Stable Isotope Analysis of the Gladius to Investigate Migration And

Fisheries Research 173 (2016) 169–174

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Fisheries Research

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Stable isotope analysis of the gladius to investigate migration and

trophic patterns of the neon ﬂying squid (Ommastrephes bartramii)

a,∗ a b b

Yoshiki Kato , Mitsuo Sakai , Haruka Nishikawa , Hiromichi Igarashi ,

b c c d

Yoichi Ishikawa , Dharmamony Vijai , Yasunori Sakurai , Toshie Wakabayshi , e

Toshiyuki Awaji

Tohoku National Research Institute, Fisheries Research Agency, 25-259 Aza Shimomekurakubo, Hachinohe, Aomori 031-0841, Japan

Japan Agency for Marine-Earth Science and Technology, 3173-25 Showa-machi, Kanazawa-ku, Yokohama 236-0001, Japan

School of Fisheries Sciences, Hokkaido University, 3-1-1 Minato-cho, Hakodate 041-8611, Japan

Department of Fisheries Science and Technology, National Fisheries University, 2-7-1 Nagata-Honmachi, Shimonoseki, Yamaguchi 759-6595, Japan

Kyoto University, Yoshida-Honmachi, Sakyo-ku, Kyoto-shi, Kyoto 606-8501, Japan

a r t i c l e i n f o a b s t r a c t

Article history: The neon ﬂying squid, Ommastrephes bartramii is broadly distributed in subtropical and temperate regions

Received 16 March 2015

of the world’s oceans. The North Paciﬁc population is comprised of two spawning cohorts; the autumn

Received in revised form

cohort and winter-spring cohort, which despite their apparent contiguous hatching periods, have marked

20 September 2015

differences in the mantle length between the two cohorts, indicating differences in behavior. Especially,

Accepted 21 September 2015

females of the autumn cohort after remaining in the subtropical zone for spring, in the ﬁrst half of the

Available online 2 October 2015

summer migrate close to the vicinity of the southern boundary of the transition area. Subsequently they

migrate into the subarctic waters to feed. However, for males details are less clear and it is considered

Keywords:

that they remain in the subtropical zone without migrating to the subarctic feeding area. However little

Ommastrephes bartramii

is known about the migration strategy of O. bartramii.

Stable isotope

Gladius Stable isotope proﬁles along the gladius (internal chitinous shell) have been recently analyzed and

Autumn cohort form a promising tool to back-calculate a chronological record of changes in the diet and habitat. In this

13 15

Migration study, ı C and ı N values were measured along the gladius to reconstruct the feeding variations and

habitat of the autumn cohort during ontogeny. The results of ı C values support previous studies which

inferred differences in migratory behavior between males and females. These differences occurred from

260 mm mantle length.

1. Introduction (Yatsu et al.,1997, 1998). The spawning grounds of O. bartramii in

the North Paciﬁc form south of the Japanese mainland in the area

The oceanic cephalopod, neon ﬂying squid (Ommastrephes bar- from the Ryukyu Islands to the Ogasawara Islands and in the waters

tramii) is broadly distributed in temperate regions of the world’s off the Hawaiian Islands in the sub-tropical areas with surface tem-

◦

oceans (Roper et al., 1984) and has been commercially exploited peratures ranging 21–25 C (Bower, 1996; Ichii et al., 2004). After

in the North Paciﬁc by Japan since 1974, and more recently by the hatching, the planktonic stage, the paralarvae, remain for several

Korean, Chinese and Taiwanese ﬂeets. Especially the annual com- months in the spawning area (Kato et al., 2014) prior to the start of

mercial catch of Japan amounts to 10,000–40,000 tonnes and is their northern migration to the feeding area in the subarctic transi-

mainly used by the processed foods industry (Ichii et al., 2006). tion region (Ichii et al., 2004). Females of the autumn cohort remain

The neon ﬂying squid (O. bartramii) has a one year life span in the subtropical zone for spring then in the ﬁrst half of the sum-

and maximum mantle length (ML) reaches 600 mm in females and mer migrate close to the vicinity of the southern boundary of the

450 mm in males in the North Paciﬁc. The ﬁshed stock is formed of 2 transition area. Subsequently they migrate into subarctic waters to

seasonal cohorts; the autumn cohort and the winter–spring cohort feed. The southern migration starts in approximately September to

the spawning grounds in the subtropical zone (Ichii et al., 2009).

However, for males details are less clear and it is considered that

∗ they may remain in the subtropical zone without a migration to

Corresponding author.

the subarctic feeding area (Yatsu et al., 1997). Individuals during the

E-mail address: [email protected] (Y. Kato).

http://dx.doi.org/10.1016/j.ﬁshres.2015.09.016

170 Y. Kato et al. / Fisheries Research 173 (2016) 169–174

spring northern migration and in the summer feeding grounds feed

on myctophids, cephalopods and crustaceans etc., with myctophids

and cephalopods being major prey items (Seki, 1993; Watanabe

et al., 2004). O. bartramii are an important prey item for large preda-

tory ﬁsh (e.g. Xiphias) and marine mammals (Seki et al., 2002). O.

bartramii form a high trophic level in the food web and due to their

abundance have a major impact on the structure of the food web

via top–down effects on prey items and can be considered as a

key species within the food web. Furthermore, O. bartramii can be

considered as an indicator species reﬂecting the condition of the

ecosystem and as such is also of signiﬁcant importance for research

on this ecosystem (Ichii et al., 2007).

Fig. 1. Schematic ﬁgure of the gladius structure (Adapted from Ruiz-Cooley et al.,

The isotopic signature of organisms has been extensively used in

2010; Lorrain et al., 2011).

ecology to establish evidence for trophic relationships within food

webs and also dietary changes during ontogeny (Ruiz-Cooley et al.,

13 15 proostracum was individually freeze–dried, it was pulverized in

2006, 2010; Parry, 2008). Changes in ı C and ı N values can be

a mortar into a powder. Then to delipify, chloroform–methanol

effective to respectively trace differences in the trophic source of

(2:1) was added and after 10 min of being centrifuged at 800 G the

food and in the trophic level of food organisms within ecosystems

supernatant was removed. This process was repeated 3 times. After

including oceanic squid (Cherel et al., 2009; Lorrain et al., 2011). In

◦

delipfying samples were dried in an oven at 80 C for 1 h. Each pow-

other isotope studies, the isotopic signature has been used for anal-

dered sample was then placed in a tin container (Thermo Scientiﬁc

ysis of squid migration routes (Lorrain et al., 2011; Ruiz-Cooley and

Co.) using an acetone washed spatula. The encapsulated tin con-

Gerrodette, 2012; Arguelles et al., 2012; Ruiz-Cooley et al., 2013).

tainer samples were then analyzed by mass spectrometry (Thermo

Especially Ruiz-Cooley et al. (2013) used a novel analysis method

Scientiﬁc Co., Delta V Isotope Ratio Mass Spectrometer). Isotope

from both bulk tissues and individual amino acids (phenylalanine

13 15

ratios of samples are reported as ı C or ı N values:

and glutamic acid) in both gladii and muscle of D. gigas captured in

the Northern California Current System enabling them to detail the

ıR = R /R − ×

sample [( samples standard) 1] 1000 (1)

various migration behaviors shown by this species. This method

13 12 15 14

also enables estimation of the trophic level by a comparison of where the Rsample and Rstandard are the C / C and N / N ratios

the N values for glutamic acid and phenylalanine (Chikaraishi of measured samples and standards, respectively. Results are pre-

et al., 2011). The method is a powerful tool for ecological food web sented in ‰ notation with respect to Pee Dee Belemnite (PDB) scale

13 15

studies, however the requirement for specialized equipment has for ı C and atmospheric N2 (Air) scale for ı N.

precluded its more generally use.

In this study, we examine the potential to use samples of internal 2.3. Oceanographic data

chitinous shell, the gladius (Hunt and Nixon, 1981), to reconstruct

ontogenetic changes of habitat and feeding habits and any dif- To describe the sampling site, we used sea surface data. The

ferences between males and females of the autumn cohort of O. water mass structure has an important role in the formation of

bartramii. spawning grounds. Sea surface temperatures were derived using

the NOAA Optimum Interpolation Sea Surface Temperature Ver. 2

climate dataset (http://www.esrl.noaa.gov/psd/data/gridded/data.

2. Materials and methods

noaa.oisst.v2.html, accessed 1 March 2013). The optimum interpo-

lation sea surface temperature (SST) analysis is produced weekly

2.1. Sample collection

on a one-degree grid. The analysis uses in situ and satellite SST’s

plus SST’s simulated by sea-ice cover. Before the analysis is com-

Sampling was carried out using individual squid sampled on

puted, the satellite data are adjusted for biases using the method

the Kaiyo-maru of the Fisheries Agency during December of 2013.

of Reynolds (1988) and Reynolds and Marsico (1993).

Table 1 shows the Sample ID, collection date, location and biological

For drawing and interpolation of environmental data we used

characteristics. All samples were individually sampled by jigging.

the Generic Mapping Tools (Wessel and Smith, 1998) provided by

The maximum hook depth was set at 150 m depth. The ﬁshing sur-

Hawaii University.

vey was carried out at each sampling station between sunset and

sunrise, and carried out for 1 h. All specimens (N = 9) were measured

2.4. Statistical model

on board for mantle length (ML), sexed, and were assessed repro-

ductive maturity. Reproductive maturity was assessed on the basis

To test differences between males and female, statistical models

of the maturity stages 1–3 proposed by Watanabe et al. (2008). The

◦ were applied. The models were built by generalized linear model

gladius of each sample was stored at −20 C until return to the land

laboratory. (GLM). The GLM was used to generate a robust predictive equation.

Two explanatory variables were included in the analysis using a

GLM (Eqs. (2) and (3)), as follows:

2.2. Stable isotope analysis

ı15

N = ˛0 + ˛1 ML + ˛2Sex (2)

Morphologically the gladius (pen) can be differentiated into 3 13

ı C = ˛0 + ˛1 ML + ˛2Sex (3)

sections, the proostracum, the conus and the rostrum (Bizikov and

Arkhipkin, 1997). Due to the clarity of the daily rings, the proost- The factor Sex is a categorical variable. ML indicates mantle

racum section of the pen has been frequently used in aging studies length. The selection of variables was also based on the Akaike

(Perez et al., 1996; Bizikov and Arkhipkin, 1997). information criterion (AIC; Akaike, 1974). The ﬁnite sample cor-

Samples of the proostracum (Fig. 1) were cleaned with distilled rected AIC was used in model selection.

water and KimWipes (Kimberly–Clark) and sectioned into 20 mm Furthermore we observed that males and females were caught

samples using acetone washed scissors. After each section of the at the same place up to around 260 mm ML (Sakai et al., 2010).

Y. Kato et al. / Fisheries Research 173 (2016) 169–174 171

Table 1

Ommastephes bartramii Sample ID, collection date, location and biological characteristics.

Sample ID Collection date Location Mantle length (mm) Body weight (g) Sex Maturity stage

◦ ◦

705-1 6 Dec 2013 28 30‘N; 170 00‘W 559 5480 Female 3

◦ ◦

705-2 6 Dec 2013 28 30‘N; 170 00‘W 383 1286 Male 3

◦ ◦

803-1 8 Dec 2013 28 00‘N; 166 59‘W 520 4144 Female 3

◦ ◦

803-3 8 Dec 2013 28 00‘N; 166 59‘W 354 1396 Male 3

◦ ◦

805-1 9 Dec 2013 29 52‘N; 166 59‘W 552 5034 Female 3

◦ ◦

805-2 9 Dec 2013 29 52‘N; 166 59‘W 352 1436 Male 3

◦ ◦

604MCN-1 2 Dec 2013 30 00‘N; 172 55‘W 510 4640 Female 3

◦ ◦

604MCN-2 2 Dec 2013 30 00‘N; 172 55‘W 372 1434 Male 3

◦ ◦

604MCN-3 2 Dec 2013 30 00‘N; 172 55‘W 348 1239 Male 3

for animals larger than 260 mm ML) by the stepwise variable selec-

tion (Table 2). The effects of Sex were not signiﬁcant and removed

for the most parsimonious model for animals up to 260 mm ML and larger.

For the relationship between ı C values and ML of males and

females Fig. 4 shows there was no difference up to a ML size of

approximately 260 mm ML, with values ranging between −19.5

and −18.5 ‰. After a size of 260 mm ML the patterns between males

and females differ, for males values range −19.0 to −18.3 ‰ indi-

cating a slight increase, while for females a decline was observed

with values at the end point ranging from −20.3 to −18.7 ‰. In

the GLM analysis, the models were improved from the full models

(AIC: −45.07 for animals up to 160 mm ML and 31.43 for animals

above 260 mm ML) to the most parsimonious models with the low-

est AIC (−46.46 for animals up to 260 mm ML and 31.43 for animals

larger than 260 mm ML) by the stepwise variable selection. The

effects of Sex were not signiﬁcant and removed for the most par-

simonious model for animals up to 260 mm ML. Whereas, Sex and

ML were taken into the model for animals larger than 260 mm ML

as signiﬁcant variables.

In Fig. 5 we show CN plots for animals up to 260 mm ML (Fig. 5a)

Fig. 2. Horizontal distribution of sea surface temperature and sampling points. Stars 15

and for sizes above 260 mm ML (Fig. 5b). The ı N ﬂuctuation range

indicate sampling points.

of animals up to 260 mm ML was larger than that of animals larger

than 260 mm ML (f-test, p < 0.05). F Based on these differences in

Therefore two GLMs were carried out separately for animals up

patterns, we suggest that the mantle length of 260 mm forms a

to 260 mm ML and animals larger than 260 mm ML by using the

boundary indicating a change in migration and feeding behavior as

statistical software R, version 2.15.3 (http://cran.r-project.org/,

discussed below.

accessed 1 March 2013).

3. Results 4. Discussion

The sea surface temperature for the sampling points and the From the environmental analysis of the sampling stations, the

◦

monthly averaged temperatures for each sampling point were com- surface waters were in the range of 22.5–24.5 C and also from evi-

pared (Fig. 2). The surface water temperatures of sampling points dence that the sampled individuals were mature for this annual

where mature individuals were collected were all in the range of species, we suggest that the samples were collected prior to spawn-

◦

22.5–24.5 C. ing in the spawning grounds. As O. bartramii dies after the spawning

Subsequently the gladius measured from the tip of the conus period (DFO, 1999), the gladii of these samples can be used to esti-

15 13

as the gladius length (GL) showed a strong correlation with the mate values of ı N and ı C during the whole life cycle.

mantle length (r = 0.976, ML = 0.944 GL + 29.412). From this result, In this research, for sizes of up to 260 mm ML, the regression

15 13 2

based on the gladius length, the mantle length at the time of each line of CN plot was steep (ı N = 1.43 ı C + 35.54, r = 0.29, p < 0.05)

point of the gladius development can be back-calculated. indicating an inclusion in the diet of higher trophic level organ-

15 15 15 13

Fig. 3 shows ı N values of the MLs. ı N values of animals up to isms based on the broad spread of values for ı N but for ı C

a size of approximately 260 mm ML showed a gradually increase. the change in values was small. On the other hand for sizes larger

However the variation was large during this stage of growth and than 260 mm ML the regression line of CN plot was less steep

15 15 13 2 15

values of ı N varied between 5 and 11‰. In all males (blue lines (ı N = 2.09 ı C + 47.87, r = 0.08, p < 0.05) with ı N showing a

in Fig. 3), the ı N value declined after reaching a size of 260 mm more moderate variation compared to up to 260 mm ML sizes but

ı13

ML. By comparing the ﬁnal values (end point for each individual) C showing a greater range of values.

between individuals sampled at the same sampling station (Fig. 3), In the relationship between ı C values and ML for males and

the ı N values are extremely close between male and female sam- females there was no difference up to a ML size of approximately

ples. 260 mm ML. On the other hand, after a size of 260 mm ML the

In the GLM analysis, the models were improved from the full patterns between males and females differ. In marine ecosystems,

models (AIC: 209.39 for animals up to 260 mm ML and 226.53 for ı C values vary greatly with latitude and/or over inshore/offshore

animals larger than 260 mm ML) to the most parsimonious models gradients (Lorrain et al., 2011). Aita et al. (2011) based on iso-

with the lowest AIC (207.4 for animals up to 260 mm ML and 224.92 tope mapping showed that there are differences in ı C values

172 Y. Kato et al. / Fisheries Research 173 (2016) 169–174

12 705-1 705-2 803-1 11 803-3 805-1 805-2 604MCN-1 10 604MCN-2 604MCN-3

8 N (‰) 15 δ 7

4 0 100 200 300 400 500 Mantle length (mm)

Fig. 3. Relationship of the mantle length and ı N [Blue lines indicate data for males and red lines for females (see Table 1 for individual data)].

Table 2

Results of the multivariate generalized linear model (GLM) analyses.

Variable Animals up to 260 mm ML Animals larger than 260 mm ML

13 15 13 15

ı C ı N ı C ı N

Coefficient s.e. P Coefficient s.e. P Coefficient s.e. P Coefficient s.e. P

Intercept −19.423 0.069 <0.001 6.069 <0.001 −17.820 0.169 <0.001 9.880 0.464 <0.001

Sex – – – – – – −0.596 0.085 <0.001 – – –

ML 0.002 <0.001 <0.001 0.010 0.003 <0.01 −0.001 0.001 0.1 1.050 0.264 <0.001

-18.0 705-1 705-2 803-1 803-3 805-1 -18.5 805-2 604MCN-1 604MCN-2 604MCN-3

-19.0 C (‰) 13

δ -19.5

-20.0

-20.5 0 100 200 300 400 500 Mantle Length (mm)

Fig. 4. Relationship between the mantle length and ı C. [Blue lines indicate data for males and red lines for females (see Table 1 for individual data)].

among different areas in the North Paciﬁc. From these results, from approximately this ML stage and subsequently the migration

ı13

C can be considered as an indicator of their habitat. Therefore, pattern differs between sexes. Until now, the phenomenon of a dif-

this also allows an examination of differences, as in the current ference in male and female migration behavior has been inferred

research between males and females at the size approximating based on ﬁsheries catch data (Yatsu et al., 1997). However inde-

260 mm ML, where the values for C differ suggesting the poten- pendent supporting evidence has not been available. Our isotope

tial phenomenon that the habitat area differed between sexes

Y. Kato et al. / Fisheries Research 173 (2016) 169–174 173

(a) 12 705-1 705-2 11 803-1 803-3 805-1 805-2 10 604MCN-1 604MCN-2 604MCN-3 9 ‰) 8 N ( 15 δ 7

-20.5 -20.0 -19.5 -19.0 -18.5 -18.0

13 δ C (‰) (b) 12 705-1 705-2 11 803-1 803-3 805-1 805-2 10 604MCN-1 604MCN-2 604MCN-3 9

‰) 8 N ( 15

δ 7

-20.5 -20.0 -19.5 -19.0 -18.5 -18.0

δ C (‰)

Fig. 5. (a) Carbon isotope versus nitrogen isotope plot of animals up 260 mm ML, (b) same as for (a) but of animals larger than 260 mm ML.

analysis provides further evidence of this phenomenon and new also forage in the same area. However from 260 mm ML females

knowledge of the size at the start of the migration. start to migrate northwards and forage over a more extensive lati-

In summary, the CN plot (Fig. 5) showed there were differences tudinal area.

between males and females of the autumn cohort. In the case of In future research, by using evidence from oxygen isotope anal-

males, they are considered to forage in a narrow latitudinal area ysis and amino acid analysis, we anticipate the history of migration

during their life span. On the other hand, females up to 260 mm ML can be analyzed in closer relation to the marine environment and

174 Y. Kato et al. / Fisheries Research 173 (2016) 169–174

thus enable a more detailed assessment of the migration behavior. Kato, Y., Sakai, M., Masujima, M., Okazaki, M., Igarashi, H., Masuda, S., Awaji, T.,

2014. Effects of hydrographic conditions on the transport of neon ﬂying squid

Furthermore, we anticipate that differences in migration strategy

Ommastrephes bartramii larvae in the North Paciﬁc Ocean. Hidrobiológica 24,

of this species can be determined by comparing samples from the 33–38.

autumn cohort and winter–spring cohort. Lorrain, A., Argüelles, 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,

Acknowledgements e22194.

Parry, M., 2008. Trophic variation with length in two ommastrephid squids,

Ommastrephes bartramii and Sthenoteuthis oualaniensis. Mar. Biol. 153,

We would like to thank the crew and captain of the Fisheries

249–256.

Agency vessel Kaiyo-maru for their assistance with the sampling.

Perez, J.A.A., O’Dor, R.K., Beck, P., Dawe, E.G., 1996. Evaluation of gladius dorsal

Also we would like to gratefully acknowledge the cooperation and surface structure for age and growth studies of the short-ﬁnned squid, (Illex

illecebrosus)(Teuthoidea: Ommastrephidae). Can. J. Fish. Aquat. Sci. 53,

advice given to us by Dr. Michel P. Seki of NOAA. Dr. Hiroya Sugisaki

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and Mr. Makoto Okazaki of FRA is thanked for his kind assistance

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