Trophic niche of squids: Insights from isotopic data in marine systems worldwide

Deep-Sea Research II ] (]]]]) ]]]–]]]

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Trophic niche of squids: Insights from isotopic data in marine systems worldwide Joan Navarro a,n, Marta Coll a, Christoper J. Somes b, Robert J. Olson c a

Institut de Cie ncies del Mar (ICM-CSIC), Passeig Marı´tim de la Barceloneta, 37-49, 08003 Barcelona, Spain GEOMAR Helmholtz Centre for Ocean Research Kiel, D¨ usternbrooker Weg, 20, 24105 Kiel, Germany c Inter-American Tropical Tuna Commission, 8604 La Jolla Shores Drive, La Jolla, CA 92037, USA b

a r t i c l e i n f o

Keywords: Squids Ecological role Stable isotopes Trophic level Bayesian isotopic analyses Isotopic baseline adjustment Spatial d15N gradients

abstract Cephalopods are an important prey resource for fishes, seabirds, and marine mammals, and are also voracious predators on crustaceans, fishes, squid and zooplankton. Because of their high feeding rates and abundance, squids have the potential to exert control on the recruitment of commercially important fishes. In this review, we synthesize the available information for two intrinsic markers (d15N and d13C isotopic values) in squids for all oceans and several types of ecosystems to obtain a global view of the trophic niches of squids in marine ecosystems. In particular, we aimed to examine whether the trophic positions and trophic widths of squid species vary among oceans and ecosystem types. To correctly compare across systems, we adjusted squid d15N values for the isotopic variability of phytoplankton at the base of the food web provided by an ocean circulation–biogeochemistry–isotope model. Studies that focused on the trophic ecology of squids using isotopic techniques were few, and most of the information on squids was from studies on their predators. Our results showed that squids occupy a large range of trophic positions and exploit a large range of trophic resources, reflecting the versatility of their feeding behavior and confirming conclusions from food-web models. Clear differences in both trophic position and trophic width were found among oceans and ecosystem types. The study also reinforces the importance of considering the natural variation in isotopic values when comparing the isotopic values of consumers inhabiting different ecosystems. & 2013 Elsevier Ltd. All rights reserved.

1. Introduction Cephalopods are widely distributed throughout all oceans and inhabit diverse ecosystems, such as coastal shelves, open oceans and the deep-sea. Approximately 800 species of cephalopods have been described, including demersal species (e.g. octopuses and cuttlefish) and pelagic cephalopods (primarily squids) (Boyle and Rodhouse, 2005). The squids (order Teuthida) is a diverse group of cephalopods with approximately 300 species classified into 29 families, with large differences in size, feeding patterns and other biological traits. In general, benthic and shallow-water squids are better studied than their pelagic or deep-sea relatives, mainly due to sampling limitations (e.g., Cherel et al., 2009). During recent decades, however, important advances have been made in understanding the ecology of squids in many marine ecosystems (Cherel and Hobson, 2005; Cherel et al., 2009; Olson and Young, 2007). Cephalopods are important organisms in terms of their economic and ecological value. From an economic perspective,

n

Corresponding author. Tel.: þ34 932309500; fax: þ 34 932309555. E-mail address: [email protected] (J. Navarro).

approximately 76% of the world cephalopod catch in 2005 was squids, according to Food and Agriculture Organization (FAO) of the United Nations (Jerb and Roper, 2005; Rodhouse and Nigmatullin, 1996). Ecologically, squids comprise large biomasses in marine communities and occupy medium to top trophic positions in food webs (Amaratunga, 1983; Coll et al., this issue). Squids are an important prey resource for fishes, seabirds and marine mammals, and are voracious predators of crustaceans, squid, fishes and zooplankton (e.g., Cherel and Duhamel, 2004; Clarke, 1996; Croxall and Prince, 1996; Kaschner et al., 2001; Klages, 1996; Olson and Young, 2007; Rodhouse and Nigmatullin, 1996; Smale, 1996; Stergiou and Karpouzi, 2001; Xavier and Croxall, 2007; Hoving and Robison, 2012). Because of their high feeding rates and generalist trophic strategy, squids have the potential to exert trophodynamic control on the recruitment of the early life stages of economically important fishes (Hunsicker and Essington, 2008; Rodhouse and Nigmatullin, 1996). In addition, cephalopods in general, and squids in particular, have been highlighted as indicators of fisheries and climate change impacts on marine ecosystems (Dawe et al., 2000; Sakurai et al., 2000; Bellido et al., 2001; Coll et al., this issue). Despite their ecological importance in comparison with other marine organisms, trophic studies on cephalopods in general, and

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Please cite this article as: Navarro, J., et al., Trophic niche of squids: Insights from isotopic data in marine systems worldwide. DeepSea Res. II (2013), http://dx.doi.org/10.1016/j.dsr2.2013.01.031i

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squids in particular, are scarce. Consequently, it is important to improve our understanding of the ecological role of squids in the marine environment. Stable isotopes are intrinsic markers that are increasingly being used to examine the trophic ecology of squids. The use of stable isotope values of nitrogen and carbon provide information on trophic position, trophic pathways and niche width for individuals to communities (see the recent review by Layman et al., 2011), and complement information from stomach-content analyses and food-web models (Coll et al., this issue). Stable isotope analysis is based on the fact that standardized stable isotope ratios of nitrogen, i.e. 15N/14N, (d15N) and carbon, i.e. 13C/12C, (d13C) are transformed from dietary sources to consumers in a predictable manner (Layman et al., 2011). d15N values show a predictable increase from one trophic level to the next, with typical enrichment of about 3% per trophic level (Post, 2002) in marine food webs (Navarro et al., 2011). Carbon isotope ratios show little change due to trophic transfer, but are useful indicators of dietary sources of carbon (Fry and Sherr, 1984; Michener and Schell, 1994). Furthermore, by analyzing both d15N and d13C data together it is possible to estimate trophic width of species, populations and ecosystems by calculating isotopic area (Layman et al., 2011). In marine systems, applications of stable isotope analysis have grown substantially in recent decades as analytical costs of have decreased, the capabilities of laboratories and the statistical methodologies for interpretation of isotopic data have improved, being more accessible for non-specialist researchers (Jackson et al., 2011; Layman et al., 2011). Recent studies have used stable isotope analysis to examine the trophic ecology of squids or the trophic relationships among squid guilds (e.g., Cherel and Hobson, 2005; Cherel et al., 2009; Fanelli et al., 2012; Hunsicker et al., 2010; Jackson et al., 2007; Lorrain et al., 2011; Ruiz-Cooley et al., 2010). However, the majority of available isotopic information on squids is dispersed in studies of the trophic ecology of numerous marine predators (Fig. 1), in which the isotope values of squids were analyzed to interpret the isotope values of their predators (e.g., Cardona et al., 2012; Ciancio et al., 2008; Hobson and Montevecchi, 1991; Navarro et al., 2009; Praca et al., 2011). Therefore a synthesis of the available isotopic data for squids is desirable. An important limitation when comparing nitrogen isotope values of consumers from different geographic locations is the

fact that the isotopic composition of seawater varies greatly at different locations, resulting in high isotopic variability of the primary producers at the base of each food web. Since the natural range of nitrogen isotopes in seawater ( 0–12%) (Somes et al., 2010) is larger than the step-wise increase per trophic level (  3%), this must be accounted for when estimating trophic position. One approach is to adjust the isotopic values of consumers by the isotopic values of organisms located at the base of the food webs, such as phytoplankton or zooplankton (Post, 2002; Carscallen et al., 2012). In this study, we synthesized the available stable isotope data from different oceans and ecosystems and adjusted squid d15N values for baseline isotopic variability derived from an ocean circulation–biogeochemistry–isotope model to obtain a global picture of the trophic niche of squids in marine ecosystems. In particular, we aimed to (1) examine whether the trophic position inferred from baseline-adjusted d15N values and (2) the trophic widths (isotopic area using d15N and d13C values) of squid species vary among oceans and among ecosystem types.

2. Materials and methods 2.1. Stable isotope records We collected stable isotope data for squids from published sources worldwide (Fig. 2a) (complete list of species and references in Table S1), using the electronic bibliographic database ISI Web of Knowledge and keywords ‘‘squid’’ and ‘‘stable isotopes’’ and the Google Scholar database. For each publication we recorded the species, geographical sampling location, ocean, ecosystem type, number of samples analyzed, type of tissue analyzed, mean and standard deviation of d15N and d13C and main focus of the study (squid or other organisms). Since squid mandibles (beaks) are depleted in d15N when compared with muscle tissue, prior to conducting statistical analyses the d15N values of beaks were adjusted by adding 3.5% to their d15N values to approximate the d15N values of muscle (see Cherel et al., 2009). We analyzed the isotopic data by ocean and ecosystem type, each sub-divided into 6 categories. The ocean factors were the Arctic (ARC), Antarctic (ANT), Atlantic (ATL), Indian (IND), Pacific (PAC) and Mediterranean (MED). Ecosystem types included the Arctic shelf (ARCS), Antarctic shelf (ANTS), open ocean (OCEAN), temperate coastal and shelf areas (TEM), tropical coastal and shelf areas (TROP) and upwelling ecosystems (UPW). 2.2. Adjustment for isotopic baseline values

Fig. 1. Cumulative numbers of published studies that contain isotopic information on squids by year of publication. Close and open circles represent studies focused only with squids or with predators or ecosystems, respectively. Squid representation used is courtesy of the Integration and Application Network, University of Maryland Center for Environmental Science /ian.umces.edu/symbols/S.

To correctly interpret and compare the isotopic values among different oceans and ecosystems, we adjusted all squid d15N values (referred to as baseline-adjusted d15N values, ‘‘BA-d15N’’) by subtracting d15N values of phytoplankton obtained for each sampling location (Fig. 2) from a global coupled ocean circulation–biogeochemistry–isotope model (Somes et al., 2010). The model includes a three-dimensional (1.81  3.61, 19 vertical levels) ocean circulation model forced with prescribed monthly climatological winds (Weaver et al., 2001). The marine ecosystem/biogeochemical component is a 2N2PZD (2 Nutrients, 2 Phytoplankton, 1 Zooplankton, and 1 Detritus) ecosystem model. The organic variables include two classes of phytoplankton: diazotrophs, which can undergo N2 fixation, and a ‘‘general’’ NO3 assimilating phytoplankton class, as well as zooplankton (Z) and sinking organic detritus (D). The inorganic variables include dissolved oxygen (O2) and two nutrients, nitrate (NO3 ) and phosphate (PO34  ), both of which are consumed by phytoplankton

Please cite this article as: Navarro, J., et al., Trophic niche of squids: Insights from isotopic data in marine systems worldwide. DeepSea Res. II (2013), http://dx.doi.org/10.1016/j.dsr2.2013.01.031i

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of organic matter in the surface ocean that eventually sinks and becomes buried in the seafloor sediments. The model captures the trend of decreasing d15N due to low levels of surface nitrate utilization in the HNLC regions of the Southern Ocean, Eastern Equatorial Pacific, and North Pacific. It also correctly predicts the high d15N values near suboxic zones where denitrification produces 15N-enriched nitrogen in the Eastern Tropical Pacific, as well as the low d15N values that occur in the tropics/subtropics where N2 fixation produces 15N-depleted nitrogen in the Western Pacific and North Atlantic (Table 1). Observed seafloor d15N values in the different ocean basins (Tesdal et al., 2012) are reproduced by the model (Table 1). The model simulates the correct deviation relative to the global mean in each region, with an average regional error of 1.1%. This suggests that the average error introduced by the model for estimating trophic position is  70.25 units. However, one known model bias is the overestimation of denitrification in the Eastern Tropical Pacific and Eastern Tropical Atlantic. This results in overestimated d15N values and trophic positions by  2% and by as much as 0.6 units, respectively, in these regions (Somes et al., 2010). For the squid, the BA-d15N values with and without the estimated model error at each location were clearly correlated, independent of the ocean and ecosystem type (Fig. S1), indicating that the effect of the modeling error in the interpretation of the BA-d15N values was low or very low.

2.3. Comparison between squid BA-d15N and unadjusted d15N values To test the effect of adjusting the d15N values of squid from the literature by the model d15N values of phytoplankton, as explained in Section 2.2, we compared the squid d15N values without and with baseline-adjustment among oceans and ecosystem types by using a dependent Student’s t-test and a Wilcoxon test for parametric and non-parametric data, respectively. Normality (Shapiro–Wilk test) and homoscedasticity (Levene’s test) of the data were verified before statistical analysis. We also calculated the difference between the unadjusted d15N and BA-d15N values of squids in each ocean and ecosystem type. Fig. 2. (a) World map showing the geographic positions of the studies containing stable isotope information of squid species used in this review; (b) spatial gradients of d15N values of phytoplankton in the oceans obtained from the ocean circulation–biogeochemistry–isotope model of Somes et al. (2010).

and remineralized in fixed elemental ratios (RC:N:P ¼106:16:1, RO:P ¼ 170). When O2 is not available in sufficient quantity (i.e., O2 o5 mM), organic matter is remineralized via denitrification, where NO3 replaces O2 as the electron acceptor and is reduced to N2 gas. The nitrogen isotope module embedded within the marine ecosystem model simulates the two stable nitrogen isotopes, 14N and 15N, in all species that contain nitrogen. Fractionation results in the preferential incorporation of the more reactive and thermodynamically preferred 14N isotope into the product of each reaction by a process-specific fractionation factor (e) (Mariotti et al., 1981). The processes in the model that fractionate nitrogen isotopes are algal NO3 assimilation (eASSIM ¼5%), zooplankton excretion (eEXCR ¼6%), water column denitrification (eWCD ¼25%), and N2 fixation (eNFIX ¼ 1.5%). The average increase in d15N per trophic level in the model (i.e., d15N-zooplankton  d15N-phytoplankton) is  4%, in agreement with previous estimates (e.g., Post, 2002). For a complete model description, see Somes et al. (2010). There is general agreement between the nitrogen isotope model and the global seafloor sediment d15N database (Tesdal et al., 2012) indicating that the model can accurately predict d15N

Table 1 Observed and modeled seafloor mean d15N values. Source: Somes et al., 2010; Tesdal et al., 2013 Region

Observed seafloor d15N (%)

Modeled seafloor d15N (%)

North Atlantic (251N–501N) Tropical North Atlantic (101N–251N) Equatorial Atlantic (101S–101N) Tropical South Atlantic (101S–251S) South Atlantic (251S–501S) North Pacific (401N–601N) Eastern Tropical North Pacific (1601W–601W, 51N–401N) Western North Pacific (1001E–1601W, 01–501N) Eastern Equatorial Pacific (1601E–601W, 101S–51N) Western South Atlantic (1501E–1601W, 01–501S) Eastern South Atlantic (1601W–601W, 101S–501S) North Indian (01–251N) South Indian (01–501S) Southern Ocean (501S–801S) Global

4.6 3.6 7.2 7.6 7.6 6.7 10.5

5.3 3.8 8.3 10.0 8.7 5.0 12.1

5.2

3.3

7.7

9.8

7.9

7.0

8.5

10.4

8.5 7.0 5.3 6.9

7.3 7.1 4.8 7.0

Please cite this article as: Navarro, J., et al., Trophic niche of squids: Insights from isotopic data in marine systems worldwide. DeepSea Res. II (2013), http://dx.doi.org/10.1016/j.dsr2.2013.01.031i

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amount of niche space occupied by the squids, and is thus a proxy for the extent of trophic diversity exploited by the squids (high values indicate high trophic width). This metric uses multivariate ellipse-based Bayesian metrics. Bayesian inference techniques allow for robust statistical comparisons between data sets with different sample sizes. We calculated isotopic standard ellipse areas using the SIBER (Stable Isotope Bayesian Ellipses in R, Jackson et al., 2011) routine, also incorporated in the SIAR library of R 2.12.2 (R Development Core Team, 2011). We estimated the trophic position of squids based on the adjusted isotopic values for the squid at each sampling position according to the algorithm proposed by Vander Zanden and Rasmussen (2001): 15

15

15

TP ¼ TLbasal þðd Nconsumer d Nbasal Þ=Dd N where d15Nconsumer and d15Nbasal were, respectively, the d15N values of the squid from each study and the d15N values of phytoplankton at the geographic location of each study. Dd15N is the isotopic discrimination factor, 3.4% (Post, 2002). Following convention, the trophic level of phytoplankton (TLbasal) is 1.0. 2.5. Statistical analysis We used the non-parametric multivariate permutational analysis of variance (PERMANOVA, in PRIMER with PERMANOVA v. 6, PRIMER-Ltd., Plymouth, UK) on the Euclidean distance matrix to investigate differences in BA-d15N, d13C and trophic position estimates for squids among oceans and ecosystem types. PERMANOVA calculates a pseudo-F statistic that is directly analogous to the F-statistic for multifactorial univariate ANOVA models, but uses permutation procedures (here 9999 permutations) to obtain p-values for each term in the model (Anderson et al., 2008). Due to the lack of replication and an unbalanced design among factors, we performed a one-way analysis with each factor using each indicator separately and used the unrestricted permutation of raw data. We normalized all variables prior to the construction of the Euclidean distance matrices (Clarke and Gorley, 2006).

3. Results 3.1. Stable isotope dataset

Fig. 3. Mean and standard error of d15N values of phytoplankton, zooplankton and squid by (a) ocean (Antarctic¼ ANT; Arctic¼ARC; Atlantic¼ ATL; Indian¼ IND; Mediterranean¼MED; Pacific¼ PAC) and (b) ecosystem type (Antarctic shelf¼ANTS; Arctic shelf¼ ARCS; open ocean¼ OCEAN; temperate coastal and shelf areas¼ TEM; tropical shelf and coast¼TROP; upwelling¼ UPW). Values of phytoplankton (Fig. 2b) and zooplankton were obtained from the ocean circulation–biogeochemistry–isotope model of Somes et al. (2010). The unadjusted d15N values of squids were obtained from the literature (Table S1).

2.4. Trophic width and trophic position of squids We calculated the trophic width encompassed by all squid species based on d15N–d13C bi-plots (Jackson et al., 2011), using Bayesian standard ellipse areas and BA-d15N values per ocean and ecosystem type. This metric represents a measure of the total

We compiled stable isotope data (d15N and d13C values) for 89 squid species in 62 published studies from 57 geographical locations (Figs. 1 and 2a, Table S1). The first study we found that reported stable isotope values for a squid was published in 1982, and the first study that focused on the trophic ecology of a squid based on stable isotopes was in 2004 (Fig. 1). Forty-six studies included stable isotope values of squids to investigate the diets of their predators (seabirds, marine mammals and fishes) or to study the structure of marine food webs, while only 15 studies focused exclusively on squids (Fig. 1). Most of the isotope data were for squids from the ANT (33% of all studies), ATL (33%) and PAC (21%), followed by the MED (8%), ARC (3%) and IND (2%) oceans (Fig. 2 and Table S1). As for ecosystem types, most of the isotope data were for squids from the TEM (49%) and ANTS (32%) ecosystems, followed by the TROP (10%), OCEAN (4%), ARCS (3%) and UPW (2%) (Fig. 2a and Table S1). 3.2. d15N values of phytoplankton, zooplankton and squids by oceans and ecosystems Comparisons of the unadjusted d15N values of squids and the model-predicted d15N values of phytoplankton and zooplankton showed the expected pattern, consistent among oceans and

Please cite this article as: Navarro, J., et al., Trophic niche of squids: Insights from isotopic data in marine systems worldwide. DeepSea Res. II (2013), http://dx.doi.org/10.1016/j.dsr2.2013.01.031i

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ecosystems: the squids had the highest values, followed by zooplankton with medium values, and phytoplankton with the lowest d15N values (Fig. 3). By ocean, the mean phytoplankton and zooplankton d15N values were highest in the PAC, MED and IND (Fig. 3a). These maxima did not fully match with the unadjusted d15N values of squids, which were highest in the PAC and ARC (Fig. 3a). The mean phytoplankton and zooplankton d15N values by ecosystem type were highest in the UPW, TROP and OCEAN (Fig. 3b). For the squids, the mean unadjusted d15N values were also highest in the UPW and TROP, followed by the ARCS, but squids in the OCEAN ecosystem had the lowest values. 3.3. Effect of the baseline adjustment on the squid d15N values Adjusting published squid d15N values by subtracting model d15N estimates for phytoplankton produced a significant reduction in d15N, and allowed us to compare among oceans and ecosystems. Mean squid BA-d15N values were significantly lower than mean unadjusted d15N values in all oceans (Table 2; Fig. 4a), but especially in the IND, MED and PAC where phytoplankton d15N estimates were the highest. The differences between unadjusted squid d15N and BA-d15N mean values were clearly highest in the PAC (mean and standard deviation; 5.0173.16%), IND (4.7270.01%) and MED (3.9570.03%) than in the ATL (1.6170.91%), ART (1.0570.53%) and ANT (0.7170.13%) (Table 2; Fig. 4a). Among ecosystem types, mean squid BA-d15N values were also significantly lower than mean unadjusted d15N values (Table 2; Fig. 4b), especially in the UPW, TROP and TEM. The differences between unadjusted squid d15N and BA-d15N values were clearly higher in the UPW (6.3572.34%) and TROP (6.04 73.15%) than in the OCEAN (3.91 74.41%), TEM (2.24 71.26%), ARCS (1.05 70.53%) and ANTS (0.7170.13%) (Table 2; Fig. 4b). These results highlight the importance of adjusting the d15N values of squids by the baseline values. 3.4. Comparison of BA-d15N, d13C, isotopic area and TP estimates among oceans The mean BA-d15N and d13C values of squids differed significantly among oceans (Fig. 5a; BA-d15N: pseudo-F 5,142 ¼8.44, p o0.0001; d13C: pseudo-F 5,137 ¼ 26.624, p o0.0001). Post-hoc

Table 2 Mean and standard deviation of unadjusted d15N (‘‘d15N’’)and baseline-adjusted d15N values (‘‘BA-d15N’’). The difference between d15N and BA-d15N values and the statistics (t in the case of dependent Student’s t-test and Z in the case of dependent Wilcoxon test) are shown. n

d15N (%)

BA-d15N (%)

Difference (%)

Test

38 5 47 2 15 36

11.29 7 3.43 11.55 7 1.23 11.31 7 2.06 11.56 7 0.09 9.597 0.82 13.38 7 2.77

10.58 7 3.39 10.51 7 1.67 9.71 7 2.29 6.84 7 0.09 5.64 7 0.82 8.37 7 3.09

0.717 1.38 1.057 0.53 1.61 7 0.91 4.72 7 0.01 3.95 7 0.03 5.017 3.16

t¼ 31.85nn Z¼  2.06n t¼ 12.14nn Z¼  3.58nnn t¼ 9.47nnn t¼ 477.11nnn

Ecosystem ANTS 38 ARCS 5 OCEAN 4 TEM 72 TROP 18 UPW 6

11.29 7 3.43 11.55 7 1.23 11.067 2.49 11.11 7 2.05 13.61 7 2.84 15.26 7 2.26

10.58 7 3.39 10.51 7 1.67 7.16 7 3.57 8.86 7 2.59 7.55 7 3.21 8.91 7 3.51

0.717 1.38 1.057 0.53 3.91 7 4.41 2.24 7 1.25 6.047 3.15 6.35 7 2.34

t¼ 31.85nn Z¼  2.06n Z ¼  1.82 t¼ 15.13nn t¼ 8.14nn Z ¼  2.21n

Ocean ANT ARC ATL IND MED PAC

n

p o 0.05. p o0.0001.

nn

Fig. 4. Mean and 95% confidence interval of unadjusted d15N and baseline-adjusted d15N values (BA-d15N) of squids by ocean (Antarctic¼ ANT; Arctic¼ARC; Atlantic¼ ATL; Indian¼ IND; Mediterranean¼MED; Pacific¼PAC) and (b) ecosystem type (Antarctic shelf¼ ANTS; Arctic shelf¼ARCS; open ocean¼OCEAN; temperate coastal and shelf areas¼TEM; tropical shelf and coast¼ TROP; upwelling¼ UPW).

pairwise tests indicated that squids in the ANT (mean and standard deviation BA-d15N¼ 10.5872.39%), ARC (BA-d15N¼ 10.5071.66%) and ATL (BA-d15N¼9.74 72.34%) had higher BA-d15N values than in the PAC (BA-d15N¼8.37 73.09%), IND (BA-d15N¼7.81 71.19%) and MED (BA-d15N¼5.64 70.82%) (Fig. 5a). For the d13C values, the squids in the ANT (d13C¼ 20.83 72.13%) and ARC (d13C¼  19.13 70.98%) had lower values than in the IND (d13C¼ 18.28 70.06%), ATL

Please cite this article as: Navarro, J., et al., Trophic niche of squids: Insights from isotopic data in marine systems worldwide. DeepSea Res. II (2013), http://dx.doi.org/10.1016/j.dsr2.2013.01.031i

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Fig. 5. Mean and standard deviation of baseline-adjusted d15N (BA-d15N) and d13C values and standard ellipse areas of squid species by (a) ocean (Antarctic ¼ANT; Arctic ¼ARC; Atlantic ¼ ATL; Indian ¼IND; Mediterranean ¼ MED; Pacific¼PAC) and (b) ecosystem type (Antarctic shelf¼ ANTS; Arctic shelf ¼ARCS; open ocean¼ OCEAN; temperate coastal and shelf areas ¼ TEM; tropical shelf and coast ¼ TROP; upwelling ¼ UPW). We show the mean isotopic areas (black dot) as well as the 50% (dark grey), 75% (light grey) and 95% (white boxes) of the isotopic area by ocean and ecosystem. The results of post-hoc tests are shown by the subscript letters (BA-d15N values) and numbers (d13C values): same letters/numbers show no significant differences.

(d13C¼  7.8171.03%), MED (d13C¼ 18.0271.18%) and PAC (d13C¼  17.3371.05%) (Fig. 5a). The squid BA-d15N values had high ranges in the ANT (16.9%), PAC (13.2%), and ATL (8.3%), and low ranges in the ARC (4.4%), MED (2.9%), and IND (2.5%) (Fig. 6a). The ranges of squid d13C also differed among oceans, with the highest values in the ANT (8.7%), ATL (5.5%), PAC (5.1%) and MED (5.1%), and lowest values in ARC (2.2%) and IND (0.2%). The isotopic areas estimated with Bayesian procedures clearly differed for squids among oceans (Fig. 5a), with the highest values in the ANT (22.7%2), followed by the PAC (10.6%2), ATL (7.7%2), ARC (6.7%2), MED (3.1%2), and IND (0.2%2), The median trophic position estimates per study (TP using BA-d15N) of squids differed significantly among oceans (Fig. 7a; pseudo-F 5,142 ¼8.44, p ¼0.0001). TP estimates were higher for squids in the ANT (mean TP ¼4.1170.99) and ARC (mean TP¼4.0170.49), followed by the ATL (mean TP¼3.86 70.68), IND (mean TP¼ 3.2970.35), PAC (mean TP¼3.46 70.91), and MED (mean TP¼2.65 70.24) (Fig. 7a).

3.5. Comparison of BA-d15N, d13C and isotopic area and TP estimates between ecosystems The mean BA-d15N and d13C values of squids differed significantly among ecosystem types (Fig. 5b; BA-d15N, pseudo-F 13 5,142 ¼3.54, p ¼0.005; d C, pseudo-F 5,137 ¼28.06, p o0.0001). Post-hoc pairwise tests indicated that squids in the ANTS (mean and SD; BA-d15N¼10.5873.39%) and ARCS (BA-d15N¼ 10.5071.66%) had higher BA-d15N values than in the TEM (BAd15N¼8.8872.59%), UPW (BA-d15N¼8.31 73.56%), TROP (BAd15N¼7.6173.23%), and OCEAN (BA-d15N¼7.1673.57%) (Fig. 5b). For the d13C values, the squids in the ANTS (d13C¼  20.8372.13%) and ARCS (d13C¼  19.1370.98%) had lower values than in the TEM (d13C¼ 17.79 71.01%), TROP (d13C¼  17.78 71.01%), OCEAN (d13C¼ 17.53 71.07%), and UPW (d13C¼ 15.81 70.67%) (Fig. 5b). The squid BA-d15N values ranged higher in the ANTS (16.9%) and TROP (11.1%), and lower in the TEM (9.5%), OCEAN (8%), UPW (7.7%) and ARCS (4.4%) ecosystems (Fig. 6b). The ranges of

Please cite this article as: Navarro, J., et al., Trophic niche of squids: Insights from isotopic data in marine systems worldwide. DeepSea Res. II (2013), http://dx.doi.org/10.1016/j.dsr2.2013.01.031i

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Fig. 6. Ranges of baseline adjusted d15N values (BA-d15N) of squid species by (a) ocean (Antarctic ¼ ANT; Arctic¼ ARC; Atlantic ¼ATL; Indian ¼IND; Mediterranean¼ MED; Pacific¼ PAC) and (b) ecosystem type (Antarctic shelf¼ ANTS; Arctic shelf¼ ARCS; open ocean¼ OCEAN; temperate coastal and shelf areas¼ TEM; tropical shelf and coast ¼ TROP; upwelling ¼UPW).

squid d13C values also differed among ecosystem types, with the highest values in the ANTS (8.7%), TEM (5.3%) and TROP (5.1%), and lowest values in the OCEAN (2.4%), ARCS (2.2%) and UPW (1.6%). The isotopic areas estimated with Bayesian procedures clearly differed for squids by ecosystem type (Fig. 5b), with the highest values in the ANTS (22.7%2), followed by the OCEAN (18.1%2), TROP (10.9%2), TEM (8.5%2), UPW (7.4%2), and ARCS (6.7%2). The trophic position estimates per species per study (TP, using BA-d15N) of squids differed significantly among ecosystem types (Fig. 7b; pseudo-F 5,142 ¼3.54, p ¼0.004). TP estimates were higher for squids in the ANTS (mean TP ¼4.1170.99) and ARCS (mean TP¼4.0170.49), followed by the OCEAN (mean TP¼3.11 71.05), TEM (mean TP ¼3.6170.76), UPW (mean TP¼3.44 71.04), and TROP (mean TP¼3.23 70.59) (Fig. 7a).

4. Discussion In this study, we present the first review of available data on two trophic markers, d15N and d13C, for squids, contributing to the knowledge of the trophic ecology of these abundant invertebrates in marine ecosystems. Since squids proliferate in a variety of ecosystems, some highly exploited by fisheries (Dawe et al., 2000; Sakurai et al., 2000; Bellido et al., 2001; Coll et al., this issue), it is desirable to improve our understanding of the

Fig. 7. Boxplots of trophic position (TP) estimates for squids by (a) ocean (Antarctic¼ ANT; Arctic ¼ARC; Atlantic ¼ ATL; Indian¼ IND; Mediterranean ¼MED; Pacific¼ PAC) and (b) ecosystem (Antarctic shelf ¼ANTS; Arctic shelf ¼ARCS; open ocean¼ OCEAN; temperate coastal and shelf areas ¼TEM; tropical shelf and coast ¼TROP; upwelling ¼ UPW). The smallest observation (sample minimum), lower quartile, median, upper quartile and largest observation (sample maximum) are indicated. The results of post-hoc tests are shown by the subscript letters: same letter indicates no significant differences between oceans or ecosystems.

ecological role of these organisms and their importance in marine ecosystem functioning. Isotope analysis provides important information on the trophic habits of squids, especially important because traditional diet analysis is difficult due to the fact that squids macerate their prey

Please cite this article as: Navarro, J., et al., Trophic niche of squids: Insights from isotopic data in marine systems worldwide. DeepSea Res. II (2013), http://dx.doi.org/10.1016/j.dsr2.2013.01.031i

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with the beak (Jackson et al., 2007). Stable-isotope analysis and other complementary methodologies provide validation for stomach-content analysis and direct feeding observations (Coll et al., this issue). Studies that focused on the trophic ecology of squids using isotopic techniques are few ( 15 published studies), but have increased steadily since 2004 (Fig. 1). Considering all published isotopic data on squids (from 1988 through 2012), the information covers all oceans and the major types of ecosystems. Our review not only promotes the understanding of the trophic ecology of squids, it also demonstrates that more information is needed in various regions, especially the Indian Ocean, Arctic Ocean and Mediterranean Sea, where most of the isotope data are derived from studies focused on marine predators of squids (e.g., Kurle and Worthy, 2001; Catry et al., 2009; Cardona et al., 2012). A well-known limitation in the use of nitrogen isotopic values for improving our understanding the trophic ecology of consumers in different habitats is that the d15N values of the primary producers vary greatly in different regions (Fig. 2b), as a consequence of variations in physical and chemical processes in seawater (Vander Zanden and Rasmussen, 1999). Therefore, the d15N values of the tissues of consumers can be reliably compared with those of other consumers only in a limited geographical range within the same system (Carscallen et al., 2012). Using d15N values of squids, for example, for estimating trophic position requires estimates of the isotopic baseline in each region and system. We used the natural variation in the d15N values of phytoplankton predicted by a model (Fig. 2b) to adjust the d15N values we compiled for squids. The results show the importance of the adjustment by baseline values at oceanic and ecosystem levels (see Fig. 4). A clear example is evident for squids in the Pacific Ocean and in upwelling ecosystems. In both cases, after the baseline adjustment, the d15N values changed from the highest values to among the lowest when compared to samples from other oceans and ecosystem types. Moreover, unadjusted squid d15N values overestimated the trophic positions of squids. The baseline-adjusted isotopic values of squids and the trophic position estimates indicated that squids occupy a wide range of trophic levels in marine food webs, in line with conclusions from a review of food web models, which are based on diet data (Coll et al., this issue). This isotopic variability clearly reflects the great trophic diversity of squids, occupying from low to top positions in marine food webs (Cherel and Duhamel, 2004; Clarke, 1996; Croxall and Prince, 1996; Kaschner et al., 2001; Rodhouse and Nigmatullin, 1996; Stergiou and Karpouzi, 2001; Xavier and Croxall, 2007), and it is consistent with the wide range of sizes that squids display. For example, large species such as the colossal squid and the Humboldt squid, which had the greatest BA-d15N values, act as top predators in some systems, preying on large fishes and other cephalopods (Cherel et al., 2008; Cheung and ¨ ¨ Pitcher, 2005; Cisneros-Montemayor, 2007; Huckst adt et al., 2007). The range of values we found (see Figs. 6 and 7) suggests that squids as a group can exploit resources across entire food webs (Cherel et al., 2008; Cherel and Hobson, 2005). When we compared results with other top predators, different squids such as the Dana octopus squid, Taningia danae, or the neosquid, Nototeuthis dimegacotyle, have isotopic values similar to sympatric top predators such as sperm whales, Physeter macrocephalus, common dolphins, Delphinus delphi, and striped dolphins, Stenella coeruleoalba in the same oceanic area (Das et al., 2003; Das et al., 2000). In contrast, other species that had low BA-d15N values such as longfin squid, Loligo pealeii, or the vampire squid, Vampyroteuthis infernalis utilize a diet composed mainly of prey located at lower positions in the food webs, such as phytoplankton, zooplankton or detritus (Mendoza, 1993; Pangallo and Reddy, 2010; Hoving and

Robison, 2012, Coll et al., this issue). However, our trophic position estimates are not to be taken as absolute values, but as relative values since changes in the trophic enrichment factor (TEF) of 3.4%, which is a global average from Post (2002), may change the absolute values of the estimated-TP. In addition, we found that the largest squid species did not necessarily occupy the highest trophic levels. Some of the largest squids, such as the colossal squid, had high TP values only in the Antarctic Ocean, which is in agreement with previous findings (Cherel and Hobson, 2005). In the Atlantic Ocean, the giant squid, Architeuthis dux, had intermediate BA-d15N values (Cherel et al., 2009), whereas small-sized species such as the bay squid, Lolious noctiluca, and the European squid, Loligo vulgaris, had higher BAd15N values (Chiaradia et al., in press; Das et al., 2003). This loose relationship between BA-d15N and body size contrasts with suppositions of strong size-based trophic dynamics structuring marine communities (Layman et al., 2005; Cherel and Hobson, 2005; Fanelli et al., 2012). Size-based relationships are important when modeling marine food-webs and our results highlight the complexity of marine organism ecology and ecosystem dynamics. We found clear differences in both trophic position and trophic width (isotopic area) of squids among oceans and ecosystem types. In general, the differences in trophic position can be explained by differences in the feeding habits of the species in each ocean or ecosystem type. In polar regions, for example, most of the squid species feed on fishes, crustaceans and other cephalopods (Heymans, 2003; Pitcher et al., 2002) and ecosystem models for polar regions characterize squids as occupying relatively high trophic positions (see Coll et al., this issue). Our results, however, show that some of the squids in the Antarctic Ocean are very low in terms of trophic positions in the food web. In the Mediterranean Sea and Indian Ocean, smaller squids mainly exploit zooplankton, detritus and small forage fishes (Sa´nchez, 1982; Christensen et al., 2003; Coll et al., 2006; Coll et al., this issue), and our trophic position estimates were lower and varied less. Trophic widths inferred by isotopic standard ellipse areas underscored that squid species utilize a generalist trophic strategy, which is consistent with food-web models and diet data (Coll et al., this issue). Differences in isotope-derived trophic width among oceans and ecosystem types are probably a consequence of different trophic behavior and ecological traits of the respective squid species in the different systems (Cherel and Hobson, 2005; Cherel et al., 2009). For example, in temperate ecosystems, where the isotopic standard ellipse areas were large, a large variety of squid species with very different ecological characteristics occur: from deep-sea squids (bush-club squid, Batoteuthis skolopsk) to shallow-water squids (common arm squid Brachioteuthis riisei) and from zooplankton-consumers (Patagonian squid Loligo gahi) to fish-consumers (greater hooked squid, Moroteuthis ingens) (Cherel and Duhamel, 2003; Cheung and Pitcher, 2005; CornejoDonoso and Antezana, 2008; Jereb and Roper, 2010). In regions where squid had low trophic widths, such as the Mediterranean Sea, the squid species are ecologically more similar (e.g. shortfin squid Illex coindetti, European squid L. vulgaris, European flying squid Todarodes sagittatus, and lesser flying squid Todaropsis eblanae) (Sa´nchez et al., 1998; Coll et al., 2006, 2007, Jereb and Roper, 2010; Tsagarakis et al., 2010). In conclusion, this review illustrates the utility of stable isotope data to improve the understanding of the trophic ecology of squids in marine systems. Stable isotope values revealed the great variability and differences in trophic positions and trophic widths of squids among oceans and ecosystem types. The study also reinforces the importance of considering natural variation in the isotopic values of primary producers when comparing among

Please cite this article as: Navarro, J., et al., Trophic niche of squids: Insights from isotopic data in marine systems worldwide. DeepSea Res. II (2013), http://dx.doi.org/10.1016/j.dsr2.2013.01.031i

J. Navarro et al. / Deep-Sea Research II ] (]]]]) ]]]–]]]

consumers inhabiting different ecosystems, especially in medium latitudes. Studies such as this may encourage the utilization of the stable isotope approach to further investigate the trophic ecology of marine predators at different organizational levels, from individual species to entire communities and ecosystems.

Acknowledgments JN was supported by a postdoctoral contract of the Juan de la Cierva program of the Spanish Government. MC was supported by a research contract of the Ramon y Cajal program of the Spanish Government. CS was supported by the SFB754 project of the German Research Foundation (DFG).

Appendix A. Supplementary Information Supplementary data associated with this article can be found in the online version at http://dx.doi.org/10.1016/j.dsr2.2013.01.031.

References Amaratunga, T., 1983. The role of cephalopods in the marine ecosystem. In: Caddy, J.F. (Ed.), Advances in Assessment of World Cephalopod Resources. FAO Fisheries Technical Paper, pp. 379–412. Anderson, M.A., Gorley, R.N., Clarke, K.R., 2008. PERMANOVA“ for PRIMER: Guide to Software and Statistical Methods. PRIMER-E, Plymouth, UK. Bellido, J., Pierce, G., Wang, J., 2001. Modeling intra-annual variation in abundance of squid Loligo forbesi in Scottish waters using generalised additive models. Fish. Res. 52, 23–39. Boyle, P., Rodhouse, P., 2005. Cephalopods: Ecology and Fisheries. Blackwell Science LtD., Oxford. Cardona, L., de Quevedo, A., Borrell, A., Aguilar, A., 2012. Massive consumption of gelatinous plankton by Mediterranean apex predators. PLoS ONE 7, e31329. Carscallen, W.M.A., Vandenberg, K., Lawson, J.M., Martinez, N.D., Romanuk, T.N., 2012. Estimating trophic position in marine and estuarine food webs. Ecosphere, 3, art25. Catry, T., Ramos, J., Jaquemet, S., Faulquier, L., Berlincourt, M., Hauselmann, A., Pinet, P., Le Corre, M., 2009. Comparative foraging ecology of a tropical seabird community of the Seychelles, Western Indian Ocean. Mar. Ecol. Prog. Ser. 374, 259–272. Cherel, Y., Ducatez, S., Fontaine, C., Richard, P., Guinet, C., 2008. Stable isotopes reveal the trophic position and mesopelagic fish diet of female southern elephant seals breeding on the Kerguelen Islands. Mar. Ecol. Prog. Ser. 370, 239–247. Cherel, Y., Duhamel, G., 2003. Diet of the squid Moroteuthis ingens (Teuthoidea: Onychoteuthidae) in the upper slope waters of the Kerguelen Islands. Mar. Ecol. Prog. Ser. 250, 197–203. Cherel, Y., Duhamel, G., 2004. Antarctic jaws: cephalopod prey of sharks in Kerguelen waters. Deep Sea Res. I: Papers 51, 17–31. Cherel, Y., Hobson, K.A., 2005. Stable isotopes, beaks and predators: a new tool to study the trophic ecology of cephalopods, including giant and colossal squids. Proc. R. Soc. B: Biol. Sci. 272, 1601. Cherel, Y., Ridoux, V., Spitz, J., Richard, P., 2009. Stable isotopes document the trophic structure of a deep-sea cephalopod assemblage including giant octopod and giant squid. Biol. Lett. 5, 364–367. Cheung, W.W.L., Pitcher, T.J., 2005. A mass-balance model of the Falkland Islands fisheries and ecosystems. In: Palomares, M.L., Pruvost, P., Pitcher, T.J., Pauly, D. (Ed.), Modeling Antarctic Marine Ecosystems. Fisheries Centre Research Reports, pp. 65–85. Chiaradia, A., Forero, M.G., Hobson, K.A., Swearer, S.E., Hume, F., Renwick, L., Dann, P. Diet segregation between two colonies of little penguins Eudyptula minor in southeast Australia. Austral Ecology, in press. Christensen, V., Garces, L.R., Silvestre, G.T., Pauly, D., 2003. Fisheries impact on the South China Sea large marine ecosystem: a preliminary analysis using spatiallyexplicit methodology. Assessment, Management and Future Directions for Coastal Fisheries in Asian Countries, pp. 51–62. Ciancio, J.E., Pascual, M.A., Botto, F., Frere, E., Plata, M., Aires, B., 2008. Trophic relationships of exotic anadromous salmonids in the southern Patagonian Shelf as inferred from stable isotopes. Limnol. Oceanogr. 53, 788–798. Cisneros-Montemayor, A., 2007. The Economic Benefit of Ecosystem-Based Marine Recreation: Implications for Management and Policy. University of British Columbia, Resource Management and Environmental Studies. Clarke, M.R., 1996. The role of cephalopods in the world’s oceans: an introduction. Philos. Trans.: Biol. Sci. 351, 979–983. Clarke, K.R., Gorley, R.N., 2006. PRIMER v6: User Manual/tutorial (Plymouth Routines in Multivariate Ecological Research). Primer-E Ltd., Plymouth.

9

Coll, M., Navarro, J., Olson, R., Christensen, V. Assessing the trophic position and ecological role of squids in marine ecosystems by means of food-web models. Deep Sea Res. II http://dx.doi.org/10.1016/j.dsr2.2012.08.020, this issue. Coll, M., Santojanni, A., Palomera, I., Tudela, S., Arneri, E., 2007. An ecological model of the Northern and Central Adriatic Sea: analysis of ecosystem structure and fishing impacts. J. Mar. Syst. 67, 119–154. Coll, M., Palomera, I., Tudela, S., Sarda , F., 2006. Trophic flows, ecosystem structure and fishing impacts in the South Catalan Sea, Northwestern Mediterranean. J. Mar. Syst. 59, 63–96. Cornejo-Donoso, J., Antezana, T., 2008. Preliminary trophic model of the Antarctic Peninsula Ecosystem (Sub-area CCAMLR 48.1). Ecol. Model. 218, 1–17. Croxall, J., Prince, P., 1996. Cephalopods as prey. I. Seabirds. Philos. Trans. R. Soc. London Ser. B: Biol. Sci. 351, 1023–1043. Das, K., Lepoint, G., Leroy, Y., Bouquegneau, J.M., 2003. Marine mammals from the southern North Sea: feeding ecology data from d13C and d15N measurements. Mar. Ecol. Prog. Ser. 263, 287–298. Das, K., Lepoint, G., Loizeau, V., Debacker, V., Dauby, P., Bouquegneau, J.M., 2000. Tuna and dolphin associations in the North-East Atlantic: evidence of different ecological niches from stable isotope and heavy metal measurements. Mar. Pollut. Bull. 40, 102–109. Dawe, E., Colbourne, E., Drinkwater, K., 2000. Environmental effects on recruitment of short-finned squid (Illex illecebrosus). ICES J. Mar. Sci. 57, 1002–1013. Fanelli, E., Cartes, J., Papiol, V., 2012. Assemblage structure and trophic ecology of deep-sea demersal cephalopods in the Balearic basin (NW Mediterranean). Mar. Freshwater Res. 63, 264–274. Fry, B., Sherr, E.B., 1984. 13C measurements as indicators of carbon flow in marine and freshwater ecosystems. Contrib. Mar. Sci. 27, 13–47. Heymans, J.J., 2003. Revised models for Newfoundland for the time periods 1985–87 and 1995–97. Fish. Centre Res. Rep. 11, 40–63. Hobson, K.A., Montevecchi, W.A., 1991. Stable isotopic determinations of trophic relationships of great auks. Oecologia 87, 528–531. Hoving, H.J.T., Robison, B.H. Vampire squid: detritivores in the oxygen minimum zone. Proc. R. Soc. B: Biol. Sci., in press. ¨ ¨ Huckst adt, L.A., Rojas, C.P., Antezana, T., 2007. Stable isotope analysis reveals pelagic foraging by the Southern sea lion in central Chile. J. Exp. Mar. Biol. Ecol. 347, 123–133. Hunsicker, M., Essington, T., 2008. Evaluating the potential for trophodynamic control of fish by the longfin inshore squid (Loligo pealeii) in the Northwest Atlantic Ocean. Can. J. Fish. Aquat. Sci. 65, 2524–2535. Hunsicker, M., Essington, T., Aydin, K., Ishida, B., 2010. Predatory role of the commander squid Berryteuthis magister in the Eastern Bering Sea: insights from stable isotopes and food habits. Mar. Ecol. Prog. Ser. 415, 91–108. Jackson, A.L., Inger, R., Parnell, A.C., Bearhop, S., 2011. Comparing isotopic niche widths among and within communities: SIBER-Stable isotope Bayesian ellipses in R. J. Anim. Ecol. 80, 595e602. Jackson, G.D., Bustamante, P., Cherel, Y., Fulton, E.A., Grist, E.P.M., Jackson, C.H., Nicols, P.D., Pethybridge, H., Philipps, K., Ward, R.D., Xavier, J.C., 2007. Applying new tools to cephalopod trophic dynamics and ecology: perspectives from the Southern Ocean Cephalopod Workshop. Rev. Fish Biol. Fish. 17, 79–99. Jerb, P., Roper, C.F.E., 2005. Cephalopds of the world. An annotated and illustrated catalogue of cephalopod species known to date. vol. 1. Chambered Nautiluses and Sepiods (Nautilidae, Sepiidae, Sepiolidae, Sepiadariidae, Idiosepiidae and Spirulidae), FAo Species Catalogue for Fishery Purposes, Rome, p. 262. Jereb, P., Roper, C.F.E., 2010. Cephalopods of the world. An annotated and illustrated catalogue of cephalopod species known to date. vol. 2. Myopsid and Oegopsid Squids. FAO Species Catalogue for Fishery Purposes. Rome 4, 605 pp. Kaschner, K., Watson, R., Christensen, V., Trites, A.W., Pauly, D., 2001. Modeling and mapping trophic overlap between marine mammals and commercial fisheries in the North Atlantic, in: Zeller, D., Watson, R., Pauly, D. (Ed.), Fisheries Impacts on North Atlantic Ecosystems: Catch, Effort and National/ Regional Data Sets. Fisheries Centre Research Reports, Vancouver, Canada, pp. 35–45. Klages, N.T.W., 1996. Cephalopods as prey. II. Seals. Philos. Trans.: Biol. Sci. 351, 1045–1052. Kurle, C.M., Worthy, G.A.J., 2001. Stable isotope assessment of temporal and geographic differences in feeding ecology of Northern fur seals (Callorhinus ursinus) and their prey. Oecologia 126, 254–265. Layman, C., Araujo, M.S., Boucek, R., Hammerschlag-Peyer, C.M., Harrison, E., Jud, Z.R., Matich, P., 2011. Applying stable isotopes to examine food-web structure: an overview of analytical tools. Biol. Rev. Cambridge Philos. Soc., http://dx.doi. org/10.1111/j.1469-185X.2011.00208.x. Layman, C.A., Winemiller, K.O., Arrington, D., Jepsen, D.B., 2005. Body size and trophic position in a diverse tropical food web. Ecology 86, 2530–2535. ¨ Lorrain, A., Arguelles, J., Alegre, A., Bertrand, A., Munaron, J.-M., Richard, P., Cherel, Y., 2011. Sequential Isotopic Signature Along Gladius Highlights Contrasted Individual Foraging Strategies of Jumbo Squid (Dosidicus gigas). PLoS ONE 6, e22194. Mariotti, A., Germon, J.C., Hubert, P., Kaiser, P., Letolle, R., Tardieux, A., Tardieux, P., 1981. Experimental determination of nitrogen kinetic isotope fractionation: some principles; illustration for the denitrification and nitrification processes. Plant Soil 62, 413–430. Mendoza, J.J., 1993. A preliminary biomass budget for the Northeastern Venezuela shelf ecosystem. In: Christensen V.P.D.e.(Ed.), Proceedings of the ICLARM Conference on Trophic Models of Aquatic Ecosystems, pp. 285–297.

Please cite this article as: Navarro, J., et al., Trophic niche of squids: Insights from isotopic data in marine systems worldwide. DeepSea Res. II (2013), http://dx.doi.org/10.1016/j.dsr2.2013.01.031i

10

J. Navarro et al. / Deep-Sea Research II ] (]]]]) ]]]–]]]

Michener, R.H., Schell, D.M., 1994. Stable isotope ratios as tracers in marine aquatic food webs. In: Lajtha, K.M.R.e. (Ed.), Stable Isotopes in Ecology and Environmental Science. Blackwell Scientific, Oxford, pp. 138–158. Navarro, J., Louzao, M., Manuel, J., Daniel, I., Delgado, A., Meritxell, A., Hobson, K.A., 2009. Seasonal changes in the diet of a critically endangered seabird and the importance of trawling discards. Mar. Biol. 159, 2571–2578. Navarro, J., Coll, M., Louzao, M., Palomera, I., Delgado, A., Forero, M.G., 2011. Comparison of ecosystem modeling and isotopic approach as ecological tools to investigate food web in the NW Mediterranean Sea. J. Exp. Mar. Biol. Ecol. 401, 97–104. Olson, R.J., Young, J.W., 2007. The Role of Squid in Open Ocean Ecosystems. GLOBEC Report 24:vi, 94 pp. Pangallo, K., Reddy, C., 2010. Marine Natural Products, the Halogenated 10 -Methyl1,20 -bipyrroles Biomagnify in a Northwestern Atlantic Food Web. Environ. Sci. Technol. 44, 5741–5747. Pitcher, T., Heymans, J.J., Vasconcellos, M., 2002. Ecosystem models of Newfoundland for the time periods 1995, 85, 1900, 1450. Fish. Centre Res. Rep. 10, 76. Post, D.M., 2002. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83, 703–718. Praca, E., Laran, S., Lepoint, G., Thome´, J.-P., Quetglas, A., Belcari, P., Sartor, P., 2011. Toothed whales in the Northwestern Mediterranean: insight into their feeding ecology using chemical tracers. Mar. Pollut. Bull. 62, 1058–1065. Rodhouse, P., Nigmatullin, C.M., 1996. Role as consumers. Philos. Trans. R. Soc. London Ser. B: Biol. Sci. 351, 1003–1022. R Development Core Team, 2011. R: A language and environment for statistical computing. Available from URL: /http://www.R-project.org/S. Ruiz-Cooley, R., Villa, E., Gould, W., 2010. Ontogenetic variation of d13C and d15N recorded in the gladius of the jumbo squid Dosidicus gigas: geographic differences. Mar. Ecol. Prog. Ser. 399, 187–198. Sakurai, Y., Kiyofuji, H., Saitoh, S., Goto, T., Hiyama, Y., 2000. Changes in inferred spawning areas of Todarodes pacificus (Cephalopoda:Ommastrephidae) due to changing environmental conditions. ICES J. Mar. Sci. 57, 24–30. Sa´nchez, P., 1982. Regimen alimentario de Illex coindetii (Verany, 1837) en el mar Catala´n. Investigacio´n Pesquera 46, 443–449.

Sa´nchez, P., Gonza´lez, F., Jereb, P., Laptikovsky, V.V., Mangold, K., Nigmatullin, C., Ragonesse, S., 1998. Chapter 4. Illex coindetii. In: Rodhouse, P.G., Dawe, E.G., O’Dor, R.K. (Eds.), Squid recruitment dynamics: the commercial Illex species. FAO Fisheries Technical Paper Num. 376, Rome, pp. 59–76. Smale, M., 1996. Cephalopods as prey. IV. Fishes. Philos. Trans. R. Soc. London Ser. B: Biol. Sci. 351, 1067–1081. Somes, C.J., Schmittner, A., Galbraith, E.D., Lehmann, M.F., Altabet, M.A., Montoya, J.P., Letelier, R.M., Mix, A.C., Bourbonnais, A., Eby, M., 2010. Simulating the global distribution of nitrogen isotopes in the ocean. Global Biogeochem. Cycles 24, GB4019. Stergiou, K.I., Karpouzi, V.S., 2001. Feeding habits and trophic levels of Mediterranean fish. Rev. Fish Biol. Fish. 11, 217–254. Tesdal, J.E., Galbraith, E.D., Kienast, M., 2012. The marine sedimentary nitrogen isotope record. Biogeosci. Discuss. 9, 4067–4097. Tesdal, J.-E., Galbraith, E.D., Kienast, M., 2013. Nitrogen isotopes in bulk marine sediment: linking seafloor observations with subseafloor records. Biogeosciences 10, 101–118. Tsagarakis, K., Coll, M., Giannoulaki, M., Papakonstantinou, C.A.M., 2010. Food-web traits of the North Aegean Sea continental shelf (Eastern Mediterranean, Greece) and comparison with other Mediterranean ecosystems. Estuarine Coastal and Shelf Sci. 88, 233–248. Vander Zanden, M.J., Rasmussen, J.B., 1999. Primary consumer d13C and d15N and the trophic position of aquatic consumers. Ecology 80, 1395–1404. Vander Zanden, M.J., Rasmussen, J.B., 2001. Variation in d15N and d13C trophic fractionation: Implications for aquatic food web studies. Limnol. Oceanogr. 46, 2061–2066. Weaver, A.J., Eby, M., Wiebe, E.C., Bitz, C.M.m, Duffy, P.B., Ewen, T.L., Fanning, A.F., Holland, M.M., MacFadyen, A., Matthews, H.D., Meissner, K.J., Saenko, O.m, Schmittner, A., Wang, H., Yoshimori, M., 2001. The UVic Earth system climate model: model description, climatology, and applications to past, present and future climates. Atmos. Ocean 39, 361–428. Xavier, J.C., Croxall, J.P., 2007. Predator–prey interactions: why do larger albatrosses eat bigger squid? J. Zool. 271, 408–417.

Please cite this article as: Navarro, J., et al., Trophic niche of squids: Insights from isotopic data in marine systems worldwide. DeepSea Res. II (2013), http://dx.doi.org/10.1016/j.dsr2.2013.01.031i