Comparative Biochemistry and Physiology, Part A 181 (2015) 1–8

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Nutritional stress in Northern gannets during an unprecedented low reproductive success year: Can extreme sea surface temperature event and dietary change be the cause? Cynthia D. Franci a, François Vézina b,c, François Grégoire d, Jean-François Rail e, Jonathan Verreault a,⁎ a Centre de recherche en toxicologie de l'environnement (TOXEN), Département des sciences biologiques, Université du Québec à Montréal, C.P. 8888, Succursale Centre-ville, Montreal, QC H3C 3P8, Canada b Département de Biologie, Chimie et Géographie, Université du Québec à Rimouski, 300 Allée des Ursulines, Rimouski, QC G5L 3A1, Canada c Centre d'études nordiques, Centre de la science de la biodiversité du Québec, 300 Allée des Ursulines, Rimouski, QC G5L 3A1, Canada d Maurice Lamontagne Institute, Fisheries and Oceans Canada, 850 Route de la Mer, Mont-Joli, QC G5H 3Z4, Canada e Canadian Wildlife Service, Environment Canada, 801-1550 ave. d'Estimauville, Quebec, QC G1J 0C3, Canada

a r t i c l e

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Article history: Received 31 July 2014 Received in revised form 20 November 2014 Accepted 20 November 2014 Available online 28 November 2014 Keywords: Northern gannets Sea surface temperature Fish Stable isotopes Corticosterone Nutritional status Triglycerides

a b s t r a c t Reproductive success of seabirds is tightly associated with availability of their prey for which the spatiotemporal distribution may be influenced by sea surface temperature (SST) fluctuations. The objective of this study was to investigate whether Northern gannets (Morus bassanus) from the largest colony in North America (Bonaventure Island, Quebec, Canada) were in negative nutritional state during the unprecedented low reproductive success year of 2012, and whether this was associated with changes in SST anomalies and diet. The incubation period of gannets in 2012 was characterized by a significant decline, from early to late incubation, in plasma triglyceride levels that was associated with an increase in plasma corticosterone levels. However, no changes in plasma glycerol and β-hydroxybutyrate levels were noted. SST anomalies recorded in this area (south of the Gulf of St. Lawrence) during the breeding period were consistently higher in 2012 compared to the previous year (a better reproductive success year). Based on signatures of stable carbon (δ13C) and nitrogen (δ15N) isotopes in gannet red blood cells and in whole fish homogenates of three major preys (mackerel, herring, and capelin), a minor dietary shift was noted between those years and incubation periods. In light of these findings, it is suggested that the extreme warm-water perturbation event that prevailed in the Gulf of St. Lawrence during summer 2012 was associated with a rapid deterioration of nutritional condition of Bonaventure Island gannets during the incubation. These suboptimal physiological changes likely contributed to the dramatic decline in reproductive success reported in this colony. © 2014 Elsevier Inc. All rights reserved.

1. Introduction Long considered as limitless resources, oceans are now facing largescale changes induced by anthropogenic activities. These changes may cause extensive stress on marine ecosystems worldwide (Halpern et al., 2008) and modulate food web interactions (e.g. predator–prey dynamics), which can have profound consequences on top predators such as seabirds (Schreiber and Burger, 2002; Grémillet and Boulinier, 2009). A growing number of studies have suggested that climate change may contribute, along with overfishing and environmental pollution, to severe impacts on reproductive success and long-term population

⁎ Corresponding author at: Département des sciences biologiques, Université du Québec à Montréal, C.P. 8888, Succursale Centre-ville, Montréal, Québec H3C 3P8, Canada. Tel. +1 514 987 3000x1070; fax: +1 514 987 4647. E-mail address: [email protected] (J. Verreault).

http://dx.doi.org/10.1016/j.cbpa.2014.11.017 1095-6433/© 2014 Elsevier Inc. All rights reserved.

stability of seabirds as well as their survival (Frederiksen et al., 2004; Jenssen, 2006; Ainley and Blight, 2009). An unprecedented low reproductive success of 8% (i.e., chick survival to fledging age) was recorded in 2012 for Northern gannets (Morus bassanus) breeding in a colony in the Gulf of St. Lawrence (Bonaventure Island, Quebec, Canada) (Montevecchi et al., 2013). Bonaventure Island is a migratory bird sanctuary (Rail, 2009), which hosts the most important breeding Northern gannet sub-population in North America (Chardine et al., 2013). A general declining trend in the reproductive success of Northern gannets from this colony has also been observed during the last decade, from around 74% between 1979 and 2004 (range: 72–77%; Rail et al., 2013) to 22% in 2011 (Montevecchi et al., 2013). A consistent decline, although less severe, has also been observed in Cape St. Mary's Northern gannet colony (Newfoundland and Labrador, Canada) with a reported reproductive success averaging 68% in 2011 and 39% in 2012 (Montevecchi et al., 2013). These observations led Montevecchi et al. (2013) to postulate that abnormally warmer sea

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surface temperatures (SSTs) recorded in the Gulf of St. Lawrence and throughout the entire Northwest Atlantic combined with limited fish prey availability might have been the driving factors behind this dramatic nest failure. Prey fish distribution is directly affected by climate-induced warming of sea surface when exceeding the thermal tolerance of the species (Perry et al., 2005). Suboptimal variations in SST may therefore represent an important factor limiting fish availability for diving seabirds by influencing the depth at which prey are found (Ropert-Coudert et al., 2009; Kokubun et al., 2010). Roberts and Hatch (1993) have shown that poor feeding conditions may result in extended foraging bouts in black-legged kittiwakes (Rissa tridactyla), thus increasing the amount of time that chicks are left unattended and exposed to predation. This has also been observed in other seabird species, e.g., Northern gannets (Hamer et al., 2007), great skuas (Catharacta skua) (Hamer et al., 1991), and common guillemots (Uria aalge) (Wanless et al., 2005). Therefore, low prey availability below a certain threshold may compromise seabird's reproductive success (Harding et al., 2007) as foraging behavior and effort during the breeding season are tightly associated with prey distribution (Ropert-Coudert et al., 2004; Wilson et al., 2005). In seabirds with long breeding period, body fat storage represents essential reserves for self-maintenance. In food deprivation condition (fasting), however, the physiological response of seabirds can be described in three phases that can be detected by variations of certain blood nutritional markers (Jenni-Eiermann and Jenni, 1998). In the first phase, readily available glycogen is used as main energy source (Alonso‐Alvarez and Ferrer, 2001). The second phase implies lipid oxidation as alternative source of energy (Cherel and LeMaho, 1985; Caloin, 2004), which is reflected in blood by an increase in glycerol and β-hydroxybutyrate levels, and a decrease in triglyceride levels (Castellini and Rea, 1992). In the last phase, as the bird begins to degrade proteins for fuel, nitrogenous waste levels increase in blood, while lipid metabolites are at their lowest (Cherel et al., 1988; Castellini and Rea, 1992; Caloin, 2004). Corticosterone, the primary glucocorticoid released by the adrenal gland cortex in birds, plays an essential role in energy metabolism (Romero and Remage-Healey, 2000; Love et al., 2004; Chastel et al., 2005) and regulation of body maintenance processes through the modification of foraging behaviors (Astheimer et al., 1992; Bray, 1993). As lipid reserves decrease, corticosterone secretion has been shown to increase in several breeding seabirds (Cherel et al., 1988; Kitaysky et al., 1999a,b), which is thought to promote foraging activities (Astheimer et al., 1995) and elicit mobilization of stored energy resources (Romero and Remage-Healey, 2000). However, high corticosterone levels in a low food supply situation has also been associated with impaired breeding success and low survival in seabirds as shown, for example, in common guillemots (Kitaysky et al., 2007). The objective of the present study was to investigate whether Northern gannets from Bonaventure Island were in negative nutritional state during the unprecedented low reproductive success year of 2012 (Montevecchi et al., 2013), and whether this was associated with changes in SST and diet. In order to address this question, plasma levels of selected nutritional markers (glycerol, triglycerides, and β-hydroxybutyrate) and corticosterone of Northern gannets as well as SST anomalies were compared between 2012 and 2011 (a year with higher reproductive success) during two periods in the incubation (early and late). The diet of Northern gannets was compared based on the estimated contribution of three major forage fish (Atlantic mackerel [Scomber scombrus], Atlantic herring [Clupea harengus harengus], and capelin [Mallotus villosus]; Jackson et al., 2009) using signatures of stable carbon (δ13C) and nitrogen (δ15N) isotopes in Northern gannet blood and whole fish. We hypothesized that Northern gannets from Bonaventure Island in 2012 were in a poorer nutritional status relative to 2011 and experienced warmer than average SSTs, which was associated with a different diet composition. More specifically, birds sampled in 2012 were hypothesized to have higher plasma glycerol and β-hydroxybutyrate levels and lower triglyceride levels combined

with higher plasma corticosterone levels in both incubation periods. The present study provides essential insights onto the challenges Northern gannets and potentially other seabirds from the Northwest Atlantic may face when experiencing extreme events in a changing ocean climate. 2. Materials and methods 2.1. Ethical procedures Bird capture and handling methods were approved by the institutional animal care committee of the Université du Québec à Rimouski (Rimouski, Quebec, Canada), and complied with the guidelines of the Canadian Council on Animal Care (CCAC). 2.2. Study area and sample collection Fieldwork was conducted from May through July 2011 and 2012 at Bonaventure Island (48° 30′ N, 64° 10′ W) located in the Île-Bonaventure-et-du-Rocher-Percé National Park (Quebec, Canada) in the Gulf of St. Lawrence. Breeding male (n = 26) and female (n = 10) Northern gannets (hereafter called gannets) were captured twice during the breeding period (early incubation: end of May to early June; late incubation: end of June to early July) from the peripheral section of the colony in both years using a noose-pole. A subset of ten birds (n = 8 males and 2 females) were selected from this sub-population for the purpose of the present study as these were the only birds that were successfully sampled (blood; see below) in both incubation periods (early and late) and years (2011 and 2012). All birds included in the present study were identified with a US Fish & Wildlife Service stainless steel ring and a color-coded plastic band. Blood samples (10–15 mL, which corresponds to less than 0.5% of this species' body mass [mean ± SD: 3050 ± 293 g]) were collected from the brachial vein of all birds using butterfly needles, 5 mL syringes, and heparinized vacutainer tubes. In order to minimize changes of corticosterone levels related to the circadian cycle, samples were all collected between 10 AM and 4 PM. Moreover, blood sample collection was performed immediately following capture (mean ± SD: 2.90 ± 0.30 min) to avoid handling-related stress effects on corticosterone secretion, and thus corticosterone levels corresponded to baseline levels. An aliquot (1–2 drops) of this blood sample was used for subsequent DNA sexing of the individuals. The birds were immediately released near their nesting site after blood sampling. While in the field, blood samples were kept on ice in a cooler before they were processed in the laboratory within 8 h of collection. In the laboratory, blood samples were centrifuged (7 min; 2500 ×g), and the resulting plasma was stored in liquid nitrogen, and subsequently in a −80 °C freezer until nutritional marker and corticosterone analyses (Sections 2.3 and 2.4, respectively), while red blood cells were kept in a regular freezer (−20 °C) until stable isotope analysis (Section 2.5). The three major fish preys of gannets were all collected in the south of the Gulf of St. Lawrence. More specifically, mackerels (n = 5) were caught using a conventional fishing rod at Percé wharf (Percé, Quebec, Canada) in July 2013. Capelins (n = 5) were collected by hand on the shore in the Bay of Chaleurs (Grande-Rivière, Quebec, Canada) during spawning in June 2013. Herrings (n = 5) were collected using fixed gillnets in September 2013 (Saint-Isidore, New Brunswick, Canada). All fish were of sizes and weights that are commonly found in gannet regurgitations that have been monitored in this breeding colony over the years (Rail J.-F., unpublished data). Whole fish were kept at −20 °C until stable isotope analysis (Section 2.5). SST anomaly data for the south of the Gulf of St. Lawrence were obtained from the National Oceanic and Atmospheric Administration's Office of Satellite and Product Operations, National Environmental Satellite, Data and Information Service website (http://www.ospo. noaa.gov/Products/ocean/sst/anomaly/index.html). SST anomalies are

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updated twice a week by deducting the long-term mean SST in a given location (spatial resolution: 0.5° or 50 km) and time of the year from the current value. Anomalies can be positive, which means that the current SST is warmer than average, or negative, signifying it is colder than normal. SST anomalies in this area for 2011 and 2012 could be obtained for six dates in each of the four breeding periods of gannets: pre-breeding (April 21st to May 10th), early incubation (May 23rd to June 11th), late incubation (June 21st to July 11th), and chick‐rearing period (July 21st to August 9th).

2.3. Nutritional marker analysis Glycerol, triglyceride, and β-hydroxybutyrate analyses in gannet plasma were conducted at the Université du Québec à Rimouski (Rimouski, Quebec, Canada). All nutritional markers were assayed on a microplate spectrophotometer (Biotec Powerwave XS2, Winooski, Vermont, USA) in 400 μL flat‐bottom microplates (Greiner Bio-One, Monroe, Louisiana, USA) using commercially available kits adapted for small volumes. Free glycerol and triglyceride levels were measured sequentially by endpoint assay (Sigma-Aldrich, Oakville, Ontario, Canada) at 37 °C, while β-hydroxybutyrate levels were measured by kinetic endpoint assay (R‐Biopharm, Darmstadt, Hesse, Germany) at room temperature (22–25 °C), both according to the manufacturer's recommendations. In both cases, standard curves were run in triplicates and undiluted samples in duplicates. Inter-assay variations were 7.6% and 6.7%, and intra-assay variations were 5.5% and 7.4% for triglycerides and β-hydroxybutyrate, respectively.

2.4. Corticosterone analysis Plasma samples of gannets were analyzed for corticosterone levels at the Université du Québec à Montréal (Montreal, Quebec, Canada) using a commercially available double antibody radioimmunoassay kit (ImmuChem Double Antibody Corticosterone I125, MP Biomedicals, Orangeburg, New York, USA) as described by Franci et al. (2014). Samples were run in five assays; the coefficient of inter-assay variation was 4.5% (n = 3 duplicates).

2.5. Stable isotope analysis Stable isotope analyses of gannet red blood cells and individual fish preys (mackerel, herring, and capelin) were conducted at the Centre de recherche en géochimie et géodynamique (GEOTOP), Université du Québec à Montréal (Montreal, Quebec, Canada). Head, tail, and skin were first removed from all fish to achieve optimal homogenization. Aliquots of gannet red blood cell and individual whole fish samples were then freeze-dried (Freezone 12, Labconco, Kansas City, Kansas, USA) and grounded into a homogenous free-flowing powder. Lipids were extracted from water-free whole fish homogenates using methanol and chloroform (50:50 volume ratio) following methods by Folch et al. (1957), with minor modifications described in Post and Parkinson (2001). The lipid content of whole fish homogenate was determined gravimetrically. Aliquots of water-free gannet red blood cell and whole fish homogenate (lipid-extracted) samples were then loaded into tin cups and weighed (±0.001 mg). Isotopic measurements were performed in duplicates using a continuous flow isotope ratio mass spectrometer (Micromass Isoprime, Cheadle, UK) coupled to an elementary analyzer (Carlo Erba NC1500, Milan, Italy). Results were expressed in delta notation (δ) relative to an international standard (Rstandard = Vienna PeeDee Belemnite (VPDB)) for δ13C and atmospheric air (AIR) for δ15N in per mil (‰) according to the equation: [δX = [(Rsample/Rstandard) − 1] × 1000], where X denoted either 13C or 15N, and R represented the ratio of 13C:12C or 15N:14N.

3

2.6. Data treatment Differences between and among periods in the incubation (early and late) and years (2011 and 2012) in plasma levels of nutritional markers (glycerol, triglycerides, and β-hydroxybutyrate) and corticosterone, and red blood cell δ13C and δ15N values in gannets were first tested using repeated measure ANOVA, followed by paired t-tests for incubation periods and years separately. For all analyses, female and male gannets were combined as low sample size for females precluded any statistical comparisons between sexes. Because residuals of all variables did not follow the normal distribution, a log-transformation was applied to achieve normal distribution. The absolute variations (in ng/mL) of triglyceride and corticosterone levels between samples collected in early and late incubation were calculated for both years (late incubation– early incubation). Simple linear regressions were then performed to investigate the strength of the relationships between the absolute variations of triglyceride and corticosterone levels. Statistical analyses were carried out using the statistical package JMP 11 (SAS, Cary, North Carolina, USA), and results with p ≤ 0.05 were considered significant. The proportions of the three major fish preys (mackerel, capelin, and herring) in gannet diet were estimated using a Bayesian multi-source stable isotope mixing model in R (SIAR; R Development Core Team 2013, version 3.0.2) (Jackson et al., 2009). SIAR provides outputs representing probability density functions (Phillips and Gregg, 2003), which were used to determine the relative contribution of each prey to the diet of gannets. δ13C and δ15N values in red blood cells of individual gannets were used in this model along with the mean (±SD) δ13C and δ15N determined in whole fish homogenates (lipid-extracted) of mackerel, capelin, and herring (n = 5 for each species). Following Votier et al. (2010), Trophic Enrichment Factors (TEFs) obtained from great skuas (Stercorarius skua) fed sprats (Sprattus sprattus) were used (i.e., 1.1 for δ13C and 2.8 for δ15N; Bearhop et al., 2002) with a standard deviation of ± 1‰.

3. Results 3.1. SST anomalies The SST anomalies recorded for 2011 were within the range of those reported during the five preceding years (2006–2010) for all these periods (pre-incubation: −2.4 to −1.2; early incubation: −2.0 to −1.0; late incubation: − 0.1 to 2.1), with the exception of the chick-rearing period that was lower (1.8 to 3.3). During the pre-incubation period, SST anomalies for the south of the Gulf of St. Lawrence were 0–1.1 °C higher in 2012 compared to 2011, although within the range reported from 2006–2010 (Table 1; Fig. S1). During early incubation, SST anomalies were 2.1–2.5 °C higher in 2012 compared to 2011. Higher SST anomalies in 2012 relative to 2011 were also consistently recorded during late incubation (1.7–1.9 °C) and chick-rearing periods (1.6–1.9 °C).

Table 1 Ranges of sea surface temperature (SST) anomalies (°C) recorded in the south of the Gulf of St. Lawrence (Canada) for six dates (see Section 2.2. for details) during pre-incubation, early incubation, late incubation, and chick-rearing periods of Northern gannets (Morus bassanus) in 2011 and 2012. Data obtained from the National Oceanic and Atmospheric Administration's Office of Satellite and Product Operations, National Environmental Satellite, Data and Information Service website (http://www.ospo.noaa.gov/Products/ocean/ sst/anomaly/index.html).

Pre-incubation Early incubation Late incubation Chick-rearing

2011

2012

−2.7 to −2.2 −2.5 to −0.8 −0.4 to 1.6 −0.2 to 1.7

−2.7 to −0.9 0 to 1.3 1.3 to 3.5 1.4 to 3.6

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In gannets, no interaction between incubation periods and years was found for glycerol (repeated measure ANOVA 1,44 = 1.91; p = 0.17) and β-hydroxybutyrate levels (repeated measure ANOVA 1,44 = 0.42; p = 0.52) (Fig. 1). In contrast, a significant interaction was found between these categorical variables for triglyceride levels (repeated measure ANOVA 1,44 = 4.36; p = 0.043) (Fig. 1). No difference was detected between both incubation periods and years in plasma levels of glycerol (paired t-test 1,7 = 1.50; p = 0.18) and β-hydroxybutyrate (paired t-test 1,7 = 0.92; p = 0.32). Levels of plasma triglycerides in 2012 were significantly higher in early compared to late incubation (paired t-test 1,7 = −3.76; p = 0.007), while in 2011 these levels tended to be lower in early compared to late incubation (paired t-test 1,7 = 2.13; p = 0.07) (Fig. 1). Moreover, plasma triglyceride levels were lower in early incubation 2011 compared to those of 2012 (paired t-test 1,7 = 3.58; p = 0.009), while no difference was found in late incubation between those two years (paired t-test 1,7 = −0.97; p = 0.36).

-Hydroxybutyrate levels (ng/mL)

3.2. Nutritional markers 0.30

-

0.25

-

0.20

-

0.15

-

0.10

-

0.05

-

A)

2011

2012

3.3. Corticosterone levels

0

-

Glycerol levels (ng/mL)

Early incubation There was no interaction between incubation periods and years for plasma corticosterone levels in gannets (repeated measure ANOVA 1,43 = 2.62; p = 0.11). Levels of corticosterone were not different between early and late incubation in 2011 (paired t-test 1,9 = − 0.066; p = 0.95) and showed a weak tendency for lower levels in early vs. late incubation 2012 (paired t-test 1,9 = 1.84; p = 0.099) (Fig. 2). However, levels of this glucocorticoid in early incubation were significantly higher in 2011 compared to 2012 (paired t-test 1,9 = − 4.29; p = 0.002), though they did not differ in late incubation between the two years (paired t-test 1,9 = −1.13; p = 0.29). A strong negative correlation was found for the variation (i.e., difference in absolute levels from late to early incubation) between triglyceride and corticosterone levels in 2012 (r2 = 0.83; p b 0.001; Fig. 3A). In contrast, no such association was uncovered between the absolute variations of these two variables in 2011 (r2 = 0.14; p = 0.28; Fig. 3B).

0.20

-

0.18

-

0.16

-

Late incubation

B)

0.14 0.12 0.10 0.08 0.06

0.04

2011

3.4. Stable isotope signature in gannets

2012

0

Early incubation 0.7

Triglyceride levels (ng/mL)

In gannet red blood cells, no interaction was found between years and incubation periods for both δ13C (repeated measure ANOVA 1,47 = 2.09; p = 0.16) and δ15N (repeated measure ANOVA 1,47 = 1.59; p = 0.21). δ13C tended to be lower in early compared to late incubation in 2011 (paired t-test 1,9 = −2.20; p = 0.055), but this was not observed in 2012 (paired t-test 1,9 = −0.0027; p = 1.00) (Fig. 4). δ13C values in early incubation were significantly lower in 2011 than those of 2012 (paired t-test 1,9 = −7.19; p b 0.0001), which was also the case for late incubation (paired t-test 1,9 = −6.86; p b 0.0001). δ15N in red blood cells did not differ significantly between periods in the incubation in both 2011 (paired t-test 1,9 = − 1.79; p = 0.11) and 2012 (paired t-test 1,9 = 1.33; p = 0.22). Early incubation δ15N values tended to be higher in 2011 compared to 2012 (paired t-test 1,9 = − 2.058; p = 0.070), however, this was not observed in late incubation between the two years (paired t-test 1,9 = 1.091; p = 0.30).

0.02

Late incubation

C)

0.6

0.5

0.4

0.3

0.2

3.5. Estimated diet composition 2011

0.1

The mean percentage lipids extracted from whole fish homogenates of the three major prey species in the diet of gannets were as follows: herring (23.2%), capelin (22.7%), and mackerel (8.6%). Profiles of δ13C and δ15N in lipid-extracted whole fish homogenates were highly similar between the three species (Fig. 5). As such, there was no difference between herring, capelin, and mackerel for both δ13C (ANOVA 1,13 = 0.22; p = 0.80) and δ15N values (ANOVA 1,13 = 0.85; p = 0.45).

2012 0

Early incubation

Late incubation

Fig. 1. Mean (± SD) plasma (A) β-hydroxybutyrate, (B) glycerol, and (C) triglyceride levels (ng/mL) in breeding Northern gannets (Morus bassanus) (n = 10) categorized by periods in the incubation (early and late) for samples collected in 2011 and 2012.

60

-

55

-

50

-

15.35

45

15.30

Early 2011

40

Late 2012

35 30

15.25

15.20

Late 2011

25

Early 2012

20

15.15

2011

15

2012

15.10

10

Early incubation

Late incubation 15.05 -19.25 -19.15 -19.05 -18.95 -18.85 -18.75 -18.65 -18.55 -18.45

Fig. 2. Mean (±SD) plasma corticosterone levels (ng/mL) of breeding Northern gannets (Morus bassanus) (n = 10) categorized by periods in the incubation (early and late) for samples collected in 2011 and 2012. Partial data (2011) from Franci et al. (2014).

Moreover, important overlap in percentage contribution of these three fish to the diet of gannets estimated using SIAR was found (Table S1). In spite of this overlap, SIAR model showed qualitatively that capelin

Variations in triglycerides (ng/mL)

5

15.40

15N (‰)

Corticosterone levels (ng/mL)

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0.4

13C (‰) Fig. 4. Mean (±SD) δ13C and δ15N (‰) in red blood cells of breeding Northern gannets (Morus bassanus) (n = 10) categorized by periods in the incubation (early and late) for samples collected in 2011 and 2012.

was consistently the most abundant prey in both early and late incubation 2011 and 2012.

A)

0.2

4. Discussion 0

4.1. Changes in nutritional status and food restriction

-0.2

Bonaventure Island gannets sampled in 2012 were in better nutritional condition early in the incubation period relative to the previous year. This was evidenced by higher plasma levels of triglycerides and lower levels of corticosterone in 2012 compared to 2011. However, the nutritional status of gannets in 2012 declined substantially over

-0.4 -0.6

-0.8 -1 -1.5

-1

-0.5

0

0.5

1

1.5

2

2.5

14.5

0.4

B)

14.0

0.2 0

δ15N (‰)

Variations in triglycerides (ng/mL)

Variations in corticosterone (ng/mL)

-0.2 -0.4

13.5

Herring Mackerel

13.0

Capelin

-0.6

-0.8 -1 -1.5

12.5

-1

-0.5

0

0.5

1

Variations in corticosterone (ng/mL) Fig. 3. Correlations of the absolute variation from early to late incubation period between plasma triglyceride and corticosterone levels (ng/mL) in breeding Northern gannets (n = 10) for (A) 2012, and (B) 2011. Dashed lines indicate no level variation between samples collected in early and late incubation. Partial data (corticosterone, 2011) from Franci et al. (2014).

12.0 -20.5

-20.3

-20.1

-19.9

-19.7

-19.5

-19.3

-19.1

δ13C (‰) Fig. 5. Mean (±SD) δ13C and δ15N (‰) in lipid-extracted whole fish homogenates of three major preys (mackerel, herring, and capelin; n = 5 per species) of Northern gannets (Morus bassanus) collected in the Gulf of St. Lawrence.

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the incubation period, from early to late (i.e., decreasing plasma levels of triglycerides associated with increasing plasma corticosterone levels) — a pattern that was not observed in 2011. These nutritional marker variations were corroborated by studies in some avian species for which a gradual decrease in plasma triglyceride levels was shown to be associated with a corresponding increase in circulating corticosterone levels (Veiga et al., 1978; Kitaysky et al., 1999a). In fact, in fasting birds, a decrease in plasma triglyceride levels coupled to an increase in glycerol and β-hydroxybutyrate levels typically correspond to a lipid oxidation phase (Castellini and Rea, 1992; Jenni-Eiermann and Jenni, 1998). However, the significant change in gannet plasma triglycerides from early to late incubation 2012 was not associated with significant changes in plasma glycerol and β-hydroxybutyrate levels. Nevertheless, plasma triglyceride levels may also reflect the average size of body fat reserves in birds (Dabbert et al., 1997; Smith and McWilliams, 2009; Devost et al., 2014). Therefore, although gannets might not have been in a severe fasting state at the time of blood collection in late incubation 2012, it remains that our data suggest a general decline in the size of energy depots as incubation progressed. The decline in circulating triglyceride levels in gannets was associated with an increase in the endocrine signal (corticosterone) characterizing a negative energy balance in birds (Sapolsky et al., 2000; Landys et al., 2006). A number of studies have suggested that enhanced synthesis of corticosterone alone may provide information on stress associated with food scarcity (Kitaysky et al., 1999b; Doody et al., 2008). For instance, the secretion of this glucocorticoid has been shown to increase during nutritional stress in breeding common guillemots (Kitaysky et al., 2007; Doody et al., 2008) and black-legged kittiwakes to promote foraging activities (Kitaysky et al., 1999a). Hence, low food availability will result in increased secretion of corticosterone, which in turn can improve survival of the individual during this stressful event (Astheimer et al., 1992; Kitaysky et al., 1999a,b). This is known as a trade-off between body maintenance, or adult survival, and reproductive investment, resulting in a decrease in breeding performance or even nest failure (chick/egg abandonment) (Silverin, 1986; Astheimer et al., 1992, 1995; Bray, 1993; Love et al., 2004). 4.2. Stable isotope profiles and diet variation The tissue signature of δ13C and δ15N is increasingly being used to reveal changes in diet composition in seabirds (e.g., Podlesak et al., 2005; Votier et al., 2010; Lavoie et al., 2012). Based on known 13C and 15N turnover rates in avian tissues, red blood cells represent nutrient assimilation over the previous 2–4 weeks (Hobson and Clark, 1993; Bearhop et al., 2002), which corresponded in present gannets to fish consumption going back to early and mid-May for blood samples collected in early incubation (early June), and to early and mid-June for those collected in late incubation (early July). The increase in gannet red blood cell δ13C between 2011 and 2012 in both incubation periods (early: + 0.46‰; late: + 0.33‰) could thus be ascribed to a minor dietary shift between those two years. However, δ15N varied only transiently between 2011 and 2012 during the same two periods in the incubation (early: −0.13‰; late: +0.07‰). Overall, these isotopic changes in gannet red blood cells were in line with the low variations in both δ15N and δ13C observed among the three major fish prey species (mackerel, herring, and capelin). This restricted isotopic range also resulted in generally overlapping percentage contribution (estimated using SIAR) of these three fish species to the gannet diet among years and incubation periods. On the basis of these results, changes in nutritional markers and corticosterone during the incubation period of gannets could not be ascribed to differences in relative prey fish contribution. As such, gannets are known generalists in their selection of pelagic prey, and hence can adapt their diet when facing poor food availability, for example, through consumption of sandlance (Ammodytes sp.), short-finned squid (Illex illecebrosus), Atlantic saury (Scomberesox saurus), or Atlantic salmon (Salmo salar) (Montevecchi,

2007). However, changes in the distribution of forage fish in the south of the Gulf of St. Lawrence may have forced gannets to increase the length of their foraging trips as reported by Montevecchi et al. (2013), thus enhancing their energy expenditure and rendering adult maintenance, and perhaps chick provisioning unachievable in 2012.

4.3. SST shift and prey distribution Galbraith et al. (2013) reported that the average SSTs in the Gulf of St. Lawrence in May–November 2012 were the second warmest after 2006 for the period 1985–2012. In this same report, the mean SST recorded in August 2012 was by far the warmest in this time series (nearly 2 °C above normal). Moreover, the substantial increase (4.1–4.5 °C) in SST anomalies from May to August 2012 in the south of the Gulf of St. Lawrence, where the average ambient summer temperature is 14.5 °C (Environment Canada, 2013), is noteworthy considering that rapid seasonal SST increases can cause disturbance on seabirds, for example, through change in spatiotemporal accessibility of their prey (reviewed by Grémillet and Boulinier, 2009). SST changes have thus been suggested to be suitable proxy for the variations in marine fish distribution (Perry et al., 2005). In accordance with Montevecchi et al. (2013), we postulate that the warmer SST recorded in the south of the Gulf of St. Lawrence during the last part of the 2012 breeding season may have exceeded certain fish prey species' thermal boundaries (Perry et al., 2005), and thus altered their vertical movements and/or geographical distribution. The thermal preference of mackerel (range: 7.3–15.8 °C; Olla et al., 1976; Overholtz and Anderson, 1976) coincides with a preferential distribution within the first 10–15 m of the water column (above the thermocline) in the southern part of the Gulf of St. Lawrence in June (Fisheries and Ocean Canada, 2013). The geographical distribution of mackerel has been documented to shift in the past few years from the southern to the northern part of the Gulf of St. Lawrence (Grégoire, F.; unpublished data). Therefore, mackerel could have moved on to colder northern areas of the Gulf of St. Lawrence during the 2012 breeding season (particularly during the chick-rearing period; Rail et al., 2013). Herring and capelin, however, prefer colder deeper water and are able to move below the thermocline (Grégoire et al., 2009), while generally remaining available (b 24 m depth; Darbyson et al., 2003) in water depths used by diving gannets (up to 19 m) (Garthe et al., 2011). Vertical movements of these species associated with the deeper thermocline or below (Sette, 1943) could similarly have resulted in limited prey accessibility for gannets, particularly in the incubation period during which capelin is important prey around Bonaventure Island (Rail et al., 2013). The availability of prey fish near Bonaventure Island during late incubation and chick-rearing periods was shown to be directly related to the long-term success of this gannet population (Garthe et al., 2014). In fact, as energetic demands peak during chick-rearing, foraging efforts must be adjusted accordingly to support offspring needs (Bolton, 1995; Bertram et al., 1996). Shaffer et al. (2003) showed that wandering albatrosses (Diomedea exulans) increased their foraging efforts (i.e., energy spent per time unit) during the chick-rearing period in order to maximize the rate of prey delivery to their progeny while maintaining short feeding bouts. However, poor prey availability may increase the length of foraging trips (e.g., Ropert-Coudert et al., 2004; Wilson et al., 2005), paralleling the amount of time that chicks are left unaccompanied and more vulnerable to conspecific attacks, and which, in prolonged cases, may lead to death by starvation (Hamer et al., 1991; Roberts and Hatch, 1993; Wanless et al., 2005; Hamer et al., 2007). Abnormally longer foraging trips and chick abandonment were indeed reported in early August 2012 in gannet colonies from both Bonaventure Island and Cape St. Mary's (Montevecchi et al., 2013) at a time when the SST anomalies were substantially higher than average.

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5. Conclusions Despite that breeding gannets from Bonaventure Island were in relatively good nutritional state in early incubation 2012 relative to the previous year, based on higher plasma levels of triglycerides and lower corticosterone levels, this condition rapidly deteriorated over the incubation period. This substantial deterioration in condition most likely was linked to a decline in the local availability and/or accessibility of pelagic prey around Bonaventure Island. This in turn could be related to the extreme warm-water perturbation event recorded that year in the southern Gulf of St. Lawrence, which reached a record peak in August. Alternatively, this could also be related to a depletion of the main gannet prey fish stocks, although this would remain to be verified as no stock status was available at the time of the study. Regardless, the suboptimal physiological condition of adult gannets is hypothesized to have further deteriorated during the chick-rearing period (August) when abnormal parental behaviors were frequently observed in this colony (e.g., mass abandonment of chicks and longer than usual adult foraging trips; Montevecchi et al. (2013)). Grémillet and Boulinier (2009) suggested that seabirds facing rapid SST changes may modify their foraging behavior in an attempt to survive and reproduce, change their distribution, and/or go extinct. A number of studies have also shown that seabirds may increase the length of their foraging trips when facing poor food availability (e.g., Ropert-Coudert et al., 2004; Wilson et al., 2005). This may lead to a trade-off favoring body maintenance over reproductive investment, hence decreasing breeding performance (Silverin, 1986; Astheimer et al., 1992, 1995; Bray, 1993; Love et al., 2004). Therefore, if extreme sea surface warming events were to occur repeatedly in the south of the Gulf of St. Lawrence, their repercussions would be irreversibly detrimental to breeding gannets from Bonaventure Island, and perhaps for other gannet colonies in the Northwest Atlantic (Chardine et al., 2013). A better characterization of the feeding ecology of gannets and distribution and behavior of their prey is thus critically needed to better understand the challenges these marine predators are facing in a changing ocean climate. Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.cbpa.2014.11.017. Acknowledgments Funding for this project was provided by the Canada Research Chair in Comparative Avian Toxicology (to J.V.). Additional funding was obtained from Environment Canada (to J.-F.R.). We would like to acknowledge Louise Champoux (Environment Canada) for funding corticosterone analyses and the National Wildlife Research Center, Environment Canada, for funding DNA sexing of the birds. We would like to thank Frédérique Paquin (Université du Québec à Montréal) for assistance with corticosterone analyses and Arianne Savoie (Université du Québec à Rimouski) for nutritional marker analyses. We would also like to thank Vincent Ouellet Jobin and Raphaël Lavoie for their valuable help with R and SIAR. We extend our appreciation to volunteers and colleagues who participated in the fieldwork at Bonaventure Island (Sylvain Christin, Isabeau Pratte, Yannick Seyer, Marie-Anne Bergeron, Lynn Miller, Émilie DeChamplain, and Josée Dumas-Campagna). C.D.F. was partly supported by a NSERC Graduate Scholarship (Alexander Graham-Bell) and the Fonds d'accessibilité et réussite des études (Université du Québec à Montréal). We further acknowledge valuable comments received from Dr. William Montevecchi, Dr. Stefan Garthe, and two anonymous reviewers on an earlier draft of this paper. References Ainley, D.G., Blight, L.K., 2009. Ecological repercussions of historical fish extraction from the southern ocean. Fish Fish. 10, 13–38. Alonso‐Alvarez, C., Ferrer, M., 2001. A biochemical study of fasting, subfeeding, and recovery processes in yellow‐legged gulls. Physiol. Biochem. Zool. 74, 703–713.

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