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 13
6 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 0
1& 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 1Š  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 3
27& for d15N and 0
09 & 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] = 31
4, P < 0
001, 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] = 37
37, P < 0
001, Table 4). Simple main effects tests identified significant differences in d13C values within prebreeding groups between years (F[1, 188] = 12
59, P < 0
001). 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] = 278
78, P < 0
001, Table 4). For d15N, ratios differed significantly between reproductive stages (F[1, 188] = 31
31, P < 0
001, 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] = 56
63, P < 0
001, 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  21
3 95% 17 12 231 711 523
8  27
6 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] = 205
6, P < 0
001) and d15N (F[4, 40] = 136
8, P < 0
001). Anchovy had the most enriched mean d13C value ( 18
16  0
36&, Fig. 1), whereas blue sprat had the most depleted d13C value ( 21
07  0
46&). Anchovy displayed the highest d15N signature (18
24  0
89 &), and juvenile pilchard contained the most depleted d15N signature (11
48  0
31&, 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 1
81 1
76 0
1 0
62 Nest success Number of fledglings per successful nest Annual reproductive success 0
18 0
73 1
11 1
57 0
23 1
54 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 19
02 20
48 18
42 18
68     Mean  SD Range 0
46 0
53 0
94 0
59 20
26 to 22
26 to 20
32 to 21
42 to 18
42 19
59 16
96 16
2 17
65 18
42 18
77 20
24     Range 1
42 0
6 2
42 0
86 13
24 to 19
41 16
72 to 20
15 13
12 to 21
58 16
2 to 21
70 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 4
8 106 71 1 1 1 1 1 188 46 84 5 278 1 1 1 188 Mean square 4
78 105
92 0
38 F P 76
1 145
6 37
4 12
6 278
8 <0
01 <0
01 <0
01 <0
001 <0
001 31
3 56
6 3
6 <0
001 <0
001 >0
05 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 0
5 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). 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