parental foraging effort and offspring growth in adélie penguins: does working hard improve...
TRANSCRIPT
Functional Ecology
2003
17
, 590–597
© 2003 British Ecological Society
590
Blackwell Publishing Ltd.
Parental foraging effort and offspring growth in Adélie Penguins: does working hard improve reproductive success?
A. TAKAHASHI,*† Y. WATANUKI,‡ K. SATO,§ A. KATO,§ N. ARAI,¶ J. NISHIKAWA** and Y. NAITO§
*
Department of Polar Science, The Graduate University for Advanced Studies, Itabashi, Tokyo 173–8515, Japan,
‡
Laboratory of Animal Ecology, Graduate School of Agriculture, Hokkaido University, Sapporo 060–8589, Japan,
§
National Institute of Polar Research, Itabashi, Tokyo 173–8515, Japan,
¶
Department of Social Informatics, Graduate School of Informatics, Kyoto University, Kyoto 606–8501, Japan, and
**
Ocean Research Institute, The University of Tokyo, Nakano, Tokyo 146–8639, Japan
Summary
1.
Studying variability of parental foraging and provisioning behaviour in relation toreproductive success is fundamental to improving understanding of regulation ofreproductive effort in animals. The hypothesis that parents with higher foraging efforthave higher offspring growth rates was tested in chick-provisioning Adélie Penguins inAntarctica over five consecutive years.
2.
Time spent diving per day, an index of foraging effort, varied among male andfemale parents, and among pairs. These daily interindividual or interpair differences intime spent diving appeared to be consistent over the 2-week study period within eachbreeding season.
3.
Frequency of meals delivered by parents was positively correlated with their broodgrowth rate. Meal frequency was, however, independent of the amount of time spentdiving per day by parents and the time spent diving did not affect brood growth rates.
4.
Rates of body mass loss of breeding pairs were positively correlated with broodgrowth rates.
5.
Our results did not support the hypothesis that parents with higher foraging efforthave higher offspring growth rates. It is suggested that parental allocation of resourcesobtained during foraging, rather than the degree of foraging effort, is the more impor-tant process determining offspring growth rates in Adélie Penguins.
Key-words
: Diving, individual variation, reproductive allocation
Functional Ecology
(2003)
17
, 590–597
Introduction
One of the central issues in life-history theory is tounderstand how animals balance the amount ofeffort in current reproduction against future survival(Stearns 1992). In long-lived seabird species, reducedparental survival due to excessive reproductive effortat one breeding attempt may greatly decrease lifetimereproductive success (Croxall & Rothery 1991; Wooller,Bradley & Croxall 1992). Regulation of reproductiveeffort in terms of provisioning to offspring is especiallyimportant for seabirds for which at-sea foraging andmeal delivery are energetically expensive and riskybehaviours (Chappell
et al
. 1993a; Ydenberg 1994).
Regulation of provisioning involves two processes:resource acquisition through foraging activity andresource allocation between parents and offspring(Boggs 1992; Weimerskirch 1999); these finally deter-mine the reproductive success of individual seabirds.Large interindividual variation in reproductive successhas been recognized widely among seabirds (see reviewin Wooller
et al
. 1992). Many studies have attemptedto determine the source of ‘individual quality’ in termsof reproductive performance (Thomas & Coulson 1988;Mills 1989; Sydeman
et al
. 1991; Phillips & Furness1998; Wendeln & Becker 1999; Catry
et al
. 1999),although only a few studies have examined variationof foraging performance, largely due to practicaldifficulties in measuring at-sea behaviour of parents.Recent studies have highlighted a positive correlationof reproductive output with body size or body condition
†Author to whom correspondence should be addressed. E-mail: [email protected]
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Foraging and reproduction of penguins
© 2003 British Ecological Society,
Functional Ecology
,
17
, 590–597
of seabird parents (Lorentsen 1996; Saether
et al
.1997; Wendeln & Becker 1999; Barbraud
et al
. 1999).These studies suggest variation in both foraging andallocation processes are important for determiningreproductive success; however, few comprehensivestudies have examined the link between foraging andreproductive output in seabirds (but see Weimerskirch
et al
. 1997; Barbraud
et al
. 1999). Thus, characterizinghow variation of foraging behaviour of parents atsea affects their reproductive performance, throughresource allocation processes, is a key towards furtherunderstanding of the regulation of reproductive effortin seabirds (Boggs 1992; Weimerskirch 1999).
Three hypotheses have been proposed about howforaging and allocation processes produce differentialreproductive output among parents. First, parentswith high foraging effort have high reproductive suc-cess (Pugesek 1995). Second, parents with high for-aging efficiency have high reproductive success (Nur1984; Reid 1988). Third, parents with higher alloca-tion of resources to offspring have high reproductivesuccess (Hillström 1995; Wendeln & Becker 1999).These three hypotheses are not mutually exclusive; forexample, parents with high foraging efficiency at seacould deliver a higher proportion of their resources totheir offspring. To test these hypotheses, it is necessaryto study variability in at-sea foraging behaviour ofindividual parents in association with simultaneousmeasurements of their reproductive output.
Penguins provide an excellent model to examine therelationship between foraging and reproductive suc-cess, because their foraging activity (diving) can bemeasured accurately for a relatively large number ofindividuals, thanks to recent technological advancesof time-depth recorders (Wilson 1995). Our study setout to examine variability in parental foraging effort(time spent diving) and its reproductive consequencesin Adélie Penguins
Pygoscelis adeliae
in Antarctica.We examine the extent of variation in foraging effortbetween individuals, and test the hypothesis thatparents with high foraging effort have high offspringgrowth rates. Furthermore, we discuss the foragingand allocation processes that potentially determineoffspring growth rates.
Materials and methods
The study was carried out at Hukuro Cove colony(69
°
13
′
S, 39
°
39
′
E), 30 km south of Syowa Station inLützow-Holm Bay, Antarctica, during five australsummers from 1995/96 to 1999/2000 (hereafter referredto as 1995–99). During the study, about 120–220 pairsof Adélie Penguins bred at the colony annually.Penguins arrive at the colony in mid-October, lay eggsin mid-November, and feed their chicks between lateDecember and early February (Watanuki
et al
. 1993).The study period was between late December and
mid-January, corresponding to brooding and the earlycrèche stage.
Parental activities, diving behaviour and reproduc-tive success were monitored for 10–20 pairs each year.Different pairs were sampled each breeding season.Parents attending chicks (around 5 days of age) for atleast 3 h were assumed to have fed their chicks, and sowere captured. Although penguins with small chickssometimes do not feed all the food they have in theirstomachs within 3 h, we believe the errors implicit inthis would be minimal because parents bring smalleramounts of food when their chicks are young (<100 gin case of Adélie Penguins; Lishman 1985). They wereweighed, measured and marked on their chests withblack hair dye. Bill depth, bill and head length weremeasured with callipers to 0·1 mm and flipper widthwas measured with a ruler to 1 mm. The bird’s sex wasdetermined from a discriminant score based on thesemeasurements following Kerry
et al
. (1992). An indexof structural body size was determined by performinga principal component analysis on these four traits(Rising & Somers 1989). An index for body conditionwas determined by regressing body mass on the indexof structural body size, and the residuals from theregression were defined as the body condition index(see Lorentsen 1996).
Electronic time-depth recorders (see below) wereattached to the back of parents with quick-set epoxyglue and cable ties (1995–98) or with Tesa (BeiersdorfAG, Hamburg, Germany) tape (1999), to record divingbehaviour. A small radio transmitter (10 mm diameter,45 mm long, 9·5 g, ATS Inc., Isanti, MN, USA) wasalso attached in 1999 to determine foraging location(Watanuki, Takahashi & Sato 2003). After about3 weeks of deployment, parents were recaptured justafter they had fed their chicks, weighed and the loggersrecovered. Body mass loss rate was calculated as thedifference between body mass at first capture (‘initialbody mass’) and recapture (‘final body mass’).
To determine the frequency of meal deliveries tochicks, we conducted 3–5 days of continuous observa-tion at nests, approximately every 7–10 days duringchick rearing. Mean meal frequency was calculatedacross the observation periods, and was considered asrepresentative of the individual birds observed. Theobservation period differed among years due to logis-tic constraints. In 1997, a single 3-day observation wasconducted between 29 and 31 December 1997.
-
Diving behaviour was recorded with two types of dataloggers (TDRs of NIPR and UME types, Little Leon-ardo Co. Ltd, Tokyo, Japan), which can record pres-sure continuously. NIPR type TDRs (14 mm diameter,85 mm length with a domed top, mass in air 27 gincluding battery) were used in 1995 (all birds), 1996(all birds) and 1997 (25 out of 31 birds). UME typeTDRs (15 mm diameter, 50 mm length with a domed
592
A. Takahashi
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© 2003 British Ecological Society,
Functional Ecology
,
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, 590–597
top, mass in air 14 g including battery) were used in1997 (six out of 31 birds), 1998 (all birds) and 1999 (allbirds). These TDRs were programmed to continuouslyrecord depths at 5-s intervals in 1995 and at 3-s inter-vals in all other years, over the 3-week period. Theabsolute accuracy of depth was 1 m and resolution was0·5 m for NIPR type and 0·1 m for UME type.
The effects of data loggers were examined only in1999, and the birds with devices had 12% smallermeal frequency (0·87
±
0·13 day
−
1
,
n
= 40 birds) thanthose without devices (0·99
±
0·12 day
−
1
,
n
= 10 birds)(Watanuki
et al
. 2003). However, the ranges of the mealfrequency values overlapped entirely between birds withand without devices (0·56–1·36 and 0·83–1·18 day
−
1
,respectively), suggesting the provisioning behaviourwas not radically modified by the device attachment. Inaddition, foraging trip duration and body mass loss ratedid not differ significantly between birds with devices(15·0
±
4·2 h, 12·4
±
9·2 g day
−
1
) and without devices(14·5
±
3·8 h, 13·9
±
10·2 g day
−
1
) (Watanuki
et al
. 2003).Moreover, this is a comparative study of individualscarrying devices of similar size, thus reducing the riskof biased results. Devices of similar size did not affectforaging trip duration of Adélie Penguins breedingin the Ross Sea, Antarctica (Ballard
et al
. 2001). Webelieve that there was no serious device impact on theforaging performance, and that the device effects weresmall enough to allow individual variation in foragingbehaviour to be analysed.
Each chick was marked with a numbered plastic flip-per tag using a cable tie and weighed every 4–6 days.Chick growth rate was calculated as the slope of thelinear regression of chick mass on date during lateDecember to mid-January, the period when chicksgrow linearly (Takahashi 2001). Brood growth ratewas calculated as a sum of growth rates of all chicks(one or two) in a nest; only nests with a two-chickbrood are used for the analysis presented here (seebelow).
Diving data were obtained from 133 birds, during1995–99. Data were analysed with custom-made soft-ware (KAISEKI.exe, MMT Co. Ltd, Tokyo, Japan)and with macro programs on Igor Pro (Wave MetricsInc., Lake Oswego, Oregon, USA). All dives less than1-m in depth were excluded as this depth was withinthe error range of the TDRs. Maximum dive depth,dive duration and surface interval were determined foreach dive. Dive data from 31 December to 15 Januaryeach year were used to standardize the period overwhich chick growth rates were measured. Time spentdiving per day was calculated as the total dive durationfor each day, when the dive record of the bird was avail-able for whole period of the day.
Consistency of interindividual differences in timespent diving per day within each breeding season wasexamined by a repeatability analysis. Repeatability, orthe intraclass correlation coefficient (
r
I
), is estimatedusing variance components calculated from meansquares values obtained from one-way
(Lessells& Boag 1987; Zar 1999). Factors influencing broodgrowth rates were investigated by applying differentmodels of
. For this analysis, only nests with twochicks were used. This excluded four, four, two, eightand two nests for 1995–99, as these nests contained onlyone chick at the start of study or one chick died duringthe study period. Brood growth rates and four covari-ates included in the
were normally distributed(Kolmogorov–Smirnov Normality Test,
P
> 0·15). Minitaband Statview software were used for statistical analysisand
P
< 0·05 was taken as the level of significance.
Results
Time spent diving per day showed high levels of vari-ation between individual birds and pairs, with thecoefficient of variation (CV) of 19·7–35·6%, 17·4–28·8%and 11·2–27·7% for female, male parents and forbreeding pairs, respectively, within each year (Table 1).There were 1·3–3·0 times differences between indi-viduals with the longest and shortest mean time spentdiving (Table 1). These interindividual or interpairdifferences in foraging effort appeared to be con-sistent over the study period, as there was a significantrepeatability of time spent diving per day within eachbreeding season (Table 1, Fig. 1).
Fig. 1. An illustrative example of interpair variation in timespent diving in Adélie Penguins at Hukuro Cove colony.Cumulative time spent diving by eight pairs of AdéliePenguins in 1995/96 is shown in relation to number of daysafter 31 December. Each line indicates an individual pair.Variation in time spent diving among pairs was consistentover the 10-day period.
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Functional Ecology
,
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, 590–597
Mean dive depth also showed high levels of vari-ation between individuals (Table 2). These interindi-vidual differences in diving depth also appeared to beconsistent over the study period, as there was a signi-ficant repeatability in the daily mean of diving depthwithin each breeding season (Table 2).
Parental initial body mass or condition did not affecteither time spent diving per day or mean dive depth inboth males and females (
r
2
= 0·00–0·04,
P
> 0·12).
The relationship between daily time spent diving byparents and growth rates of their brood was examinedusing two models of
(Table 3, Fig. 2). Onemodel allowed only the effect of study year togetherwith time spent diving (Model 1). The other modelallowed the effect of other three parental characteristicstogether with the effect of year and time spent diving
(Model 2). Interaction terms (e.g. Year * Dive time)were not included in both models because no interac-tion terms had significant effects when included.
Daily time spent diving by parents showed no signi-ficant relationship with brood growth rates in bothmodels of
(Table 3). Among the other threecovariates considered in Model 2, meal frequency had astrong relationship with brood growth rates. Mealfrequency was independent of time spent diving infemales, in males and in pairs (
r
2
= 0·00–0·01,
P
> 0·43).Male initial body condition also had a significant pos-itive correlation with brood growth rates (Table 3).Both the rate of body mass decrease by females and theaverage rate of body mass decrease by male and femalein a breeding pair appeared to have a positive relation-ship with brood growth rates, though not significantlyin this model (
P
= 0·07 and 0·08; Table 3).The effect of mass decrease rate of females and pairs
on brood growth rates was also examined. This modelincorporates year, meal frequency and mass decrease
Table 1. Variation in time spent diving for Adélie Penguins during five breeding seasons
Year
Time spent diving per day (h) Repeatability analysis
Mean SD CV Range No. of birds or nests F df ri
Female 1995 5·1 1·4 27·3 2·7–7·1 12 6·9 11,179 0·27***1996 5·1 1·8 35·6 2·9–8·8 13 9·7 12,181 0·37***1997 4·7 0·9 19·7 3·2–6·6 12 2·9 11,165 0·12**1998 3·8 1·0 25·0 2·5–5·3 8 5·7 7,110 0·24***1999 4·7 1·2 24·3 3·1–7·2 20 4·6 19,219 0·23***
Male 1995 4·8 1·4 28·8 2·8–7·4 13 5·7 12,180 0·26***1996 4·6 1·1 23·5 2·8–6·5 14 3·3 13,210 0·12***1997 3·9 0·8 20·6 2·3–5·2 13 2·3 12,163 0·09**1998 3·7 0·7 19·6 3·0–5·5 9 3·0 8,132 0·12**1999 3·5 0·6 17·4 2·6–4·7 19 1·7 18,215 0·06*
Pair (female + male) 1995 10·2 2·8 27·7 6·4–13·8 8 16·1 7,106 0·51***1996 10·0 2·6 25·9 5·6–14·4 10 9·7 9,146 0·36***1997 8·6 1·5 17·1 6·6–10·6 10 4·6 9,117 0·22***1998 7·5 0·8 11·2 6·4–8·6 5 2·3 4,70 0·081999 8·0 1·5 19·1 5·6–10·9 18 6·5 17,161 0·36***
*P < 0·05, **P < 0·01, ***P < 0·001.
Table 2. Variation in dive depth for Adélie Penguins during five breeding seasons
Year
Dive depth (m) Repeatability analysis
Mean SD CV Range No. of birds F df ri
Female 1995 23·4 4·2 17·8 16·8–29·9 12 3·3 11,165 0·13**1996 14·7 6·7 45·7 3·5−29·3 13 12·5 12,176 0·44***1997 14·3 9·3 65·0 2·9–29·2 12 31·4 11,165 0·67***1998 19·2 3·9 20·1 13·1−25·8 8 4·4 7,110 0·19***1999 13·2 4·0 30·0 6·1−21·6 20 9·5 19,218 0·42***
Male 1995 20·2 10·6 52·4 5·6–46·2 13 18·8 12,169 0·56***1996 12·4 6·2 50·2 5·6−26·0 14 13·7 13,205 0·45***1997 16·2 6·1 37·7 4·8−24·2 13 10·4 12,161 0·41***1998 18·3 5·6 30·6 9·3−26·1 9 11·7 8,132 0·41***1999 12·6 3·9 30·5 5·7–18·4 19 10·7 18,214 0·44***
**P < 0·01, ***P < 0·001.
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© 2003 British Ecological Society,
Functional Ecology
,
17
, 590–597
rate, but excludes time spent diving and body condi-tion that showed low statistical values in Model 2.According to this model, the rate of mass decrease ofpairs had a significant positive relationship with broodgrowth rates (coefficient = 1·2,
F
1,53
= 4·4,
P
< 0·05,
N
= 60 pairs; Fig. 3), together with the effect of mealfrequency (coefficient = 45·1,
F
1,53
= 13·7,
P
< 0·01) andwith no significant effect of study year (
F
4,53
= 1·5,
P
=0·23). The rate of mass decrease by female appeared tohave similar positive relationship with brood growthrates, though not significantly (coefficient = 0·7,
F
1,57
=3·0,
P
= 0·09,
N
= 64).The rate of mass decrease of parents was negatively
correlated with initial body mass in females (coefficient=
−
13·4,
F
1,70
= 23·3,
P
< 0·001) and males (coefficient
Fig. 2. Relationships between brood growth rates of two-chick broods (sum of growth rates of both chicks) andaverage time spent diving per day by parents: (a) females (b)males and (c) pairs.
Tab
le 3
.
Ana
lysi
s of
cov
aria
nce
of b
rood
gro
wth
rat
es (
g da
y
−
1
) in
rel
atio
n to
stu
dy y
ear,
tim
e sp
ent
divi
ng (
dive
tim
e) a
nd o
ther
par
enta
l cha
ract
eris
tics
. In
Mod
el 1
, onl
y th
e ef
fect
of
dive
tim
e (a
s a
cova
riat
e)an
d ye
ar (a
fact
or) w
ere
exam
ined
. In
Mod
e! 2
, the
eff
ect o
f di
ve ti
me
and
year
wer
e ex
amin
ed to
geth
er w
ith
mea
l fre
quen
cy, b
ody
cond
itio
n an
d m
ass
decr
ease
rat
e of
par
ents
(as
cova
riat
es).
Coe
ffici
ent v
alue
sar
e pr
esen
ted
wit
h 95
% c
onfid
ence
inte
rval
s.
F
-val
ues
are
calc
ulat
ed u
sing
adj
uste
d m
ean
squa
res
(Typ
e II
I)
Mod
elV
aria
bles
in t
he m
odel
Fem
ale
(
n
= 5
5)M
ale
(
n
= 5
5)P
air
(
n
= 4
4)
Coe
ffici
ent
(95%
CI)
FP
Coe
ffici
ent
(95%
CI)
FP
Coe
ffici
ent
(95%
CI)
FP
1F
acto
rY
ear
2·51
0·05
32·
720·
042·
320·
07C
ovar
iate
Div
e ti
me
(h d
ay
−
1
)3·
5 (
−
3·7,
10·
7)0·
940·
342·
2 (
−
8·7,
13·
1)0·
160·
691·
6 (
−4·1
, 7·3
)0·
330·
57
2F
acto
rY
ear
1·75
0·16
1·92
0·12
0·97
0·44
Cov
aria
tes
Div
e ti
me
(h d
ay−1
)1·
2 (−
5·4,
7·8
)0·
140·
710·
8 (−
9·2,
10·
9)0·
030·
871·
2 (−
4·3,
6·6
)0·
190·
67M
eal f
requ
ency
(n
day−1
)50
·7 (
8·9,
92·
6)5·
95<
0·05
75·0
(26
·8, 1
23·2
)9·
80<
0·01
45·6
(6·
1, 8
5·1)
5·48
<0·
05B
ody
cond
itio
n9·
0 (−
21·1
, 39·
0)0·
360·
5533
·0 (
3·8,
62·
2)5·
18<
0·05
4·7
(−11
·4, 2
0·7)
0·35
0·56
Mas
s de
crea
se r
ate
(g d
ay−1
)1·
0 (−
0·1,
2·2
)3·
380·
07−0
·1 (
−1·2
, 1·1
)0·
010·
921·
5 (−
0·2,
3·1
)3·
260·
08
595Foraging and reproduction of penguins
© 2003 British Ecological Society, Functional Ecology, 17, 590–597
= −15·7, F1,69 = 44·1, P < 0·001) with no significanteffect of year (females: F4,70 = 2·36, P = 0·06, males:F4,69 = 2·4, P = 0·77). Interaction term (Year * Initialbody mass) had no significant effect when included(males: F4,65 = 2·5, P = 0·051, females: F4,66 = 0·49, P =0·74). This indicates that male and female parents withhigher initial body mass lost more body mass.
Discussion
Few comprehensive studies have examined inter-individual variation in foraging effort in seabirds.Time away from a breeding colony has been used asan index of foraging effort (e.g. Pugesek 1995), butthis may not be an appropriate measure of foragingtime, as seabirds undertake other activities in addi-tion to foraging while they are away from their nest.Penguins from our study colony are ideal to studyinterindividual variation in foraging effort, as mostdives can be considered as dives for foraging activity(Watanuki et al. 1993). This is because the sea aroundour study colony is covered by fast sea ice, and pen-guins walk between the breeding colony and theirforaging location (usually less than 4 km: Watanuki,Miyamoto & Kato 1999; Watanuki et al. 2003; Yodaet al. 2001).
The results of the present study showed that thereare high levels of interindividual variation in timespent diving among Adélie Penguins breeding at theHukuro Cove colony. The differences between indi-viduals appeared to be consistent within a breedingseason: some individuals tended to dive consistentlyshorter or longer than others on a daily basis (Table 1,Fig. 1). In our study, foraging effort did not depend onbody mass or condition of individuals. This may indicateconsistent variation in at-sea foraging performance
among individuals; for example there may be goodforagers and poor foragers. Furthermore, the resultsimply that variation in time spent diving could be asource of differential reproductive costs to parents, ashigher metabolic or predation costs could be presentas parents spend longer time at sea (Chappell et al.1993a; Bevan et al. 2002).
Consistent interindividual variation in at-sea forag-ing performance and its relationship to body mass orcondition has been suggested for other seabirds, fromobservations of provisioning behaviour. Larger bodymass or larger sized individuals have shorter foragingtrips (up to 2·0 times difference in duration) in SnowPetrels Pagodroma nivea (Barbraud et al. 1999), andindividuals of better condition brought larger mealsfor a similar trip duration in Antarctic Petrels Thalas-soica antarctica (Lorentsen 1996). Interindividual vari-ation was an important factor explaining variability offoraging trip duration in Adélie Penguins breeding onRoss Island, Ross Sea, although the causes of inter-individual variation were unclear (Ballard et al. 2001).Weidinger (1998) also reported consistent individualdifferences in foraging trip duration of Cape PetrelsDaption capense, with repeatability values being statis-tically significant and varying between 0·12 and 0·26among sexes and study localities. Boyd (1999) reportedconsistent individual differences in time spent diving ina marine mammal, the Antarctic Fur Seal Actocephalusgazella, although no comparable statistics to our studywere provided.
Our results did not support the hypothesis that parentswith high foraging effort have higher offspring growthrates. Time spent diving per day, an index of foragingeffort, varied greatly among individuals or amongpairs breeding at the same season, but did not have anyeffects on brood growth rates. Brood growth ratesincreased positively with frequency of meals deliveredby parents, but foraging effort of parents had nosignificant effect on meal frequency. One possibilitywould be that we could not detect the relationshipbetween time spent diving and brood growth ratebecause of low statistical power of the tests. However,we believe that the statistical power of our tests werenot particularly low; for example the power to detectthe coefficient of 10 (i.e. increase of brood growth ratesby 10 g day−1 with increase of time spent diving by1 h day−1) at the 0·05 level were 78%, 44% and 93%for the tests of females, males and pairs (Model 1 inTable 3). In addition, because we detected statisticallysignificant relationships between other variables (e.g.meal frequency) and brood growth rates in Model 2,time spent diving should appear significant in our testsif it is a strong determinant of brood growth rates.
Understanding why individuals working hard, interms of diving, do not have higher offspring growth
Fig. 3. Relationships between brood growth rates of two-chick broods and mass decrease rate of pairs (mean value ofmale and female) during 1995–99. Regression line isY = 159·5 + 1·5X (N = 60, r 2 = 0·10, P < 0·05).
596A. Takahashi et al.
© 2003 British Ecological Society, Functional Ecology, 17, 590–597
rates is complex. Chappell et al. (1993a,b) have sug-gested that Adélie Penguin parents would gain moreenergy, as they increase their time diving. If averageforaging efficiency was similar among individuals, thevariation in time spent diving would lead to large dif-ferences in total amount of food intake and that avail-able for reproduction and self-maintenance of parents.Two hypotheses could explain why there are no effectsof foraging effort on meal frequency and brood growthrates: large interindividual variation in (1) foragingefficiency and/or (2) allocation of food between parentsand offspring.
First, interindividual variation in foraging efficiencyhas been reported in some species of seabirds, gulls(Sibly & McCleery 1983; Pierotti & Annett 1990)and Pigeon Guillemots Cepphus columba (Golet et al.2000). Variation in foraging efficiency was associatedwith individual specialization of habitat use or preytaken by individuals in these seabirds, and was animportant factor determining reproductive success.High levels of individual variation in foraging locationhave been reported from our study colony in 1999;however, neither variation in foraging area nor dis-tance to foraging site affected the frequency of mealsdelivered by parents (Watanuki et al. 2003). We haveno data about individual variability of prey taken byour study penguins. Stomach content analysis showedthat penguins from our study colony fed on both krill(Euphausia superba and E. crystallorophias) and fish(mainly juvenile Pagothenia borchgrevinki ) in the first 3years (1995–97), but almost exclusively on krill in the later2 years (1998 and 1999) (Endo et al. 2002; Takahashi2001). Thus, individual specialization toward differentprey species is unlikely, especially in the later 2 years.As the degree of individual variation in diving beha-viour in the first 3 years appears to be similar to thatin later 2 years, we suggest that prey differences be-tween individuals would not be an important factorfor individual diving and reproductive performance.Although reproductive variability associated withindividual habitat use or diet would be unlikely, wecould not rule out a possibility that there was indi-vidual variation in the amount of prey taken per divingtime due to other factors, i.e. differences in foragingskills (Nur 1984; Reid 1988).
Second, individual variation in allocation of foodbetween parents and offspring has been suggested forCommon Terns Sterna hirundo (Wendeln & Becker 1999)and Pied Flycatchers Ficedula hypoleuca (Hillström1995), as birds with high breeding success showed highbody mass loss rate. This appears to be partly true forour Adélie Penguins, as pairs that lost mass more rapidlyhad higher brood growth rates, although the mass lostby either male or female parent on its own did not havea significant effect. That both parents provision chicksmay be a reason that why there is a relationship be-tween brood growth rates and body mass loss rate ofpairs, but this does not apply to individual parents.Parental initial body mass appeared to be a factor
determining body mass loss rates: parents with higherbody mass lost more mass during chick rearing. Parentsmight be able to change the amount of food allocatedto offspring, using a delayed digestion of food in stomachas a mechanism for regulating the supply to offspring(Wilson, Ryan & Wilson 1989; Peters 1997).
Why initial body condition of males, but notfemales, had a significant effect on brood growth rateis uncertain. As the initial body mass and condition ofmales were higher than those of females (Takahashi2001), males may have a greater potential to allocatemore resources into chick rearing. However, meal fre-quency did not relate to body condition of males, andbody mass loss rate of male parents did not relate tobrood growth rates. Size of meals delivered showed apositive correlation with body size or condition of parentsin Chinstrap Penguins Pygoscelis antarctica (de Leon,Fargallo & Moreno 1998), Antarctic Petrels (Lorentsen1996) and Snow Petrels (Barbraud et al. 1999), and thispossibility should be studied further.
In conclusion, there was a large variation in timespent diving per day between individuals or amongpairs of Adélie Penguins. Despite the large variation,parents with high diving effort did not have high off-spring growth rate. Parental allocation of resourcesthat were obtained during foraging, rather than thedegree of foraging effort, appeared to be the moreimportant determinant of offspring growth rates.
Acknowledgements
We would like to thank Yoshinori Miyamoto, HideoIchikawa and Maki Kuroki for their extensive helpwith data collections, and all the members of 37th−41st Japanese Antarctic Research Expeditions forlogistic support. Thanks are also due to Peter Rotheryfor invaluable statistical advice, to Richard Phillips forhelpful discussions and to Phil Trathan, two anony-mous reviewers and the Editor Steven Chown for theirthoughtful and constructive comments that greatlyimproved the manuscript. A.T. was partly supportedby the Japan Society for the Promotion of Science (JSPS)Postdoctoral Fellowships for Research Abroad (atBritish Antarctic Survey) during the writing of the paper.
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Received 13 September 2002; revised 29 April 2003; accepted3 May 2003