Maternal Investment in Eggs Is Affected by Male Feet Colour... Blue-Footed Booby, Sula nebouxii

Maternal Investment in Eggs Is Affected by Male Feet Colour and Breeding Conditions in the
Blue-Footed Booby, Sula nebouxii
Author(s): Fabrice Dentressangle, Lourdes Boeck and Roxana Torres
Source: Behavioral Ecology and Sociobiology, Vol. 62, No. 12 (Oct., 2008), pp. 1899-1908
Published by: Springer
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Behav Ecol Sociobiol (2008) 62:1899-1908
DOT 10.1007/s00265-008-0620-6
ORIGINAL PAPER
in eggs is affectedby male feetcolour
Maternal investment
and breedingconditionsin the blue-footedbooby,
Sula nebouxii
• Lourdes Boeck• Roxana Torres
FabriceDentressangle
Received:21 September2007 /Revised: 14 May 2008 /Accepted:5 June2008 /Publishedonline:5 July2008
2008
© Springer-Verlag
in and volumeand delayedthe layingof the second egg,
AbstractFemales are expectedto vary investment
of theyear.Absoluteyolkandrostenedione
accordingto variablesthatmay influencethe independently
offspring
fitnessin a way thatoptimisesher inclusive (A4) concentration
T) in second
(but not testosterone,
offspring
context.
fitness
fora particular
Thus,whensexualornaments eggs was higherduringa poor yearthanduringa good
signalthe qualityof the male, femalesmightinvestin year.Only duringa yearwithpoor breedingconditions,
males decreasedthe
of their femalespaired with experimental
of the attractiveness
as a function
reproduction
in the secondegg
not
mate.We testedwhetherbreedingconditionsand male relativeA4 concentration
T)
(but
blue-footed
females.
to
control
blue-footed
of
decisions
Thus,
feetcolourinfluence
booby
compared
reproductive
booby,male feetcolour femalesprobablyfavourbrood reductionby decreasing
boobyfemales.In theblue-footed
betweenchicks
size asymmetry
is a dynamiccondition-dependent
sexuallyselectedtrait egg qualityand increasing
are poor.
mate
conditions
thatis relatedto paternaleffort.
Duringtwo consecutive whenthebreedingand the
years,an El Nino year(poor breedingconditions)and a
•
•
•
year withgood breedingconditions,we experimentally KeywordsSexualtraitsEggqualityLayingasynchrony
•
•
effects
theirfeetcolour YolkandrogensSula nebouxiiMaternal
reducedmaleattractiveness
by modifying
femaleinvestment
afterthefirstegg was laid and recorded
in thesecondegg. We foundthat,relativeto thefirstegg
in theclutch,femaleslaid heaviersecondeggs duringthe Introduction
pooryearthanduringthegood year.Femalespairedwith
in offspring
males withdullerfeetcolour reducedsecond-eggmass Females are expectedto vary investment
the
influence
that
offspring
may
accordingto variables
fora
fitness
inclusive
her
that
in
a
fitness
optimises
way
Communicated
by J. Graves
context(Mousseauand Fox 1998a,b; Christians
particular
• R. Torres(M)
F. Dentressangle
et al. 2003; Sockmanet al. 2006; Sheldon
Verboven
2002;
de Ecologia Evolutiva,
Institute
de Ecologia, Departamento
in somebirdspecies,femalesallocate
2000).
Accordingly,
Laboratoriode ConductaAnimal,
both
resourcesin relationto variablesthatmayinfluence
UniversidadNacional Autonomade Mexico,
AP 70 275,
suchas environmental
andthemother
theoffspring
fitness,
Mexico, DF 04510, Mexico
conditions(Mousseau and Fox 1998a, b; Gil 2003, Gil
e-mail:[email protected]
et al. 2004a), breedingdensity(Mazuc et al. 2003; Müller
et al. 2004) and chicksex (Mülleret al. 2003; Saino et al.
L. Boeck
Laboratoriode HormonasEsteroides,
when sexual ornaments
signal the
2003). Furthermore,
Biologia de la Reproduction,
qualityof themale,femalesmightadjustthelevelof their
Nacional de Ciencias Médicas y de la Nutriciôn,
Institute
of theattractiveas a function
in reproduction
investment
SalvadorZubiran,
allocationhypothesis,
nessoftheirmate(differential
Burley
Mexico, DF, Mexico
& Springer
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1900
Behav Ecol Sociobiol (2008) 62: 1899-1908
and
in some birdspecies,females withbrightgreen-bluefeet,have betternutritional
1986, 1988). Accordingly,
in eggs healthconditioncomparedto maleswithdullerblue feet,
males modifyinvestment
pairedwithattractive
can changein less than48 h ifno food
producinglargereggs (Cunninghamand Russell 2000; and feetcoloration
is provided(TorresandVelando2003; Velandoetal. 2006).
Ulleretal. 2005) orvarythelevelsofyolktestosterone
(Gil
et al. 1999,2004b; Tanvezet al. 2004), antibodies(Saino A cross-fostering
experimentshowed that blue-footed
withthe feetcolour
conditioncorrelates
et al. 2002a) and antioxidants(Saino et al. 2002b; boobyoffspring
and to a lesserdegree,withthefeet
of the fosterfather,
Williamson
et al. 2006).
allocatedtoeggsby colour of the genetic father(Velando et al. 2005).
Theamountandqualityofresources
femalesdecreasedsecond-eggvolumewhen
on the behaviour, Furthermore,
has
a
influence
mothersoften
strong
to a dullerblueafter
growthand survivalof the progeny(Schwabl 1993; themalefeetcolourwas manipulated
et al. 2005). In the firstegg was laid (Velandoet al 2006), and smaller
Williams1994; Christians
2002; Groothuis
birds, egg size is positivelycorrelatedwith hatching eggs have lower hatchingsuccess and producelighter
and earlygrowthand survivalof the young chicks at hatching(D'Alba and Torres2007). In this
probability,
how femalesadjust
we further
Christians
1994;
investigated
2002). In addition,increasing experiment,
(Williams
in eggsafter
ofmale
a suddendeterioration
derived theirinvestment
evidenceindicatesthatvariationsin maternally
than
24
h
first
was
feet
colour.
Less
after
the
feet
can
have
laid,
egg
positive
duringearlydevelopment
yolkandrogens
was
to
males
modified
duller
of
et
al.
colour
on chickdevelopment
effects
blue,
experimental
(Schwabl1996; Eising
and femaleinvestment
malesin low condition,
2001; Eising and Groothuis2003; Navara et al. 2006), mimicking
concenhave also beenreported
(Sockman in secondegg's mass,volumeand yolkandrogen
thoughnegativeeffects
and Schwabl2000; Mülleret al. 2005; Navaraet al. 2005; trationand layingintervalwas measured.Reproductive
influenced
et al. 2006; Tobler successof theblue-footed
Ruboliniet al. 2006; Von Engelhardt
by
boobyis strongly
relatedto El Nino Southern
concen- climaticvariation
et al. 2007). For instance,highyolktestosterone
Oscillation,
have been shownto enhancebeggingbehaviour whichmay affectthe onsetof breeding,the growthof
trations
et al.
theamountof foodreceivedby black-headed chicksandtherateof nestabandonment
and thereby
(Drummond
of
the
effects
To
evaluate
et
al.
Groothuis
and
chicks
1986; Wingfield
1999).
2003)
(Lams ridibundus;
Eising
gull
in
investment
on
maternal
environmental
annual
chicks
of
andthesocialrankafterfledging canary
variability
(Serinus
two
consecutive
was
the
in asynchronously eggs, experiment repeatedduring
canaria, Schwabl 1993). Furthermore,
environmental
breedingconditions:
hatchingclutches,increasedandrogensin the last egg yearswithcontrasting
conditions
(mean
could compensatefor competitiveasymmetries
among 2005,an El Ninoyearwithpoorbreeding
success of the colony0.18 fledglings
probrood mates (Schwabl 1993, 1997; Sockman and reproductive
ducedpertotalnests)and 2006,a yearwithgoodbreeding
Schwabl2000; Eisinget al. 2001; Sockmanet al. 2006;
conditions(1.43 fledglingsproduced per total nests;
Sandeilet al. 2007).
H. and TorresR., unpublished
Drummond
influence
females
data).Iffemales
Besides modifying
may
egg quality,
the
clutch
within
investment
between
interval
the
accordingto expected
fitnessby varying laying
adjust
offspring
we
at
of
breedingconditions, predictedthat,to mitigatethe
asynchrony
eggs and consequentlythe degree
betweenbrood mates,duringa poor year
a key traitforsiblingcompetition
(Lack 1954; asymmetries
hatching,
in secondeggs (egg
increaseinvestment
should
Mock and Parker 1997; Drummond2006). Hatching females
concentration)
compared
asynchronydeterminesinitial differencesin size and volume,massand yolkandrogen
ifthe
a
in
second
investment
to
Yet,
can
be
which
mates
brood
year.
good
during
eggs
amplified
among
development
a decreasein male
thenutritional,
indicating
physiolog- matefeetcolourdeteriorates
affecting
by siblingcompetition
and survivalbetweenchicks condition,comparedto femalesin the controlgroup,
ical and social asymmetries
2006). Furthermore, femalespairedwithmaleswithdullerfeetcolourshould
(Mock and Parker1997; Drummond
to decrease second-eggmass, volume and yolk androgen
of
of
the
asynchrony
degree hatching
adjustment
parental
and maydelaythelayingof thesecondegg,
has
been
offood
theabundanceorpredictability
interpreted concentration
conditions.
in
as an adaptationto optimisethe numberand qualityof particularly yearswithpoorbreeding
undervariablebreedingconditions
(Lack 1954;
offspring
Wiebeand Bortolotti
1995; Wiebeet al. 1998). Thus,by
thedegree Materialsand methods
and consequently
thelayinginterval
modifying
femalesmay facilitatebrood
of hatchingasynchrony,
The studywas carriedoutin thebreedingcolonyof bluereduction.
is
a
colour
male
feet
In theblue-footed
dynamic footedboobiesat Isla Isabel,offthePacificcostofMexico
booby,
trait
selected
(Torresand (25° 52' N, 105° 54' W), fromMarchto April2005 and
sexually
condition-dependent
to May 2006.
Velando2003; Velandoet al. 2006). Preferred
males,those fromJanuary
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Behav Ecol Sociobiol (2008) 62:1899-1908
The blue-footedbooby
The blue-footedbooby is a long-livedbird with a modal
clutchsize of two eggs (Drummondet al. 1986), laid with
an average intervalof 3.9±1.5 days (D'Alba and Torres
2007); and the laying intervalis positivelyrelated to the
hatchingintervalbetweenchicks(D'Alba and Torres2007).
Both parentsincubatethe clutch for roughly41 days and
care for the characteristicbrood of two chicks during
approximately4 months (Drummond et al. 1986; Torres
and Drummond 1999). Chicks hatch on average at an
intervalof 4 days and the resultingasymmetryin size and
developmentbetween themfacilitatesthe establishmentof
a dominant-subordinaterelationship (Drummond et al.
1991; Osorno and Drummond 1995). Typically,the senior
outcompete the younger chick, resulting in differential
mortalityof the subordinatenestling (in 136 two-chick
broods,20.56% ofjunior chicksdied while 5.88% of senior
chicks died, Drummondet al. 1986). Male contributionto
parentaleffortseems to be importantfor female breeding
success: experimentalreductionof paternal efforthad a
negativeeffecton the conditionand probablyfuturereproductionof females(Velando and Alonso-Alvarez2003).
Experimentalmodificationof male feetcolour
Courtingpairs were monitoreddaily to determinelaying
date. We manipulatedfeetcolour of 26 males duringa poor
year (2005) and 64 males duringa good year (2006) less
than24 h afterthe firstegg was laid. Males were captured,
banded witha numberedmetalringand randomlyassigned
to either the experimentalor the control group. In the
experimentalgroup, feet colour was modifiedto a duller
blue witha non-toxicintensivemakeup to mimica male in
low condition(Torres and Velando 2003). In the control
group,we simulatedthe manipulation(using a crayonin a
plastic bag) withoutchangingthe originalmale feetcolour
(Torres and Velando 2003). This method of colour
modificationhas been used beforewith no effectson bird
behaviourand the artificialcolour on experimentalmales
lasts for 5-6 days (Torres and Velando 2003). Total
handlingtime per bird was less than 5 min. Feet colour
was measured with a spectrophotometer(MINOLTA
2600d) before and after the manipulation. Before the
manipulation, feet colour of control and experimental
males did not differ (peak of maximum reflectance:
control 514.8±2.80 nm, experimental 518.4±2.98 nm;
Mann-Whitneytest,JV=48,(/=214.5, />=0.09; total reflectance: control l,296.90±20.93, experimental 1,335.26±
34.56; flf46=0.93, P=0.35). Also, previousto manipulation,
feetcolour of males duringa poor and a good year did not
differ(peak of maximumreflectanceMann-Whitneytest,
Af=48, (/=205.5, P=0.10; totalreflectancetu 46=2.14, P=
1901
0.38). After the manipulation, the peak of maximum
reflectance on the feet colour of experimental males
decreased 11.18% (460.4±0.40 nm), and total reflectance
decreased 46.4% (7 15.11±39.99); nevertheless,the lower
values remained within the natural range of variation
reportedforcourtingmales in the same population(Velando
et al. 2006).
Nest monitoringand yolk sampling
Nests were checked daily until the complete clutch had
been laid, and all freshlylaid eggs were markedwitha nontoxic pen. Egg mass was determinedwith an electronic
balance (±0.1 g), and theirmaximumlengthand widthwere
measuredwitha calliper(±0.1 mm) to calculateegg volume
in cubic centimeter (lengthx width2x 0.5 1/1,000; Hoyt
1979). Less than 24 h afterlaying, a yolk sample (1520 mg) was obtainedby introducinga syringe(needle type
21G) into the egg through a small hole in the shell
(Schwabl 1993). The hole was sealed using a tinydrop of
dentistal cement (VIARDEN, Mexico) and immediately
afterthe egg was placed back in the nest. Yolk samples
were stored in liquid nitrogenuntil laboratoryanalyses
were performed.Overall, hatchingsuccess formanipulated
eggs was low: 21.6% of the eggs thatwere yolk-sampled
hatched. For the analysis, clutches of two and threeeggs
were used: 12 two-eggclutches(five fromthe experimental
groupand seven fromthe controlgroup) from2005 and 26
two-eggclutches (13 in the experimentalgroup and 13 in
the controlgroup) and 14 three-eggclutches (five in the
experimentalgroup and nine in the control group) from
2006. In 2006, clutchsize did not differbetweentreatments
(Mann-Whitneytest,W=52, £/=964.5, P=0.63), and the
numberof eggs in a clutch did not have an effecton the
second-egg volume (general linear model (GLM), F2, 50=
0.39, />=0.67), mass (GLM, F2, 5o=0.17, />=0.86) or
androgen concentration(GLM, A4, F2, 48=0.40, />=0.52;
T, F2, 49=0.08, P=0.77). Hence, the firsttwo eggs from
these three-eggclutches were included in the analyses.
Females thatfailedto lay a second egg were not includedin
the analysis (14 in 2005 and 18 in 2006).
Hormone assays
Yolk androgen concentrationswere determinedby radio
immune assay (RIA, Schwabl 1993). In order to extract
androgens,10-15 mg of yolk were homogenisedin 1 ml of
distilledwater; 0.5 ml of this homogenised solution was
mixed with 5 ml of diethyl ether and vortexed during
1 min. The etherphase was decantedaftersnap freezingin
an alcohol bath at -30°C and evaporated.The driedextract
was redissolved in 1 ml of isooctane. This wet extract
passed through celite chromatographycolumns under
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1902
BehavEcol Sociobiol(2008)62:1899-1908
fluxin orderto separateandrostenedione
nitrogen
(A4),
(DHT), and finallytestosterone
dihydrotestosterone
(T),
using3.5 ml of isooctane(100%), 3.5 ml of isooctaneand
ethylacetate(95%:5%) and 3.5 ml of isooctaneand ethyl
acetate(85%:15%), respectively.
Each extractwas evaporatedand redissolved
in 1 ml of phosphatebuffer
(0. 1 M
with1% of gelatin).The restof themethodfollowedthe
standardRIA technique(Wingfieldand Farner 1975;
et al. 1999).
Wingfield
All androgenswere determined
in duplicateand were
incubatedovernightat 4°C with 5,000 cpm with its
[H3] androgenbeforethequantification.
respective
Duplicate values of each samplewerecomparedto a standard
curvethatrangedin concentration
from12.5 to 400 pg for
A4, from9.9 to 316.8 pg forT andfrom6.25 to 200 pg for
DHT. The meanrecoveryvalueswere64% forA4, 57%
forDHT and 58% forT. The coefficient
interof variation
was
6.87%
for
A4
and
for
8.38%
while
T,
assay
intra-assay
variation
was 3.07% forA4 and 3.24% forT. SpecificA4
and DHT antibodieswereprovidedby MP Biomedicals,
LLC, OH, USA (cataloguenumber;A4: 61320 and DHT:
61340). T antibodieswere providedby World Health
RIA ReagentProgramme
Organisation
(cataloguenumber:
oftheantibodies
wereA4:
K200710).Thecross-reactivities
T=4.5%, T:A4=3.5%, T:DHT=1.3%, DHT:A4=2.4% and
DHT:T=22.7%.
was performed
afterthe first
manipulation
experimental
egg in theclutchwas laid, and egg allocationadjustment
withinthe clutchis probablyrelevantin the blue-footed
femalesadjustandrogens
booby,we also analysedwhether
to thesecondegg relativeto thefirst
transferred
egg in the
clutch.Relativeconcentrations
werecalculatedas (A4 or T
concentration
in thesecondegg* 100 /A4 or T in thefirst
Positive
values indicatethat second eggs
100.
egg)receivedmoreA4 or T thanthe firstegg and negative
Aftera significant
valuesindicatethecontrary.
interaction
wereperformed
posthoc comparisons
usingt test.Laying
date was initiallyincludedin all models but was not
excludedthis
(P>0.05 in all cases); we therefore
significant
variablefromanalysis.Concentrations
of yolkDHT could
notbe detectedin botheggs in 29 out of the52 clutches;
of
then,thisandrogenwas notanalysed.Layingintervals
controland experimental
clutcheswere comparedwitha
generalisedlinearmodel withPoisson errordistribution.
Mean ± SE are shown throughout
the manuscript
and
P<0.05 was consideredsignificant.
Results
First-laid
eggs (thatis, eggs laid beforetheexperimental
fromcontroland experimental
manipulation)
pairsdid not
x
differ
in mass(treatment,
F\t48=1.15,P=0.28; treatment
Statistical
analysis
yearFu 48=0.23,P=0.63), volume(treatment,
Fh 48=0.70,
x year Fu 48=0.44, P=6.10) and
P=0.41; treatment
The mass, volume and absoluteconcentration
of yolk concentration
of T (treatment,
Fu 47=0.44, P=0.51;
* yearFu 47=3.25,P=0.08; Table 1); although
androgensof second eggs were analysedusing general treatment
mixedmodelsin PROC MIXED in SAS withnormalerror duringthegood year,firsteggs in thecontrolgrouphad
distribution
(SAS Institute1999) and the Satterthwaite greaterconcentrationsof A4 than fist eggs in the
for the denominator
approximation
degreesof freedom experimentalgroup (treatment,
Flt 46=0.01, P=0.94;
x yearFu 46=7.93,P=0.007, Table 1, posthoc:
et
al.
The
models
included
clutchidentity
as
treatment
(Littell
1996).
a randomfactorand thetreatment,
betweenyears,first
yearand eithermass, fi,39=2.48,P=0.01). Whencomparing
volumeor yolkandrogens
of first
As
eggsas fixedfactors.
eggs in a good yearwereheavier(61.32±0.67 g in 2006
variation
in yolkandrogen
concentrations
betweenfemales and 56.91±1.37 g in 2005; Fu 48=6.82,P=0.01) and had
is big andmayhavean intrinsic
thatdetermine moreT (20.52±1.65 pg/mgof yolkin 2006 and 14.08±
component
to some extenthormones
1.68 pg/mgof yolkin 2005; Fu 49=4.26,/>=0.044)than
deposition(Sandellet al. 2007;
Tobleret al. 2007), yolk androgenconcentrations
of the firsteggs in the El Nino yearof 2005, but theydid not
firstegg were included in the models. Because our differ
insize (56.83±0.74 cm3in2006 and54.04±1.12cm3
Table 1 Mean± SE concentrationsofyolkandrostenedione Androgens
(A4) andtestosterone
(inpicoofyolk)of
grampermilligram
first
andsecondeggsfrom
^
clutches
inthecontrol
and
Firsteggs
a
experimental
groups
during
Secondeggs
condiyearwithpoorbreeding
tions(2005)anda yearwith
Testosterone
conditions
goodbreeding
Firsteggs
(2006)
Secondeggs
~~~
Pooryear(2005)
Goodyear(2006)
Control
(Af=7)
(N=5)
Experimental
Control
(Af=22)
18)
Experimental
(AT=
- -
307.43±74.15
541.55±138.35
586.31d=134.45
645.45±139.99
704.31±83.05
586.83±53.74
466.11±36.78
503.40±35.75
10.75il.07
16.68±1.80
18.74±2.67
19.74±2.21
22.39±2.33
17.48±2.28
18.36±2.27
18.31il.50
£} Springer
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1903
Behav Ecol Sociobiol (2008) 62:1899-1908
in 2005; F\%48=3.61, /^=0.06) nor in yolk concentrations
of
A4 (602.01 ±53.06 pg/mgof yolk in 2006 and 423.64±
78.78 pg/mgof yolk in 2005; F,, 48=3.45, P=0.069).
Effectsof male feetcolour modificationon egg investment
Egg mass and volume
As predicted,females paired with males with duller feet
laid lightersecond eggs than females in the controlgroup
between
(Table 2; Fig. la). The mass of second eggs differed
yearsand was positivelyrelatedto the mass of the firstegg
in the clutch (Table 2), but the interaction between
treatmentand year was not significant(P=0.92). Second
eggs were slightlyheavierin thepoor yearthanin the good
year, when the mass of the firstegg was controlledfor
(60. 11±0.89 g in 2005 and 59.35±0.40 g in 2006; Table 2).
The experimentalmanipulationof male feet colour had a
similareffecton egg volume. Females in the experimental
grouplaid smallersecond eggs thancontrolfemales(Table 2;
Fig. lb). The volume of second eggs was positively
relatedto the volume of the firstegg in the clutch,but there
in the volume of second eggs between
were no differences
years(Table 2). Aftercontrollingforthe volume of the first
egg in the clutch, the volume of second eggs in the
experimentalgroup was 2.97% smallerthan in the control
group(Table 2).
Laying asynchrony
Females paired withexperimentalmales deferredlayingof
the second egg in the clutch. Irrespective of year,
Table 2 Comparisonof mass and volumeof second eggs laid by 23
femalesand 29 controlfemales
experimental
Model and terms
df
Second-eggmass
Treatment
Year
First-eggmass
First-eggmass x year
1,47
1,47
1,47
1, 47
Second-eggvolume
Treatment
Year
First-eggvolume
First-eggvolumex treatment
1,47
1,47
1, 44.5
1, 47
F
P
7.02
11.48
46.76
10.26
0.01
0.001
<0.0001
0.002
28.33
1.73
184.73
25.91
<0.0001
0.19
<0.000 1
<0.0001
In theexperimental
group,less than24 h afterthe firstegg was laid,
male feetcolourwas manipulated
to a dullerblue. Data wereanalysed
withgenerallinearmixedmodels.The modelsincludedtheidentity
of
thenestas a randomfactor(Wald Z testsforrandomeffects:egg mass,
Z=4.22, P<0.001; egg volume,Z=4.85, /><0.001). The initialmodels
includedall second-degreeinteractions
butnon-significant
termswere
excludedto obtaintheminimumadequatemodel
Fig. 1 Least squaresmeans(LSM ± SE) of second-egg(a) mass and
clutchesduringa yearwith
(b) volumefromcontroland experimental
poor breedingconditions(control,N=l\ experimental,N=5) and
during a year with good breeding conditions (control, N=22;
N=18). LSM were estimatedfromthe models that
experimental,
and year of studyas
includedfirst-eggmass or volume, treatment
fixedfactorsand nestid as a randomfactor
experimentalfemales delayed on average 0.77 days more
thancontrolfemalesthe layingof the second egg (treatment
x
FXy48=6.37, />=0.01; yearF,, 48=0.14, />=0.70; treatment
yearF,, 48=0.93, P=0.33; Fig. 2).
Absoluteyolk androgen concentrations
The concentrationof A4 in second eggs did not differ
between control and experimentalgroups (Fjt 44=2.30,
P>0.12, Table 1).
P=0.13; all interactionswith treatment
Concentrationof A4 of firstand second eggs withinthe
clutch was positively correlated and variation among
â Springer
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1904
Behav Ecol Sociobiol (2008) 62:1899-1908
Fig. 2 Laying interval(days) betweenfirstand second eggs in the
controland experimental
groupsfromthepooled sampleof bothyears
of study
clutcheswas significant
(firstegg A4, F^ 44=28.84,P<
0.0001; randomeffect
Z=4.69, P<0.001). Yet,A4 concentration
in secondeggswas on average6.69% greater
in the
pooryear(584.85±96.42 pg/mgof yolk)thanin thegood
in the
year(548.17±33.51pg/mgof yolk),whenvariation
concentration
of A4 of thefirstegg was controlled
(year
*
first
P=0.069,
A4,
44=3.46,
44=9.00,
year
egg
Fu
Flf
P=0.004, Fig. 3).
The concentration
of T in second eggs did not differ
betweenexperimental
treatments
(Fu 42=0.30,P=0.58; all
interactions
withtreatment
P>0.5\) or years(Fu 42=0.14,
P=0.71, all interactions
P>0.5\). Therewas significant
variation
ofT (random
amongclutchesintheconcentration
effectZ=4.52, /><0.001), but the concentration
of T in
thefirstand thesecondegg was notrelated(F\ 42=0.60,
P=0.44).
of firstand second eggs duringa year
Fig. 3 Yolk A4 concentration
withpoor breedingconditions(2005) and a yearwithgood breeding
conditions(2006)
clutchesdid not differ(2006, /,,39=2.45,P=0.12), yet,
clutcheshadlowerrelative
duringa pooryear,experimental
T concentration
did
thancontrols,
althoughthisdifference
notreachsignificance
(2005, tu l0=3.47,P=0.068).
Discussion
in eggsinthe
investment
Thisstudysuggeststhatmaternal
is
influenced
blue-footed
by expectedconditions
booby
chick
(Mousseauand Fox 1998a,b;
during
development
Verbovenet al. 2003; Sandeilet al. 2007). Femaleswere
Relativeallocationofandrogens
Therelative
allocationofA4 differed
betweenyearsandthe
interaction
betweentreatment
and year was significant
(Table3; Fig. 4). Overall,secondeggsreceivedon average
moreA4 thanfirsteggsduringa pooryearthan
relatively
showedthat,
duringa goodyear,andposthoc comparisons
comparedto the controlgroup, females paired with
males decreasedtheirrelativeallocationof
experimental
A4 in secondeggs duringa pooryear(2005, t\%
iO=6.81,
P=0.01; Fig. 4) butnotin a good year(2006, tu 38=2.14,
/>=0.15,Fig. 4).
Secondeggs receivedrelatively
moreT thanfirsteggs
duringa pooryearthanduringa goodyear(Table3). There
was a significant
interaction
betweenthetreatment
and the
year,but this was because the controlgroupsdiffered
betweenyears(t^ 2i= 11.53,P=0.001). Duringa goodyear
therelativeconcentration
of T in controland experimental
Table 3 Relativeconcentration
of androstenedione
(A4) and testosterone(T) in second eggs
Termsin model
A4 in second eggs
Treatment
Year
* year
Treatment
T in second eggs
Treatment
Year
x year
Treatment
df
F
P
1,46
1,46
1, 46
2.46
9.20
8.95
0.12
0.004
0.004
1,47
1,47
1,47
0.77
4.08
5.70
0.38
0.049
0.02
Data were analysedwith generallinearmixed models. The models
of thenestas a randomfactor(Wald Z testsfor
includedthe identity
random effects:A4, Z=3.64, P=0.0001; T, Z=4.85, /><0.001).
Sample size were 22 experimentaland 28 controlclutchesfor the
and 29 controlclutchesforthe
analysisof A4 and 22 experimental
analysisof T. The initialmodels includedegg volumeand egg mass
£} Springer
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Behav Ecol Sociobiol (2008) 62:1899-1908
1905
duringa poor year,suggestingthatfemalesmay varytheir
investmentin eggs of differentlaying order according to
annual breedingconditions.Moreover,when the male feet
colourwas modifiedto a dullerblue, femalesdecreasedsize
and mass of second eggs. Thus, blue-footedbooby females
seem to anticipaterearingconditionsand adjust investment
accordingly using a combination of signals that may
directlyaffecther own conditionand access to food, such
as annual variationsof breeding conditions,and indirect
signals,such as the male feetcolour,a phenotypictraitthat
indicatesmale condition(Velando et al. 2006) and paternal
investment(Velando et al. 2005).
In bothyears of study,femalespaired withexperimental
males delayed the laying of the second egg compared to
controlfemales.In a similarstudy,Velando et al. (2006) did
not detect such an effectprobably because in theirstudy
of A4 in second eggs of controland
Fig. 4 Relativeconcentration
clutchesduringa year with poor breedingconditions male feetcolour manipulationwas done 24 to 48 h afterthe
experimental
firstegg was laid, whereas in the presentstudy,male feet
(2005) and a year with good breedingconditions(2006). Relative
= ([A4 in thesecondegg]x 100 / [A4 in thefirstegg])concentration
colour was manipulatedless than 24 h afterthe firstegg
in
100. Values greaterthan zero indicategreaterA4 concentration
was laid, givingfemalesa longerperiod to varyinvestment
secondthanin firsteggs withina clutch
in eggs and layingdates. The blue-footedbooby is a species
with aggressive sibling competitionand facultativebrood
reduction(Drummondet al. 1986). The seniorchick within
able to adjust egg size and contentaccording to annual
a brood hatcheson average 4 days beforethejunior chick,
variationof breedingconditionsand as a functionof male
and this asynchronyat hatchingis key in determiningthe
feetcolour,a traitthatindicatesmale condition(Velando et
al. 2006) and probablymale feedingeffort(Velando et al.
output of sibling competition (Osorno and Drummond
to
a
duller
was
modified
blue,
1995). Experimentalduplication of the hatchinginterval
2005). Aftermale feetcolour
resultedin poorergrowth,50% increaseof aggressionand a
females were able to rapidly adjust egg investment,not
forjunior chicksin theexperimentalgroup
greatermortality
onlythrougha decrease of second-eggvolume,as foundby
Velando et al. (2006), but also by decreasing second-egg
compared to the control group (Osomo and Drummond
mass and the relativeyolk concentrationof A4 in second
1995). Thus, by postponingthe laying of the second egg,
with
mated
females
females
a
Furthermore,
pairedwithmales withdullerblue feetare probably
eggs during poor year.
The
of
second
the
males
deferred
eggs.
increasing the competitive asymmetriesbetween brood
laying
experimental
mates and facilitatingbrood reduction.
fact that females adjusted investmentin eggs based on a
Blue-footedbooby females were able to transferandromale sexual trait supports the differentialinvestment
hypothesis(Burley 1986, 1988; Gil et al. 1999; Cunningham gens in relationto expected breedingconditions.Females
more T to firsteggs duringa good year than
and Russell 2000; Groothuiset al. 2005). The resultssuggest transferred
various egg compothatfemalesare capable of fme-tuning
during a year with poor breeding conditions, and for
nents depending on prevailing mate and environmental second-laid eggs, the absolute and relative concentration
of yolk A4 and the relativeconcentrationof yolk T were
breedingconditions.
influence
females
and
mass
size,
may
higherduring a poor year compared to a good year. An
By decreasingegg
theembryodevelopment,hatchingsuccess, size and weight
increasing number of studies indicate that even minor
variationsof maternallyderived yolk androgenscan have
at hatching,chick growthrateand survival(Williams 1994;
importantfitness effects on offspring(Schwabl 1996;
Cunninghamand Russell 2000; Christians2002; Wagner
has
size
Groothuiset al. 2005; Rubolini et al. 2006; Von Engelhardt
and Williams2007). In the blue-footedbooby,egg
et al. 2006; Tobler et al. 2007). For instance,in the blacka positive effecton hatchingsuccess and females seem to
in second eggs comparedto
reducetheirrelativeinvestment
legged kittiwake,Rissa tridactyla,concentrationsin the
firsteggs as the season advance and breedingconditions yolk of A4 and IgGs are positivelycorrelated(Gaspariniet
deteriorate(D'Alba and Torres2007). In the presentstudy, al. 2007), and in vitroexperimentsshowed that,contraryto
we found that,compared to eggs produced duringa poor
T, A4 enhances immune system (Yao and Shang 2005).
and
heavier
females
a
Moreover,it has been suggestedthathigherconcentrations
produced
year, during good year
in
the
of
to
the
first
relative
first
but
clutch,
yolk A4 may be related to the productionof highly
egg
eggs,
larger
second
females produced heavier, but not larger,
eggs
competitivephenotypesin species withcommunallybreed& Springer
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All use subject to JSTOR Terms and Conditions
1906
Behav Ecol Sociobiol (2008) 62: 1899-1908
within
betweensiblingsmayinfluence
siblingasymmetries
ingsystemsor coloniallife(Carielloet al. 2006; Gil et al.
whichpartlydependson environ- a clutch(Schwabl1997;Sockmanetal. 2006; Sandelletal.
2007). Femalecondition,
in a
mentalbreedingconditions,
has been shownto influence 2007), whichmaybe an adaptivestrategy
particularly
siblicidalbird.
depositionof androgensin eggs (Verbovenet al. 2003;
In thisstudy,we showthatblue-footed
Sandellet al. 2007). Experimental
of food
boobyfemales
manipulation
to
in
to
in
are
able
investment
showed
that
females
eggs accordingto
previous egg laying
rapidlyadjust
availability
in
conditions
and in response
condition
reduced
of
their
variations
the
content
good
yolkandrogen
expectedbreeding
In thisspecies
trait
such
as
male
feet
colour.
without
et
to
a
(Verboven
dynamic
eggs
alteringoffspring
performance
with
of paternal
a
of
reduction
al. 2003) and modifiedthewithin-clutch
of yolk
longperiod parentalcare,
pattern
thecondition
affects
future
and,probably,
negatively
androgenallocation(Sandell et al. 2007). If increasing effort
of females(Velando and Alonso-Alvarez
levels of yolk androgenshave a positiveeffecton blue- reproduction
footedboobyoffspring,
moreabsoluteand 2003). Rearinga brood witha mate in poor condition
by transferring
relativeconcentrations
of A4 and morerelativeconcentra- duringa poor breedingyear is likelyto be costlyfor
tionofT intosecondeggs,femalesareprobablyincreasing females,
either
becausefemaleswillhavetocompensate
for
theprobability
or becausethereproductive
value of
ofsurvivalofsecond-hatched
chickduringa
a low paternaleffort
the brood will decrease.Then, underthese conditions,
pooryear.
when
the
feet
of
the
was
colour
mate
Interestingly,
adjustingvarious egg componentsto facilitatebrood
modified
to a dullerblue,femalestransferred
reduction
less
Moreover,
maybe an adaptivefemalestrategy.
relatively
A4 (butnotT) to secondeggsthanto firsteggswithinthe this studysuggeststhat mate evaluationand breeding
clutchduringa pooryearbutnotduringa goodyear.In our decisionscontinueafterpairing;therefore,
males should
first
attractive
feetcolourbeyondthecourtship
more maintain
study,
eggsin thecontrolgrouphadsignificantly
period
A4 thanfirsteggs in the experimental
(Torresand
groupduringthe anduntillayingis completeto assurepaternity
of theresultsshouldbe
Velando2003) and to increasefemaleinvestment
in eggs.
good year;thus,theinterpretation
takenwithcaution.In principle,
the
relative
by analysing
allocationto firstand secondeggs withinthe clutch,we
Acknowledgment We are gratefulto M. Cerbôn,A. Côrdoba,H.
havetakenintoaccountthisvariation,
yetmorestudieswill Drummond,D. Gil, A. Velando,K. Renton,twoanonymousReferees
be neededto confirm
the results.At present,the results and J. Graves forhelpfulcommentsand discussionduringthe study,
that
suggest
duringa poor year femalesare probably to E. Villasenor,D. Gonzalez and A. Nava Sânchesfortheirgreathelp
the probabilities
of survivalof second chicks duringfieldworkand to theLaboratoriode HormonasEsteroidesdel
increasing
Instituto
Nacional de Ciencias de la Salud y de Nutriciônforlogistic
moreandrogens
to secondeggs,butwhen
by transferring
The projectwas supported
supportforthe androgendetermination.
by
matefeetcolourdeteriorates
duringa poor yearfemales the UniversidadNacional Autônomade Mexico (UNAM, PAPIIT
decrease the survivalprobabilityof second chicks by IN211406) and CONACYT (47599). Logisticsupportwas providedby
less A4 to secondeggs.In a previous theArmadade Mexico, thestafffromtheParqueNacionalIsla Isabel
transferring
relatively
and the fisherman
fromSan Bias, Nayarit.The experiments
comply
studyin theblue-footed
boobycarriedoutat theendof an with the currentlaws of Mexico; permissionswere grantedby
El Ninoevent,thusfemaleswereprobably
extended
inpoor SEMARNAT and theParqueNacionalIsla Isabel. Duringthestudy,F.
condition
and ecologicalprospectsforincubating
was supported
forgraduatestudiesfrom
clutches Dentressangle
by a scholarship
UNAM.
andfeeding
chicksmayalso havebeenpoor,no differential
allocationof T and DHT accordingto layingorderwas
less A4 than
detected;
yetsecondeggsreceivedmarginally
firsteggs (Drummondet al. 2008). Experimental
studies
have foundthat femalesmodifiedthe levels of yolk References
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