after the onset of netting over the clutch in order to prevent felight (0800) and lasting a maximum of 2 h. The males from having tactile contact with their individual timing of follicular disruption was eggs.Experimentalclutch sizes(15.17 + SD of than seven eggs. Although the proportion of
not correlated
with
mean individual
clutch size
(r• = 0.437, P > 0.05); acrossfemales, the time of follicular disruption tended to decrease slightly as clutch size increased:Y = 16.516 0.506X (95% confidence limits of slope were -0.889 and -0.288).
5.15) and control clutch sizes (14.67 + 4.78) obtained from the same females (n = 12) were not
statisticallydifferent (t22= 0.236,P > 0.05). This experiment is, in my opinion, invalidated by the fact that females
were allowed
to sit on the
floor next to the eggs and, hence, actually re-
October1993]
Sensory Control ofClutch Size
783
Kestrelscontroltheir clutchsize in sucha way (Beukeboomet al. 1988, Haywood 1993a) that contactwith an almost complete clutch days there is good evidence that visual stimulus before the first egg is laid will be required to (probablyrelatedto the availability of suitable induce a significant responseto egg addition. hostnests)maybeinvolvedin controllingclutch Rock Doves respond to egg addition to the exceivedthe tactile stimulusneededto trigger the cessationof egglaying. To date,it is only among parasitic speciesof cuckoosand cowbirds that
size (Haywood 1993a). Egg-removal experiments started on the sec-
tent that some females
will
incubate
a clutch
added prior to laying (Poulsen 1953), but egg ond to fifth day of the egg-layingperiod (Table formation and therefore laying, even of a re1, experiments 8-11) show that the disruption duced clutch, becomede facto physiologically impossible.As shown here in the Zebra Finch, of ovarian follicular growth occurson the third or fourth day of laying. Further egg-removal changes in clutch size that some species can experiments (experiment 19) demonstrate that produce as a result of egg removal or egg adfollicular disruptionis irreversiblesometimeaf- dition are mere consequences of the way they ter 1300 but before 1500 on the third day of control their clutch size. Any tactile indeterlaying (i.e. 5-7 h after dawn [14L:10D]).In other minate layers (i.e. speciesin which egg stimuli respects,the period during which females are are needed to trigger the disruption of ovarian responsiveto the tactilestimulusendinglaying follicular growth), therefore, will respond to can be experimentallydelayedor advancedby both egg-removal and egg-addition experichanging the day when egg(s) first appear in ments. the nest. Removing eggs for n days from the In Zebra Finchesthe sensitiveperiod, during start of laying increasedthe clutch by n - 1 which tactile stimulation builds up to reach a eggs (Table 1). In contrast,eggs added before stagewhere folliculardisruptioncaneffectively the first egg is laid bring about a reduction of occur,lasts less than two days. Thereafter, fethe size of the clutch. Adding eggsn daysprior maleswill remainresponsiveto any prolonged, to egg laying reduced the clutch by approxi- tactile stimulation of the brood patch for several mately n - 1 eggs(Table 1). Theseresultsshow days.Femaleswhoseeggswere removedasthey that, although follicular disruption occurs on were laid for a period of up to 12 days,subsethe third day of laying, the timing of this event quently ceasedlaying within three to four days relative to the onsetof laying is determined on after egg removals were stopped. It was nonethe secondday of the laying period.Thus,eggs thelessdifficult to assess rigorouslythe precise not only provide a stimulusresponsiblefor the maximum duration of the sensitive period bedisruptionof ovarianfollicular growth, but they cause, as mentioned earlier, the male who also also provide stimulation for the onset of sen- incubatesthe clutch, often prevents the female sitivity to the stimulusresponsiblefor follicular from gettingsufficientcontactwith the eggsleft disruption. The fact that the timing of follicular in the nest. This sensitiveperiod and the factors disruption can be moved back and forth during that affect its duration therefore would be more the laying period demonstratesthat the timing easily investigatedin a specieswhere the male of tactile sensitivity to eggs is not internally doesnot take part in incubating the clutch. related to the onset of egg laying. The present data on Zebra Finches demonIt has been suggestedthat somespeciesmay strate that the disruption of ovarian follicular alter their clutch size in responseto egg re- growth is not triggered significantly later in moval, but not to egg addition (e.g. Common femaleslaying the largest clutches.The hyKestrel [Falco tinnunculus],or vice versa, Rock pothesisthat variation in the timing of the stimDove [Columba livia];Kennedy 1991).Hence, the ulus provided by eggsaccountsfor individual hypothesisthat suchspeciescategorizedas"re- variation in clutch size, therefore, is not valid. moval indeterminate" or "addition indetermiIt may be argued that the lack of variation in nate,"respectively,haveindependentlyevolved the timing of follicular disruption in relation mechanismsallowing them to cope with egg to clutchsize in 12 femalesbred in captivityfor lossor eggparasitism(Kennedyand Power 1990, many generations might have resulted from a Kennedy 1991). This distinction is based pri- bottleneck effect when captive breeding was marily on artifacts;evidence that separatere- initiated and/or from subsequentinbreeding. sponseshave evolved due to egg removal or If we assumethat some significant variation of egg addition per se is yet to be found. Common the timing of follicular disruption existsin the
784
SACHA HAYWOOD
1993b).In this species,a lack of variation in the timing of follicular disruption would limit clutchesto three or more likely two sizes,according to the number of yolky follicles undertaking rapid growth simultaneously.In Zebra Finches, data collected by Sossinka(1970) do not supportthe view that significantlymore
50
'D Wild []
40
•
[Auk,Vol. 110
Domesticated
30
variation
occurs
in the
wild.
Distributions
of
E 20
clutch sizes from 10 females taken from the wild
•:•
(n = 74 clutches) and 16 domesticated females (n = 69), both maintained under the same con-
10
ditions in captivity, were not statisticallydifferent (Kolmogorov-Smirnovtest for goodness of fit, D = 0.0519,P > 0.05;Fig. 4). As expected if a steadytiming of follicular disruption is the rule in the Zebra Finch, the vast majority of
0
1
2
3
4
5
Clutch
Fig. 4.
6
7
8
9
size
Clutch size from wild and domesticated
clutches were restricted
to three sizes. Clutches
ranging from four to six eggsrepresented87.8 in captivity. Wild females (n = 10) and domesticated and 85.5%of all clutcheslaid by wild and dofemales(n = 16) laid 74 and 69 clutches,respectively, mesticatedfemales, respectively.Therefore, it over three seasons(data from Sossinka 1970). is likely that, asfor the variabletiming of clutchZebra Finches maintained
under the same conditions
size determination
uncovered in Blue Tits, a
steadytiming is characteristicof the way Zebra Finches as a speciescontrol their clutch size. wild, clutch size likewise would be more vari-
able. For instance,variable timing of follicular disruption, which has been reported for wild Blue Tits (ParuscaeruIeus), allows them to lay clutchesvarying from 6 to 13 eggs(Haywood
Knowingthat the timing of folliculardisruption showsno positiverelationshipwith clutch size, how are individual
variations in clutch size
generated?In theory, egg stimuluscould act at two differentstagesof oocytedevelopment:fol-
(Inhibitory input)
,1
Oviposition
Eggs Yolky follicles
I
I
[
I
I
I
I
I
I
I
I
I
I
I
I
Time (days) Fig. 5. In theory, how inhibitory input from eggspresentin nest affectsovarian activity may either result in (1) disruption of follicular recruitment, or (2) disruption of follicular growth.
October1993]
Sensory Control ofClutchSize
785
Inhibitory input i
Clutch removed
Eggs Yolky follicles
Time (days) Fig. 6. Representation of a five-eggclutchdetermination in the ZebraFinch.Inhibitoryinputprovided by eggspresentin nestand responsible for disruptinggrowthof smalleryolkyfollicles(emptycircles)occurs
onthirddayof laying,6 + 1 h afterdawn(14L:10D). Removal of clutchonfifthdayof layingallowsfollicular growth to resumeon sameday.
licular recruitmentand follicular growth (Fig. becomeatretic,the clutchsize will be five eggs 5). Cessationof egg laying through disruption (Fig. 6), and so forth. The greaterthe number of follicular recruitmentwould inevitably pro- of growing follicles affectedby the female conduceclutchesof at leasteight eggs(Fig. 5), since tactwith eggs,the smallerthe clutch. Sincethe five days are required to form an egg in the timing of follicular disruption shows no variZebra Finch (S. Haywood unpubl. data). As this
ation between females in relation to clutch size,
prediction doesnot matchthe observedrange the depressiveactionbrought aboutby the conof clutchsizes,the hypothesisthat eggstimulus tactwith eggsaffectsdifferentlygrowingyolky actson the ovary by disrupting foliicular re- folliclesof differentages.Growthof folliclesin cruitment must be rejected. The impact on fol- their first or secondday of developmentis syslicular recruitmentduring follicular disruption tematically disrupted since no normal clutches is in fact minor or null. In effect, the bulk of reacha sizeof eight or seveneggs,respectively, relaying periodsare as shortas five days(Fig. but the extent to which follicles in their third 3), which implies that in most cases,at the time and fourth day of developmentare affectedby of foliicuiar disruption, follicular recruitment is continued without interruptions; the follicle correspondingto the egg laid after such fiveday periods is recruited into growth within a
day of the removal of the clutch(Fig. 6). The range of clutch sizesobservedin Zebra Finchesimplies that the mechanismresponsible for individual variation in clutch size specifically involves disrupting follicular growth. If all growing follicles up to the one in its last day of growth become atretic, the clutch size will be four eggs.Similarly,if all growing folliclesup to the one in its third day of growth
the inhibitory input from eggs is responsible for
clutch-size
variation
in the
Zebra
Finch.
Which factor(s)determineswhether the growth of these large yolky follicles is disruptedis not known. However,
it is known that conditions
experiencedby female Zebra Finchesat an early age (nestling stage)have considerableeffecton individual variation in clutch size (Haywood and Perrins 1992).Investigatingthe endocrine
controlof follicular disruptionand its regulation at the level of the brain would help answer how clutch-sizevariation are generatedin this species.
786
SACHA HAYWOOD ACKNOWLEDGMENTS
I thank Euan K. Dunn, Andy G. Gosler, Larry C. Holcomb, Peter J. Jones,John R. Krebs, Ken J. Norris,
Chris M. Perrins, Peter J. Sharp, and an anonymous reviewer for many helpful commentson an earlier draft. I am greatly indebted to Chris M. Perrinsfor making this study possible.
[Auk,Vol. 110
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