Stomach content and stable isotope analysis of sailfish (Istiophorus platypterus) diet in eastern Taiwan waters

G Model

ARTICLE IN PRESS

FISH-3989; No. of Pages 8

Fisheries Research xxx (2014) xxx–xxx

Contents lists available at ScienceDirect

Fisheries Research journal homepage: www.elsevier.com/locate/fishres

Stomach content and stable isotope analysis of sailfish (Istiophorus platypterus) diet in eastern Taiwan waters Chung-Nan Tsai a , Wei-Chuan Chiang b , Chi-Lu Sun a,∗ , Kwang-Tsao Shao c , Shu-Ying Chen d , Su-Zan Yeh a a

Institute of Oceanography, National Taiwan University, 1 Section 4, Roosevelt Road, Taipei 10617, Taiwan Eastern Marine Biology Research Center, Fisheries Research Institute, 22, Wuchuan Road, Chenkung, Taitung 96143, Taiwan c Biodiversity Research Center, Academia Sinica, 128 Academia Road, Section 2, Nankang, Taipei 11529, Taiwan d Department of Biomedical Engineering, I-Shou University, 8, Yida Road, Jiaosu Village Yanchao District, Kaohsiung 82445, Taiwan b

a r t i c l e

i n f o

Article history: Received 7 April 2014 Received in revised form 22 October 2014 Accepted 27 October 2014 Handled by A.E. Punt Available online xxx Keywords: Istiophorid Opportunistic predator Stomach contents Stable isotopes Stable-isotope mixing model

a b s t r a c t Stomach content analysis (SCA) and stable isotope analysis (SIA), coupled with isotopic-mixing model analysis, were used to estimate diet composition of sailfish Istiophorus platypterus in eastern Taiwan waters. SCA provided information on diet, but the high occurrence of empty stomachs (48.5%) limited this analysis. According to the index of relative importance (%IRI), the most important prey items were Priacanthus macracanthus (38.7%), followed by Auxis spp. (35.9%), and Trichiurus lepturus (8.5%). However, the most important prey groups for adult sailfish (>181 cm, LJFL) as estimated by the stable isotope-mixing model were T. lepturus (32.6%), Katsuwonus pelamis (15.8%), and P. macracanthus (11.3%), and for maturing sailfish were K. pelamis (12.9%), P. macracanthus (10.4%), and T. lepturus (32.6%), respectively. Juvenile sailfish feed primarily on smaller prey items with lower ␦15 N values, while adult sailfish preferred larger prey items with higher ␦15 N values. Our findings suggested that an integrated SCA and SIA is considerably more powerful than using SCA alone in determining diet composition of sailfish over long time scales. In summary, a high diversity in the diet composition of sailfish was found and included an array of coastal, benthic, pelagic, and mesopelagic species. Sailfish are most likely opportunistic feeders consuming the most abundant prey items in eastern Taiwan waters. © 2014 Elsevier B.V. All rights reserved.

1. Introduction Sailfish Istiophorus platypterus (Shaw and Nodder, 1792) are apex predators in pelagic ecosystems (Kitchell et al., 2006), and are distributed in tropical and temperate waters worldwide (Nakamura, 1985). Sailfish are opportunistic foragers (RosasAlayola et al., 2002) and the abundance, diversity and distribution of prey items changes in different foraging habitats. In the western Pacific near the Kuroshio Current, sailfish spawn around eastern Taiwan (Chiang et al., 2006a,b) and are seasonally abundant to local fisheries from April to October, with a peak from May to July. They are primarily targeted with gill nets, set nets, and harpoon fleet and are also retained by inshore pelagic longline fisheries (Chiang et al., 2004). Sailfish has a high economic value and is ecologically importance in eastern Taiwan. For the past decade, the annual landings of sailfish in Taiwan fluctuated between 500 and 1000 mt, with 80%

∗ Corresponding author. Tel.: +886 2 23629842; fax: +886 2 23629842. E-mail address: [email protected] (C.-L. Sun).

captured off the eastern coast. Although sailfish are an important resource for the local fishery, there are few reports about their diet composition in the western Pacific. Any reductions in the abundance of top predators have the potential to alter food web dynamics and trophic structure in marine systems (Paine, 1966; Hinke et al., 2004), while changes in the prey community can also affect top predators (Rosen and Trites, 2000). Trophic studies are essential to ecosystem analyses to infer biological niche overlap, suitable habitat, and level of fisheries interactions (Lopez et al., 2010). Determining trophic interactions between species is a major step toward a better understanding of the ecosystem dynamics. Stomach content analysis (SCA) is the most widely used method in tropho-dynamics to gauge niche overlap and to construct food webs, although it can be biased by opportunistic feeding and different digestion rates of prey. However, SCA can provide detailed information on diet composition, prey size, distribution, consumption rates and foraging habitats over short timescales (Chipps and Garvey, 2007). Stable isotope analysis (SIA) tracks diet over longer timescales, but is dependent on tissue turnover rates (Gannes et al.,

http://dx.doi.org/10.1016/j.fishres.2014.10.021 0165-7836/© 2014 Elsevier B.V. All rights reserved.

Please cite this article in press as: Tsai, C.-N., et al., Stomach content and stable isotope analysis of sailfish (Istiophorus platypterus) diet in eastern Taiwan waters. Fish. Res. (2014), http://dx.doi.org/10.1016/j.fishres.2014.10.021

G Model FISH-3989; No. of Pages 8

ARTICLE IN PRESS C.-N. Tsai et al. / Fisheries Research xxx (2014) xxx–xxx

2

1998). The analyses of natural biological tracers, such as the stable isotope ratios of carbon (␦13 C) and nitrogen (␦15 N), are often employed for trophic ecology studies, to trace energy flow pathways through food webs (Cabana and Rasmussen, 1996; Post, 2002). The ␦15 N value of a predator, when compared with the trophic level of a primary consumer, provides a general and integrated view of the trophic position at which the species feeds, although it does not stipulate specific dietary information (Post, 2002). Though the food habits of sailfish have been documented from the analysis of stomach contents in Mexico and the eastern Pacific (Rosas-Alayola et al., 2002; Arizmendi-Rodríguez et al., 2006), comparable information in the western Pacific is lacking. A previous study by Tsai et al. (2014) was conducted in Taiwan using stable isotopes and found that body size of sailfish was significantly correlated with ␦15 N values, which indicated a presumed shift in diet and trophic position through different size-classes. However, the relationship between sailfish and their prey still needs further exploration. To estimate diet composition of sailfish, we investigated food and feeding ecology of sailfish by stomach content and stable isotope analyses. Linear mixing models using multiple sources and two isotopes incorporating a Bayesian framework (Parnell et al., 2010) were applied to estimate diet composition for juvenile, maturing and adult sailfish and extend the study of Tsai et al. (2014). This additional information in turn can be used to estimate food consumption rates and biomass of different prey groups eaten by sailfish. Moreover, predator-prey relationships and energy flow can be quantified in order to assess the impact of resources in the community, which can be subsequently used for ecosystembased management.

2. Materials and methods 2.1. Data collection and samplings Sailfish specimens were caught by commercial fisheries (i.e., harpoon, longline, gillnet and set nets), between August 2009 and August 2012 off eastern Taiwan (∼20◦ 20 –23◦ 40 N, and ∼120◦ 40 –123◦ 20 E) (Fig. 1). The whole weight of each specimen was weighed to the nearest kg and the lower jaw fork length (LJFL) was measured to the nearest cm at the Shinkang fish market. After measuring length and weight, sailfish samples were brought to the Eastern Marine Biology Research Center, Fisheries Research Institute, located nearby the Shinkang fish market, for further analysis.

2.2. Stomach content analysis A total of 505 stomachs of sailfish specimens collected at Shinkang fish market were used for SCA. Sailfish were caught by inshore commercial fisheries and refrigerated immediately with ice on board to keep freshness of body. We obtained these sailfish samples after competitive bidding and stomachs were removed for analysis at the laboratory. Each stomach was cut open, and contents were washed through a 1-mm mesh size sieve. Identification on taxa was carried out to the lowest possible taxonomic level. Wet weight and fork length (FL) of prey items were measured to the nearest g and cm, respectively. Taxonomic level based on published guides and online keys (Froese et al., 2013; Shao, 2014). Diet was analyzed by calculating three diet indices for each prey taxon: (1) percentage by wet weight (%W), (2) percentage by number (%N), and (3) frequency of occurrence (%FO). For quantitative analysis of gastric contents, the index of relative importance (IRI) was calculated to represent the most important prey items (Pinkas

et al., 1971; Cortés, 1997) as a percentage relative to the diet composition by the following equation: IRI = (%W + %N) × %FO

(1)

To readily allow comparison among prey items, the IRI was standardized to %IRI for each prey item (Cortés, 1997). All identifiable prey items were aggregated into 14 taxonomic categories for analysis and interpretation based on relative importance and abundance. Fish prey species were pooled as 13 groups: Auxis spp., Priacanthus macracanthus, Trichiurus lepturus, Decapterus spp., Mene maculate, Scomber japonicus, Katsuwonus pelamis, Exocoetidae, Belonidae, Gempylidae, Clupeidae, Tetraodontidae, and Bramidae. Cephalopods were categorized together as a separate group (Table 1). Minor fish prey families, unidentified fish or invertebrates and debris were grouped together into an “others” category. To remove the bias relating to overestimation of squid beaks or other identifiable hard parts which are not digestible, only undigested and partially digested prey items were used for the analysis, and stomachs with prey in the nearly digested state were regarded as empty (Shimose et al., 2006). 2.3. Stable isotope analysis According to a previous reproductive (Chiang et al., 2006a) and a stable isotope studies (Tsai et al., 2014); 50% of sailfish reached sexual maturity at ∼166 cm (LJFL) and stable isotope values were also reported to significantly shift (P < 0.001) over the size range 161–180 cm (LJFL). Therefore, to examine whether there was a shift in diet between different life stages, we collected sailfish samples and pooled them into three groups; juvenile sailfish (<140 cm), maturing sailfish (141–180 cm) and adult sailfish (>181 cm, LJFL). A stable isotope mixed model analysis was used to examine the diet composition in different life-history stages (Parnell et al., 2010). White muscle tissue samples (∼1 cm3 ) of 31 juvenile sailfish, 41 maturing sailfish and 33 adult sailfish, were examined for SIA (Table 2). Muscle samples from 2 to 9 specimens of each of the 14 prey items (Table 2) were taken to predict sailfish diet composition using SIA and stable isotope mixing model analysis (Varela et al., 2013). Muscle tissue below the dorsal fin was usually taken for fish and sections of mantle were collected from cephalopods (Revill et al., 2009). Sailfish and prey sampled tissues were frozen at −80 ◦ C until processing. Dissected tissues were acidified (10% HCl) to remove any residual carbonates, rinsed with distilled water and were freeze-dried for approximately 48 h. Stable isotopes were determined for sailfish and their prey following Davenport and Bax (2002) and Tsai et al. (2014). To standardize isotope measurement, isotopic values were expressed in parts per thousand (‰) as deviations from known standards (Peedee belemnite limestone for ␦13 C and nitrogen in air for ␦15 N): ıX = [(Rsample /Rstandard ) − 1] × 1000

(2)

where X is 13 C or 15 N and R is the corresponding 13 C/12 C or 15 N/14 N ratio, respectively (Peterson and Fry, 1987). The trophic level (TL) of sailfish and their prey sampled was estimated using the equation: Trophic level = (ı15 Nconsumer − ı15 Nbaseline )/TEF + 2

(3)

␦15 N values provide an indication of the trophic level of consumers (Post, 2002). Primary producers are trophic level 1, primary consumers are trophic level 2, and so on. The trophic enrichment factor (TEF) represents the best estimate of isotopic enrichment between sailfish and its diet. We adopt a TEF of 2.4‰, the mean TEF for marine fishes based on Vanderklift and Ponsard’s (2003) review of literature that reported consumer-diet ␦15 N enrichment (Caut et al.,

Please cite this article in press as: Tsai, C.-N., et al., Stomach content and stable isotope analysis of sailfish (Istiophorus platypterus) diet in eastern Taiwan waters. Fish. Res. (2014), http://dx.doi.org/10.1016/j.fishres.2014.10.021

G Model

ARTICLE IN PRESS

FISH-3989; No. of Pages 8

C.-N. Tsai et al. / Fisheries Research xxx (2014) xxx–xxx

3

East China Sea

CHINA 26° N

Taipei

TAIWAN 24° N

Pacific Ocean

Penghu

Shinkang

Taiwan Strait

22° N

20° N

118° E

120° E

122° E

124° E

Fig. 1. Map of study area showing area of capture of sailfish taken for stomach contents and isotopic analyses in eastern Taiwan waters during April 2009 and February 2012.

2009). The ␦15 Nbaseline based on the average value of 6.24‰ ± 0.29 SD (n = 5) for the herbivorous marine snail Chlorostoma argyrostoma argyrostoma from the eastern coast of Taiwan was used as a trophic baseline (Tsai et al., 2014), which corresponded to the mean value of primary consumers isotopic values. 2.4. Mixing model A Bayesian mixing model, stable isotope analysis conducted in R (SIAR) (i.e., multiple sources, dual-isotope linear mixing-model;

Parnell et al., 2010), was used to estimate the relative proportion of multiple prey species in the diet. The mixing model discussed in this paper uses the same basic methodology for estimating proportional source contributions to the diets of animals. For example, a dual element (X, Y), three source, mass-balance, linear mixing model is described by the following equations (Schwarcz, 1991): ␦Xm = f1 ␦X1 + f2 ␦X2 + f3 ␦X3

(4)

␦Ym = f1 ␦Y1 + f2 ␦Y2 + f3 ␦Y3

(5)

Table 1 Diet composition of Istiophorus platypterus in eastern Taiwan waters by stomach content analysis. Length of fish prey items given in fork length, “Others” indicates unidentified fish or invertebrates and debris contents (FO: frequency of occurrence, N: number, W: wet weight, IRI: index of relative importance). Prey item Auxis spp. (Bullet tuna) Priacanthus macracanthus (Red bigeye) Trichiurus lepturus (Hairtail, cutlassfish) Decapterus spp. (Scad) Mene maculata (Moonfish) Scomber japonicus (Chub mackerel) Katsuwonus pelamis (Skipjack) Exocoetidae (Flyingfish) Belonidae (Needlefish) Gempylidae (Snake mackerel) Clupeidae (Anchovy, herring) Tetraodontidae (Pufferfish) Bramidae (Pomfret) Cephalopoda (Squid) Others Total

FO 55 40 24 24 9 9 9 5 7 11 2 5 2 21 9 232

%FO

N

%N

W (g)

%W

IRI

%IRI

%IRI rank

FL (cm)

23.71 17.24 10.34 10.34 3.88 3.88 3.88 2.16 3.02 4.74 0.86 2.16 0.86 9.05 3.88

90 151 56 46 30 13 33 7 10 21 13 5 2 29 9

17.48 29.32 10.87 8.93 5.83 2.52 6.41 1.36 1.94 4.08 2.52 0.97 0.39 5.63 1.75

9285 12412 4439 5094 1533 1494 839 552 464 266 372 444 152 1148 623

23.74 31.73 11.35 13.02 3.92 3.82 2.14 1.41 1.19 0.68 0.95 1.14 0.39 2.93 1.59

977.01 1052.60 229.88 227.12 37.80 24.61 33.18 5.97 9.44 22.56 3.00 4.54 0.67 77.54 12.96

35.93 38.71 8.46 8.35 1.39 0.91 1.22 0.22 0.35 0.83 0.11 0.17 0.02 2.85 0.48

2 1 3 4 6 8 7 12 11 9 14 13 15 5 10

6–27 8–22 15–74 8–37 5–14 14–36 17–31 18–32 20–42 6–34 8–14 13–23 7–9 4–31 1–16

515

39117

2718.86

Please cite this article in press as: Tsai, C.-N., et al., Stomach content and stable isotope analysis of sailfish (Istiophorus platypterus) diet in eastern Taiwan waters. Fish. Res. (2014), http://dx.doi.org/10.1016/j.fishres.2014.10.021

G Model

ARTICLE IN PRESS

FISH-3989; No. of Pages 8

C.-N. Tsai et al. / Fisheries Research xxx (2014) xxx–xxx

4

Table 2 Isotopic values of ␦15 N (‰) and ␦13 C (‰) for sailfish and prey items sampled in eastern Taiwan waters where LJFL is the lower jaw fork length measurement. Differentiation between maturity stages based on Chiang et al. (2006a). Sailfish

n

Juvenile (<140 cm, LJFL) Maturing (141–180 cm, LJFL) Adult (>181 cm, LJFL)

31 41 33

␦13 C

␦15 N

Mean

SD

Max

Min

Mean

SD

Max

Min

−18.39 −17.27 −17.47

1.41 0.95 1.02

−16.01 −16.06 −16.03

−21.66 −19.93 −22.04

10.01 11.89 13.15

1.18 0.75 0.49

11.45 13.67 14.15

7.51 10.34 12.23

Prey item

n

␦13 C Mean

SD

Max

Min

Mean

SD

Max

Min

Auxis spp. Priacanthus macracanthus Trichiurus lepturus Decapterus spp. Mene maculate Scomber japonicus Katsuwonus pelamis Exocoetidae Belonidae Gempylidae Clupeidae Tetraodontidae Bramidae Cephalopoda

8 6 6 8 6 5 4 2 3 4 2 5 3 8

−17.89 −17.80 −16.91 −17.43 −17.77 −17.11 −17.95 −17.15 −17.37 −17.76 −17.18 −18.13 −17.87 −18.25

0.33 0.39 0.43 0.39 0.62 0.33 0.28 0.01 0.24 0.25 0.76 0.38 0.55 1.07

−17.35 −17.08 −16.41 −16.81 −17.17 −16.68 −17.62 −17.16 −17.10 −17.51 −16.64 −17.65 −17.36 −16.55

−18.21 −18.24 −17.53 −18.06 −18.70 −17.48 −18.27 −17.15 −17.57 −18.00 −17.72 −18.56 −18.45 −19.67

9.55 10.38 12.80 9.42 8.02 10.71 10.62 8.12 7.31 8.74 6.84 8.19 6.43 8.71

0.78 0.50 0.87 1.65 1.60 0.95 0.83 0.15 1.42 0.89 0.21 0.80 0.56 1.53

10.83 11.26 14.09 10.76 9.40 11.68 11.09 8.23 8.89 9.51 6.98 8.83 7.08 10.24

8.77 9.87 11.77 6.15 5.96 9.18 9.06 7.98 6.13 7.54 6.69 7.03 6.04 6.14

(6)

This system of three equations yields three unknown proportional source contributions (f1 , f2 , f3 ) for a mixture (m) when ␦Xm and ␦Ym values are known for mixtures and sources (Hopkins and Ferguson, 2012). The SIAR model estimates the probability distributions of multiple source contributions to a mixture while accounting for the observed variability in source and mixture isotopic signatures, dietary isotopic fractionation, and elemental concentration (Polito et al., 2011). Mixing model analyses requires accurate estimation of isotopic discrimination factors between source (i.e., prey), and mixture (i.e., consumers), tissues to reliably ascertain quantitative diet estimates (Bond and Diamond, 2011). In this study, we applied prey-muscle discrimination factors previously estimated for Atlantic bluefin tuna (13 C (‰) = −0.16 ± 0.64, 15 N (‰) = 1.64 ± 0.20; Varela et al., 2011). 3. Results 3.1. Stomach content analysis Sailfish ranged from ∼111 to 243 cm (LJFL), with weights ranging between ∼4 and 79 kg. Length-frequency distribution (10 cm bins) of the 505 sailfish specimens is shown in Fig. 2. Of the stomachs examined, 260 (51.5%) contained food and 245 (48.5%) were empty. In total, 34 prey species were identified comprising 31 teleost species and 3 cephalopod species. Prey species with similar body sizes and habitat preferences were aggregated into the same group and are shown in Table 1. The most important prey groups found in the stomachs in terms of weight (%W) for sailfish were P. macracanthus (31.7%), Auxis spp. (23.7%) and T. lepturus (10.9%) (Table 1). According to the %IRI, the most important prey items were P. macracanthus (38.7%), followed by Auxis spp. (35.9%), T. lepturus (8.5%), Decapterus spp. (8.4%) and cephalopods (2.9%) with other prey collectively representing less than 1% of %IRI (these include Gempylidae, S. japonicus, Belonidae, Tetraodontidae, Exocoetidae, Clupeidae, Bramidae and other unidentified taxa and debris). Sailfish consumed not only epipelagic prey (e.g., Auxis spp., Exocoetidae, Belonidae) and coastal prey (e.g., P. macracanthus,

T. lepturus), but also small proportions of mesopelagic prey (e.g., Gempylidae, Bramidae). 3.2. Stable isotope analysis Stable isotope values of ␦15 N and ␦13 C for sailfish and their prey items are listed in Table 2. Stable isotope values of juvenile sailfish ranged from 7.51 to 11.45‰ for ␦15 N (10.01 ± 1.18‰; mean ± SD) and −21.66 to −16.01‰ for ␦13 C (−18.39 ± 1.41‰). Maturing sailfish stable isotope values ranged from 10.34 to 13.67‰ for ␦15 N (11.89 ± 0.75‰) and −19.93 to −16.06‰ for ␦13 C (−17.27 ± 0.95‰), and adult sailfish ranged from 12.23 to 14.15‰ for ␦15 N (13.15 ± 0.49‰) and −22.04 to −16.03‰ for ␦13 C (−17.47 ± 1.02‰), respectively. Nitrogen stable isotopic values showed variation among the three size classes comprising juvenile, maturing and adult sailfish and showed large differences across a wide range of prey groups (Table 2). For example, mean ␦15 N values ranged from 6.43 (Bramidae) to 12.80‰ (T. lepturus) ( 6.37‰), but did not exhibit this level of change in ␦13 C values ranged from −18.13 (Tetraodontidae) to −16.91% (T. lepturus) ( 1.22‰). DeNiro and Epstein (1978, 1981) 180 160

149

140 120 Frequency

1 = f1 + f2 + f3

␦15 N

103 100

91

80 65 60 41 40 20 3

5

6

7

12

11

9

2

1

0 110

130

150

170

190

210

230

250

Length (LJFL: cm)

Fig. 2. Size (lower jaw fork length, LJFL) distribution (10 cm intervals) of 505 sailfish collected in eastern Taiwan waters analyzed for stomach contents.

Please cite this article in press as: Tsai, C.-N., et al., Stomach content and stable isotope analysis of sailfish (Istiophorus platypterus) diet in eastern Taiwan waters. Fish. Res. (2014), http://dx.doi.org/10.1016/j.fishres.2014.10.021

G Model

ARTICLE IN PRESS

FISH-3989; No. of Pages 8

C.-N. Tsai et al. / Fisheries Research xxx (2014) xxx–xxx

5

15 Auxis spp.

14

Priacanthus macracanthus Trichiurus lepturus

Sailfish adult (>181 cm)

13

Trichiurus lepturus

Decapterus spp. Mene maculate

12

Sailfish maturing (141-180 cm)

11

Scomber japonicus Katsuwonus pelamis

Katsuwonus pelamis

Scomber japonicus

Exocoetidae Sailfish juvenile (<140 cm)

Belonidae

Decapterus spp.

15

δ N‰

Priacanthus macracanthus

10

9

Gempylidae

Cephalopoda Tetraodontidae Mene maculate

8

Gempylidae Clupeidae Tetraodontidae

Exocoetidae

Bramidae Belonidae

7

Cephalopoda

Clupeidae

Sailfish juvenile (<140 cm)

Bramidae

6

Sailfish maturing (141-180 cm) Chlorostoma argyrostoma argyrostoma

5

Sailfish adult (>181 cm) Chlorostoma argyrostoma argyrostoma

4 -22

-21

-20

-19

-18

-17

-16

-15

-14

-13

-12

13

δ C‰ Fig. 3. Bi-plot of ␦13 C and ␦15 N values (mean ‰ ± SD) from sailfish and their prey in eastern Taiwan. Distribution of carbon and nitrogen stable isotope ratios among the different groups composing the food web are shown. Differentiation between maturity stages based on Chiang et al. (2006a).

suggested that ␦15 N > 3.4‰ and ␦13 C > 1.1‰ indicate one tropic level difference. An isotope bi-plot for juvenile, maturing and adult sailfish and their prey (includes fishes and cephalopoda) is shown in Fig. 3. The highest isotope values of ␦15 N is adult sailfish, and the corresponding values for juvenile sailfish segregate intermediate among prey sources. Of prey groups, T. lepturus exhibits the highest trophic position, while Bramidae and Clupeidae exhibit the lowest position in bi-plot (Fig. 3).

3.4. Stable isotope mixing model The results derived from the stable isotope mixing model of dietary contributions of the 14 prey items are summarized in Fig. 5 and Appendix A. As estimated by the stable isotope mixing model, the most important prey groups for juvenile sailfish were Bramidae (15.9%), M. maculate (11.0%) and Tetraodontidae (9.6%). However, the most important prey groups for adult sailfish were T. lepturus (32.6%), K. pelamis (15.8%), and P. macracanthus (11.3%), respectively.

3.3. Trophic level

4.88

4.73

Trophic level (TL)

5

4.35 3.73

4

3.86 3.83

3.33

3.57

3.38

3.03 2.74

3.04 2.78

2.81

2.45

3 2.25

2.08

2

Au xi s m sp Tr acr ac p. ic hi ur ant hu us D s le ec ap ptu ru te s r u M s e sp Sc n e p. om m ac b ul Ka er a ts j uw apo te n on us icus pe la Ex oc mis oe tid Be a e lo G nid em ae py li d ae C Te lupe tra id ae od on tid ae Br am C id ep ae h Sa alo po ilf s da Sa ih j u ilf is ven h m ile a Sa tur in i lf g is h ad ul t

1

Pr ia ca nt hu s

The estimated trophic level for juvenile, maturing and adult sailfish and their prey inferred from ␦15 N is shown in Fig. 4. The trophic level is estimated to be 3.57 ± 0.49 (mean ± SD) for juvenile, 4.35 ± 031 for maturing, and 4.88 ± 020 for adult sailfish, respectively. Estimated trophic positions for the most important prey items are: Auxis spp, 3.38 ± 0.33; P. macracanthus, 3.72 ± 0.21; T. lepturus, 4.73 ± 0.36; Decapterus spp., 3.32 ± 0.69. Coastal and benthic prey items such as T. lepturus and P. macracanthus had higher trophic levels, while pelagic and mesopelagic prey such as Bramidae, Clupeidae, Belonidae and Gempylidae had lower trophic levels. We found prey groups had a high degree of overlap in isotope values (Fig. 3). Bramidae, Clupeidae, Exocoetidae, Belonidae and M. maculate occupied the lowest TLs among prey groups, while Auxis spp., Decapterus spp., Gempylidae and Cephalopoda made up the intermediate TLs. T. lepturus, S. japonicus, K. pelamis and P. macracanthus had the highest TLs (Fig. 4).

6

Fig. 4. Estimated trophic level (TL) (mean ± SD) for sailfish and their prey, using ␦15 N concentrations of the herbivorous marine snail, Chlorostoma argyrostoma argyrostoma, 6.24‰ ± 0.29 SD as a trophic baseline (Tsai et al., 2014).

Please cite this article in press as: Tsai, C.-N., et al., Stomach content and stable isotope analysis of sailfish (Istiophorus platypterus) diet in eastern Taiwan waters. Fish. Res. (2014), http://dx.doi.org/10.1016/j.fishres.2014.10.021

G Model

ARTICLE IN PRESS

FISH-3989; No. of Pages 8

C.-N. Tsai et al. / Fisheries Research xxx (2014) xxx–xxx

6 50%

(a) Juvenile

40% 15.90 Percentage

30% 11.04 8.79 20%

9.02

9.62

9.19 8.13

6.13

5.23

4.47 3.93

10%

2.93

3.67

1.94

0%

50%

(b) Maturing

Percentage

40%

30%

12.90 9.43

10.36

9.57

10.03

20%

6.71

7.56

7.41 5.00

4.22

5.31 4.26

4.03

3.26

10%

0% 50%

(c) Adult

32.63

Percentage

40% 15.82 30% 11.30 8.41 20%

6.36 4.54

10%

4.89 2.19

3.84

2.03

3.68

2.04 3.22

1.91

Pr ia ca

nt

hu s

Au

xis

sp m p. ac ra Tr ca ic nt hi hu ur s us le D pt ec ur ap us te ru s M sp en p. e Sc m a om cu la be te rj Ka ap ts on uw ic on us us pe la m Ex is oc oe tid ae Be lo ni da G e em py lid ae C lu pe Te id ae tra od on tid ae Br am id C ae ep ha lo po da

0%

Fig. 5. Estimated percentage contributions (mean and 95% confidence intervals) by stable isotope mixing model of prey consumed by (a) juvenile (<140 cm, LJFL), (b) maturing (141–180 cm, LJFL) and (c) adult (>181 cm, LJFL) sailfish.

4. Discussion 4.1. Diet composition Sailfish diet off eastern Taiwan is mainly comprised of fish and cephalopods with fish species generally dominating the composition of prey items. The dominance of fish in sailfish stomachs has been documented previously (Rosas-Alayola et al., 2002) although cephalopods are equally important, or are the main prey item in Mexico (Arizmendi-Rodríguez et al., 2006). Comparisons of our results with previous studies (Rosas-Alayola et al., 2002; Arizmendi-Rodríguez et al., 2006) indicate that the diet of sailfish varies by location. Observed variation in diet composition among locations seems to be more related to abundance rather than preferences in particular food items (Rosas-Alayola et al., 2002). In the less productive waters of the Kuroshio Current, we found teleost fish species were the main prey group for sailfish and were dominated by P. macracanthus, T. lepturus and Decapterus spp. These species have wide distributions in Taiwan coastal waters and are generally associated with the Kuroshio Current and surface waters. Many of the stomachs examined contained prey that were in various stages of decomposition and some contents were virtually

unidentifiable, presumably due to prolonged soak times of surface longline sets and elevated water temperatures which accelerated decomposition. High rates of empty stomachs (48.5%) were found in this study. We believe several factors could explain empty stomachs including fast digestion, uneven digestion rates of different food items, and regurgitation of stomach contents during fishing operations (Carey et al., 1984; Chase, 2002). Sailfish in the Pacific near Mexico are generalist predators, feeding mainly on epipelagic species in coastal and oceanic waters, and occasionally diving to prey on demersal fish (Rosas-Alayola et al., 2002). SCA indicated that sailfish in eastern Taiwan were also generalist predators feeding mainly on coastal and epipelagic fishes, but also mesopelagic fish. Sailfish fed across a broad spectrum of prey species and sizes, and over a wide spatial range demonstrating significant feeding plasticity (Chancollon et al., 2006). As a result, sailfish could be considered opportunistic pelagic predators. However, since time of prey capture was not known in this study, it is probable mesopelagic fish were consumed during their nocturnal vertical migrations near the surface. Sailfish exhibit diel vertical movements similar to other istiophorid billfishes (Holland et al., 1990; Brill et al., 1993; Chiang et al., 2011; Hoolihan et al., 2011) and spend the majority of time during daytime and nighttime in the surface mixed-layer (Chiang et al., 2011). As a foraging strategy, like other billfish and tuna species, sailfish may mirror the vertical migration of prey to the extent allowed by their respective physiological limitations (Musyl et al., 2003). Sailfish are primarily associated with the upper surface waters within the top 20 m but undertake short-duration vertical movements below the mixed-layer to depths of 50–150 m, and dive on rare occasions to the depths of up to 250 m (Chiang et al., 2011; Hoolihan et al., 2011; Kerstetter et al., 2011). The preference of sailfish to spend a large proportion of time near the surface which results in an increased vulnerability to capture by gillnets and other surface gears (Chiang et al., 2011). The diet composition reported in the current study, including epipelagic and mesopelagic fishes, is in agreement with the diel vertical behavior of sailfish (Chiang et al., 2011; Kerstetter et al., 2011). Thus, information from diet studies and data on diving patterns appears to correlate and indicate sailfish occupy a surface niche. 4.2. Trophic structure Sailfish are generally considered apex predators (Kitchell et al., 2006), sharing a place at the top of the food chain with other large pelagic fishes including elasmobranchs, tunas, and other istiophorid billfishes (Estrada et al., 2003). Evidence from stomach contents and particularly from stable isotopic analysis in this study both support this conclusion. Trophic level of adult sailfish was higher (4.88 ± 020), however, than juvenile sailfish which occupied an intermediate position (3.57 ± 0.49) in the pelagic ecosystem in Taiwan. Removal of apex predators can have severe consequences that can trigger catastrophic cascades down multiple trophic levels (e.g., Baum and Worm, 2009). Additionally, declines in top predator abundance have resulted in fisheries targeting at lower trophic levels (Pauly et al., 2002; Myers and Worm, 2003). As a preemptive measure, we contend that it is important to monitor predator diets over the long-term which might allow for the early detection of critical trophic changes in the western Pacific ecosystem. 4.3. Stable isotope mixing models SCA provides the taxonomic information required to define trophic links in ecosystem models (e.g. Cox et al., 2002; Olson and Watters, 2003) while isotopic data may provide better estimates of biomass flow (Olson et al., 2010). SIA yields numeric values for

Please cite this article in press as: Tsai, C.-N., et al., Stomach content and stable isotope analysis of sailfish (Istiophorus platypterus) diet in eastern Taiwan waters. Fish. Res. (2014), http://dx.doi.org/10.1016/j.fishres.2014.10.021

G Model FISH-3989; No. of Pages 8

ARTICLE IN PRESS C.-N. Tsai et al. / Fisheries Research xxx (2014) xxx–xxx

7

Table A1 Estimated percentage contributions (mean and 95% confidence intervals) by stable isotope mixing model of prey consumed by juvenile (<140 cm, LJFL), maturing (141–180 cm, LJFL) and adult (>181 cm, LJFL) sailfish. Differentiation between maturity stages based on Chiang et al. (2006a). Prey item

Juvenile sailfish (<140 cm, LJFL) Mean (95% confidence intervals)

Maturing sailfish (141–180 cm, LJFL) Mean (95% confidence intervals)

Adult sailfish (>180 cm, LJFL) Mean (95% confidence intervals)

Auxis spp. Priacanthus macracanthus Trichiurus lepturus Decapterus spp. Mene maculate Scomber japonicus Katsuwonus pelamis Exocoetidae Belonidae Gempylidae Clupeidae Tetraodontidae Bramidae Cephalopoda

5.23% (0–13.39%) 3.93% (0–10.56%) 1.94% (0–5.37%) 4.47% (0–11.84%) 11.04% (0.23.52%) 2.93% (0–8.24%) 3.67% (0–9.84%) 6.13% (0–15.03%) 8.79% (0.19.21%) 9.02% (0–20.04%) 9.62% (0.20.82%) 9.19% (0–20.54%) 15.90% (1.09–30.24%) 8.13% (0–18.33%)

9.34% (0–19.80%) 10.36% (0–21.13%) 10.03% (0.59–18.72%) 6.71% (0–15.77%) 5.00% (0–12.93%) 7.41% (0–16.60%) 12.90% (0.41–25.43%) 4.22% (0–11.37%) 4.03% (0–10.85) 5.31% (0–13.30%) 3.26% (0–8.93%) 7.56% (0–17.12%) 4.26% (0–10.90%) 9.57% (0–20.04%)

6.36% (0–15.57%) 11.30% (0.24–25.11%) 32.63% (22.61–42.35%) 4.54% (0–11.94%) 2.19% (0–5.91%) 8.41% (0–19.81%) 15.82% (0.01–29.94%) 3.84% (0–6.83%) 2.03% (0–5.44%) 2.04% (0–7.05%) 3.22% (0–4.83%) 3.68% (0–9.37%) 1.91% (0–5.16%) 4.89% (0–11.77%)

consumers and their diets and stable isotope mixing models define and verify relationships between sailfish and their prey. However, fine-scale taxonomic resolution of SCA can provide additional detail and information not afforded by the SIA. The results from the mixing model (Fig. 5) provided a general summary and good depiction of sailfish diet which was dominated by T. lepturus, K. pelamis and P. macracanthus. By contrast, these results were different from the most important food items identified in SCA. Stomach contents also reflect a “snapshot” of an individual’s recent diet and can be highly variable. SIA can avoid many of the problems (e.g., variable digestion rates of prey items), and temporal biases of SCA. However, different prey groups with similar isotopic values can be difficult to be distinguished by the stable isotopic mixing model. There were significant differences in diet composition between juvenile and adult sailfish (Fig. 5). Juvenile sailfish feed primarily on smaller prey with lower ␦15 N values, while adult sailfish preferred to feed on larger prey with higher ␦15 N values. Mene maculate and Bramidae comprise the majority of diet item of juvenile sailfish and that are small, laterally compressed species with weak swimming ability. Consequently, these forage species feed at the bottom of the food web and have lower ␦15 N values. By contrast, adult sailfish have the ability to feed on predatory prey species such as P. macracanthus, T. lepturus, K. pelamis, S. japonicus, and Auxis spp. which, due to their feeding ecology, have higher ␦15 N values. The shift to feeding at higher trophic levels in some species is related to offshore migration and segregation by size that increases the availability of prey, reduces intra-specific competition and enhances feeding opportunities that allows for larger fish a greater selection of prey resources that maximizes reproductive potential (Davenport and Bax, 2002). A possible bias could result from potential variation in prey isotopic values (Kurle et al., 2011; Chouvelon et al., 2012). Assumptions with SIA include tissue isotopic steady-state with local food webs, consistent trophic discrimination factors among species, relatively stable baseline isotopic values, and constrained movement within the time-scale of tissue turnover rates (Logan and Lutcavage, 2013). The present observations suggest that SIA coupled with the mixing model is more suitable than SCA to track variability in diet composition of sailfish in different life-history stages. By employing tissues that integrate diets over medium and long time scales, isotopic mixing models can avoid biases inherent to SCA (Varela et al., 2013). High rates of empty stomachs and opportunistic feeding were characterized for sailfish. It is suggested that using the stable isotope mixing model is a better approach for elucidating long-term dietary patterns of sailfish. That is, integration of both SCA and SIA would be more suitable and considerably more powerful analysis than using SCA alone.

In summary, we found differences in the diet among juvenile, maturing and adult sailfish. Sailfish consume a high diversity of species in their diet that includes coastal, benthic, pelagic, and mesopelagic fish species. Sailfish in eastern Taiwan are generalists but also opportunistic predators feeding on available prey species. Acknowledgements We thank two anonymous reviewers for providing valuable comments on previous drafts of this manuscript. This study was in part supported financially by the National Science Council of Taiwan through the grant NSC 101-2611-M-056-001 to W.-C. Chiang, C.-L. Sun (co-PI), and K.-T. Shao (co-PI). Thanks to M. Musyl for editing the text. Appendix A. See Table A1 References ˜ Arizmendi-Rodríguez, D.I., Abitia-Cárdenas, L.A., Galván-Magana, F., TrejoEscamilla, I., 2006. Food habits of sailfish Istiophorus platypterus off Mazatlan, Sinaloa, Mexico. Bull. Mar. Sci. 79, 777–791. Bond, A.L., Diamond, A.W., 2011. Recent Bayesian stable-isotope mixing models are highly sensitive to variation in discrimination factors. Ecol. Appl. 21, 1017–1023, http://dx.doi.org/10.1890/09-2409.1. Baum, J., Worm, B., 2009. Cascading top-down effects of changing oceanic predator abundances. J. Anim. Ecol. 78, 699–714, http://dx.doi.org/10. 1111/j. 1365-2656.2009.01531.x. Brill, R.W., Holts, D.B., Chang, R.K.C., Sullivan, S., Dewar, H., Carey, F.G., 1993. Vertical and horizontal movements of striped marlin (Tetrapturus audax) near the Hawaiian Islands determined by ultrasonic telemetry, with simultaneous measurements of oceanic currents. Mar. Biol. 117, 567–574. Cabana, G., Rasmussen, J.B., 1996. Comparison of aquatic food chains using nitrogen isotopes. Ecology 93, 10844–10847. Carey, F.G., Kanwisher, J.W., Stevens, E.D., 1984. Bluefin tuna warm their viscera during digestion. J. Exp. Biol. 109, 1–20. Caut, S., Angulo, E., Courchamp, F., 2009. Variation in discrimination factors (15 N and 13 C): the effect of diet isotopic values and applications for diet reconstruction. J. Appl. Ecol. 46, 443–453, http://dx.doi.org/10.1111/j. 1365-2664.2009.01620.x. Chancollon, O., Pusineri, C., Ridoux, V., 2006. Food and feeding ecology of Northeast Atlantic swordfish (Xiphias gladius) off the Bay of Biscay. ICES J. Mar. Sci. 63, 1075–1085. Chase, B.C., 2002. Differences in diet of Atlantic bluefin tuna (Thunnus thynnus) at five seasonal feeding grounds on the New England continental shelf. Fish. Bull. 100, 168–180. Chiang, W.C., Sun, C.L., Yeh, S.Z., Su, W.C., 2004. Age and growth of the sailfish (Istiophorus platypterus) in waters off eastern Taiwan. Fish. Bull. 102, 251–263. Chiang, W.C., Sun, C.L., Yeh, S.Z., Su, W.C., Liu, D.C., Chen, W.Y., 2006a. Sex ratios, size at sexual maturity, and spawning seasonality of sailfish Istiophorus platypterus from eastern Taiwan. Bull. Mar. Sci. 79, 727–737. Chiang, W.C., Sun, C.L., Yeh, S.Z., Su, W.C., Liu, D.C., 2006b. Spawning frequency and batch fecundity of the sailfish (Istiophorus platypterus) in waters off eastern Taiwan. Zool. Stud. 45, 483–491.

Please cite this article in press as: Tsai, C.-N., et al., Stomach content and stable isotope analysis of sailfish (Istiophorus platypterus) diet in eastern Taiwan waters. Fish. Res. (2014), http://dx.doi.org/10.1016/j.fishres.2014.10.021

G Model FISH-3989; No. of Pages 8 8

ARTICLE IN PRESS C.-N. Tsai et al. / Fisheries Research xxx (2014) xxx–xxx

Chiang, W.C., Musyl, M.K., Sun, C.L., Chen, S.Y., Chen, W.Y., Liu, D.C., Su, W.C., Yeh, S.Z., Fu, S.C., Huang, T.L., 2011. Vertical and horizontal movements of sailfish Istiophorus platypterus near Taiwan determined using pop-up satellite tags. J. Exp. Mar. Biol. Ecol. 397, 129–135, http://dx.doi.org/10.1016/j.jembe.2010.11.018. Chipps, S.R., Garvey, J.E., 2007. Assessment of food habits and feeding patterns. In: Guy, C., Brown, M. (Eds.), Analysis and Interpretation of Freshwater Fisheries Data. American Fisheries Society, Bethesda, pp. 473–514. Chouvelon, T., Spitz, J., Caurant, F., Mèndez-Fernandez, P., Chappuis, A., Laugier, F., Le Goff, E., Bustamante, P., 2012. Revisiting the use of 15 N in meso-scale studies of marine food webs by considering spatio-temporal variations in stable isotopic signatures – the case of an open ecosystem: the Bay of Biscay (North-East Atlantic). Prog. Oceanogr. 101, 92–105, http://dx.doi.org/10.1016/j.pocean.2012.01.004. Cortés, E., 1997. A critical review of methods of studying fish feeding based on analysis of stomach contents: application to elasmobranch fishes. Can. J. Fish. Aquat. Sci. 54, 726–738. Cox, S.P., Essington, T.E., Kitchell, J.F., Martell, S.J.D., Walters, C.J., Boggs, C., Kaplan, I., 2002. Reconstructing ecosystem dynamics in the central Pacific Ocean, 1952–1998. II. A preliminary assessment of the trophic impacts of fishing and effects on tuna dynamics. Can. J. Fish. Aquat. Sci. 59, 1736–1747. Davenport, S., Bax, N.J., 2002. A trophic study of a marine ecosystem off south eastern Australia using stable isotopes of carbon and nitrogen. Can. J. Fish. Aquat. Sci. 59 (3), 514–530. DeNiro, M.J., Epstein, S., 1978. Influence of diet on the distribution of carbon isotopes in animals. Geochim. Cosmochim. Acta 42, 495–506, http://dx.doi.org/10.1016/0016-7037(78)90199-0. DeNiro, M.J., Epstein, S., 1981. Influence of diet on the distribution of nitrogen isotopes in animals. Geochim. Cosmochim. Acta 45, 341–351, http://dx.doi.org/10.1016/0016-7037(81)90244-1. Estrada, J.A., Rice, A.N., Lutcavage, M.E., Skomal, G.B., 2003. Predicting trophic position in sharks of the north-west Atlantic Ocean using stable isotope analysis. J. Mar. Biol. Ass. 83, 1347–1350. Froese, R., Pauly, D. (Eds.), 2013. FishBase. World Wide Web electronic publication www.fishbase.org, version (12/2013). Gannes, L.Z., Martinez del Rio, C., Koch, P., 1998. Natural abundance variations in stable isotopes and their potential uses in animal physiological ecology. Comp. Biochem. Physiol. 119, 725–737. Hinke, J., Kaplan, I., Aydin, K., Watters, G., Olson, R., Kitchell, J., 2004. Visualizing the food-web effects of fishing for tunas in the Pacific Ocean. Ecol. Soc. 9, 10. Holland, K.N., Brill, R.W., Chang, R.K.C., 1990. Horizontal and vertical movements of Pacific blue marlin captured and released using sportfishing gear. Fish. Bull. 88, 397–402. Hoolihan, J.P., Luo, J., Goodyear, C.P., Orbesen, E.S., Prince, E.D., 2011. Vertical habitat use of sailfish (Istiophorus platypterus) in the Atlantic and eastern Pacific, derived from pop-up satellite archival tag data. Fish. Oceanogr. 20, 192–205, http://dx.doi.org/10.1111/j.1365-2419.2011.00577.x. Hopkins III, J.B., Ferguson, J.M., 2012. Estimating the diets of animals using stable isotopes and a comprehensive Bayesian mixing model. PLoS ONE 7 (1), e28478, http://dx.doi.org/10.1371/journal.pone.0028478. Kerstetter, D.W., Bayse, S.M., Fenton, J.L., 2011. Sailfish habitat utilization and vertical movements in the southern Gulf of Mexico and Florida straits. Mar. Coast. Fish. 3, 353–365, http://dx.doi.org/10.1080/19425120.2011.623990. Kitchell, J.F., Martell, S.J.D., Walters, C.J., Jensen, O.P., Kaplan, I.C., Watters, J.R., Essington, T.E., Boggs, C.H., 2006. Billfishes in an ecosystem context. Bull. Mar. Sci. 79, 669–682. Kurle, C.M., Sinclair, E.H., Edwards, A.E., Gudmundson, C.J., 2011. Temporal and spatial variation in the ␦15 N and ␦13 C values of fish and squid from Alaskan waters. Mar. Biol. 158, 2389–2404, http://dx.doi.org/10.1007/s00227-011-1741-4. Logan, J.M., Lutcavage, M.E., 2013. Assessment of trophic dynamics of cephalopods and large pelagic fishes in the central North Atlantic Ocean using stable isotope analysis. Deep Sea Res. II. 95, 63–73, http://dx.doi.org/10.1016/j.dsr2.2012.07.013.

Lopez, S., Melendez, R., Barrıa, P., 2010. Preliminary diet analysis of the blue shark Prionace glauca in the eastern South Pacific. Rev. Biol. Mar. Oceanogr. 45, 745–749. Musyl, M.K., Brill, R.W., Boggs, C.H., Curran, D.S., Kazama, T.K., Seki, M.P., 2003. Vertical movements of bigeye tuna (Thunnus obesus) associated with islands, buoys, and seamounts near the main Hawaiian Islands from archival tagging data. Fish. Oceanogr. 12, 152–169. Myers, R.A., Worm, B., 2003. Rapid worldwide depletion of predatory fish communities. Nature 423, 280–283. Nakamura, I., 1985. FAO Species Catalogue. Vol. 5. Billfishes of the world. An annotated and illustrated catalogue of marlins, sailfishes, spearfishes and swordfishes known to date. FAO Fish. Synop. 125 (5), 65. Olson, R.J., Watters, G.M., 2003. A model of the pelagic ecosystem in the eastern tropical Pacific Ocean. Inter-Am. Trop. Tuna. Comm. Bull. 22, 133–218. ˜ F., LennertOlson, R.J., Popp, B.N., Graham, B.S., López-Ibarra, G.A., Galván-Magana, Cody, C.E., Bocanegra-Castillo, N., Wallsgrove, N.J., Gier, E., Alatorre-Ramírez, V., Balance, L.T., Fry, B., 2010. Food web inferences of stable isotope spatial patterns in copepods and yellowfin tuna in the pelagic eastern Pacific Ocean. Progr. Oceanogr. 86, 124–138, http://dx.doi.org/10.1016/j.pocean.2010.04.026. Paine, T., 1966. Food web complexity and species diversity. Am. Nat. 100, 65–75. Parnell, A., Inger, R., Bearhop, S., Jackson, A., 2010. Source partitioning using stable isotopes: coping with too much variation. PLoS ONE 5 (3), e9672, http://dx.doi.org/10.1371/journal.pone.0009672. Pauly, D., Christensen, V., Guenette, S., Pitcher, T.J., Sumaila, U.R., Walters, C.J., Watson, R., Zeller, D., 2002. Towards sustainability in world fisheries. Nature 418, 689–695. Peterson, B., Fry, B., 1987. Stable isotopes in ecosystem studies. Annu. Rev. Ecol. Evol. Syst. 18, 293–320. Pinkas, L.M., Oliphant, S., Iverson, I.L.K., 1971. Food habits of albacore, bluefin tuna and bonito in California waters. Calif. Fish Game. 152, 1–105. Polito, M.J., Trivelpiece, W.Z., Karnovsky, N.J., Ng, E., Patterson, W.P., Emslie, S.D., 2011. Integrating stomach content and stable isotope analyses to quantify the diets of pygoscelid penguins. PLoS ONE 6 (10), e26642, http://dx.doi.org/10.1371/journal.pone.0026642. Post, D.M., 2002. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83, 703–718. Revill, A.T., Young, J.W., Lansdell, M., 2009. Stable isotopic evidence for trophic groupings and bio-regionalization of predators and their prey in oceanic waters off eastern Australia. Mar. Biol. 156, 1241–1253, http://dx.doi.org/10.1007/s00227-009-1166-5. ˜ F., Abitia-Cárdenas, L.A., Rosas-Alayola, J., Hernández-Herrera, A., Galván-Magana, Muhlia-Melo, A.F., 2002. Diet composition of sailfish (Istiophorus platypterus) from the southern Gulf of California, Mexico. Fish. Res. 57, 185–195. Rosen, D., Trites, A., 2000. Pollock and the decline of Steller sea lions: testing the junk-food hypothesis. Can. J. Zool. 78, 1243–1250. Schwarcz, H.P., 1991. Some theoretical aspects of isotope paleodiet studies. J. Archaeol. Sci. 18, 261–275. Shao, K.T., 2014. The Fish Datebase of Taiwan. WWW Web electronic publication http://fishdb.sinica.edu.tw (01.11.14). Shimose, T., Shono, H., Yokawa, K., Saito, H., Tachihara, K., 2006. Food and feeding habits of blue marlin, Makaira nigricans, around Yonaguni Island, southwestern Japan. Bull. Mar. Sci. 79, 761–775. Tsai, C.N., Chiang, W.C., Sun, C.L., Shao, K.T., Chen, S.Y., Yeh, S.Z., 2014. Trophic sizestructure of sailfish Istiophorus platypterus in eastern Taiwan estimated by stable isotope analysis. J. Fish Biol. 84, 354–371, http://dx.doi.org/10.1111/jfb.12290. Vanderklift, M.A., Ponsard, S., 2003. Sources of variation in consumer-diet ␦15 N enrichment: a meta-analysis. Oecologia 136, 169–182. ˜ Varela, J.L., Larranaga, A., Medina, A., 2011. Prey-muscle carbon and nitrogen stableisotope discrimination factors in Atlantic bluefin tuna (Thunnus thynnus). J. Exp. Mar. Biol. Ecol. 406, 21–28, http://dx.doi.org/10.1016/j.jembe.2011.06.010. Varela, J.L., Rodríguez-Marín, E., Medina, A., 2013. Estimating diets of pre-spawning Atlantic bluefin tuna from stomach content and stable isotope analyses. J. Sea Res. 76, 187–192, http://dx.doi.org/10.1016/j.seares.2012.09.002.

Please cite this article in press as: Tsai, C.-N., et al., Stomach content and stable isotope analysis of sailfish (Istiophorus platypterus) diet in eastern Taiwan waters. Fish. Res. (2014), http://dx.doi.org/10.1016/j.fishres.2014.10.021