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Cite this article: Salton M, Saraux C, Dann P,
Chiaradia A. 2015 Carry-over body mass efect
from winter to breeding in a resident seabird,
the little penguin. R. Soc. open sci. 2: 140390.
http://dx.doi.org/10.1098/rsos.140390
Received: 17 October 2014
Accepted: 22 December 2014
Carry-over body mass
efect from winter to
breeding in a resident
seabird, the little penguin
Marcus Salton1 , Claire Saraux2,3 , Peter Dann1
and André Chiaradia1
1 Research Department, Phillip Island Nature Parks, PO Box 97, Cowes,
Victoria 3922, Australia
2 Institut Pluridisciplinaire Hubert Curien UMR7178 CNRS, 23 Rue Becquerel,
67087 Strasbourg, France
3 IFREMER, UMR 212 Exploited Marine Ecosystems, Avenue Jean Monnet, BP 171,
34203 Sète Cedex, France
1. Summary
Subject Category:
Biology (whole organism)
Subject Areas:
behaviour/ecology
Keywords:
capital-income breeding, penguin monitoring
system, parental investment, timing of laying,
breeding success, seabirds
Author for correspondence:
André Chiaradia
e-mail: achiaradia@penguins.org.au
Using body mass and breeding data of individual penguins
collected continuously over 7 years (2002–2008), we examined
carry-over effects of winter body mass on timing of laying
and breeding success in a resident seabird, the little penguin
(Eudyptula minor). The austral winter month of July consistently
had the lowest rate of colony attendance, which confirmed our
expectation that penguins work hard to find resources at this
time between breeding seasons. Contrary to our expectation, body
mass in winter (July) was equal or higher than in the period
before (‘moult-recovery’) and after (‘pre-breeding’) in 5 of 7 years
for males and in all 7 years for females. We provided evidence
of a carry-over effect of body mass from winter to breeding;
females and males with higher body mass in winter were more
likely to breed early and males with higher body mass in winter
were likely to breed successfully. Sex differences might relate to
sex-specific breeding tasks, where females may use their winter
reserves to invest in egg-laying, whereas males use their winter
reserves to sustain the longer fasts ashore during courtship. Our
findings suggest that resident seabirds like little penguins can
also benefit from a carry-over effect of winter body mass on
subsequent breeding.
2. Introduction
To determine which factors shape breeding performance of a
species, studies usually focus on conditions during breeding.
However, it is crucial to understand whether the parental
investment into tasks associated with preparation before breeding,
2015 The Authors. Published by the Royal Society under the terms of the Creative Commons
Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted
use, provided the original author and source are credited.
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such as maintenance of a breeding site, acquisition of a breeding partner and allocation of food resources
are linked to the offspring’s chance of survival [1]. Events and processes during pre-breeding preparation
stages can have an influence, i.e. have a carry-over effect, on the performance of an individual in
subsequent stages of the breeding cycle [2]. In fact, carry-over effects can explain a large amount of
variation in individual fitness [3].
Carry-over effects generally manifest when variations in the ability to use resources result in
individuals making the transition between stages with different levels of physical condition (state), thus
affecting downstream events such as reproduction or survival [3]. For instance, supplemental feeding
experiments have demonstrated that increasing access to food for blue tits (Cyanistes caeruleus) during
winter can advance laying dates and increase fledging success in the subsequent breeding season [4]. In
a natural setting, proxies for resource availability, such as body condition, relate pre-migration condition
of snow geese (Chen caerulescens atlantica) to breeding onset, with individuals of high body condition
arriving at the breeding grounds earlier and laying eggs earlier in the season [5]. The advantage of
carrying stored energy (e.g. in the form of fat and muscle) from wintering areas to the breeding grounds is
presumably that the energy requirements for breeding may not meet the food availability on the breeding
grounds [6]. Similarly, resident species can encounter important temporal variability of their prey, so that
the food availability may not be sufficient during the breeding season and that stored energy could confer
an important advantage during breeding. In any case, females (and males depending on the species)
need an important energy budget to breed [7] which can be accumulated before breeding or acquired
gradually during breeding, the capital or income models [7]. In practice, the dichotomy between income
and capital breeders does not discriminate or explain fully the source of stored reserves for breeding
[8–10]. Surely, there is no clear dichotomy between capital and income breeding; rather these two extreme
strategies set the life-history strategy range in between which organisms have to compromise, so that
most species actually exhibit a mixture of these two strategies. Conditions between breeding seasons,
i.e. inter-breeding season, have the ability to shape life histories [3] as some species may have carryover benefits of acquiring good physical condition at this time. However, the difficulty of monitoring
certain species continuously throughout the inter-breeding season has limited our ability to understand
the mechanisms behind carry-over effects.
Reproductive decisions begin at the inter-breeding season when individuals can decide where to
breed, who to breed with and when to initiate a breeding attempt [11]. The importance of these
decisions is usually species-specific, owing to differences in life-history strategies among species. Once a
breeding attempt has been initiated, a parent or parents (in bi-parental species) must consider how they
will balance the energy requirements of the breeding attempt (such as incubating egg(s) and feeding
young) with their own energy requirements [12]. Parents who are better able to manage the trade-off
between competing energy requirements are more likely to successfully raise young to independence
and consequently improve their reproductive success [13]. Those that are less efficient at balancing these
demands are more likely to fail reproduction [13].
In little penguins, as is the case for most birds, studies that assess mechanisms driving variation in
individual fitness have mainly focused on conditions and events during the breeding season, at the most
energetically demanding phase of the annual life cycle [14]. From such work, it is clear that body mass
or body condition of little penguins during the breeding season is related to their timing of breeding,
breeding success and is related to an individual’s foraging behaviour during chick rearing [15,16].
There is limited work outside the breeding season, but in the case of little penguins, there is evidence
of parents investing in future breeding during the inter-breeding season (e.g. maintaining a nest site
and associating with previous and future breeding partners; [17]), which indicates potential for carryover effects on conditions experienced at this time on subsequent breeding. Indeed, the general body
condition of adult little penguins (i.e. mean adult mid-sex weight), specifically during the winter month
of August (i.e. middle of the inter-breeding season), is negatively correlated with annual mean laying
date in the subsequent breeding season [18]. However, until recently, establishing details about interindividual and inter-annual elements of such carry-over effects has been limited by the ability to monitor
known individuals continuously throughout their breeding cycle and across multiple years. Adult body
mass does fluctuate over time [19] and has been related to changes in prey distribution and abundance
[20], diet [21], energy requirements [14] and breeding chronology [15]. Further, there is evidence of
individual differences in foraging ability, such that some individuals seem to be better equipped to
manage periods of poor food availability than others [16]. While the mechanisms are not clear, little
penguins that breed early are more likely to hatch their eggs successfully and produce heavier chicks
[22]. Earlier laying is also more likely to result in relaying and, consequently, more clutches per season
[17]. Although this suggests there should be selection for early breeding, the spread of laying dates can
3.1. Monitoring little penguins
The study site was located on the Summerland Peninsula on Phillip Island (38◦ 30′ S, 145◦ 15′ E), Victoria,
Australia [25]. During each breeding season between 2002/2003 and 2008/2009 (2002 and 2008 for
brevity), 100 artificial penguin burrows were monitored three times a week to determine individual
laying dates (date first egg was laid for the season) and individual breeding success (the number of
chicks fledged (0, 1 or 2) relative to the number of eggs laid (0, 1)). Birds were implanted with numbered
23 mm ISO HDX transponder (initially TIRIS, USA and later Allflex, Australia) either as chicks prior to
fledging or when first encountered as an adult. Marked penguins were monitored continuously through
an automated penguin monitoring system [26], which recorded presence and body mass of individual
penguins every time they arrived or departed from the colony [25]. Like all penguins, little penguins
have a single catastrophic moult [27] when they moult all feathers at once. Prior to moult, little penguins
almost double their body mass foraging at sea before fasting for two to three weeks ashore with a
sharp decrease in body mass [28]. Therefore, the attendance patterns and changes in body mass of little
penguins were used to establish the start and end of moult. Adult penguins were sexed using bill depth
measure [8].
At Phillip Island, the little penguin’s moult typically occurs in February–March [28]. As a resident
species, they continue to come ashore during austral autumn and winter months, travelling between their
colonies and foraging at sea. In spring, their attendance ashore increases until laying a clutch of two eggs
[25] in their second and third year after fledging [24]. Given that the moult is a predictable annual event,
we defined the inter-breeding season as the period between the end of moult and subsequent laying date.
As winter has the lowest productivity in temperate waters [29], we then expected the greatest disparity
in foraging [21] and lowest colony attendance [17]. We identified the month of consistently lowest
attendance by calculating the mean frequency of attendance per penguin (i.e. the number of individual
crossings relative to the number of penguins) within each month of the year. The month of consistently
lowest attendance across the 7 years (defined as ‘winter’) was subsequently a cut-off month to split the
inter-breeding into three periods: moult-recovery, winter [30] and pre-breeding. The winter month was
used to assess the potential for inter-breeding season carry-over effects on subsequent breeding.
3.2. Recording body mass
An individual’s body mass, presence and identification (ID) were recorded each time little penguins
arrived at the colony from January 2002 to the December 2008. The automated penguin monitoring
................................................
3. Methods
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span over five months within a breeding season [17,22,23]. These variations in parent’s ability to prepare
for breeding support the hypothesis that there are some carry-over effects from the inter-breeding season
to breeding.
Here, we used a detailed, longitudinal dataset of body mass of known individuals recorded every time
the individual moved in and out of the colony over a 7 year period to further develop our understanding
of the importance of winter condition on subsequent breeding. Specifically, using this dataset, we were
able to separate ‘annual effects’, from within-year ‘individual effects’. We hypothesized that individuals
in better condition during the inter-breeding season will be in a better position to breed earlier and
perhaps attain greater reserves (or capital) in the following months leading up to breeding (i.e. individual
effects). Alternatively, in years when conditions are better than average in the inter-breeding season,
individuals will be more likely to breed earlier compared with other years (i.e. annual effects). The
winter months of the inter-breeding season are particularly characterized by long foraging trips, far
from the colony [19], low food consumption [21], high field metabolic rate [14] and low body mass [24].
This suggests penguins may be ‘working hard’ to find food resources at this particular time within the
inter-breeding season. Indeed, this is likely given that prey biomass is low and prey are more sparsely
distributed during winter [20]. Therefore, in this study, we focused our attention on the carry-over effects
of body mass in the worse winter month (i.e. that in which they appear to be working hardest). In line
with this, we expect body mass to be lower in this winter month relative to previous months, where
penguins coming ashore will have recovered from moult, or after months, where penguins will be in
the final stages of preparing for breeding. Finally, we tested whether body mass during winter may act
as sufficient capital to buffer resource deficiencies during breeding and therefore have carry-over effects
(either individual effects or annual effects) on subsequent breeding success.
3.3.1. Changes in body mass along the inter-breeding season
Three factor variables and their two- and three-way interactions were used to predict changes in
body mass: inter-breeding season periods (moult-recovery, winter, pre-breeding), year (2002–2008 as a
factor) and sex (male or female). Body mass was first standardized to account for the sexual body size
dimorphism. Standardized body mass was calculated as an individual’s body mass relative to the global
mean and standard deviation of body mass for the relevant sex. Repeated measures of each individual
were accounted for using linear-mixed models (LMMs), where the random effect was individual identity
and the error distribution was Gaussian with an identity link function. Where there was a significant
interaction, between-group effects were assessed (i.e. comparison of the inter-breeding season periods)
by applying Wilcoxon single-rank tests.
3.3.2. Efect of body mass on laying dates and breeding success
Both members of a pair were not always recorded by the penguin monitoring system platform in every
year of the study. Rather than removing individuals from the data analysis in any given year when
their partner was not recorded in that year (n = 111 out of 519 breeding attempts), all individuals were
retained and male and female effects were assessed separately. This allowed identification of sex-specific
carry-over effects. This method assumes any potential carry-over effects of a parent’s winter body mass
on laying date and breeding success are independent of their partner’s winter body mass.
Annual differences in the level of synchrony in laying date were quantified using a Levene’s test,
and then we test for the effect of body mass on subsequent laying date or breeding success. For that,
all records of body mass within the winter month within a year were averaged (mean), so that a single
but robust mean value for each individual body mass could be related to its laying date or breeding
success. This prevented inflating degrees of freedom and reduced the chance of type II error if we had
retained all records of body mass in the analysis. We used data in two different formats in our body mass
analysis: standardized and normal (unstandardized) to address the inter-individual verses inter-annual
questions. We standardized individual’s body mass data against its ‘long-term’ mean (i.e. body mass over
the whole study period) to look at mass change across all years, i.e. whether individual body condition
and breeding success (for that individual) was related to a good or bad breeding season [33]. This
addressed our inter-annual questions. The unstandardized data were used to compare inter-individual
................................................
3.3. Data analysis
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system, designed by the Australian Antarctic Division [26], consists of a weighing platform
(calculating mass to the nearest gram), a transponder reader and a computer that stores each ID
and body mass and time–date. The weighing platform performs 50 weight readings per second
and processes raw weight data to generate an averaged weight and its standard error at the
end of each penguin’s crossing. Two or more birds could cross the weighing platform at once,
which can generate high or lower averages outside a little penguin weight range, followed by
high standard error and therefore invalidating that given body mass measurement. We made two
corrections to the body mass data to account for these errors. First, a ‘step-wise’ change in the
zero weight for the weighing system was calibrated using an object of known weight. On one
given day (i) of each month, a 1004 g object was weighed n times (n ranged 3–10) on the weighing
platform and an average deviance (x) of the monitoring system weight from 1004 g was calculated
(i.e. x(i) = Σ(1004 g—monitoring system weight(i) )/n(i) ). All records of body mass between the day of
the calibration and the previous calibration were adjusted by adding the mean deviance. Outliers were
detected and excluded from the data analysis, which included records with a body mass outside the
known range for little penguins at Phillip Island between 550 and 2130 g [24] and beyond the maximum
change in body mass for a foraging trip between 1 and 14 days long (maximum change in weight = 420 g,
mean 101.1 g ± 8; A. Chiaradia 2003–2004, unpublished data).
We used direct body mass instead of calculating body condition. While there is variation in body
size in little penguins, body mass has been shown to highly correlate with body condition (body mass
adjusted for body size, r2 = 0.8932) producing similar patterns of body mass/condition changes [31].
Also against the use of body condition is that the addition of a linear measure of body size to calculate
body condition has the potential for this index to inflate estimated variance [32]. Finally, our study had
only a small sample of marked individuals with a known linear measure of body size to calculate a much
smaller sample with body condition. For those reasons, we used body mass rather than body condition
as a measure of an individual’s physical condition between breeding seasons.
BM
year
+
BM : year
AICc
#AIC
ω
+
5245.7
0
0.74
+
5248.6
ED (%)
k
7
10
.........................................................................................................................................................................................................................
2.91
0.17
6
10
.........................................................................................................................................................................................................................
+
+
+
5249.9
4.21
0.09
13
10
.........................................................................................................................................................................................................................
5801.2
+
555.5
0
1
0.1
.........................................................................................................................................................................................................................
5811.2
565.5
0
0
AIC
#AIC
ω
k
1
13
females
BM
year
BM : year
+
+
+
ED (%)
.........................................................................................................................................................................................................................
4198.2
0
11
.........................................................................................................................................................................................................................
+
4232.3
34.1
0
6
11
.........................................................................................................................................................................................................................
+
+
4233.9
35.7
0
7
10
.........................................................................................................................................................................................................................
+
4677.7
479.5
0
1
0.1
.........................................................................................................................................................................................................................
4689.5
490.3
0
0
.........................................................................................................................................................................................................................
differences in winter body mass on breeding within a year as we expected a negative relationship
between winter body mass of individuals and timing of laying and breeding success within each given
year. Our models on carry-over effect of winter body mass on laying date used Julian laying date with
a Gaussian error distribution and an identity link function. Further models investigating the carry-over
effect of winter body mass on breeding success used the number of chicks fledged relative to the number
of eggs laid with a binomial error distribution and a logit link function. The model addressing interannual differences within individuals contained standardized body mass as a fixed effect and individual
identity as a random factor. The model addressing individual differences in a carry-over effect within a
year contained year (as a factor), unstandardized body mass in the winter and their interaction as fixed
effects, as well as individual identity as random effect. Each of these models was applied to the two
response variables: laying date and breeding success (tables 1 and 3). In the second model (i.e. interindividual differences), a significant interaction indicates different relationships between body mass and
the response variable within each year. To understand the differences in the effect of body mass on
laying date or breeding success within each year (i.e. individual differences within a year), a significant
interaction was explored further by running separate models between body mass and the response
variable for each year separately. Separate models were necessary to prevent between-year variations
from confounding the effect if only a global model were used. Given that a single breeding attempt was
monitored per individual within a year, these within-year models did not require a random effect for
individual identity.
All statistical analyses were computed using the R statistical framework, version 2.15.0 [34].
A maximum of likelihood-mixed model approach was used to assess the importance of the models, with
model selection based on the Akaike information criterion (AIC) using both #AIC and Akaike weight
(ωi ) [35]. The explained deviance (ED) was estimated as the ratio of deviance explained by the model
(null deviance − residual deviance) and the null model deviance and provided evidence for the amount
of variability explained by the model [36]. Variables were considered significant for p < 0.05, and means
are presented with standard errors.
4. Results
4.1. Monitoring throughout the breeding cycle
Between 2002 and 2008, 173 individual penguins were recorded crossing the penguin monitoring system
and were subsequently recorded breeding in the same year. Most individuals were monitored across
................................................
males
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Table 1. Model selection to explain timing of laying (Julian laying date) variability in little penguins, using the factor year to prevent from
inter-annual efects and highlight inter-individual efects of winter (July) body mass (BM). (The best it model (italics) was determined
according to the lowest Akaike’s information criterion (AIC), supported by Akaike weights (ω). k is the number of parameters in the model.
ED stands for explained deviance, i.e. the ratio of deviance explained by the model relative to the null model.)
6
10
5
0
Jan Feb Mar Apr May June July Aug Sep Oct Nov Dec
month
Figure 1. Mean frequency of attendance by individual little penguins across a penguin monitoring system at Phillip Island, Australia.
Each point represents the mean (± s.e.) of the monthly frequency of attendance in each of the 7 years (2002–2008).
Table 2. Annual data from monitoring individual little penguins (IDs) crossing an automated penguin monitoring system throughout the
inter-breeding season and the associated breeding chronology: length of the laying period (LLP in days), mean laying date (MLD in Julian
days), and breeding success (CPP, chicks per pair). (The number of individuals that were recaptured from a previous year/s are indicated
in parentheses. The number of body mass records collected by the penguin monitoring system within an inter-breeding season is divided
between the moult-recovery (MR), winter (July; W) and pre-breeding (PB) periods.)
no. body mass records
year
2002
no. unique IDs
(recaptures)
59
MR
52
W
48
PB
LLP
MLD
CPP
59
100
249
1.6
.........................................................................................................................................................................................................................
2003
67 (50)
65
64 (49)
63
64
66
45
317
1.2
.........................................................................................................................................................................................................................
2004
61
62
35
285
1.0
.........................................................................................................................................................................................................................
2005
78 (55)
69
79 (59)
79
72 (56)
72
105 (83)
102
73
75
129
284
1.2
.........................................................................................................................................................................................................................
2006
78
78
98
311
0.7
.........................................................................................................................................................................................................................
2007
70
71
108
316
1.2
.........................................................................................................................................................................................................................
2008
100
100
105
280
0.7
.........................................................................................................................................................................................................................
all years
173 (126)
.........................................................................................................................................................................................................................
multiple years (73%, 126 out of 173 individuals), so that a total of 519 breeding attempts were recorded.
Within a year, between 59 penguins (in 2002) and 105 penguins (in 2008) were monitored (table 2). Some
penguins (12 individuals; 7%) were monitored in all 7 years.
The number of penguins crossing the penguin monitoring system varied throughout the year. The
mean frequency of attendance at the colony by an individual penguin was consistently high during
the breeding months (October–January), lower during the moulting period (February and March) and
consistently lowest during the winter month of July (mean 5.88 crossings ± 0.48; figure 1). July was
therefore selected as the cut-off winter month to define the three periods of inter-breeding. Records
between moult and July being ‘moult-recovery’ period and between July and laying being ‘pre-breeding’
period. Most individuals were recorded at least once within each of the three periods (79%, 411 out of
519 individuals within each year). Some individuals crossed the monitoring system up to 54 times within
one of the three periods (mean 9 ± 0.22 crossings) and up to 12 times in July (mean 2 ± 0.09 crossings).
The global mean body mass for all seven inter-breeding periods combined was 1119 g for females
(n weights = 7038, N birds = 87, s.e. = 2.04) and 1247 g for males (n weights = 6614, N birds = 86,
s.e. = 2.17). Throughout each inter-breeding period, body mass of males and females deviated from this
global average in an inconsistent pattern among the three inter-breeding periods: moult-recovery, winter
month and pre-breeding (figure 2). Within a year, the pattern of change in body mass between interbreeding periods was also different for males and females (figure 2). Indeed, model selection identified
the sex, inter-breeding period and year three-way interaction as an important variable predicting
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mean frequency attendance
20
2002
2003
2004
2005
2006
2007
7
0.5
0.5
standardized body mass
0
–0.5
0.5
0
–0.5
2008
0.5
0
males
females
–0.5
MR
W
PB
inter-breeding stage
Figure 2. Mean standardized body mass (±s.e.) of male (solid lines) and female (dashed lines) little penguins in each inter-breeding
season period (moult-recovery (MR), winter (July) (W), pre-breeding (PB)) of 7 years (2002–2008) at Phillip Island, Australia. The dotted
line at zero provides a reference to the standard body mass for males and females throughout the study. Positive values indicate body
mass higher than the standard and negative values are lower than standard.
variation in body mass (log ratio = 30.40, d.f. = 1, p = 0.002, Akaike weight = 0.956). Males in 2005 and
2007 and females in 2005 had higher body mass in July than the moult-recovery and pre-breeding stages
(Wilcoxon tests p < 0.05; figure 2). In all years, body mass of females was higher in the pre-breeding than
moult-recovery stages (Wilcoxon tests p < 0.05). This was also the case for males in 3 years (2002, 2003,
2005), but in 2008, body mass of males was lower in the pre-breeding than moult-recovery stages and in
3 years body mass of males was not significantly different in the pre-breeding and moult-recovery stages
(2004, 2006, 2007; Wilcoxon tests with p < 0.05; figure 2).
4.2. Winter body mass, laying date and breeding success
There were significant variations in the synchrony of laying between years (Levene’s test: F6,512 = 7.97,
p < 0.001). The earliest laying date recorded was 3 August (in the year 2005), and the latest was 4 January
(in the year 2007). The spread of laying dates within a year was as short as 35 days in 2004 and as long as
129 days in 2005 (table 2). There were also annual differences in the mean laying dates, with mean laying
date being as early as 6 September in 2002 and as late as 14 November in 2003 (table 2).
................................................
–0.5
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0
This study examined body mass variation during the inter-breeding season and the effect of winter
body mass on the breeding performance of a resident seabird, the little penguin. We expected body
mass to be low during winter, when colony attendance was consistently low (this study) and penguins
conduct long foraging trips to the more distant foraging grounds [19]. While generally, body mass
increased between moult-recovery and pre-breeding, contrary to our expectations, the winter body
mass of males and females was typically equal to or higher than other inter-breeding periods. This
increase in body condition in winter was probably to restore body condition lost during the previous
energetically expensive breeding season and annual moult [14,37,38]. High body mass is usually
associated with success during the breeding period of a bird’s life cycle [9,39–43]. Here, we advance
further the importance of body mass for breeding birds by providing evidence of a carry-over effect of
body mass in winter with timing of breeding and reproductive success. In line with our predictions, in
years where parents have higher winter body mass they were more likely to lay their eggs early, and
for males (but not females), they were also more likely to breed successfully. Further, in the year of
................................................
5. Discussion
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Within a year, the timing of laying was generally not related to inter-individual differences in winter
body mass. The relationship between timing of laying within a year and winter body mass of the
male member of the pair was consistent among years (non-significant body mass and year interaction:
log ratio = 7.79, d.f. = 1, p = 0.254; table 1): a linear slope between winter body mass of males and
timing of laying consistently showing a non-significant difference from zero in all years (all t < 2.00,
p > 0.05). In other words, inter-individual differences in winter body mass of males within a year did
not explain differences in timing of laying within that year. The relationship between timing of laying
within a year and winter body mass of the female member of the pair was consistent among all years,
except 2007 (significant body mass and year interaction: log ratio = 47.67, d.f. = 1, p < 0.001; table 1): a
linear slope between winter body mass of females and timing of laying consistently showing a nonsignificant difference from zero in most years (t < 2.00, p > 0.05), except in 2007 where, contrary to our
prediction, there was a positive effect of winter body mass of females on subsequent timing of laying
(LM: slope = 0.04, t1,32 = 2.15, p = 0.039, r2 = 0.10). In other words, inter-individual differences in winter
body mass of females within a year usually did not explain differences in timing of laying within that
year, but in 2007, lighter females were more likely to breed earlier than heavier females.
Alternatively, when an individual’s body mass is standardized against its ‘long-term’ average body
mass, it is clear that annual differences in an individual’s body mass explains annual differences in
an individual’s timing of laying. In years when males and females were heavier than their average
in winter (i.e. relative to their body mass in other years), they were more likely to lay earlier in that
year (LMM: males slope = −4.21, t542 = −4.02, p < 0.001, ED = 0.3%, n = 622, N = 79, #AIC 14.1; females
slope = −4.72, t407 = −3.62, p < 0.001, ED = 0.3%, n = 488, N = 80, #AIC 11). Indeed, in the 4 years with
the earlier mean laying dates (2002, 2004, 2005 and 2008), the mean standardized body mass of both males
and females was above the ‘long-term’ average inter-breeding body mass for each of the sexes (figure 2).
Breeding success varied among years. Number of chicks raised per pair was highest in 2002 (1.6 chicks
per pair) and lowest in 2006 (0.7 chicks per pair; table 2). The value of inter-individual differences in
winter body mass of males and females to predict subsequent breeding success was inconsistent among
years (male body mass and year interaction: χ62 = 23.35, p < 0.001; female body mass and year interaction:
χ62 = 16.59, p = 0.011; table 3). In all years (but 2005), inter-individual differences in winter body mass of
males and females did not predict subsequent breeding success within the year (females: all z < 1.7,
p > 0.05; males: all z < 1.8, p > 0.05). In 2005, the variation in breeding success among individuals was
attributed to their winter body mass, both in males and females (GLM: males slope = 0.005, z = 2.731, p =
0.006, AIC = 75.07, AIC null = 89.315; females slope = 0.006, z = 2.209, p = 0.027, AIC = 72.46, AIC null =
97.32). In 2005, the average winter body mass of males and females that successfully raised two chicks to
fledging from two eggs was 1153 and 1023 g, respectively, which was greater than the winter body mass
of males and females who failed to raise any chicks from two eggs (1125 and 982 g, respectively).
Annual differences in breeding success were also related to annual effects on an individual’s winter
body mass, but for males only. In years when a male’s winter body mass was heavier (relative to other
years), it was more likely to raise its chicks to fledging in that year (GLMM slope = 0.182, z = 2.315,
p = 0.021, n = 622, N = 79, AIC = 985.26, AIC null = 988.44, #AIC 3.18). Annual differences in a female’s
winter body mass did not predict subsequent breeding success (GLMM: z = −0.865, p = 0.387, n = 488,
N = 80, AIC = 821.75, AIC null = 820.46).
BM
+
year
+
BM : year
+
AIC
865.5
#AIC
0
ω
0.984
k
13
ED (%)
15
.........................................................................................................................................................................................................................
874.4
+
8.9
0.012
6
13
.........................................................................................................................................................................................................................
+
876.4
+
10.9
0.004
7
13
.........................................................................................................................................................................................................................
987.1
+
121.6
0
1
0.3
.........................................................................................................................................................................................................................
988.5
122.9
0
0
#AIC
ω
k
ED (%)
0.80
13
22
females
BM
year
BM : year
AIC
+
+
+
662.9
.........................................................................................................................................................................................................................
0
.........................................................................................................................................................................................................................
+
666.8
3.89
0.12
6
20
.........................................................................................................................................................................................................................
+
+
667.5
4.59
0.08
7
20
.........................................................................................................................................................................................................................
820.5
157.59
0
0
.........................................................................................................................................................................................................................
+
821.2
158.32
0
1
0.2
.........................................................................................................................................................................................................................
greatest asynchrony in timing of laying (2005), inter-individual differences in winter body mass of males
influenced inter-individual differences in breeding success. While seabirds can meet energy requirements
for reproduction by foraging concurrently during breeding (i.e. income breeders) [20,44,45], our findings
support the hypothesis that they can also benefit from a carry-over effect of winter body mass on
subsequent reproduction.
Winter body mass predicted laying date and breeding success and was driven by inter-annual effects
on individuals, and less so on inter-individual differences within a year. In years of good resource
availability, individuals in good condition are more likely to breed early. This is consistent for male and
female little penguins. Male little penguins appear to be more involved in nest preparation [17], and
mate guarding [25] and females are responsible for producing the clutch of eggs. It appears that winter
conditions can influence the ability of males and females to achieve these roles earlier. Early laying
has advantages: parents have time to make multiple attempts at breeding. Laying multiple clutches
increases the potential to produce four chicks within a season [46], make a second attempt if the first
clutch is not successful, or feed chicks longer in the event that conditions deteriorate for a period of
time during the breeding season. This is particularly important in the marine environment of little
penguins, as they rely on thermally stratified water masses to locate prey and forage more efficiently,
but favourable conditions can disappear rapidly during breeding [47,48]. Similarly, inter-annual effects
on the importance of winter body mass for subsequent breeding success in males, but not females,
suggest resource availability during winter can vary dramatically and have significant repercussions
for the entire subsequent breeding season, as opposed to just timing of laying. Alternatively, the sex
difference in carry-over effect could be owing to individual variation in body size masking the signal for
a carry-over effect of female body mass in winter on subsequent breeding success. But females are only
slightly smaller (approx. 10%) than males [8], so variations in female body size alone could only have a
small influence on sexual differences. Thus, it is more likely that the sex difference in carry-over effect
of winter body mass indicates that females use reserves accumulated during winter for investment in
laying [49], whereas males use their winter reserves to increase their chance of sustaining body condition
throughout their longer periods ashore during courtship. Sustaining these fasts may result in sufficient
energy reserves to buffer against periods of poor feeding conditions during breeding and translate into
improved breeding success.
The lack of within-year differences (but 2005) might suggest either inter-individual differences in
winter body mass are less important for within-year carry-over effects onto breeding or alternatively,
................................................
males
9
rsos.royalsocietypublishing.org R. Soc. open sci. 2: 140390
Table 3. Model selection to explain breeding success (number of chicks ledged relative to the number of eggs laid) variability in little
penguins, using the factor year to prevent from inter-annual efects and highlight inter-individual efects of winter (July) body mass (BM).
(The best it model (italics) was determined according to the lowest Akaike’s information criterion (AIC), supported by Akaike weights (ω).
k is the number of parameters in the model. ED stands for explained deviance, i.e. the ratio of deviance explained by the model relative
to the null model.)
research permit issued by the Department of Sustainability and Environment of Victoria, Australia.
................................................
Ethics statement. Fieldwork protocol was approved by the ethics committee of the Phillip Island Nature Parks with a
10
rsos.royalsocietypublishing.org R. Soc. open sci. 2: 140390
inter-individual differences in quality may prevent a clear relationship from being apparent. Previous
studies in the same location during breeding have shown that little penguins have a distinct individual
quality that persists over time, regardless of sex [20]. It may be that good quality individuals are able to
efficiently require resources when they are needed and therefore do not need to acquire high levels of
reserves in winter in order to breed early. Or perhaps it is differences in experience, as demonstrated
in breeding and foraging efficiency [22,50,51] that result in some individuals using winter reserves
to improve their breeding potential, whereas others are less equipped to capitalize on this carryover benefit. The differences only observed in 2005 illustrated that an exceptional good winter could
influence subsequent breeding. Under such favourable conditions, individuals with greater winter body
mass could better manage the unpredictable conditions in winter. Consequently, they would be better
equipped to manage the costs of a breeding attempt and benefit from greater reproductive success. The
distinction between inter-annual effects and inter-individual effects highlights the benefits of applying
our analytical approach to longitudinal data on individuals.
Variation in reproduction can be explained by changes in many factors immediately prior to and
during breeding, such as food availability [33] and sea surface temperature [18,23,48], pair bond duration
[22], foraging performances [52], age and experience [53]. Further to that, our significant results that
winter body mass explains variability in timing of breeding and reproductive success illustrate the
importance of a carrying-over effect of winter body mass to the subsequent breeding. The body reserves
can influence the birds’ ability to sustain periods of fasting, with higher reserves allowing individuals
to fast longer [54–56]. If large reserves reduce an individual’s dependence on local resource availability,
then even during lower resource availability these parents sustain parental duties: establish a breeding
site and partner sooner, while still investing in a clutch of eggs, enabling them to breed earlier than lighter
parents. If winter condition is maintained up to the egg-laying period, parents would benefit from fasting
ability during incubation. The ability to fast during incubation is important in bi-parental care systems,
as it can allow parents to continue incubation if the partner has an extended foraging trip [56,57]. This
can improve synchronization of incubation shifts, which reduces the risk of nest failure and improves the
reproductive success [25,57]. Alternatively, if lighter parents cannot sustain fasts, they may only be able to
meet energetic requirements of breeding if there was high food availability close to the breeding site. One
strategy to manage the risk of meeting energy demands of breeding without jeopardizing the parent’s
survival is to acquire and maintain good body condition while preparing for breeding, as suggested in
this study.
Body mass can influence foraging behaviour of parents and subsequently limit an individual’s ability
to balance energy between provisioning and self-maintenance [58]. Parents with higher body mass
exhibit a greater capacity to feed their chicks while maintaining their own condition, resulting in heavier
chicks at fledging [16]. In little penguins, parents conduct several short trips in a row to feed the chicks
often and abundantly until their body mass decreases to a point that they go out for longer trips to restore
their reserves [13]. Little penguins with higher body mass may then be able to conduct a higher number
of short trips than their lighter conspecifics, a behaviour increasing their reproductive success [13].
Similarly, puffins and Antarctic petrels with higher body mass feed their chicks more than those parents
with lower body mass [59]. In little penguins, Zimmer et al. [53] found no relationship between body mass
of individuals and their diving behaviour, but Saraux et al. [13] found body mass was an important factor
influencing an individual’s foraging trip duration. If body mass does influence an individual’s ability to
balance energy between provisioning and self-maintenance during chick provisioning, this may explain
the relationship between body mass at winter and reproduction.
The link between body mass during the inter-breeding period and subsequent breeding warrants
further investigation on whether there is an optimal mass to breed and whether birds skip breeding
under a certain threshold as shown in blue petrels (Halobaena caerulea) [55]. While being heavier is
generally beneficial for breeding, there are physiological and strategic adaptations to lighter body
mass, including more efficient locomotion, improved foraging efficiency and reduced predation risk
[60]. To determine the importance of body mass for breeding will, therefore, require knowledge of
energetic costs of locomotion for a parent of varying body mass and a better understanding of strategies
used by parents to accommodate changes in energy demands of the breeding attempt (e.g. higher
during chick rearing). If there is an optimal body mass for breeding, then conditions influencing
body mass prior to breeding appear to be important in determining timing and level of parental
investment into a breeding attempt, and thus evidence of a carry-over effect between periods of the
breeding cycle.
Data accessibility. Meta data are available on National Ecological Meta Database at the Bureau of Meteorology, Australia,
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Acknowledgements. We are grateful for all people who assisted on the data collection, in particular P. Wasiak, P. Fallow,
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Author contributions. M.S. collected field data in 2006 and 2008, processed data, carried out data analysis and statistical
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Funding statement. This work was supported by research and travel grants from BHP-Billiton, Penguin Foundation and
Department of Environment and Sustainability of Victoria, Australia and Australian Academy of Science.
Competing interests. We have no competing interests.
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