Ontogenetic shifts in diet and trophic position of walleye pollock, Theragra chalcogramma, in the western East Sea (Japan Sea) revealed by stable isotope and stomach content analyses

Fisheries Research 204 (2018) 297–304

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Short communication

Ontogenetic shifts in diet and trophic position of walleye pollock, Theragra chalcogramma, in the western East Sea (Japan Sea) revealed by stable isotope and stomach content analyses Hyun Je Parka, Tae Hee Parka, Chung-Il Leea, Chang-Keun Kangb, a b

T

⁎

Department of Marine Bioscience, Gangneung-Wonju National University, Gangneung, 25457, Republic of Korea School of Earth Sciences & Environmental Engineering, Gwangju Institute of Science and Technology, Gwangju, 61005, Republic of Korea

A R T I C LE I N FO

A B S T R A C T

Handled by B. Morales-Nin

We determined the dietary composition and trophic position (TP) of walleye pollock in the western East Sea (Japan Sea), based on the δ13C and δ15N values of this species, sympatric dominant fish and invertebrates, and their putative food sources in winter. A broad range of the consumer δ13C′ (lipid-corrected) values reflected clear distinctions between benthic and pelagic feeders, differentiating benthic vs. pelagic trophic pathways. The intermediate δ13C′ and δ15N values of pollock fell between those of benthic and pelagic feeders, indicating their trophic links through both pathways. Increases of their isotopic values with increasing body length suggest an ontogenetic change in dominant diets from pelagic to benthic prey as confirmed by stomach content analysis. Their ontogenetic pattern in resource utilization might be associated with deeper migration range with size, increasing TP during ontogeny.

Keywords: Walleye pollock Dietary composition Trophic pathway Ontogeny Stable isotopes East Sea

1. Introduction Walleye pollock, Theragra chalcogramma (hereafter ‘pollock’), is a sub-arctic gadid species distributed in the North Pacific Ocean from Korean waters to the central California coast (Bailey et al., 1999; Makino et al., 2014). The annual global catch of pollock in 2011 was about 3.2 million tons, making it among the world’s largest fisheries (FAO, 2013). Because of its wide distribution and high abundance, this species forms an intermediate key component of the marine food web as a predator of mesozooplankton and forage fish, or as prey for demersal fish and marine mammals (Springer, 1992; Tamura et al., 1998; Napp et al., 2000; Mueter et al., 2006). Fluctuations in pollock abundance have the potential to affect the entire marine ecosystem via top–down pressure (Springer, 1992; Bailey et al., 2005). Understanding the trophic ecology of the pollock is crucial to our overall knowledge of energy flow within the pollock habitats, which has begun to undergo appropriate assessment and management as a sustainable fishery (Adin and Mueter, 2007). Feeding habits of pollocks are very opportunistic, and changes in their dietary composition reflect the variation in their physical and biological environments (Bailey et al., 2005; Yamamura et al., 2013). Many studies have reported the feeding strategy of pollocks in association with seasonal, geographical, and ontogenetic dietary changes (Adams et al., 2007; Wilson et al., 2011; Yamamura

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et al., 2013; Buckley et al., 2016). These studies commonly showed that pollocks feed exclusively on pelagic prey items and shift ontogenetically from mesozooplankton to mesopelagic fishes, juvenile pollock and/or benthic animals, based on stomach content analysis. In addition, Yamamura et al. (2002) found that large-sized pollocks are generally distributed in deeper water, which is closely associated with their flexible feeding habits to utilize a wide range of resource items and habitats. In Korea, pollock has been consumed widely and the domestic consumption was about 380,000 tons annually from 1985 to 2010 (Kim et al., 2014). The annual domestic production of the species increased continuously from the early 1970s (about 16,000 tons) to the early 1980s (about 165,000 tons) (MIFAFF, 2012). Despite the large amount of pollock consumption, however, the annual production underwent a drastic decline during the 1990s (to less than 1000 tons) and there has been no meaningful production since 2000 (MIFAFF, 2012). Pollock stock in Korean waters accounts for the southwestern end of the distributional range in the North Pacific. While warming of the sea and overfishing of juvenile and adult individuals are assumed to be the cause of the severe decrease in the overall stock size and production in Korean waters (Kang et al., 2000; Kang and Kim, 2015), questions remain on what induced the collapse of pollock stock in Korean waters of the western East Sea (Japan Sea). Given the important prey–predator

Corresponding author. E-mail address: [email protected] (C.-K. Kang).

https://doi.org/10.1016/j.fishres.2018.03.006 Received 20 August 2017; Received in revised form 21 February 2018; Accepted 2 March 2018 0165-7836/ © 2018 Elsevier B.V. All rights reserved.

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Fig. 1. Map of the sampling areas located at the southern boundary of the North Korea Cold Current (NKCC) in the western East/Japan Sea. Field circle indicates the sampling site collected for animals and organic matter sources. SPF, subpolar front; LC, Liman current; EKWC, East Korean Warm Current; and TC, Tsushima Warm Current.

that support their production (Tieszen et al., 1983; see Layman et al., 2012). The main goal of this study was to determine the dietary composition and TP of walleye pollock in the western East Sea (Japan Sea) using carbon and nitrogen stable isotope tracers in combination with stomach content analysis. Based on the known changes in diet composition and feeding strategy of this species (Adams et al., 2007; Wilson et al., 2011; Yamamura et al., 2013; Buckley et al., 2016), we hypothesized that δ13C (prey resources) and δ15N values (TP) of pollock would change with ontogenetic stage, and thereby with distribution depth. For this purpose, we analyzed the stable carbon and nitrogen isotope ratios of pollock, sympatric dominant fish, and their putative food sources in winter. Because pollock fishing is limited to the winter, we collected pollock specimens and other related fish and invertebrate samples only at that season. To our knowledge, this investigation is the first isotopic approach to study the trophic ecology of pollock in the western East Sea (Japan Sea).

interactions created by pollock in marine food webs, knowledge about biological and ecological characteristics of this species could be a key in explaining the collapse of its stock in local environmental conditions. While some basic biological research has been conducted regarding biometry and reproductive cycle of the pollock (Kang and Kim, 2015), there is little information on dietary composition determining their trophic ecology in the western East Sea (Japan Sea). Traditionally, stomach content analysis has been used widely to quantify dietary composition and to delineate the trophic relationships of marine consumers (Baker et al., 2014). However, this method may offer snapshot information on food consumed over a short time. Several dietary items stay longer in the consumer stomachs and thus can bias stomach content analysis toward refractory items such as prey with hard carapaces of decapods or shells of bivalves and gastropods (Pinnegar and Pollunin, 2000; Daveport and Bax, 2002). Alternatively, stable isotope ratios of consumer tissues can provide temporal integration of assimilated diets over the long term (Peterson and Fry, 1987; Michener and Schell, 1994; Layman et al., 2012). This method allows us to explore the feeding relationships of animals and trophic transfer through food webs. The carbon isotopic ratio (δ13C) can provide information about the origin of organic matter assimilated by consumers, because the δ13C value of an animal generally occurs at a slight enrichment (0.5–1.2‰) compared with that of its prey (DeNiro and Epstein, 1978; Fry and Sherr, 1984). By contrast, the nitrogen isotopic ratio (δ15N) can be used to evaluate the trophic position (TP) of organisms because this value is enriched by 2–4‰ with each trophic level (Minagawa and Wada, 1984; Vander Zanden and Rasmussen, 2001; Post, 2002). In this way, stable isotope studies have elucidated the relative contributions of dietary sources to fish nutrition and the ontogenetic shift in TP of fish species (Gu et al., 1997; Jennings et al., 2002; Melville and Connolly, 2003; Marsh et al., 2017). While this diettissue isotope fractionation of nutrients can sometimes mislead the interpretation of predators’ diets (Gannes et al., 1997), stable isotope techniques are useful for identifying broad sources of production and differentiating benthic and pelagic trophic pathways (Fry and Sherr, 1984). A combination of two complementary techniques of stomach content and stable isotope analyses can provide insight into a more complete dietary history of consumers and the major trophic pathways

2. Materials and methods 2.1. Sample collection The North Korea Cold Current (NKCC), a branch of Liman Current in the northern East Sea (Japan Sea), flows to the south off the northeast coast of the Korean Peninsula (Lee et al., 2009, 2016). This cold current encounters the East Korea Warm Current, one of the branches of the Tsushima Warm Current, which flows to the north along the southeast coast of the Korean Peninsula, forming a subpolar front in the vicinity of our study area. Our sampling site is located at the southern boundary of the NKCC in the western East Sea (Japan Sea) (Fig. 1). All specimens of pollock (a total of 60 individuals) and other fish and crustaceans (40 individuals) were collected during the winter (January to March) of 2016. Samplings were conducted using a trammel net (outer 60 cm mesh, inner 8.5 cm mesh) from a commercial fishing vessel over 24 h. Fishing depth range was 300–450 m. Total lengths and weights of the specimens were measured to the nearest 0.1 cm and 0.1 g, respectively, on board. Then the samples were stored on ice (−20 °C) and transported to the laboratory. 298

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or 15N/14N. To calibrate the system, international standards for sucrose (ANU C12H22O11; NIST, Gaithersburg, MD, USA) and ammonium sulfate ([NH4]2SO4; NIST) were used as laboratory reference standards. The analytical reproducibility based on 20 replicate measurements of urea was within 0.09‰ and 0.22‰ for δ13C and δ15N, respectively. For the fish samples, because of interspecific differences in the concentration of 13C-depleted lipids compared with other biochemical components, the isotopic correction, which eliminates the effects of variation in the δ13C values due to the lipid content in the fish tissues was performed using the following equation by Post et al. (2007): δ13 δ13Cnormalized = δ13Cuntreated − 3.32 + 0.99 × C: N (ratios ), where Cnormalized and δ13Cuntreated are the lipid-normalized and measured values of the sample, respectively; C and N are the proportions of carbon and nitrogen in the sample. Post et al. (2007) found that this equation can apply to all aquatic animals to eliminate lipid-related biases in δ13C if their C:N ratios are > 3.5. The TPs of pollock and other consumers were calculated using the equation: TPi = (δ15Ni − δ15Nbaseline)/Δ15N + 2, where δ15Ni represents the nitrogen isotope value of the target consumer; δ15Nbaseline is the nitrogen isotope value of baseline species (obtained for an herbivorous calanoid copepod as a primary consumer in this study); Δ15N is the enrichment factor in δ15N per TP (3.4‰ derived from Post (2002)); and 2 represents the reference value of primary consumers in the food web.

Zooplankton were obtained by oblique towing at the same station, using a Bongo net (0.25 m2 mouth opening, 300 μm mesh) equipped with a flowmeter. Partial zooplankton samples were preserved in 70% ethanol for later taxonomic identification in the laboratory and the remainder were frozen in 200 mL polyethylene bottles on dry ice. Suspended particulate organic matter (SPOM) was collected from seawater samples at each sampling occasion. To collect SPOM, about 20 L of seawater was collected using a van Dorn water sampler and then prefiltered through a 200 μm mesh sieve to remove any possible remains of zooplankton and large particles. The SPOM was retained on precombusted (450 °C for 4 h) Whatman GF/F glass fiber filters using a vacuum pump. The samples were then frozen on dry ice for later processing. 2.2. Laboratory processing In the laboratory, all fish samples for stable isotope analysis were dissected out and white muscle tissues were obtained from the anterior dorsal region. Stomach was also separated from the pollock individuals and its contents were preserved with 70% ethanol for later analysis. For crustaceans, the muscle tissues for the isotope analysis were carefully extracted from the shell and cuticle. Zooplankton were subsampled and the major dominant zooplankton groups (copepods and euphausiids) were identified under a dissecting microscope. These animal samples were dried in a drying oven for 72 h at 50–60 °C and ground into a homogeneous powder with a mortar and pestle. The filtered samples of SPOM for isotope analysis were acidified by fuming overnight over 1 N HCl to remove inorganic carbonates and then oven dried at 50 °C for 48 h. All pretreated samples were kept frozen in a deep freezer (−70 °C) until isotope analysis.

2.5. Data analysis The statistical analyses were conducted using a commercial statistic program. All data were first tested for normality and homogeneity of variance using the Shapiro–Wilk procedure and Levene’s test, respectively. One-way analysis of variance (ANOVA) was used to test for significant differences in the δ13C and δ15N values of animal samples, and Tukey’s honest significant difference (HSD) multiple-comparison post hoc test was used to evaluate differences among variables. Linear regressions were used to examine the relationships between length, weight, and δ15N values of pollock, which provide information on their size-based dynamics in food sources and TP. The TPs of pollock were compared between large and small individuals based on the size of body length 40 cm, that is the size class occurring ontogenetic shift in the pollock diets observed by Dwyer et al. (1987) and Yamamura et al. (2002). All values are presented as the mean ± one standard deviation (SD).

2.3. Stomach content analysis The preserved stomach contents were identified to the lowest possible taxonomic level and enumerated under a stereomicroscope. The wet weight of each food item was then measured to the nearest 1 mg. To reduce the bias of stomach content analysis, fresh and partially digested prey items were used for the analysis. Partially digested fish and cephalopods were identified from sagittal otoliths and beaks, respectively. Prey items were quantified by percent frequency of occurrence (%F, number of stomach in which a particular prey item occurred as a percentage of the total number of stomachs examined, excluding individuals with empty stomachs), percent numerical frequency (%N) of each prey item to the total number of identifiable prey items, and percent wet weight (%W) of each prey item to the total wet weight of identifiable prey items. Then, an index of relative importance (IRI) for all prey items was calculated with the formula [IRI = (%N + %W) × % F], as described by Pinkas et al. (1971), and expressed as a percentage n IRIi × 100 , where n is the total (%IRI) as follows: %IRI = IRIi / ∑ i=1 number of food categories considered at a given taxonomic level.

3. Results The δ13C and δ15N values of SPOM did not differ significantly for the three months studied (January, February, and March; ANOVA, p > 0.05), and so were pooled (Table 1). SPOM had mean values of −21.2 ± 0.7‰ for δ13C and 4.9 ± 0.7‰ for δ15N. For zooplankton, two groups were analyzed (calanoid copepods and euphausiids). No monthly variations were observed in the δ13C and δ15N values of both zooplankton groups (ANOVA, p > 0.05 for all cases) and these values were also pooled. The copepods had mean δ13C and δ15N values of −23.0 ± 0.5‰ and 5.7 ± 0.7‰, respectively. Both the δ13C and δ15N values for euphausiids were significantly higher than those determined for copepods, with mean values of −22.3 ± 0.3‰ for δ13C and 7.2 ± 0.4‰ for δ15N. During the study period, 60 pollock specimens and 40 other animals (12 fish species and three macroinvertebrate species) were collected from the study site (Table 2). Because all fish samples had mean C:N ratios greater than 3.5, their δ13C values (δ13C′) were corrected for lipid content (Post et al., 2007). The δ13C and δ13C′ values of pollock ranged from −21.3 to −18.2‰ (mean −20.1 ± 0.7‰) and from −21.1 to −17.8‰ (−19.8 ± 0.7‰), respectively. The δ15N values ranged from 12.4 to 15.0‰ (13.5 ± 0.6‰). The δ13C′ values of the other specimens analyzed (with the exception of pollock) ranged from −21.6 ± 0.3‰ (Arctoscopus japonicus) to −17.3 ± 0.3‰ (Argis lar). By contrast, the

2.4. Stable isotope analysis To measure the carbon and nitrogen stable isotope ratios, aliquots (1.0–2.0 mg) of the powdered samples were weighed in tin combustion cups (5 × 9 mm, D × H) using a microbalance. For filtered samples, the entire filter was sealed by a tin disk. The sealed samples were combusted at 1030 °C in a CHN elemental analyzer (vario MICRO cube, Hanau, Germany) and the resultant gases were analyzed using a linked continuous-flow isotope ratio-mass spectrometer (CF-IRMS; IsoPrime 100, Cheadle, U.K.). The stable isotope ratios are expressed in δ notation relative to conventional standard reference materials (Vienna Pee Dee Belemnite for carbon, and atmospheric N2 for nitrogen), as follows:

⎡ Rsample ⎞ ⎤ 13 15 13 12 3 δX(‰) = ⎢ ⎜⎛ R ⎟ − 1 ⎥ × 10 , where X is C or N and R is C/ C s tan dard ⎠ ⎣⎝ ⎦ 299

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Table 1 δ13C and δ15N values of organic matter (SPOM, suspended particulate organic matter) and zooplankton (calanoid copepods and euphausiids) collected during winter 2016 in the western part of the East/Japan Sea. One-way ANOVA and mean values of δ13C and δ15N values for SPOM and two zooplankton groups among three months (January, February, and March). Data represent mean ± 1SD. January

Organic matter SPOM Zooplankton Calanoid copepods Euphausiids

February

March

Mean

Significance (p)

n

δ13C

δ15N

n

δ13C

δ15N

n

δ13C

δ15N

δ13C

δ15N

δ13C

δ15N

6

−21.4 ± 0.8

4.7 ± 0.8

7

−21.1 ± 0.9

4.9 ± 0.6

7

−21.2 ± 0.5

5.1 ± 0.8

−21.2 ± 0.7

4.9 ± 0.7

0.720

0.568

4 3

−23.1 ± 0.4 −21.8 ± 0.2

5.6 ± 0.6 7.0 ± 0.3

6 3

−23.0 ± 0.6 −21.6 ± 0.4

5.3 ± 0.6 7.2 ± 0.6

6 3

−22.8 ± 0.6 −22.1 ± 0.3

6.1 ± 0.7 7.3 ± 0.3

−23.0 ± 0.5 −21.8 ± 0.3

5.7 ± 0.7 7.2 ± 0.4

0.767 0.197

0.158 0.722

δ15N values ranged from 10.9 ± 0.5‰ (Berryteuthis magister) to 16.2 ± 0.3‰ (Eumicrotremus birulai). An isotope bi-plot for all consumers showed a broad range of δ13C and δ15N values (Fig. 2). Demersal fish and benthic invertebrates had high δ13C and δ15N values compared with pelagic fish and zooplankton. Pollock had intermediate δ13C and δ15N values, between the pelagic and benthic feeders on the dual isotope plot. Total lengths of pollock individuals ranged from 20.1 to 68.7 (40.4 ± 11.5) cm and their body weight from 46.2 to 1,746.4 (451.7 ± 389.1) g. Their δ13C′ and δ15N values increased significantly with length (r 2 = 0.371 and 0.584, respectively; p < 0.001 for both; Fig. 3). Calanoid copepods had the lowest δ15N value of 5.7 ± 1.1‰ and thus this value was set as TP 2 representing primary consumers (Table 2). The TPs of all fish samples ranged from 3.5 ± 0.2 for B. magister to 5.1 ± 0.1 for E. birulai. The TPs of pollock increased from 4.2 ± 0.1 for small (< 40 cm) individuals to 4.4 ± 0.2 for large (> 40 cm) individuals, with a mean value of 4.3 ± 0.2. Of the 60 pollock stomachs examined, nine (15%) were empty. A total of 24 prey taxa were identified, comprising 10 categories (three Amphipoda species, Mysidacea, Euphausiacea, Squillidae, seven Macrura species, five Cephalopoda species, Polychaeta, two Stelloridea groups, two Pisces species, and eggs) but four were unidentifiable (Table 4). The most important prey groups found in the stomachs of pollock were Macrura (73.0%) and Cephalopoda (38.4%) in terms of frequency of occurrence (%F), Euphausiacea (69.6%) and Amphipoda (14.4%) in terms of percent number (%N), and Cephalopoda (40.4%) and Macrura (27.1%) in terms of weight (%W). According to the %IRI, the most important prey items were Macrura (35.9%), followed by

Fig. 2. Dual isotope plot of δ13C and δ15N values of animals (gray squares, zooplankton; gray triangles, walleye pollock; black circles, other fish; white circles, macrobenthic consumers) and organic matter sources (black squares: SPOM, suspended particulate organic matter) at the sampling site. Values are mean δ13C and δ15N (% ± 1 SD). Species codes indicate the fish and macrobenthic consumers (Fish: STc, Theragra chalcogramma, < 40 cm; LTc, Theragra chalcogramma, > 40 cm; Aj, Arctoscopus japonicas; Bm, Berryteuthis magister; Cr, Careproctus rastrinus; Ds, Dasycottus setiger; Eb, Eumicrotremus birulai; Gm, Gadus microcephalus; Gs, Glyptocephalus stelleri; Li, Liparis ingens; Ll, Lumpenella longirostris; Lt, Lycodes tanakai; Mg, Malacocottus gibber; Pd, Paroctopus dofleini; Macroinvertebrate: Al, Argis lar; Co, Chionoecetes opilio; Pe, Pandalus eous).

Cephalopoda (25.5%) and Euphausiacea (21.3%). The most common prey items of pollock changed from Pisces (48.0%) and Mysidacea (42.6%) for small individuals (< 40 cm in length) to Cephalopoda (45.5%) and Macrura (27.5%) for large individuals (> 40 cm in length) in terms of percent weight (%W). This reflected that large pollock

Table 2 Total length (TL, cm), biomass (g), δ13C and δ15N values, and trophic position (TP) of fish and macroinvertebrates collected during winter (January to March) 2016 in the western part of the East/Japan Sea. Data represent mean ± 1SD. Species name Fish Theragra chalcogramma < 40 cm > 40 cm Total Arctoscopus japonicus Berryteuthis magister Careproctus rastrinus Dasycottus setiger Eumicrotremus birulai Gadus macrocephalus Glyptocephalus stelleri Liparis ingens Lumpenella longirostris Lycodes tanakai Malacocottus gibber Paroctopus dofleini Macroinvertebrate Argis lar Chionoecetes opilio Pandalus eous

n

TL (cm)

Biomass (g)

δ13C

28 32 60 5 5 3 5 3 3 5 3 5 1 4 1

20.1–39.5 40.1–68.7 20.1–68.7 16.7–23.3 17.5–23.0 21.9–33.5 14.9–29.5 11.2–13.1 33.6–37.6 21.6–31.0 27.1–39.6 25.9–36.1 47.1 17.5–27.9 10

46.2–419.0 245.6–1746.4 46.2–1746.4 34.9–86.9 204.4–389.5 136.3–396.4 53.5–397.1 70.8–146.0 307.6–565.6 52.8–179.3 228.0–785.8 57.4–181.3 475.1 74.5–476.0 336.6

−20.2 −19.5 −19.8 −21.6 −21.2 −18.9 −18.6 −19.8 −18.2 −17.9 −18.7 −19.6 −20.1 −20.6 −18.7

3 3 2

5.9–14.0 45.6–73.2 7.6–8.1

15.3–16.5 37.0–144.6 11.9–14.6

−17.3 ± 0.3 −17.7 ± 0.3 −19.1 ± 0.1

300

δ15N

± ± ± ± ± ± ± ± ± ± ± ±

0.5 0.6 0.7 0.3 0.4 0.2 0.2 0.2 0.3 0.4 0.2 0.3

± 0.3

13.1 13.9 13.5 12.3 10.9 14.1 15.8 16.2 14.2 13.6 14.9 15.9 12.4 16.0 15.7

TP

± ± ± ± ± ± ± ± ± ± ± ±

0.4 0.5 0.6 0.3 0.5 0.2 0.4 0.3 0.3 0.4 0.4 0.3

± 0.1

14.2 ± 0.4 13.3 ± 0.3 11.8 ± 0.4

4.2 4.4 4.3 3.9 3.5 4.5 5.0 5.1 4.5 4.3 4.7 5.0 4.0 5.0 4.9

Code

± ± ± ± ± ± ± ± ± ± ± ±

0.1 0.2 0.2 0.1 0.2 0.1 0.1 0.1 0.1 0.2 0.1 0.1

± 0.1

4.5 ± 0.1 4.2 ± 0.1 3.8 ± 0.1

STc LTc Aj Bm Cr Ds Eb Gm Gs Li Ll Lt Mg Pd Al Co Pe

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to uncover how their feeding habits respond to local hydrographic conditions. A δ13C–15N dual isotope plot of consumers discriminates between benthic and pelagic feeders along the 13C axis (Fig. 2). The Kuro shrimp, A. lar, a small benthic invertebrate, had higher δ13C and δ15N values than those of the larger pelagic fish, B. magister and A. japonicus. Likewise, demersal fish and benthic invertebrates were more 13 C- and 15N-enriched than pelagic sources and consumers, differentiating between benthic and pelagic TPs. Higher δ13C and δ15N values in benthic food webs than those in pelagic food webs are typical of continental-shelf and deep-sea ecosystems, generating isotopically distinct TPs because benthic feeders consume organic matter sinking to the seafloor (Davenport and Bax, 2002; Le Loc’h et al., 2008; Boyle et al., 2012). Sediment trap experiments in the vicinity of our study area highlighted that particles sinking to the sea floor had increased δ13C and δ15N values (−21.2‰ to −17.5‰ and 5.0–7.9‰, respectively) compared with those (annual means of −21.1 and 3.4‰, respectively) of SPOM in surface waters (Kwak et al., 2017). Benthic animals have higher δ15N values than epipelagic species with similar feeding strategies in pelagic food webs, as a result of the rich 15N-enrichment in sinking material relative to the surface water SPOM through colonization by bacteria (Drazen et al., 2008). Furthermore, Polunin et al. (2001) found that some bathyal consumers exhibited an increasing pattern of δ13C and δ15N values with increasing depths, which result from biogeochemical processes of sinking phytodetritus as the basal organic matter of benthic food webs. The δ13C and δ15N values of pollock were intermediate between those of benthic and pelagic feeders, indicating their trophic links through both pathways. Here, relatively wide ranges recorded for the δ13C′ and δ15N values of pollock (−21.1 to −17.8‰ and 12.4–15.0‰, respectively) reflected isotopic shifts with increasing length (Fig. 3). This result clearly suggests that pollocks undergo an ontogenetic diet change in association with changes in feeding habits and prey abundance. The dietary composition of this species varies markedly with body size and with the abundance of prey organisms, indicating their opportunistic feeding characteristics (Yamamura et al., 2013). As gadid species grow, dietary changes with increasing body length occur by increased contributions of larger prey to their diets (Link and Garrison, 2002). Pelagic prey such

Fig. 3. Relationship between a) δ13C′ – total length (cm) and b) δ15N – total length (cm) of walleye pollock collected from the western East/Japan Sea during winter 2016.

individuals consumed more meso- and bathypelagic prey (e.g., Gonatopsis makko, Berryteuthis magister, Pandalus eous) and bathyal benthic prey (e.g., Argis lar). 4. Discussion 4.1. Ontogenetic diet change Our study provides information on the ontogenetic pattern of diet utilization for pollock in the western East Sea (Japan Sea) and helping

Table 3 The calculated trophic position (TP) of walleye pollock, based on δ15N values for pollock and calanoid copepods, in different regions including our study. Data represent mean ± 1SD. Location

Species

Size

δ15N

TP

Reference

Gulf of Alaska

Pollock

Large Small

4.1 2.7

Hobson et al. (1997)

Bering Sea

Copepod Pollock

3.9 3.6 2.9 2.3

Kurle and Worthy (2001)

Bering Sea- inner shelf

Copepod Pollock

Bering Sea- shelf break

Copepod Pollock

Alaska Peninsula

Copepod Pollock

15.7 ± 0.7 10.9 ± 0.2 8.5 16.3 ± 0.3 15.2 ± 0.2 12.7 ± 0.2 10.8 ± 0.1 9.8 ± 0.2 14.8 ± 0.5 13.2 ± 0.5 8.0 ± 0.2 13.0 ± 0.7 13.1 ± 0.9 8.1 ± 0.2 14.2 ± 0.3 13.4 ± 1.4 9.0 ± 0.3 13.2 ± 0.2 9.1 ± 0.2 14.2 ± 2.0 9.7 ± 0.3 15.0 ± 0.5 15.1 ± 1.1 10.5 ± 0.2 13.9 ± 0.5 13.1 ± 0.4 5.7 ± 0.7

Eastern Chukchi Sea

Copepod Pollock Copepod Pollock Copepod Pollock

Western East/Japan Sea

Copepod Pollock

Kodiak Island, Alaska Bering Strait

29.9 cm 24.4 cm 14.6 cm 3.2 cm Adult Juvenile Adult Juvenile Adult Juvenile Adult

9.4–12.3 cm 9.0–10.8 cm Large (< 40 cm) Small (> 40 cm)

Copepod

301

4.0 3.5

Schell et al. (1998) Hirons (2001)

3.4 3.5 3.5 3.3 3.2 3.3 3.4 3.8 4.4 4.2

Dehn et al. (2007) Schell et al. (1998) Marsh et al. (2017) Schell et al. (1998) This study

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observed by stomach content analysis of pollock collected at the same time during winter. From pollock individuals of the 25–80 cm length range, our stomach content analysis shows that smaller individuals preyed primarily on mesozooplankton, such as amphipods, mysids, and euphausiids, and the main dietary change, as pollock grew, involved the increased contribution of cephalopods and shrimps to the diets. Ontogenetic change in fish diets is generally related to a mechanism of energy optimization and resource partitioning (Griffiths, 1975; Gerking, 1994). Changes in feeding habit might be associated with increased abundance of larger individuals that feed on larger prey, or on a variety of types of food with age. Several studies have reported that juvenile and adult pollock inhabit different oceanic environments (Bailey et al., 2005; Adams et al., 2007; Yamamura et al., 2013). Some fish species may differentiate their trophic niche by differing distribution depth during ontogenetic progression and thereby partitioning dietary resources (Collins et al., 2005). The ontogenetic shift in the pollock diets might be also related to their size-dependent distribution depths and feeding behaviors. Large pollock generally reside in deeper waters than do small individuals (Yamamura et al., 2002). Opportunistic strategy in resource utilization is common in such fish (Juanes et al., 2002; Adin and Mueter, 2007). Given that fish can feed on both pelagic and benthic food types via enhanced prey-catchability with growth (Le Loc’h et al., 2008; Boyle et al., 2012), size-dependent patterns in resource utilization at different distribution depths could be a general phenomenon in continental-shelf and deep-sea ecosystems. As a result, the ontogenetic dietary change in pollock might be influenced by intraspecific difference in the catchability of suitable food items at their migration depths.

Table 4 Composition of the stomach contents of walleye pollock (Theragra chalcogramma) by percent frequency of occurrence (%F), number (%N), wet weight (%W), the index of relative importance (%IRI) expressed as a percentage of the sum of the IRI values, and ontogenetic variation in percent wet weight (%W, individuals of smaller and larger than 40 cm in total length) during winter (January to March) 2016 in the western part of the East/Japan Sea. + represents less than 0.1%. Bold values represent the sum of each taxonomical group.

Amphipoda Anonyx ampulloides Euprimno macropa Themisto japonica Unidentified Mysidacea Euphausiacea Squillidae Macrura Palaemonidae Pandalus eous Pandalopsis japonica Pandalidae Neocrangon communis Argis lar Crangonidae Unidentified Cephalopoda Gonatopsis makko Berryteuthis magister Watasenia scintillans Todarodes pacificus Octopus sp. Unidentified Polychaeta Stelloridea Asterinidae Myophiurida Pisces Bothrocara hollandi Arctoscopus japonicus Unidentified Eggs

%F

%N

%W

%IRI

%W (< 40 cm)

%W (> 40 cm)

28.9 1.1

14.4 +

4.1 +

8.4

3.0

3.7 +

1.5

0.1

+

23.2

14.1

3.9

3.0 9.5 17.5 0.4 73.0 0.4 6.1 2.7

0.3 8.7 69.6 + 4.2 + 0.3 0.1

0.1 2.1 7.9 + 27.1 0.3 6.6 1.7

8.4 0.4

0.5 +

3.0 +

30.0 1.9 23.2 38.4 0.8

1.6 0.6 1.1 1.9 +

12.0 0.1 3.3 40.4 2.0

4.6

0.2

23.1

19.4

6.8

0.5

3.9

2.9

1.5

0.1

5.9

3.5

0.8 24.0 0.4 1.1 0.4 0.8 24.7 4.2

+ 1.1 + 0.1 + + 1.0 0.2

1.4 4.1 + 0.1 + + 17.6 3.9

1.5

0.1

1.4

19.0 0.4

0.7 +

12.2 0.7

+

1.6 21.3 + 35.9

2.9

3.2

0.1 42.6

+ 0.7 6.7

6.0

27.5 6.1 2.5 4.5

5.7 0.4 25.5

0.4

0.4 + +

7.2

11.5 0.1 2.7 45.5 15.3

4.2. Trophic position (TP) estimation TP estimations for a species must be interpreted with caution because a variety of factors can influence it, such as change in the feeding strategy of consumers as well as geographic and temporal factors (Lorrain et al., 2015). The δ15N values of fish species have been considered a useful indicator of their TPs due to the enrichment of 15N through trophic transfer (Polunin and Pinnegar, 2002; Post, 2002). In the present study, a significant positive trend of the δ15N values of pollock with increasing length suggests a gradual increase in their TP as they grow. The 15N-enrichment of fish tissues over time may be explained by the increase in TPs of prey with increasing body length (Pinnegar and Polunin, 2000; Reñones et al., 2002; Iitembu et al., 2012). The positive relationship between TP and size of pollock would result from an ontogenetic change in the pollock’s preferred dietary items from lower TP (zooplankton and pelagic prey of lower δ15N values) towards higher TP (cephalopods and benthic prey of higher δ15N values). This result indicates that the increase of the pollock TP with size may be related to the shift in preferred food type as well as its availability in their foraging depth. The TP estimation of an individual or a group of organisms may be influenced by δ15N values of food-web baselines (Choy et al., 2012; Lorrain et al., 2015). In the present study, we made a comparison of TP estimations for pollock in different sea areas, based on the δ15N values of pollock and calanoid copepods (Table 3). Regional variation in the δ15N values of pollock tended to be explained by regional difference in the δ15N values of baselines (i.e., calanoid copepods). The range of δ15N values of pollock in our study area fell within the range reported in different regions. However, our pollock TP estimations (means of 4.2 and 4.4 for small and large individuals, respectively) were relatively higher than 3.4–3.8 in the Chukchi Sea (Marsh et al., 2017), 2.7–4.1 in the Gulf of Alaska (Hobson et al., 1997), and 2.3–4.0 in the Bering Sea (Schell et al., 1998; Hirons, 2001; Dehn et al., 2007; Kurle and Worthy, 2001). This regional variation is attributable to the difference in pollock sizes analyzed. Indeed, TPs recorded for smaller pollock (< 20 cm) in the Bering Sea and the Gulf of Alaska were 2.3–2.9, and for larger adults (> 20 cm), TPs were 3.6–4.1 in the same sea areas. In contrast, even

0.8 3.7 0.1

48.0 11.2

15.3 2.0 1.0

36.8 +

12.3 0.6

as euphausiids and copepods constitute the most important food items in many sea areas (Bailey et al., 2005; Buckley et al., 2016). In contrast, in the eastern Bering Sea, while euphausiids were the major prey item for pollock individuals of < 40 cm, benthic animals contributed considerably to the diet of individuals of > 40 cm (Dwyer et al., 1987). An ontogenetic dietary change of pollock was also reported in the western Bering Sea, where euphausiids were the most important component of the diets for pollock < 50 cm, whereas individuals > 50 cm fed on juvenile pollock and other fishes (Shuntov et al., 2000). Similarly, while the primary diet of 30–40 cm pollock in the Doto area off northern Japan was euphausiids, individuals of > 40 cm feed mainly on juvenile pollock (Yamamura et al., 2002). Despite seasonal and geographical differences in the relative importance of different prey items to the pollock diets, there seems likely to be a general trend of an ontogenetic shift from zooplanktivory to piscivory in the length-specific predator–prey relationship. Our results also showed significant differences in both the δ13C′ and δ15N values of pollock between size classes below and above 40 cm length, confirming a clear ontogenetic dietary shift. Similar ontogenetic variation in the pollock diets was clearly 302

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smaller (9.0–12.3 cm) individuals in the Chukchi Sea had TPs of 3.4–3.8. Regional differences in oceanographic conditions can lead to differences in resource utilization and thereby in the TPs of a predator inhabiting different marine regions (Vander Zanden and Fetzer, 2007). Water masses off the eastern coast of the Korean Peninsula are characterized by a strong thermocline (Park et al., 2016; Kwak et al., 2017). The vertical profile of the hydrographic conditions might restrict the vertical migration ranges of pollock, a cold-water species, to deeper water and subsequently affect their resource utilization. As a result, relatively high TPs of pollock in our study can be interpreted by the important consumption of benthic prey, which have relatively high δ15N values, as available dietary items within the deep layer. In conclusion, pollock generally occupy trophic levels of intermediate predators in marine ecosystems, and exhibit a dietary shift with growth from consuming mesozooplankton to mesopelagic fish and benthic animals (Dwyer et al., 1987; Yamamura et al., 2013). The increased δ13C and δ15N values for large individuals are consistent with the dietary increases in larger fish and benthic animals, as indicated by stomach-content data. Given slightly more 15N-enrichment in benthic feeders than in pelagic feeders, the δ15N baselines representing both benthic and pelagic pathways should be considered for the TP estimation of a consumer (Drazen et al., 2008; Le Loc’h et al., 2008). In this respect, our result, based on a single δ15N baseline of calanoid copepods, could result in a slight overestimation of the pollock TPs. Nonetheless, our results highlight ontogenetic shifts in the diets and TPs of pollocks in the western East Sea (Japan Sea).

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