Functional Ecology 2013
doi: 10.1111/1365-2435.12216
Linking dietary shifts and reproductive failure in
seabirds: a stable isotope approach
Nicole D. Kowalczyk*1,, Andre Chiaradia1,2, Tiana J. Preston1 and Richard D. Reina1
1
School of Biological Sciences, Monash University, Clayton, Victoria 3800, Australia; and 2Research Department, Phillip
Island Nature Parks, PO Box 97, Cowes, Victoria 3922, Australia
Summary
1. Diet-related breeding failure in seabirds has been attributed to declines in key prey abundance, the quality of prey and overall prey availability. However, identifying which aspect of
diet is responsible for reproductive failure is challenging due to the practicalities of measuring
prey utilization and the actual availability and abundance of those resources.
2. In this study, stable isotope-based Bayesian models, in combination with indices of resource
availability, were used to assess the links between prey availability, seabird diet and reproductive success in a generalist, inshore top predator, the little penguin, Eudyptula minor.
3. The most probable causes for the sharp decrease in little penguin reproductive performance
were diminished localized populations of anchovies, Engraulis australis, in combination with
the scarcity of alternative prey. Low dietary diversity and the consumption of low trophic
value prey were observed in this period. In the contrasting following year, penguins consumed
increased levels of anchovy as well as a high diversity of prey. High dietary diversity and the
consumption of high trophic value prey were observed in birds’ pre-breeding and breeding diet
and likely led to early breeding and high reproductive success.
4. Our results highlight that resource abundance and the availability of a variety of prey taxa
are critical factors in enabling this inshore seabird to adjust to changes in environmental conditions and fluctuations in prey.
5. An understanding of seabird diet is integral to their conservation and management. Monitoring seabird trophic niche dimensions and reproductive parameters can elucidate causes for
population declines and can provide information about particular prey species and foraging
locations that require protection.
Key-words: Bayesian models, isotopic niche width, seabird ecology, stable isotopes
Introduction
According to the life-history theory of senescence, when
faced with resource limitations, adults of long-lived species
are predicted to favour their own condition over that of
their young in order to increase their lifetime reproductive
success (Stearns 1992). Seabirds are generally long lived,
and their reproductive output and offspring survival are
often used as indicators of resource levels available to parents during breeding (Monaghan, Nager & Houston 1998;
Weimerskirch et al. 2003; Apanius, Westbrock & Anderson 2008; Fairhurst et al. 2011). Several seabird studies
have shown that limited resources can deplete parental
energy reserves to the point where the parent/parents
decide to abort breeding (Erikstad et al. 1997;
*Correspondence author. E-mail: nicole.kowalczyk@monash.edu
Weimerskirch et al. 2003) or may prevent the birds from
breeding at all (Chastel, Weimerskirch & Jouventin
1995b). Likewise, offspring condition and phenotypic
development have been found to vary depending on adult
condition and food availability, indicating the extent to
which chicks face the costs of reproduction (Monaghan
et al. 1989; Chastel, Weimerskirch & Jouventin 1995a;
Apanius, Westbrock & Anderson 2008).
Understanding the links between resource availability,
seabird diet and reproductive success is integral to seabird
conservation and management. Dietary changes have been
linked to population declines and can provide information
about foraging conditions, particular prey species and foraging locations that require protection (Wanless et al.
2005; Camphuysen et al. 2012; Karnovsky, Hobson &
Iverson 2012). However, identifying which resource characteristics are directly linked with poor reproductive
© 2013 The Authors. Functional Ecology © 2013 British Ecological Society
2 N. D. Kowalczyk et al.
performance in seabirds is challenging due to the practicalities of measuring prey utilization and the actual availability and abundance of those resources.
Stable isotopes are increasingly used to evaluate
resource utilization in seabirds because of their ability to
provide information on spatial and temporal patterns of
habitat useand prey assimilation (Hobson, Piatt & Pitocchelli 1994; Quillfeldt et al. 2008; Newsome et al. 2012).
When two or more stable isotope signatures are presented
in a-space, they essentially represent the isotopic niche of
individuals or populations and can be used to identify
shifts in isotopic niche width and isotopic niche position in
response to fluctuations in resource availability (Jackson
et al. 2011). These parameters can then be used to test foraging theory, to study characteristics of predator–prey
interactions, and trophic diversity (Layman et al. 2012).
Furthermore, stable isotopes integrate dietary information
that reflect specific periods of time and can be used to provide information about a species’ dietary requirements at
critical life-stages, including the pre-breeding and reproductive periods (Inger & Bearhop 2008; Tierney et al.
2008). In spite of the valuable information stable isotopes
provide, they cannot be used alone as an index of resource
abundance; other measures of prey availability and abundance are necessary to determine the impact of resource
fluctuations on seabird breeding performance.
The foraging dynamics of little penguins (Eudyptula
minor) provide an excellent opportunity to better understand the links between resource availability and seabird
reproductive ecology. Little penguins have one of the shortest foraging ranges among seabirds and generally remain
inshore, within 20 km of their colony during breeding (Collins, Cullen & Dann 1999; Hoskins et al. 2008; Preston
et al. 2008). Their population dynamics are therefore largely regulated by local prey availability and their reproductive success is strongly influenced by fluctuations in local
resource abundance (Numata, Davis & Renner 2000; Chiaradia, Costalunga & Kerry 2003; Chiaradia & Nisbet 2006).
The St Kilda little penguin colony forages exclusively
within Port Phillip Bay during the breeding period (Preston et al. 2008; Chiaradia et al. 2012). The relatively low
habitat complexity of this semi-enclosed embayment (Gratwicke & Speight 2005), and the small foraging range
exploited by little penguins improve our ability to estimate
actual resource abundance in the Bay, to detect changes in
little penguin resource use, and to determine how these
predators respond to fluctuations in their resources.
Anchovies (Engraulis australis) have displayed a perennial and dominant presence in the St Kilda little penguin
diet, ranging from a minimum relative prey proportion of
36% in 2008 (Preston 2010) to a maximum proportional
contribution of 78% in 2004 (Chiaradia et al. 2012). Their
strong dependence on anchovy between 2003 and 2008 led
to the prediction that changes in the distribution and
abundance of anchovies (through overfishing, variation in
recruitment, etc.) would have a negative impact on the
reproductive success of this penguin colony, given that
anchovy is the only species of prey that is available year
round within the Bay (Chiaradia et al. 2012) and its peak
availability coincides with the breeding period of little penguins (Hirst et al. 2011).
In this study, we investigated the influence of prey
availability and diet on the reproduction of little penguins at St Kilda. Data from independent fish monitoring
programmes in Port Phillip Bay (Hirst et al. 2010, 2011)
were used to provide indices of actual prey abundance
and availability within the Bay, over 2 years with low
anchovy abundance (2010 and 2011). Penguin tissue stable d13C and d15N isotope ratios were used to monitor
how the pre-breeding and breeding diet of penguins
shifted in response to fluctuations in prey. We then
assessed how changes in prey availability and shifts in
penguin diet may have influenced the reproductive success of this long-lived seabird.
Materials and methods
STUDY SITE
The study was carried out at St Kilda breakwater, within Port
Phillip Bay, Victoria, Australia (37°51′S, 144°57′E) during the
2010 and 2011 breeding seasons. The Bay is a semi-enclosed tidal
embayment and encloses an area of approximately 1930 km2, with
a mean depth of 136 m – although over half the bay is <8 m deep
(Harris 1996). The breakwater is located in the north of Port Phillip Bay and comprised cobble to boulder size rocks. The spaces
between rocks have been occupied by c. 800–1000 little penguins
who reside on the breakwater year round (Z. Hogg, unpublished
data). Breeding seasons are defined as beginning on 1-May and
finishing on 30-February of the following year and are referred to
the calendar year in which they commenced. Little penguins typically lay a clutch of two eggs (range: 1–3 eggs; Stahel & Gales
1987), and up to three clutches in a season (Preston 2010).
FIELD PROCEDURES
A subset of 44 nests in 2010 and 45 nests in 2011 were monitored
two–three times a week during the breeding seasons. Nest contents
were monitored to identify mated pairs (via passive integrated
transponders, Trovan Ltd., Australia) to assess laying date, hatching date and hatching and fledging success. As monitoring was
carried out two–three times per week, at times, exact lay and
hatching dates were not known. In such cases, lay and hatch dates
were estimated as mid points between visits.
Annual reproductive success (counted as mean number of young
reared per female) was calculated using the equation:
ARS ¼ c1 s1 k1 þ c2 s2 k2 þ cn sn kn
where c1, c2 and cn are the number of clutches laid per female,
and s1, s2 and sn are the probabilities of rearing young from the
first, second and nth clutch respectively and where k1, k2 and kn
are the mean number of young reared in successful first, second
and nth broods respectively in accordance with the methods outlined in Murray (2000). Additional breeding parameters were
defined as follows: (i) egg success, the proportion of chicks fledged
out of eggs laid; (ii) nest success, the number of successful nests/
the number of nests with eggs; and (iii) the number of fledglings
produced per successful clutch, the total number of fledglings/
number of successful nests (Murray 2000).
© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology
Implications of trophic niche shifts in seabirds
During late incubation or early chick guard (chick rearing) the
adult was temporarily removed from the burrow, an empty eggshell
sample was obtained, and a blood sample was collected from the
adult. Because adults alternate incubation and chick guard shifts
every 1–2 days, we were able to sample both adults of the pair in
most cases. Adults were sexed based on bill depth measurements
(Arnould, Dann & Cullen 2004).
SAMPLE COLLECTION, PROCESSING AND ANALYSIS
Eggshell samples
Eggshells provide information on diet during a brief period prior to
breeding (Schaffner & Swart 1991; Polito et al. 2009). Eggshells were
collected opportunistically between August and October from 29
nests in 2010 and 25 nests in 2011. Isotope values were obtained from
the organic content of shells. Carbonate was removed by adding
2 9 50 lL aliquots of 10% HCl to 10 mg of finely ground shell in a
glass vial. Acidified samples were placed in an oven for 48 h at
60 °C. These steps were repeated until no effervescence of inorganic
matter in the shell was observed. Between 6 and 8 mg of ground eggshell was loaded into silver capsules (4 9 6 mm) for isotope analysis
following protocols outlined in Polito et al. 2009.
transferred to glass vials and dried at 60 °C until they reached a
constant weight. Dried samples were ground and two samples
were obtained from each vial; one was immediately prepared for
stable isotope analysis (samples were freeze dried, ground and
loaded into tin caps) and the second underwent lipid extraction
(Sweeting, Polunin & Jennings 2006; Logan et al. 2008). To
remove lipids, samples were placed in glass centrifuge tubes and
submerged in 2 : 1 chloroform: methanol solution. Samples were
stirred and centrifuged for 10 min at 1318 g. The supernatant containing solvent and lipids was removed. This process was repeated
until the supernatant solvent was clear and colourless after centrifugation. Samples were then dried at 60 °C for 24 h. Treated samples were freeze dried, ground and loaded into silver caps.
STABLE ISOTOPE ANALYSIS
Samples were analysed on an ANCA-GSL2 elemental analyser
and resultant CO2 and N2 gases were analysed using a coupled
Hydra 20 : 22 isotope ratio mass-spectrometer (Sercon Ltd.,
Cheshire, UK) with every five unknowns separated by laboratory
standards. Sample precision was 01& for both d13C and d15N.
Stable isotope abundances are expressed in d notation in per
mille units (&) following the equation:
d13 C ord15 N ¼ ½ðRsample =Rstandard Þ
Blood samples
Whole blood reflects food assimilated over a period of 3–4 weeks
and in this study reflects the incubation and/or guard period (Hobson, Alisauskas & Clark 1993). Approximately, 150 lL of blood
was collected from the tarsal vein of 50 adults (23 females, 27 males)
in 2010 (from September to January) and from 88 adults (45 females,
43 males) in 2011 (from August to November). Blood samples were
transferred onto a microscope slide (Bugoni, McGill & Furness
2008), dried at ambient air temperature in the field before being frozen in the laboratory. Blood samples were freeze dried before being
ground, loaded into tin caps, weighed and sealed. Lipids were not
extracted prior to analysis as the lipid component of blood is less
than 1% of the total wet mass of whole blood (Bearhop et al. 2000).
Prey samples
Clupeoids are the predominant prey for little penguins and usually
comprise a large percentage of their diet (Cullen, Montague & Hull
1991; Chiaradia et al. 2010, 2012). Four species of clupeoids that
were sampled in the ‘Fish Stock and Recruitment Monitoring
Programme’ (see details below) and which have been found in the
gut contents of St Kilda little penguins previously (Preston 2010)
were included in this analysis. Prey items were obtained from commercial fishing boats that operate within the Bay in December
2011, corresponding with the end of the 2011 breeding season. Prey
items included: anchovy (Engraulis australis), juvenile and adult pilchards (Sardinops sagax), sandy sprat (Hypherlophus vittatus) and
blue sprat (Spatelloides robustus). Pilchards were measured and categorized into age classes (juvenile, young adult) according to size.
The juvenile cohort corresponded to standard lengths < 70 mm,
and young adults correspond to lengths between 105 and 155 mm
in accordance with length-frequency data for pilchards obtained
from commercial catches in Port Phillip Bay (Neira, Sporcic &
Longmore 1999). Size variations in other prey sources were not distinct, and these preys were therefore not separated into age classes.
Prey treatment
Approximately 3 g of tissue was obtained from the caudal muscle
of clupeoids. Samples were thawed, rinsed in deionized water and
3
1 1000;
where R = (13C/12C or 15N/14N) of the sample and standards or
where R is the ratio of the heavy (rare) isotope to the light (common) isotope in the sample and standard (Fry 2006). The international standards for carbon and nitrogen stable isotope rations
were Pee Dee Belemnite and atmospheric N2 respectively.
INDICES OF PREY ABUNDANCE AND DIVERSITY WITHIN
PORT PHILLIP BAY
Indices of prey abundance and diversity within Port Phillip Bay were
obtained from published data, measured over a 4 year period as part
of the ‘Fish Stock and Recruitment Monitoring Programme’ by the
Department of Primary Industries, Queenscliff, Victoria (Hirst et al.
2010, 2011), hereafter referred to as ‘independent fish surveys’. The
abundance and distribution of anchovy, and other pelagic species
within the Bay, were monitored during May in 2010 and during May
and June in 2011 using a demersal trawl net and sonar, coinciding
with the wintering/pre-breeding period in little penguins. In 2010, 22
sites were monitored using trawl and sonar and the remaining 45
sites were monitored using sonar only. In 2011, 32 sites were sampled
using trawl and sonar and 35 sites were sampled using only sonar. A
‘fixed-site’ sampling design was used to provide a direct species
diversity and abundance estimate (Table 1) (Hirst et al. 2010, 2011).
We referred to dietary analyses of the St Kilda and Phillip
Island little penguin colonies to assess how many of the species
identified in the fish survey are targeted as potential prey taxa by
little penguins (Table 1) (Chiaradia et al. 2010; Preston 2010).
STATISTICAL ANALYSIS
Student’s t-tests were used to assess whether there were significant
differences in the stable nitrogen and carbon isotope blood signatures between sexes. No sex-related differences in d13C and d15N
values were identified and isotope signatures were subsequently
pooled between sexes for further analysis. After assessing assumptions for factorial ANOVA, differences in d13C and d15N between
years and breeding stage were tested using two factor ANOVA with
type III sums of squares. For d13C, a simple main effects test,
using breeding stage as a factorial subset, was analysed using
MSResid from the global model.
© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology
4 N. D. Kowalczyk et al.
Differences in d13C and d15N between prey species (and between
juvenile and adult pilchard) were examined using multivariate
analysis of variance (MANOVA).
Stable Isotope Analysis in R (SIAR) (Version 4.1.3) (Parnell
et al. 2008) was used to calculate the isotopic niche width of consumers and to estimate the relative contribution of prey taxa to
penguin diet. Standard ellipse areas were calculated to measure
the mean isotopic niche of pre-breeding and breeding adults. Standard ellipses represent the isotopic niche width of 40% of typical
individuals within the groups based on bivariate normal distributions. We used the corrected version of the standard ellipse area
(SEAc) to account for the loss of an extra degree of freedom when
calculating bivariate data and to control for small sample sizes
(Jackson et al. 2011). SEAc was used to calculate the degree of
dietary overlap among groups. Density plots showing the confidence intervals of standard ellipse areas were then calculated to
quantify isotopic niche width to measure dietary similarity among
groups (Jackson et al. 2011).
Mixing models were solved within the SIAR Bayesian framework. A non-informative Dirichlet prior distribution, with zero
concentration dependencies, and default SIAR MCMC estimation
(iterations = 2 9 105, burning = 5 9 104, thinning = 15) were
included in the model. An isotopic mean discrimination factor of
327& for d15N and 009 & for d13C was applied to mixing models. These factors were based on fractionation values obtained
from little penguins fed experimentally with a monospecific pilchard (Sardinops sagax) diet (A. Chiaradia, unpublished data).
Diagnostic matrix plots were used to identify correlations between
sources to identify the performance of the model and to check for
differentiation between sources. Proportion densities for each
group were then assessed and are displayed with 50%, 75% and
95% credibility intervals in figures. All statistical analyses were
performed using R software, version 2.14.1 (R Development Core
Team 2011).
Results
REPRODUCTIVE SUCCESS
In 2010, the onset of egg-laying commenced on 8 July
2010 and peak laying activity occurred at the start of October. The last clutch was laid on 28 December 2010. The
following year (2011), egg-laying commenced 15 May 2011
with peak laying activity observed in August. The last
clutch was laid on 20 November 2011. Mean lay date
occurred significantly earlier in 2011 than in 2010
(t[107] = 314, P < 0001, t-test). Mean clutch size did not
differ significantly between years, however, in 2010, the
monitored subset of 44 females laid a total of 92 eggs in 51
separate clutches and in 2011, 45 females laid a total of
119 eggs in 64 clutches, laying a higher number of double
clutches and demonstrating higher reproductive potential
than observed in 2010. Only 10% of eggs in 2010 produced
chicks compared to 62% in 2011. In 2010, 18% of clutches
produced fledglings compared to 73% in 2011. The number of fledged chicks per female in 2010 was considerably
lower than observed in 2011 (Table 2).
EGGSHELL AND BLOOD STABLE ISOTOPE RATIOS
The stable isotope values (d13C and d15N) of little penguin eggshell (pre-breeding diet) and blood (breeding
diet: incubation and chick guard) from years 2010 and
2011 varied within and between years (Table 3). A significant year by breeding stage (pre-breeding and breeding)
interaction was found for d13C values (d13C: F[1,
188] = 3737, P < 0001, Table 4). Simple main effects tests
identified significant differences in d13C values within prebreeding groups between years (F[1, 188] = 1259,
P < 0001). The 2011 pre-breeding diet was more
enriched in d13C relative to the 2010 pre-breeding diet
indicating that in 2011 females consumed greater quantities of prey with energy derived from benthic primary
producers while in 2010, females consumed prey with
energy derived from the euphotic zone. Similarly, in
2011, breeding penguins consumed prey with a more
enriched basal resource (inshore basal resource) than
2010 breeding adults (F[1, 188] = 27878, P < 0001,
Table 4).
For d15N, ratios differed significantly between reproductive stages (F[1, 188] = 3131, P < 0001, Table 4) where
breeders consumed prey of higher trophic value than prebreeding females. In 2011, pre-breeding and breeding
adults consumed prey with a higher trophic value than
2010 pre-breeding and breeding adults (F[1, 188] = 5663,
P < 0001, Table 4).
Table 1. Indices of prey abundance and diversity within Port Phillip Bay measured in 2010 and 2011 as part of the 4 year ‘Fish Stock and
Recruitment Monitoring Program’ conducted by the Department of Primary Industries, Victoria, Australia (Hirst et al. 2010, 2011)
Port Phillip Bay anchovy study results
Anchovy abundance (number of individual anchovies caught in surveys)
Estimated total anchovy biomass for Port Phillip Bay (tonnes)
Percentage of anchovy in total pelagic fish caught
Number of pelagic species identified in surveys
Number of pelagic species identified in survey that have been
previously identified in little penguin gut contents
(Chiaradia et al. 2010, Preston 2010)
Total abundance of all pelagic species previously identified in
penguin gut contents (number of individuals caught in surveys)
2010
2011
104 050
299 213
95%
17
12
231 711
5238 276
70%
15
10
111 214
332 865
Commercial catch (tonnes) values of anchovy in Port Phillip Bay between years 2003 and 2011: 03/04 – 61 tonnes, 04/05 – 48 tonnes, 05/
06 – 34 tonnes, 06/07 – 32 tonnes, 07/08 – 86 tonnes, 08/09 – 55 tonnes, 09/10 – 44 tonnes, 10/11 – 19 tonnes, 11/12 – insufficient data to
report. Data obtained from the Department of Primary Industries 2013.
© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology
Implications of trophic niche shifts in seabirds
PREY STABLE ISOTOPE RATIOS
A relatively wide range of isotopic values of prey was
observed among species (Fig. 1). There were significant differences among species for d13C (F[4, 40] = 2056, P < 0001)
and d15N (F[4, 40] = 1368, P < 0001). Anchovy had the
most enriched mean d13C value ( 1816 036&, Fig. 1),
whereas blue sprat had the most depleted d13C value
( 2107 046&). Anchovy displayed the highest d15N signature (1824 089 &), and juvenile pilchard contained
the most depleted d15N signature (1148 031&, Fig. 1).
5
sources (with the exception of blue sprat) displayed a mean
proportional contribution between 21% and 28%. Blue
sprat contributed marginally with a mean proportional
contribution of 4%.
Similarly, during the 2011 breeding season, adults displayed a diverse diet with similar contributions of anchovy
(29%), adult pilchard (25%) and sandy sprat (29%). Juvenile pilchard and blue sprat were detected at relatively low
levels (mean proportional contribution of 8% and 9%
respectively).
Discussion
ISOTOPIC NICHE WIDTH AND OVERLAP
The isotopic niche width and isotopic niche position of
penguins varied within and between years (Figs 2 and 3).
The smallest isotopic niche was displayed by breeding
adults in 2010 and the widest was observed several months
later in the 2011 pre-breeding diet of females (Fig. 2), coinciding with high resource diversity and abundance in Port
Phillip Bay (Table 1). In addition to the narrow isotopic
niche displayed by 2010 breeding adults, these adults consumed a higher proportion of prey with depleted 13C values leading to a substantial shift in13C position (Fig. 3).
The isotopic niche of 2010 breeding adults did not overlap
with any of the other groups indicating these adults
consumed an exceptionally 13C depleted subset of prey
compared to all other groups.
MIXING MODEL OUTPUTS
The diet of pre-breeding females in 2010 was dominated by
juvenile pilchard which had a mean proportional contribution of 45% (Fig. 4). Adult pilchards were a second significant prey resource, with a mean proportional contribution
of 24%. Anchovy and blue sprat contributed least (mean
proportional contribution of 13% and 3% respectively) to
the pre-breeding diet of penguins in 2010.
During the 2010 breeding season, blue sprat was the
most important dietary component, and had a mean proportional contribution of 57%. Juvenile pilchards were a
second significant prey resource, with a mean proportional
contribution of 34%. Anchovy contributed least with a
mean proportional contribution of 3% to the 2010 breeding diet of penguins.
In 2011, the pre-breeding diet of females was diverse
and not dominated by a particular prey species. All prey
Table 2. Reproductive success parameters collected in the 2010
and 2011 breeding seasons
Year
Mean
clutch
size
Egg
success
2010
2011
181
176
01
062
Nest
success
Number of
fledglings per
successful
nest
Annual
reproductive
success
018
073
111
157
023
154
We found that a sharp decline of anchovy abundance in
Port Phillip Bay was associated with low annual reproductive success, concurring with predictions that declines in
anchovy would have a negative impact on the reproductive
success of this colony of little penguins (Chiaradia et al.
2012). Furthermore, our results suggest that the adverse
effects of low anchovy abundance on little penguin reproductive success were exacerbated by the overall scarcity of
alternative prey taxa. The 2010 independent fish survey
documented that in addition to a 76% decline in anchovy
abundance from 2009, anchovy comprised 95% of the
total pelagic fish biomass in Port Phillip Bay ( Parry et al.
2009; Hirst et al. 2010). Low anchovy levels combined
with overall scarcity of prey coincided with the poor reproductive performance of little penguins in 2010.
The 2011 independent fish survey recorded a 75% increase
in anchovy abundance compared to 2010; however, anchovy
abundance was still significantly lower than 2010 levels
(Parry et al. 2009; Hirst et al. 2010, 2011). Anchovy comprised 70% of the combined biomass of all species of pelagic
fish in Port Phillip Bay. Pilchards, sandy sprat and blue
sprat, which are important prey for little penguins at St Kilda and elsewhere (Chiaradia et al. 2010; Preston 2010), were
significantly more abundant in 2011 than in 2010 and provided a diverse prey base for little penguins (Hirst et al.
2011). A diverse diet consisting of almost equal proportions
of anchovy, pilchard and sandy sprat are evident in our
results obtained from mixing models. In 2011, despite relatively low anchovy abundance, little penguin breeding
started early and penguins displayed high annual reproductive success. These results suggest that the abundant and
diverse prey base in Port Phillip Bay in 2011 compensated
for the decline of anchovy to some degree. Our findings highlight that while anchovy is an important prey species for little
penguins at St Kilda and across Australia (Gales & Pemberton 1990; Chiaradia, Costalunga & Kerry 2003; Chiaradia
et al. 2012), the availability of alternative prey is equally
important to their breeding performance.
PRE-BREEDING ISOTOPIC NICHE
Unconstrained by the demands of incubation and chick
rearing, pre-breeders can adopt an opportunistic and wide
ranging foraging strategy, often reflected in the diverse
© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology
6 N. D. Kowalczyk et al.
Table 3. Mean ( SD) values of stable carbon and nitrogen isotopes from little penguin eggshells and blood over two breeding seasons
d13C (&)
Year
Tissue
n
2010
2010
2011
2011
Eggshell
Blood
Eggshell
Blood
29
50
25
88
d15N (&)
Mean SD
1902
2048
1842
1868
Mean SD
Range
046
053
094
059
2026 to
2226 to
2032 to
2142 to
1842
1959
1696
162
1765
1842
1877
2024
Range
142
06
242
086
1324 to 1941
1672 to 2015
1312 to 2158
162 to 2170
Table 4. Differences in stable d13C and d15N isotope ratios between breeding stage (Pre-breeding and Breeding) and years (2010 and
2011). Bold type indicates significant effects at P < 0.05
Source
d13C
Group (Breeding stage)
Year
Group:Year
Pre-Breeding – Year
Breeding – Year
Resid
d15N
Group (Breeding stage)
Year
Group:Year
Resid
Type III sum of squares
d.f.
29
55
14
48
106
71
1
1
1
1
1
188
46
84
5
278
1
1
1
188
Mean square
478
10592
038
F
P
761
1456
374
126
2788
<001
<001
<001
<0001
<0001
313
566
36
<0001
<0001
>005
24
22
δ15N
20
18
16
14
12
–22
–20
–18
δ13C
pre-breeding diet and/or broad isotopic niche width of seabird species (Clausen et al. 2005; Hedd et al. 2010).
Although a narrow isotopic niche is not necessarily indicative of limited prey diversity (i.e. different prey taxa can
possess the similar isotopic compositions), the narrow isotopic niche in 2010 pre-breeding females was likely due to
–16
Fig. 1. Biplots represent the mean ( SD)
value of stable carbon and nitrogen isotopes from four clupeoid species obtained
within Port Phillip Bay. Symbols represent
the breeding stage of penguins.
constrained foraging conditions. Ecological opportunity
sets an upper bound on an individuals’ or populations’
niche width (Stephens & Krebs 1986), and in this study
likely constrained the ability of penguins to choose among
potential prey species. This conjecture is supported by the
independent fish survey which found that anchovy
© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology
Implications of trophic niche shifts in seabirds
7
22
20
δ15N
18
16
Fig. 2. Biplot depicting d13C and d15N isotope ratios of little penguins at pre-breeding and breeding stage in 2010 and 2011.
Ellipses represent the isotopic niche width
of 40% of typical individuals within the
group based on bivariate normal distributions.
14
2010 Pre−breeding
2010 Breeding
2011 Pre−breeding
2011 Breeding
12
–22
−21
−20
−19
−18
−17
−16
δ13C
C
A
A
B
Fig. 3. Density plot depicting the mean standard ellipse areas (represented by black dots) and their confidence intervals for little
penguins at the pre-breeding or breeding stage in 2010 and 2011.
Shaded boxes represent the 50%, 75% and 95% intervals from
dark grey to light grey. Letters indicate significant differences in
standard ellipse area between groups.
comprised 95% of the total pelagic fish biomass in Port
Phillip Bay and that overall clupeoid diversity and abundance was low (Hirst et al. 2010). Pilchard (Sardinops
sagax) comprised 90% of the remaining clupeoid biomass
after anchovy.
Mixing models indicated the dominant prey of prebreeding females were juvenile and adult pilchards (45%
and 24% dietary contribution respectively), even though
pilchard accounted for a small percentage of the total pelagic fish catch. Penguins therefore not only had to deal with
the low anchovy quantities but relied on a scarce subset of
alternative taxa. The consumption of small and scarce
clupeoids would have increased foraging effort whilst
decreasing foraging efficiency, creating an energetic
trade-off for adults. This trade-off was likely reflected in
the late onset of breeding.
Life-history theory predicts that when resources are
scarce, seabirds can skip breeding events, can delay breeding, or terminate breeding early in the breeding cycle to
maintain their own condition and future reproductive
€
potential (Drent & Daan 1980; Shealer 2001; Osterblom
et al. 2008). Skipped breeding has not been recorded in little penguins and like arctic terns (Sterna paradisaea)
(Monaghan et al. 1989) or common diving petrels (Pelecanoide surinatrix) (Chastel, Weimerskirch & Jouventin
1995a) little penguins can persevere with breeding activities
even when foraging conditions are poor (Chiaradia &
Kerry 1999). However, little penguins are known to delay
breeding when resources are scarce, presumably as a
means to time chick growth with abundant resources
(Dann et al. 2000; Chiaradia, Costalunga & Kerry 2003).
Many inshore seabird species lay clutches containing
two eggs, with some species varying this number (Furness
& Monaghan 1987). While reduced clutch size in response
to food limitation has been reported in some seabirds
(Regehr & Montevecchi 1997; Clifford & Anderson 2001;
Ainley 2002), variation in clutch size in response to food
shortages has not been reported in little penguins. The
observed invariable clutch size between years in our study
suggests that females delay breeding instead of reducing
their clutch size to increase reproductive potential.
In contrast, in 2011, the isotopic niche width of prebreeding females was broad as reflected in mixing model
results as well as the diverse prey base recorded in Port
Phillip Bay that year (Hirst et al. 2011). Overall, females
consumed prey of higher trophic value than in 2010,
potentially capitalizing on larger or more energetically
profitable prey types (Davenport & Bax 2002) to assist
with the production of eggs, which is an energetically
costly process for birds (Monaghan, Nager & Houston
1998). Their consumption of large quantities of anchovy,
© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology
8 N. D. Kowalczyk et al.
1·0
Anchovy (Engraulis australis)
Proportion
0·8
0·6
0·4
0·2
0·0
1·0
Juvenile pilchard (Sardinops sagax)
Proportion
0·8
0·6
0·4
0·2
sandy sprat, juvenile and adult pilchard coincided with
early breeding onset confirming studies that have identified abundant prey as a trigger for early breeding in this
species (Kemp & Dann 2001; Priddel, Carlile & Wheeler
2008).
Intraspecific variations in isotopic position and niche
width often reflect differences in foraging areas (Navarro
et al. 2009). However, St Kilda penguins forage in Port
Phillip Bay during the breeding season and there is no
evidence to suggest they forage outside of the Bay, in different foraging areas, during the pre-breeding period. During the non-breeding season, Port Phillip Bay becomes an
important foraging ground for penguins from nearby Phillip Island which suggests the Bay is productive at this time
of year (Collins, Cullen & Dann 1999; McCutcheon et al.
2011). Therefore, the observed differences in isotope ratios
during the pre-breeding seasons are likely reflective of variations in local prey availability, rather than a reflection of
alternative foraging sites.
0·0
1·0
BREEDING ISOTOPIC NICHE
Pilchard (Sardinops sagax)
Proportion
0·8
0·6
0·4
0·2
0·0
1·0
Sandy sprat (Hypherlophus vittatus)
Proportion
0·8
0·6
0·4
0·2
0·0
1·0
Blue sprat (Spatelloides robustus)
Proportion
0·8
0·6
0·4
0·2
0·0
2010
Pre-bre
2010
Breeding
2011
Pre-bre
2011
Breeding
Fig. 4. Mixing model estimated prey source contributions to the
pre-breeding and breeding diet of little penguins in 2010 and 2011
( 95, 75 and 50% credibility intervals).
No overlap in the isotopic position of 2010 and 2011 breeding penguins was observed suggesting a notable shift in diet
between these years. In 2010, breeders consumed greater
quantities of prey with an offshore basal resource and on
prey of lower trophic value than 2011 breeders. Furthermore, breeding penguins had access to relatively low prey
availability. These dietary characteristics were associated
with extremely low hatching and fledging success.
In bi-parental species, where incubation duties are
shared, co-ordination of nest attendance is essential to
hatching success. The low hatching success observed in
2010 may have occurred due to failed co-ordination of incubation shifts as a result of resource scarcity. When resources
are scarce during the incubation period, little penguins usually extend foraging trips to increase resource intake (Numata, Davis & Renner 2000). The prolonged foraging trip
has consequences for their fasting partner and increases the
likelihood of egg desertion and incubation failure (Numata,
Davis & Renner 2000; Kato, Ropert-Coudert & Chiaradia
2008). The high numbers of abandoned eggs in this study
suggest mismatches in nest attendance may have been largely responsible for the low level of hatching success. Similarly, the low nest success (number of successful nests/
number of nests with eggs) and low number of fledglings
produced per successful clutch in 2010 imply that the low
local abundance and availability of prey reduced the breeding performance of little penguins.
In 2011, the isotopic niche width of breeders was wider
than breeders 1 year earlier; they consumed prey with
more enriched basal resources and prey of higher trophic
value. The abundance and diversity of resources in Port
Phillip Bay in 2011 likely enabled breeders to capitalize on
energy-rich or large prey types during the energetically
demanding egg production, incubation and chick rearing
period (Gales & Green 1990). The consumption of diverse
© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology
Implications of trophic niche shifts in seabirds
and high quality prey agrees with foraging theory which
predicts that individuals should forage in ways that maximize their foraging efficiency, particularly during the
breeding season when young are dependent on parental
resources for survival (Pyke, Pulliam & Charnov 1977;
Ceia et al. 2012). Several seabird species provision their
chicks with prey of high trophic and/or nutritional value
(e.g. Magellanic penguins, Spheniscus magellanicus,Forero
et al. 2002; Adelie penguins, Pygoscelis adeliae, Cherel
2008) and this appears to be a foraging strategy to
improve resource intake to deal with the costs of rearing
chicks. In 2011, hatching success and the number of fledglings produced per successful clutch was significantly
higher than found in 2010. Furthermore, a greater number
of females laid second clutches with a high fledging rate,
confirming studies that have found second broods to indicate good foraging conditions (Johannesen, Houston &
Russell 2003; Priddel, Carlile & Wheeler 2008).
ECOLOGICAL IMPLICATIONS
Annual fluctuations in prey abundance and diversity in
Port Phillip Bay were detected through independent fish
surveys (Hirst et al. 2010, 2011) and these shifts are evident in the intra-and inter-annual isotopic characteristics
of little penguins. Measures of penguin isotopic niche
width reflected species diversity in Port Phillip Bay; however, isotopic mixing model outputs did not match the relative abundance of fish species in the Bay. This was
particularly evident in 2010 when anchovy accounted for a
small proportion of penguin diet yet comprised 95% of the
pelagic fish biomass in Port Phillip Bay. These results
either reflect temporal and spatial mismatches in fish surveys and penguin foraging areas (Fauchald 2009; Certain
et al. 2011), or highlight anomalies within mixing models
(Parnell et al. 2010; Cummings et al. 2012; Layman et al.
2012). Nevertheless, our results show that little penguins
display dietary plasticity and switch between prey types in
response to changes in prey. This likely improves their
ability to deal with declines in prey, which is particularly
important during the breeding season, when adults are
restricted in time and space, due to the need to feed their
offspring. Flexibility in the timing of breeding and reproductive output provides a further buffer against unpredictable marine resources (Gales & Green 1990; Chiaradia &
Nisbet 2006). However, the capacity of little penguins to
adjust to declines in prey is determined by resource diversity and abundance.
In certain regions, the foraging and reproductive ecology
of particular seabirds are established indicators of ecosystem status and their population demographics are used to
guide fisheries management (Hislop, Harris & Smith 1991;
Regehr & Montevecchi 1997). For example, in the North
Sea, when the breeding success of black-legged kittiwakes
(Rissa tridactyla) fell below 05 for three consecutive
years, commercial fishing of the local sandeel (Ammodytes
marinus) population was halted (Furness & Tasker 2000;
9
Lewis et al. 2001). While links between prey composition
and seabird reproductive success are established in certain
areas, defining these links requires detailed, long-term data
sets of actual prey availability and seabird breeding parameters which are often not available.
Our results highlight that by monitoring the trophic
dimensions and annual reproductive success of generalist
seabirds we can gain insight into resource diversity and
abundance in localized areas, and better understand how
prey conditions influence seabird breeding performance.
For example, a narrow breeding isotopic niche width in
association with high annual reproductive success is likely
indicative of an abundance of a particular species or subset
of prey taxa. In contrast, a narrow breeding isotopic niche
width in combination with low reproductive success likely
indicates a lack of both prey diversity and abundance.
Alternatively, a broad isotopic niche width, in association
with high annual reproductive success, likely indicates an
abundance and diverse prey base while a broad isotopic
niche and poor breeding performance suggest a diverse yet
scare prey base. This simple approach of measuring predator–prey interactions, particularly when used in combination with other indicators of ecosystem productivity and/
or dietary information, can be used as a powerful tool to
infer shifts in ecosystems.
Acknowledgements
Research was conducted under scientific permits issued by the Victorian
Department of Sustainability and the Environment (10003848, 10005601),
and approved by the Animal Ethics Committee of Monash University
(BSCI/2010/22, BSCI/2011/33). We thank Fisheries Victoria, Department
of Environment and Primary Industries for permitting us to publish results
obtained in the fish surveys and we thank Parks Victoria for permission to
work along the breakwater. Thanks to Earthcare St Kilda, particularly Zoe
Hogg, for their ongoing research and logistical support. Thanks to all field
work assistants. Funding from the Holsworth Wildlife Research Trust, Penguin Foundation, Monash University, Birds Australia, and Australian Geographic made this research possible. We also thank Phillip Island Nature
Parks for their continued support.
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Received 15 July 2013; accepted 31 October 2013
Handling Editor: Jennifer Grindstaff
© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology