The Auk 112(4):860-869, 1995
THE
ROLE
OF PARENTS
REDUCTION
IN SIBILICIDAL
OF TWO
BOOBY
BROOD
SPECIES
DAVID J. ANDERSON
Departmentof Biology,LeidyLaboratory,
Universityof Pennsylvania,
Philadelphia,
Pennsylvania
19104,USA;and
Departmentof Biology,WakeForestUniversity,Winston-Salem,
North Carolina27109USA•
ABSTRACr.--Parental
regulation of the probability and timing of avian brood reduction is
expectedto existand evolve becausenatural selectionshould favor parentsthat matchbrood
size to food availabilitymostefficiently.Sincefood availabilityvariesamongspecies,interspecificvariation in this regulation is expected.Comparativestudy of specieswith different
brood reduction systemsis one way to test the hypothesisthat these mechanismsevolve as
adaptations.Previouswork on obligately siblicidal Masked Boobies(Sula dactylatra)and
facultativelysiblicidalBlue-footedBoobies
(S.nebouxii)
hasshownthattheirdifferenthatching
asynchroniescannotfully explain the qualitativedifferencein their broodreductionsystems.
In this study,I reportinterspecificdifferencesin nestshapethat appearto contributeto early
siblicide in Masked Boobies,but that suppressearly siblicide in Blue-footedBoobies.BluefootedBoobynestshapeis closelyregulatedby parents.Differencesin eggsizesof nestmates
do not appear to contributeto the differencein socialsystems.Received19 January1995,
accepted
2 July 1995.
FATAL SIBLING AGGRESSION,known as "siblicide," often reduces the brood size of a number
of bird species(Stinson1979,Mock et al. 1990).
Lack's(1954)brood-reductionhypothesisis the
basisfor the common evolutionary interpreta-
1987). Thus, parentsmay benefit from regulating siblicide. Specifically, they are expectedto
have experiencednatural selectionfor regula-
tory mechanismsthat rank offspring for sur-
strategyof hatching as many nestlingsas can
vival within a competitive hierarchy, but suppress siblicide that is not in the parents' best
interests.Whether the first or secondobjective
is emphasizedduring selectionwill depend on
the extent of brood reduction that is optimal
for parents,and is expectedto vary acrossspe-
be raised in the best conditions,
cies.
tion of siblicide, and of brood reduction (Rick-
lefs 1965) in general. When food supply for
nestlings cannot be predicted reliably at the
time of laying, selectionis expectedto favor a
and then of
Past interest has focused on two mechanisms
eliminating nestlingsafter hatching, if necessary,to bring demandinto line with supply(see to regulatesibling competition.Variation in the
also Temme
and Charnov
1987, Forbes and
Ydenberg 1992). Siblicide provides parents an
optimizing tool with a notable advantage: individual nestlings are best able to gauge their
own physiological condition and can use that
interval between successivehatchings of nest
mates (hatching asynchrony) and in egg size
explain much of the variation in competitive
ability within a brood (Ricklefs 1965, Parsons
1970, 1975, Hahn 1981, Braun and Hunt 1983,
information,in conjunctionwith a competitive Slagsvoidet al. 1984,Hebert and Barclay1986,
hierarchy, to maximize efficiencyof brood re- Plogerand Mock 1986,Skagen1987,Amundsen
duction (Mock et al. 1987a).
Reliance on dominant offspring to conduct
siblicide also carries a notable disadvantage.
Offspring may commit siblicide under lessstringentconditionsthan is optimal for parents,
especially if parent-offspring conflict exists
(Trivets 1974, O'Connor 1978, Dickins and Clark
and Stockland 1988, Hebert and Barclay 1988,
Anderson1989a,Magrath 1992,Joveret al. 1993),
with hatching asynchrony being the more important (Stokland and Amundsen 1988, Magrath 1992). In specieswith sibling aggression,
available
evidence
shows that food distribution
parallels the competitive hierarchy within the
brood (Poole 1979, Braun and Hunt 1983, Fu-
Present
jioka 1985, Inoue 1985, Mock 1985, Cash and
Evans1986,Drummond et al. 1986,Hagen 1986,
Ploger and Mock 1986). Parents create acom-
address.
860
October
1995]
Siblicide
inBoobies
petitive hierarchyand, by not distributingfood
counterto the hierarchy, reinforceit through
positive feedback.
Only rarely have comparativestudiestested
the hypothesisthat differencesbetweenspecies
in siblicidal phenomena are explained by differencesin regulatorymechanisms.
Ideally,such
studies should compare speciesthat differ in
outcomeof siblingcompetition,they shouldfocuson interspecificvariation in traitsknown to
influence competitive hierarchies, and they
should eliminate to the extent possible confoundingeffectsof phylogeneticand ecological
dissimilarity. Two studieshave compared the
hatching asynchroniesof obligately siblicidal
eagles(Edwardsand Collopy 1983)and boobies
(Anderson1989a)with thoseof faculativelysiblicidal congeners.Longer hatching asynchronies (presumablyunder at leastpartial control of
parents)give greater competitiveadvantageto
elder chicks of many siblicidal species (see
above);both studiesfound that hatching asynchronies of obligately siblicidal specieswere
longerthan thoseof facultativelysiblicidalcongeners.Mock and associates
found that the degreeto which food deliveredby parentscanbe
monopolized explains variation between two
ardeid speciesin the probability of siblicide
(Mock 1984, 1985, Mock et al. 1987a, Mock et
al. 1987b);however, whether parentsactively
manipulatefood monopolizabilityas a regulatory mechanismis unknown.
In this study,I presentcomparativedatafrom
two siblicidal booby speciesof potential influ-
encesof sibling aggression.My goal is to identify mechanismsthat parentsuseto regulatethe
outcomeof sibling aggression,and to test the
hypothesisthat differencesin regulatorymechanisms
contribute
to differences
in the social
systemsof thesespecies.
THE STUDY SYSTEM
Masked Boobies(Sula dactylatra)and Blue-footed
Boobies(S. nebouxii)are colonial, ground-nesting, piscivorousseabirdsthat breed sympatricallythroughout most of the Blue-footedBooby'srange (Nelson
1978). Blue-footedBoobieslay one to four eggsper
clutch (usually two) and are faculatively siblicidal;
first-hatchedchicks("A-chicks")kill youngersiblings
in times of food stress(Drummond et al. 1986, Drummond and Garcia Chevelas 1989). Nonetheless, more
than one offspring often (Nelson 1978) or usually
fledge(66%in caseof Drummond et al. 1986).Masked
Boobieslay one- or two-egg clutches,and are obli-
861
gatelysiblicidal.If both eggshatch,the A-chick ejects
the second-hatched chick ("B-chick") from the nest
scrape,and the victim dies from exposureor predation. The timing of siblicidealso differs;the average
age at death of victim Blue-footedBoobiesis 18 days
(Drummond et al. 1986),while that of Masked Booby
victims is 1.8 days (Anderson 1989a).Masked Booby
parentsare preventedfrom fledging two offspringby
unrelenting sibling aggression(Nelson 1978,Anderson 1989a); the insurance value of the second egg
againstthe first egg'sfailure to hatch apparently explains why they lay two eggs (Dorward 1962, Anderson1990a).Somedatasuggestthat parent Masked
Boobiescouldprovide enoughfood for two surviving
nestlings (Anderson 1990b, Anderson and Ricklefs
1992),but A-chicks do not permit parentsto try. Even
if the parents could suppresssiblicide behaviorally,
both parentsare absentfrom the nest site for up to 8
h daily in experimentally-managedtwo-chickbroods
(Anderson 1990b). During these periods a subordinate has no protectionfrom its sibling'sattacks.Parents avoid investing in a doomed offspring and Achicksexpendlesseffortwhen siblicideoccursshortly
after hatching of the B-chick.
A previousexperimental study showed that the degree of hatching asynchronyinfluenced the probability and timing of siblicidein MaskedBoobies(Anderson 1989a).Broodshatching at intervals of at least
4 daysvirtually alwayslostthe B-chickwithin 20 days
(total nestling period ca. 100 days);the averagetime
to brood reduction was 1.8 days. Early brood reduction becameincreasinglyunlikely as hatching asynchrony was decreasedfrom three to one days in experimental broods.As expectedunder the "doomedoffspring"scenarioabove,the meanhatchinginterval
in Masked Booby broods was 5.4 days (range 3-10
days),abovethe "early reductionthreshold"(Anderson 1989a)of 3 days.Anderson (1989a)also showed
that hatching intervals of Blue-footedBoobies(:• =
3.5 days) were significantly shorter than those of
Masked Boobies, but that more than 50% of Blue-
footed Boobybroodshatched at intervals exceeding
the three day early reductionthreshold.A Masked
BoobyB-chickhatchesfour daysafter its sibling and
can expectto be killed within three daysof hatching.
However, a Blue-footedBooby B-chick in a similar
situationin the Galfipagos
will probablyfledge,if it
escapespredators(Anderson 1989a, 1991, Anderson
and Hodurn 1993)and bad weather (this paper). The
degreeof hatching asynchronyis the primary regulatoryvariableinvestigatedin studiesof aviansibling
competition,but it cannot explain the qualitative differencebetween the socialsystemsof these two siblicidal species.
A MaskedBoobyA-chick ejectsits sibling by grasping in its beak the sibling'sneck, appendage,or skin
and extending its neck to thrust the B-chick across
the nest scrape.Then, an A-chick often repeatsthe
thrust after moving its own body 2 to 10 cm toward
862
DAVIDJ. ANDERSON
the displacedB-chick.A seriesof thrustsoften moves
the B-chick from the shade castby the parent. Behavioral data, both observational (Nelson 1978:565,
this study) and experimental(Lougheed1995),show
that hatchlingBlue-footedBoobyA-chicksdisplaythe
same behavior, but at lower frequency and without
lethaloutcome.Experimentalcross-fostering
of chicks
of one speciesinto nests of the other speciesdemonstratedthat both parentsand chicksplay regulatory
roles vis-a-visexpressionand outcomeof sibling aggression(Lougheed1995).In the presentstudy,I focuson parentalinfluencesthat facilitatethe B-chick's
ejectionin MaskedBoobybroodsand suppressit in
Blue-footedBoobybroods.
MATERIALS AND METHODS
Data presented here were collected from 1984
through 1986 as part of a long-term study of the
breeding ecologyand behavior of Masked and Bluefooted boobiesat Punta Cevallos,Isla Espafiolain the
GallpagosArchipelago(for detailsof studysite,see
Anderson and Ricklefs 1987). This period fell between
the
E1 Nifio-Southern
Oscillation
events
of
1982-1983 and 1986-1987 (Anderson 1989b). My assistants and I recorded
nest histories
and measured
chick growth of approximately250 Masked Booby
and 100Blue-footedBoobybreedingattemptsin each
season.We checked nests daily between 1200 and
1430,markednewly laid eggs,andweighedand measuredchicksdaily until the ageof 10 days.We measuredthe maximumlength and breadthof eachegg,
andapproximatedthe egg'svolumewith the equation
[Auk, Vol. 112
gressionor of their own disorientation.Thus, hatching asynchronyand time required for brood reduction were measuredin increments of one day.
Both specieslay their eggsdirectly on the ground
in circular nest scrapesthat have been cleared of debris. I measured
the diameters
of 75 Blue-footed
Boo-
by and 45 Masked Boobynest scrapesby placing a
meter stick acrossthe scrapeat its maximum diameter
and recordingthe distancebetweenpointsof contact
with the ground. A secondmeasurementwas made
horizontally perpendicular to the first, and the av-
erageof the two wastakenasthe nest'sdiameter.The
maximum depth was measured at the center of the
scrapewith another ruler held perpendicularto the
horizontal meter stick. The nest scrape'smaximum
steepness
(r, the angle in degreesmadeby horizontal
plane and tangent to surfaceof scrapewhere surface
nearsground level) is approximatedby
I • = 180ø - 2[tan-•(R/D)],
(2)
where R is the radius (cm) and D is the maximum
depth (cm; seeAppendix for a proof).
Statisticalanalyseswere done with SYSTAT (SYSTAT, Inc. 1984), CSS:STATISTICA (StatSoft, Inc. 1991),
and STATISTICA (StatSoft,Inc. 1994) software. Stepwise multiple regressionsof dependentvariableson
hatchinginterval and egg-volumeratio attemptedto
include hatching interval in the model first, at a-toenter = 0.15, where a is determined by an independentvariable'st-value(e.g.Neter andWasserman1974:
386).
RESULTS
V = •rLB2/6,
(1)
where V is volume (cc), L is length (cm), and B is
breadth (cm; Preston 1974). We measuredchick masses with Pesolaspring scales;wing length was measured by holding the metacarpalsat a right angle to
the radius and ulna, and straightening the manus or
longestprimary. The A- and B-chickswere individually identified using ink spots we placed on the
head,plumagedevelopment,and, after about30 days
of age,their U.S. Fish and Wildlife Servicealuminum
leg bands. I excludedfrom analysespresentedhere
three three-eggBlue-footedBoobyclutches,and two
Masked Boobybroodsin which brood reduction did
not occurby 20 days after the B-chickhatched(see
Anderson 1989a).
A chickwas recordedashatchedat a given midday
nestcheckwhen the chickwascompletelyoutsideits
egg shell, or the chick was still attachedto the egg
shell but had split the eggshell into two halves.Brood
reduction
was recorded when a chick was absent from
its nest scrapeat a particular day's nest checkand,
subsequently,
did not return;frequently,chicksof
bothspeciesreturnedto their nestscrapeafterbeing
recordedoutsidethe scrapeas a result of sibling ag-
Egg-volume
differences.--Variation
in egg size
explainssignificantvariation in the posthatch-
ing growth rate of somebird species,and differencesin egg size within a clutch could influence
the
outcome
of
siblicidal
behavior
throughan effecton body-sizedifference(Anderson 1989a).To do so, egg volume must influencebody size.In order to explain interspecific differences in siblicidal behavior, the two
speciesmust have different egg-volumeratios.
Eggvolumeexplains46.4and50.9%of variation
in hatching massof Masked and Blue-footed
boobies,respectively,and the effectdecayswith
increasingage but remainssignificantat least
througheight daysof age(Table1).Egg-volume
ratios(i.e. volumeA-egg/volumeB-egg)of the
two speciesdiffer in associationwith the broodreduction system: Masked Booby A-eggs usu-
ally were largerthan B-eggs(Anderson1990a),
while 24.4%of Blue-footedBoobyA-eggswere
the smallerof the two (Fig. 1, Table 2). A twoway ANOVA, with speciesand year as main
October 1995]
Siblicidein Boobies
Blue-lootedBoobies
MaskedBoobies
70
863
the hatching-massratio on hatching interval
and egg-volume ratio showed,that both independent variables accounted for significant
variation in the hatching-massratio in Masked
Boobies(hatching asynchrony, t = 5.54, P <
60
0.001; volume ratio, t = 2.91, P = 0.005), but not
in Blue-footed Boobies (volume ratio did not
4o
enter model at P = 0.15). Thus, the egg-volume
ratio appearsto favor A-chicks in Masked Boobies,
but favors neither chick consistentlyin
• 2o
Blue-footedBoobies.However, the egg-volume
lO
ratio had no significant effect on an indicator
of competitiveadvantage(i.e. number of days
o
Masked BoobyA-chicks required to kill their
siblings). In a multiple regressionof days to
brood reduction on hatching asynchrony and
egg-volumeratio, the effectof egg-volumeratio
Egg-volume Ratio
was not significant (t = 0.18, P = 0.86).
Fig. 1. Frequencyhistogram of egg-volume ratios
Rather than indicating adaptive differences
(volume of A-egg/volume of B-egg) for Masked (n =
in the brood-reduction system,the differences
171) and Blue-footed(n = 74) booby clutches.
between the species in the egg-volume ratio
may be proximate phenotypic effectsof differencesin food supply. Blue-footedBoobieslay
effects,revealeda significantspecieseffect(F•,239 larger clutches,raise larger broods,and make
= 24.91,P < 0.001).MaskedBoobieshad a larger shorter foraging trips than do Masked Boobies
mean egg-volume ratio than did Blue-footed (Nelson 1978, Anderson and Ricklefs 1987), all
3o
Boobies (œ= 1.11 + SD of 0.11, and œ= 1.03 ___ consistentwith greaterfood availability for fe-
of 0.07,respectively;
seeTable 2).
male
Hatching interval explains significant variation
in the ratio
of the A-chick's
mass to the
B-chick'smasson the day of the B-chick'shatching (hatching-massratio; r 2 = 0.41 for Masked
Boobies, r 2 = 0.39 for Blue-footed Boobies;An-
Blue-footed
Boobies
than
for
female
Masked Boobieswhen allocatingphysiological
resourcesfor secondeggs. If so, Blue-footed
Booby B-eggs should vary less in size across
yearsthan thoseof MaskedBoobies;data from
1984through 1986supportthis prediction.The
derson1989a).Stepwisemultiple regressionof
volume of A-eggs in two-egg Masked Booby
TABLE1. Proportionsof variance (r2-values)in body
size(asindicatedby massor wing length) explained
by variation in egg size. Only A-chicks from twoegg clutchesused so as to minimize variation due
to parent quality.
clutchesdid not vary significantly acrossthe
three years (F2,•68
= 1.66, P > 0.05), while that
of B-eggsdid (F•,•s= 8.36, P < 0.001);neither
A-/nor B-eggvolumesof Blue-footedBoobies
were heterogeneousacrossyears (A-eggs, F•,•
= 0.46, P > 0.05; B-eggs,F•,• = 0.33, P > 0.05).
As a result, the egg-volume ratio was hetero-
Masked Booby
Age
(days)
0a
2
4
6
8
10
Mass
Wing
length
0.464*
0.163'
0.110'
0.139'
0.154'
0.068*
0.050*
0.083*
0.062*
0.032
0.050*
0.042
Blue-footedBooby
Mass
0.509*
0.722*
0.387*
0.444*
0.382*
0.021
geneousacrossyearsfor Masked Boobies(F2,]•
= 6.40, P < 0.01), but not for Blue-footed Boo-
Wing
length
bies (F•;• = 0.16, P > 0.05).
0.179'
0.449*
0.090*
0.120
0.400*
0.266*
Nest-shape
differences.--Both
speciesnest on
the ground, but while MaskedBoobiessimply
clear debris from a nest site and deposit eggs
there, Blue-footedBoobyeggsand small chicks
are containedwithin a bowl-shapeddepression
* P < 0.05.
ßRegression
equationsof mass(M, in g) on eggsize(E,in cc)for age
0 days:MaskedBooby,M = 0.820E 5.081(significance
of slope,Ft,•
= 76.2,P < 0.001;of intercept,t = 0.78,P > 0.08);Blue-footedBooby,
M = 0.583E- 9.867(significance
of slope,Fx,•t= 32.2, P < 0.001;of
intercept,t = 1.60,P > 0.08).
(Nelson 1978:plate 12). On two occasionsdur-
ing nestwatches,I observedBlue-footedBooby
A-chickspushingtheir hatchlingsiblingsfrom
under the brooding parent in the manner of
Masked Boobychicks(unpubl. data). However,
864
D^VID J. ANDERSON
[Auk, Vol. 112
TABLE
2. Mean egg volumesand egg-volumeratios(+SD) for two-eggboobyclutches.Mean egg-volume
ratiosdiffer fromratioof meanA-volumeto meanB-volumebecause
A- andB-eggvolumescovary(Anderson
1989c; see Welsh et al. 1988).
Volume (cc)
Year
n
A -egg
1984
1985
1986
66
46
59
70.68 + 5.44
68.82 + 4.53
69.80 + 5.78
1984
1985
1986
45
18
11
59.24 + 5.30
60.15 + 5.70
60.84 + 5.83
Egg-volume
ratio
B-egg
Masked Booby
65.64 + 5.43
62.16 + 6.12
61.40 + 6.92
1.079 + 0.058
1.113 + 0.089
1.148 + 0.156
Blue-footed Booby
in both casesthe Blue-footed Booby B-chicks
rolled down the steep sidesof the nest into the
shade of the parent when releasedby the Achick, suggestingthat parents could use nest
shapeto influence the outcomeof the A-chick's
efforts.Specifically,obligatelysiblicidalMasked
Boobieswill facilitate early siblicideby using a
flat nest,and facultativelysiblicidalBlue-footed
Boobieswill suppressearlysiblicidewith a steepsided, bowl-shaped nest.
A two-wayANOVA of I', the maximumsteepnessof the nest scrape,with speciesand nestage class(10- to 13-dayintervalssincelaying of
first egg;seeFig. 2) asmain effects,showedthat
Blue-footed Booby nests were significantly
steeperthan were Masked Boobynests(species
effect,F•,•32= 64.1, P < 0.001). This difference
33
30
ß Blue-lootedBooby
ß Masked Booby
27
57.42 + 5.03
58.48 + 5.55
58.29 + 5.25
1.034 + 0.072
1.030 + 0.030
1.045 + 0.068
was most marked preceding and during the 44to 53-day age class,when Masked Boobysiblicide occurs. Blue-footed Booby chicks in this
age classwere in wider (radius of 175 vs. 127
mm, t = 4.36, df = 14, P < 0.001) and deeper
(44.7 vs. 21.6 mm, t = 4.71, df = 14, P < 0.001)
nest scrapesthan were Masked Booby chicks.
This is a meaningful differenceto a highly altricial (i.e. feeble) nestling with a body length
of 15 mm. A chickattemptingto evict its sibling
from a Blue-footed Booby nest would face a
slope 64% steeper and 38% longer than would
a chick in a Masked Boobynest.
In comparisonto ground-nestingseabirdspecies that are not obligately siblicidal, Masked
Boobieshad the flattest nests measured (Table
3), further suggestinga link between nest steepnessand the brood-reductionsystem.Masked
Boobyparentsused existing slight depressions
as nest-scrapelocations,but Blue-footedBooby
parents actively excavatedand regulated bowl
depth. This point was demonstrated experimentally with eight Blue-footedBoobynestsat
the eggstageby filling them with dirt and pack-
ing the fill. The nests'dimensionswere measuredthree timesin the subsequent48.5 h, and
the measurementscomparedwith the original
24
21
e
18
nest dimensions.
(/'3
15
tently affectedby the manipulation.Nest depth
was initially significantly different from the
12
Nest
width
was not
consis-
original depth, but returned gradually to the
original dimensionswithin 48.5 h (Table 4).
Nest Age (days)
When I' valueswere classedby time sincethe
(I•) of MaskedandBlue- eggswere laid (Fig. 2), variation acrossageclass
Fig.2. Maximumsteepness
=
footedboobynestsin relation to time sincelaying of was significant in Blue-footed Boobies(F6,9o
nest'sfirstegg.Eggshatchedat approximately44 days. 3.19,P < 0.01), but not in MaskedBoobies(Fs,•
Period of Masked Boobysiblicideindicatedby shad- = 1.41, P > 0.05). Blue-footed Booby parents
ing. Data presentedas œ+ SE.
were remarkablyattentive to the shapeof their
0-12
13-22
23-33
34-43
44-53
54-63
64-73
October 1995]
865
Siblicidein Boobies
TABLE
3. F-values(• + SD with n in parentheses)for ground-nestingseabirds.
Nesting-cycle
stage
Species
Single-egg,single-chickspecies
Red-tailedTropicbird(Phaethon
rubricauda)
Egg
Hatchling
P (degrees)
Source
a
32.4 + 6.0 (18)
29.2 + 3.9 (8)
1
1
54.6 + 10.6 (16)
64.9 + 3.6 (7)
63.6 (21)
65.6 (21)
24.8 + 4.6 (51)
29.5 + 3.7 (48)
2
2
3
3
4
4
17.8 + 3.4 (27)
18.0 + 4.5 (17)
4
4
Multiple-chick species
Cape Cormorant (Phalacrocorax
capensis)
Crowned Cormorant (P. coronatus)
Egg
Egg
Egg
Hatchling
Egg
BankCormorant(P. neglectus)
Blue-footedBooby
Hatchling
Obligately siblicidal species
Egg
Hatchling
MaskedBooby
ßSource:(1) D. J. Anderson,unpublished
datafrom Johnston
Atoll, CentralPacificOcean;(2) R. E. Ricklefs,unpublisheddatafrom Malgas
Island,South Africa;(3) Cooper 1986;(4) this study.
nests. Parents restored their experimentally
filled neststo a steepnessthat closelymatched
the original steepness(Spearmanrank correlation, r = 0.93, n = 6, P < 0.01). In nonexperimental nests,F increasedimmediatelyprior to
hatching, with peak values and lowest variability during the critical period in which siblicide occursin MaskedBoobynests(i.e. during
the first 10daysafter hatching),but not in Bluefooted Boobynests(Fig. 2). I did not attempt to
lingswere partially submergedin a pool of water, and Masked Booby hatchlings were completely dry. In 1986,rain fell on 25 of the total
daysthat I was presenton the island (Fig. 3).
The totalaccumulationduring 17 of thosedays
was lessthan 10 mm; little mortality occurred
of Blue-footedBoobynestlingsof 20 days or
less(threedeaths).On the remainingeightdays,
10 to 43 mm were recordeddaily, filling Bluefooted Booby nests with water and causing
observe the behavior used to form nest bowls.
hatchlingbody temperaturesto drop (pets.obs.).
However,the soil in Blue-footedBoobynesting On theseeight days,17 Blue-footedBoobynestareasis dry and fine-grained,and easilycanbe lings of 20 daysor lessdied (Fig. 3). Causesof
excavatedwith a tool resemblinga booby'sfoot mortality other than hypothermia(e.g. predation and starvation) could be ruled out in most
(K. Huyvaert unpubl. data).
Blue-footedBoobynest steepnessis greatest of these17 cases.Nestlingsolder than 20 days
at preciselythe time that steepnessis required were not affectedby heavy rainfall: only 2 of
for suppressionof hatchling siblicide,and is 24 (0.08) deathsin this age group occurredon
lesssteepand deep at other times (Fig. 2). I dayswith at least10mm of rain, comparedwith
identified a possiblecost to maintenanceof a 17 of 32 (0.53) deaths in the 0- to 20-day age
deep nest: hypothermia of hatchlingsduring group.
heavy rains, when Blue-footed Booby hatchI comparedthe mortality rates of nestlings
TAnrE4. Nestshapes(widthand length,• + SD;ram)followingexperimental
filling of Blue-footed
Booby
nest scrapes.An egg hatchedin two nestsbefore the secondmeasurement;thesenestsnot measuredafter
hatching occurred.
Hours
after
Paired
filling
of
nest
Paired
comparison
n
Width (ram)
t
comparison
P
Depth (ram)
t
P
Original
8
298.8 + 41.9
--
--
29.0 + 5.42
--
--
4.5
24.5
48.5
8
6
6
284.5 + 36.2
270.0 + 27.2
293.3 + 28.8
1.35
2.91
1.38
>0.20
<0.05
>0.10
15.6 + 6.55
24.2 + 6.68
31.8 + 5.91
6.30
2.36
0.06
<0.001
0.07
>0.90
866
D^VIDJ. ANDERSON
50
[Auk,Vol. 112
prior to hatching,Blue-footedBoobynestswere
still steeperthan Masked Boobynestsduring
the first four nest age classes(Fig. 2; two-way
ANOVA, nest age classand speciesas main effects;specieseffect F•,70= 32.52, P < 0.001).
•,• 30
r•
10
DISCUSSION
• •o
Jan
1 Feb
1 Mar
1 Apr
1 May
Fig. 3. Rainfall (above) and Blue-footed booby
nestling mortality for birds in 0- to 20-day age class
in 1986.
from the 0- to 20-dayagegroupthat were present on a given day as a function of rainfall on
that day. I useddata from the period of 6 January through 7 March only, becauseafter 7
March the number of nestlingsin this age group
never exceededthree, reducing the precisionof
the mortality-rate estimate. During the 6 January to 7 March period, the number present
averaged11.4+ 5.8 nestlingsper day. A higher
proportion of these nestlings present died on
dayswith at least I0 mm of rain than died on
dayswith lessthan I0 mm (mean arc-sintransformed daily proportions were 0.39 and 0.03,
respectively;t = 7.44, df = 68, P < 0.001).This
test is conservativewith respectto the conclusionthat rainfall and mortality are linked, given
that three of the four deaths that occurred
after
7 March happenedon dayswith at least I0 mm
of rain.
Masked
Boobies
in
their
flatter
nests
re-
mained dry during rainfalls, and none of the
17 deathsof A-chicksin the 0- to 20-day posthatching age group occurredon days with at
least I0 mm of rainfall. Blue-footedBoobyparents that had nests characteristic
My goal was to identify factorsthat contribute to the differences
Date
of Masked
Boo-
bies might have similarly low hatchling mortality, but the limited variation in Blue-footed
Boobynest shapearound the time of hatching
(Fig. 2) did not allow that comparison.However, nest shapesof Blue-footedBoobiesprior
to hatching were consistentwith regulation toward flatness:a one-wayANOVA of F showed
significantheterogeneityacrossnestageclasses
(F6,90
= 3.19, P < 0.01), and nestswere consistently flatterprior to hatchingthan during and
shortly after hatching (Fig. 2). Masked Booby
F-valuesdid not showsimilarheterogeneity(Fs,•
= 1.41,P = 0.24).In spite of the relative flatness
between
Masked and Blue-
footed boobies in their brood-reduction systems. I detected no contribution
of within-clutch
egg-sizedifferences,althoughinterspecificdifferencesin this factorare consistentwith a regulatoryrole.However,a novel factor,nestshape,
differs between the two species:Blue-footed
Boobynests,like thoseof other ground-nesting
seabirdssampled,have steepsidesthat impede
ejectionby hatchling chicks,but Masked Boobies have atypicallyflat nests,facilitatingejection. Moreover,nestshapeis closelyregulated
by Blue-footedBoobiesin a manner that should
suppresssiblicidal ejection of hatchling offspring.
Comparativestudiesallow one to testthe hypothesisthat regulatorymechanismsare adapted to maximizereproductivesuccess.
Two studies have approachedthis issue by comparing
hatching asynchroniesof obligately and facultatively siblicidal eagles (Edwards and Collopy 1983)and boobies(Anderson 1989a).Both
found that parentsof obligately siblicidal species hatched eggsat longer intervals (thus establishing more biasedcompetitive hierarchies)
than did parentsof facultatively siblicidal species.Becauseobligatelysiblicidal offspringprevent parentsfrom raising more than one chick,
even with short hatching intervals (Anderson
1989a),thesedataare consistentwith a hypothesisof adaptive adjustmentof hatching asynchrony that cutslossesearly. However, they are
alsoconsistentwith a proximate-levelhypothesis that the food limitation
that restricts brood
size also restrictsthe rate of egg formation.
The contrastingnestshapesof parentMasked
and Blue-footed
boobies offer clearer evidence
of an adapted regulatory mechanismthat has
respondedevolutionarily to both costsand benefits.The differenceis not explainedby the most
likely alternative hypotheses. For example,
thermalconsiderationssuggestthat nestlingsin
the hotter
environment
should
have
a flatter
nest to increaseexposureto air flow. The study
site is equatorial,and both speciesnest in ther-
October 1995]
Siblicidein Boobies
mally stressfulsituations,but the pattern is the
oppositeof that predicted:Masked Boobieshave
significantlycooler,windiet nest sitesthan do
Blue-footed Boobies(Anderson et al. unpubl.
manuscript).Another alternativehypothesisin-
867
G. Hunt, Jr., D. Mock, R. Ricklefs, D. Rubenstein, J.
Smith, and D. Westneat for comments on an earlier
version of the manuscript;and P. Petraitisfor statistical advice.
volves the nature of the substrate:possiblya
LITERATURE CITED
bowl-shapednest is optimal for both species,
but perhapsthe soil in Masked Boobycolonies AMUNDSEN,T., ANDJ. N. STOKLAND.1988. Adaptive
does not permit formation of a bowl. Masked
and Blue-footedboobiesdo show nesting segregation into different areas (Duffy 1984), but
the easeof digging in the two areasis not substantially different. A similar degreeof digging
effort yields a hole approximately20%shallower in Masked Boobyareasthan in Blue-footed
Booby areas (Anderson et al. unpubl. manuscript), but the difference in nest depths that I
found in this studyapproached100%at the time
of hatching.
In conclusion,hatching asynchronyclearly
influences the speed of obligate siblicide in
Masked Boobies,but cannot provide a proximate-levelexplanationfor the differencein social systemsbetween Masked and Blue-footed
boobyhatchlings(Anderson1989a).Hatchlings
of both speciesare capableof siblicidal behavior, but Blue-footedBoobyA-chicks face a sig-
nificantobstacleto ejectingsiblingsin the wider, steepernestbowl than MaskedBoobychicks
face. Experimentalmodificationsof nest shape
in thesetwo speciesthat do not disturb parents
and especially during periods of heavy rain
would complementthis comparativeapproach
to costsand benefitsof nest steepness.Manipulation of the "arena" in which sibling aggression occurshasnot been suggestedpreviously
as a mechanismfor regulating the outcomeof
the interactions;this appearsto have a proximate effect on brood size in these two species.
ACKNOWLEDGMENTS
significanceof asynchronoushatching in the
Shag:A test of the brood reductionhypothesis.
J. Anim. Ecol. 57:329-344.
ANDERSON,
D. J. 1989a. The role of hatching asynchrony in siblicidalbrood reductionof two booby species.Behav.Ecol.Sociobiol.25:363-368.
ANDERSON,
D. J. 1989b. Differential responsesof
boobiesand other seabirdsin the Gal•pagosto
the 1986-87 E1 Nifio-Southern
Gal•pagos,and in particularto S. Harcourt,for lo-
event.
hypothesis.Am. Nat. 135:334-350.
ANDERSON,
D.J. 1990b. Evolution of obligate sibli-
cide in boobies.2: Food limitation and parentoffspringconflict.Evolution 44:2069-2082.
ANDERSON,
D. J. 1991. Apparent predator-limited
distributionof Gal•pagosRed-footedBoobiesSula
sula. Ibis 133:26-29.
ANDERSON,D. J., m',lD P. J. HODUM. 1993. Predator
behaviorfavorsclumped nestingin an oceanic
seabird. Ecology 74:2462-2464.
ANDERSON,D. J., m,ao R. E. RICKLEFS. 1987. Radio-
tracking Masked and Blue-footed boobies (Sula
spp.)in the Gal•pagosIslands.Natl. Geogr.Res.
3:152-163.
ANDERSON,D. J., m,ao R. E. RICKLEFS. 1992. Brood
size and food provisioningin Maskedand Bluefootedboobies(Sulaspp.).Ecology73:1363-1374.
BRAUN,B. M., AND G. L. HUNT, JR. 1983. Brood re-
ductionin Black-leggedKittiwakes.Auk 100:469476.
CASH, K. J., AND R. M. Evm',ls. 1986. Brood reduction
in the American White Pelican (Pelecanus
erythrorhynchos).
Behav.Ecol. Sociobiol. 18:413-418.
COOPER,
J. 1986. Biologyof the BankCormorant,part
4: Nest construction
I am grateful to the staff of the Charles Darwin
ResearchStationand the ServicioParque Nacional
Oscillation
Mar. Ecol. Progr. Ser. 52:209-216.
ANDERSON,
D. J. 1990a. Evolution of obligate siblicide in boobies.1. A test of the insurance egg
and characteristics.
Ostrich
57:170-179.
DICKtNS,
D. W., ANDR. A. CLARK.1987. Gamestheory
andsiblicidein the kittiwakegull, Rissatridactyla.
gisticalsupport during fieldwork and to R. Ricklefs
J. Theor. Biol. 125:301-305.
for sharingunpublisheddata. Fieldwork was supported by the National GeographicSociety,Sigma
Xi--the ScientificResearch
Society,a Universityof
MichiganBlockGrant,the FrankM. ChapmanFund,
and the GeorgeD. Harris Fund. I wassupportedby
DRUMMOND, H.,AND C. GARCIA-CHq.
1989. Food
shortageinfluencessiblingaggression
in the Bluefooted Booby.Anim. Behav.37:806-819.
DRUMMOND,H., E. GONZALEZ,ANDJ. L. OSORNO. 1986.
an NSF Pre-doctoralFellowship during parts of this
Parent-offspringcooperationin the Blue-footed
Booby(Sulanebouxii):
Socialroles in infanticidal
work. I thank: R. Brubaker, L. Hamilton, P. Hodurn,
brood reduction.
R. Ricklefs,and especiallyS. Fortner for their field
assistance;
D. Cheney, D. Duffy, A. Dunham, F. Gill,
372.
DUFFY,D.C.
Behav. Ecol. Sociobiol.
19:365-
1984. Nest site selection by Masked
868
DAVID J. ANDERSON
and Blue-footedboobieson Isla Espafiola,Gal•pagos.Condor 86:302-304.
EDWARDS
T. C., AND M. W. COLLOP¾.1983. Obligate
and facultativebrood reduction in eagles:An examination
of factors that influence
fratricide.
Auk
100:630-635.
FORnES,L. S., AND R. C. YDENn•RG. 1992. Sibling
rivalry in a variable environment. Theor. Popul.
[Auk, Vol. 112
cific test of the prey-sizehypothesis.Anim. Behav. 35:1386-1393.
NEI_SON,
J.B. 1978. The Sulidae. Oxford Univ. Press,
Oxford.
NETER,J.,AND W. W,•.SSERMAN.
1974. Applied linear
statistical models. Richard D. Irwin, Inc., Homewood, Illinois.
O'CONNOR,R.J. 1978. Brood reduction in birds: Selection for fratricide,
Biol. 41:135-160.
FUJIOKA,
M. 1985. Sibling competitionand siblicide
in asynchronously-hatching
broodsof the Cattle
Egret Bubulcus
ibis.Anim. Behav.33:1228-1242.
HAGEN,J. M. 1986. Temporal patterns in pre-fledging survival and brood reduction in an Osprey
colony.Condor88:200-205.
HAHN, D.C. 1981. Asynchronoushatching in the
LaughingGull: Cutting lossesand reducing rivalry. Anim. Behav. 29:421-427.
HEnERT,
P. N., AND R. M. R. BARCt.
A¾. 1986. Asynchronousand synchronoushatching:Effect on
Anim.
infanticide,
and suicide?
Behav. 26:79-96.
PARSONS,
J. 1970. Relationshipbetweeneggsizeand
post-hatchingchickmortality in the Herring Gull
(Larusargentatus).
Nature 228:1221-1222.
PARSONS,
J. 1975. Asynchronous
hatchingand chick
mortality in the Herring Gull, Larusargentatus.
Ibis 117:517-520.
PLOGER,
B. J.,ANDD. W. MOCK. 1986. Role of sibling
aggression
in fooddistributionto nestlingCattle
Egrets(Bubulcus
ibis).Auk 103:768-776.
POOLE,
A. 1979. Sibling aggressionamong nestling
Ospreysin Florida Bay.Auk 96:415-416.
early growthand survivorshipof Herring Gull,
F.W. 1974. The volume of an egg.Auk 91:
Larusargentatus,
chicks.Can.J.Zool. 64:2357-2362. PRESTON,
HESERT,P. N., AND R. M. R. BARCt.•¾. 1988. Parental
investmentin Herring Gulls: Clutch apportionment and chick survival.
Condor
132-138.
RICKLEFS,R.E.
billed
90:332-338.
1965. Brood reduction in the Curve-
Thrasher.
Condor
67:505-510.
INOUE,Y. 1985. The processof asynchronous
hatching and sibling competition in the Little Egret
Egrettagarzetta.Colon. Waterbirds8:1-12.
SKAGEN,
S.K. 1987. Hatching asynchronyin American Goldfinches:An experimental study. Ecology 68:1747-1759.
JOV•R,L., X. RU•Z, AND M. GONZaLEz-MARTiN. 1993.
SLAGSvOLD,
T., J. SANDVIK,G. ROFSTAD,O. LORENTSEN,
Significanceof intraclutch egg size variation in
the Purple Heron. Urnis Scand.24:127-134.
LACK,D. 1954. The natural regulation of animal
numbers. Clarendon Press, Oxford.
LOUGHEED,
L. W. 1995. Proximate level investigations of behavioral reproductive tacticsof two
Galfipagos
boobyspecies.M.S. thesis,WakeForest Univ., Winston-Salem, North Carolina.
MAGRATH,R. D. 1992. Roles of egg massand incubation pattern in establishmentof hatching hierarchies in the Blackbird (Turdus merula). Auk
109:474-487.
MOCK, D. W. 1984. Siblicidal aggression and resourcemonopolizationin birds.Science225:731-
685-697.
STATSOFt, INC. 1991. CSS:STATISTICA, version 3.1.
StatSoft, Inc., Tulsa, Oklahoma.
STATSOFt, INC. 1994. STATISTICA for Windows,
version 4.5. StatSoft, Inc., Tulsa, Oklahoma.
STINSON,
C. H. 1979. On the selectiveadvantageof
fratricide in raptors. Evolution 33:1219-1225.
STOKLAND,J. N., AND T. AMUNDSEN. 1988. Initial size
hierarchyin broodsof the Shag:Relativesignificanceof eggsizeand hatchingasynchrony.Auk
105:308-315.
SYSTAT,INC. 1984. SYSTAT,the systemfor staffstics, versions 1.1 and 1.3. SYSTAT, Inc., Evanston,
733.
MOCK, D. W. 1985. Siblicidal brood reduction: The
MOCK, D. W., H. DRUMMOND, AND C. H. STINSON.
Avian
siblicide.
Am. Sci. 78:438-449.
MOCK, D. W., T. C. LAMEY,AND B. J. PLOGER. 1987a.
Proximate
and ultimate
roles of food amount
in
regulating egret sibling aggression.Ecology68:
adjustmentin birds: Economicaltracking in a
temporallyvarying environment.J. Theor. BioL
126:137-147.
TmVERS,
R. L. 1974. Parent-offspringconflict. Am.
Zool.
14:249-264.
WELSH, A. H., A. T. PETERSON,AND S. A. ALTMANN.
1760-1772.
MOCK, D. W., T. C. LAM•,
Illinois.
TEMME, D. H., AND E. L. CHARNOv. 1987. Brood size
prey-sizehypothesis.
Am. Nat. 125:327-343.
1990.
ANDM. HUSBY.1984. On the adaptive value of
intraclutch egg-sizevariation in birds. Auk 101:
C. F. WILLImaS, AND A.
PELLL•rlER.
1987b. Flexibility in the development of heron sibling aggression:An intraspe-
1988. The fallacyof averages.Am. Nat. 132:277288.
October
1995]
Siblicide
inBoobies
APPENDIX
C
This proof,in conjunctionwith Figure4, showsthat
the angle FAD (which approximatesthe steepnessof
a nest) can be calculated when the lengths of lines
AD and DE are known
from field measurements.
869
The
stepsin the proof are as follows: (1) Angle AED =
tan-• (AD/DE). (2) Angle ACE = 180ø - 2(AED) becausetriangle ACE is isocelestriangle. (3) Angle ACB
is complementof angle ACD, and angle CAD is complement of angle FAD. (4) Angle ACB equalsangle
CAD becauselines BCand AD parallel, soangle ACD
= angle FAD = angle ACE. (5) Thus, from 1 and 2,
angle FAD = 180ø - 2[tan-• (AD/DE)].
D ••.•//G
ro
u
n•
u
rfa
ce
FJõ.•. Idealized•e•tJcalc•oss-secQo•
o• a boobx
•est. O•IX shaded•e•Jo• existsat actual •est site.
A•ies a•d shapesdescribed
cula•shape•ep•ese•tsassumptJo•
that •est-bowlsu••acesconform to that o• a sectJo•o• a sphere.