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FISHERIES OCEANOGRAPHY

Fish. Oceanogr. 24:4, 335–346, 2015

Spatial difference in elemental signatures within early ontogenetic statolith for identifying Jumbo flying squid natal origins

BI LIN LIU,1,2,3,4 YONG CHEN4 AND XIN JUN CHEN1,2,3,* 1

College of Marine Sciences, Shanghai Ocean University, 999 Hucheng Ring Road, Lingang New City, Shanghai 201306, China 2 The Key Laboratory of Sustainable Exploitation of Oceanic Fisheries Resources, Ministry of Education, 999 Hucheng Ring Road, Lingang New City, Shanghai 201306, China 3 Collaborative Innovation Center for Distant-water Fisheries, 999 Hucheng Ring Road, Lingang New City, Shanghai 201306, China 4 School of Marine Sciences, University of Maine, Orono, Maine 04469 U.S.A.

ABSTRACT Signatures of trace elements and isotopes in the parts of hard structures formed in the early ontogenetic stages can be used as potential natural tags of adult cephalopods to trace their origins. The Jumbo flying squid, Dosidicus gigas, is widely distributed in the eastern Pacific Ocean. Fourteen detected elemental signatures (7Li, 23Na, 24Mg, 39K, 43Ca 55Mn, 59Co, 60Ni, 63 Cu, 66Zn, 88Sr, 137Ba, 208Pb and 238U) were determined in the nuclear zone (N), representing the embryonic stage, and the postnuclear zone (PN), representing the paralarval stage of statoliths for adult D. gigas collected off the Costa Rican, Peruvian and Chilean Exclusive Economic Zones (EEZs) using laser ablation inductively coupled plasma mass spectrometry (LA-ICP-MS). All measured signatures were significantly different between embryonic and paralarval statoliths, except for Sr, Ba and Pb. Over the three regions, a significant difference was found for Na and Ba within embryonic statoliths and Zn and Ba within paralarval statoliths. A high Ba/Ca ratio in statoliths obtained from Costa Rica was because of the prevalence of strong upwelling in the area. Elemental signatures, especially Ba/Ca, in early ontogenetic statoliths could be used as a proxy for distinguishing different

geographical groups and identifying natal origins. However, elemental signatures in embryonic statoliths tended to be a better natural tag than those in paralarval statoliths indicating that paralarvae with the same origin had distinct dispersal pathways. Additionally, stepwise discriminant analysis (SDA) showed there were at least two migration-based groups: ‘northern’ and ‘southern’ in the eastern Pacific Ocean. Overall, the derived results can improve our knowledge of the population structure, connectivity and life history of D. gigas. Key words: Dosidicus gigas, early ontogenetic stages, elemental signatures, natal origins, population, statoliths

INTRODUCTION

*Correspondence. e-mail: [email protected] Received 22 September 2014 Revised version accepted 3 May 2015

Dosidicus gigas (d’Orbigny, 1835), commonly known as the Humboldt or Jumbo (flying) squid, is an eastern Pacific nerito-oceanic species distributed along the eastern coast of the Americas from Alaska to Chile and inhabiting from the sea surface down to a depth of 1200 m (Nigmatullin et al., 2001). The abundance of this species tends to be closely related to both environmental conditions (e.g., temperature and predator abundance) and spawner-recruitment dynamics (Waluda et al., 2006; Zeidberg and Robison, 2007; Keyl et al., 2008). Dosidicus gigas is a key species in pelagic ecosystems because of its high abundance and important role in trophic dynamics (Rosas-Luis et al., 2008). This squid species supports important fisheries in four areas: the Gulf of California (Nevarez-Martınez et al., 2000; Morales-Bojorquez et al., 2001), the region off the Costa Rica Dome (Ichii et al., 2002), the coastal and oceanic waters of Peru (Taipe et al., 2001; Waluda et al., 2004a; Chen and Zhao, 2006) and within and outside the Chilean Exclusive Economic Zones (EEZ) ~iga et al., 2008; Liu et al., (Rocha and Vega, 2003; Zun 2010). The intra-specific population structure of D. gigas is complicated. Three groups have been identified based on the size of adult females and males (Nigmatullin

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et al., 2001): a small-sized group (140–340 and 130– 260 mm for females and males, respectively) occurring mainly in the equatorial waters; a medium-sized group (280–600 and 240–420 mm, for females and males, respectively) distributed over the whole range of the species; and a large-sized group (550–650 to 1000– 1200 mm and >400–500 mm, for females and males, respectively) only inhabiting the northern and southern extremes of its ranges. However, other studies have grouped D. gigas into just two stocks being the ‘northern’ and ‘southern’ stocks based on their migration patterns (Nesis, 1983; Clarke and Paliza, 2000; Sandoval-Castellanos et al., 2007). Understanding the population structure and connectivity of marine organisms is critical for studying their population dynamics and developing effective conservation and sustainable management strategies (Thorrold et al., 2001; Gillanders, 2002). Recently natural geochemical signatures of trace elements and isotopes in the hard structures of marine animals, such as bivalve shells, fish otoliths, octopus styles and squid beaks and statoliths, have been successfully utilized to investigate the population distribution of animals (Campana, 1999; Ikeda et al., 2003; Becker et al., 2005; Cherel and Hobson, 2005; Doubleday et al., 2008). The elemental signature is considered to be a potential complement to more commonly used genetic and morphologic methods for defining cephalopod cohorts and population structures (Arkhipkin, 2005). The hard parts of organisms formed in the early ontogenetic stages potentially carry natural tags recording the environmental history experienced at or near the place where they were born (Campana, 1999; Thorrold et al., 2001). Thus, elemental signatures in invertebrate larval statoliths are considered as useful tags of the natal source (Zacherl et al., 2003; Zacherl, 2005). For example, Ba/Ca was generally considered as an indicator element for upwelling events, thus the population with a higher Ba/Ca value always experiences a strong upwelling water mass (Arkhipkin et al., 2004; Zumholz et al., 2007). Signatures in the pre-hatching region of the adult otolith can be used to identify the source of populations because they are shown to match with signatures from equivalent structures from juveniles (Forrester and Swearer, 2002; Hamer et al., 2005). The same is found in the statoliths of squid (Warner et al., 2009). During the late 1990s and early 2000s, protoninduced X-ray emission (PIXE) and electron microprobe analysis (EPMA) were commonly used to examine cephalopod statolith micro-chemistry (Durholtz et al., 1997; Yatsu et al., 1998; Ikeda et al., 2002, 2003). However, these studies focused on Sr, the most

abundant element incorporated into the aragonite matrix of statoliths. Recently, laser ablation inductively coupled plasma mass spectrometry (LA-ICPMS) has become increasingly popular for examining lower concentration trace elements such as Ba, Mg and Mn (Zumholz et al., 2006, 2007; Doubleday et al., 2008; Warner et al., 2009; Liu et al., 2011). In this study, we used LA-ICP-MS to determine the elemental signatures in the statoliths nuclear (N), representing the embryonic stage, and postnuclear (PN), representing the paralarval stage, of D. gigas off the EEZs in the Eastern Pacific Ocean (Arkhipkin, 2005). The objectives of this paper were to detect the elemental composition in N and PN of adult statoliths, to determine if elemental signatures differ among different geographical groups, to determine the validity of using elemental signatures in discriminating populations and to identify the most suitable part of a statolith for population identification. This study provides an alternative way to evaluate the D. gigas population structure on the three major fishing grounds, which can improve our knowledge of population connectivity, natal origins and the life history of fisheries management. MATERIALS AND METHODS Sampling A total of 59 specimens were sampled in Chinese scientific surveys from 2007 to 2010 off the EEZ of Costa Rica, Peru and Chile in an area, defined from 75°000 W to 96°300 W and from 9°300 N to 37°300 S, in the Eastern Pacific Ocean. The surveys were conducted with commercial vessels using jigging (Fig. 1, Table 1). Statoliths were removed in the field and stored in 90% alcohol for further analyses. Detailed information of the samples is summarized in Table 1. Sample preparation Each individual statolith was ground on a longitudinal plane with 3Mâ commercial waterproof sandpaper (600, 1200 and 2000 grit) until the nucleus was exposed. It was then turned over and ground to the nucleus from the other side. Eventually, the ground statolith was polished with 0.3-lm alumina powder for further elemental signature analyses. Elemental signatures analysis To minimize the interference from contaminants, the ground statolith sections were rinsed in MillIQ water (resistivity > 18 Ω) for 5 min and air dried in a Class100 laminar flow bench prior to trace element analysis. The first sampling spot was within N and the second © 2015 John Wiley & Sons Ltd, Fish. Oceanogr., 24:4, 335–346.

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southeastern Pacific Ocean, is slow and broad, which must be responsible for the elemental signatures incorporated for the squid from both places (Chavez et al., 2008). Such a conclusion is consistent with the ~ez et al. (2011), who genetic view presented by Iban concluded that there was a single, large population in the Humboldt Current System. Moreover, they suggested that demographic population expansion in the currents is consistent with the oceanographic changes associated with the last glacial–interglacial transition. Sandoval-Castellanos et al. (2007) recommended that currents may partially explain the population interchange between Chile and Peru. They believed that the Chile population may have originated in the Peruvian waters and migrates to Chile by the countercurrents of the Peru Currents. Previous studies inferred that the jumbo squid in the southern hemisphere might spawn in tropical waters off the coast of northern Peru (Tafur et al., 2001; Sakai et al., 2008), where higher primary production provides nourishing and plentiful food for paralarval squid (Fiedler and Talley, 2006; Montecino and Lange, 2009). The differences in cross-validation between embryonic and paralarval statoliths, in this study, are mostly attributed to misclassification rates for Peruvian and Chilean squids rather than Costa Rican individuals, which can be seen from the variation in the correct classification rate for each of the separated groups (Table 5). This at least made us conclude that, unlike the Costa Rican Dome waters, the paralarvae of D. gigas from the Peruvian and Chilean waters were advected away from their natal source by oceanic currents. If the coastal water of northern Peru was indeed the spawning ground as concluded above, the paralarvae from the southern hemisphere must drift northward by the Humboldt Current rather than stay on the spawning ground for food. This conclusion is consistent with the view proposed by Anderson and Rodhouse (2001). In addition, they also suggested that juvenile squid are ultimately carried to the west of the South Equatorial Current and adults who remain in this tropical area grow to a small size, but others migrate southward to further south of Peru and Chile. In conclusion, all measured signatures were significantly different between embryonic and paralarval statoliths, except for Sr, Ba and Pb. Na and Ba within embryonic statoliths and Zn and Ba within paralarval statoliths where significant differences were found in the three regions. A significantly higher Ba/Ca ratio in the statoliths collected from Costa Rica was found, compared with those from Peru and Chile, which might result from the prevalence of strong upwelling

in Costa Rica, and a similar Ba/Ca between Peru and Chile might be influenced by the Humboldt Current. Elemental signatures in embryonic statoliths were considered to be a better natural tag than those in paralarval statoliths, although both of them could be used as a proxy for distinguishing different groups. The paralarvae of the same populations followed different dispersal trajectories, which might be responsible for their differences. We prefer to believe that the northern (Costa Rica) and southern (Peru and Chile) groups potentially have different natal origins and migration patterns. The northern population was putative spawning adjacent to the Costa Rica Dome, and the Equatorial Counter Current meant that the paralarvae remained in the spawning ground for food. In contrast, the southern population might spawn in the coastal waters off northern Peru, and the paralarvae would be carried northward rather than stay at the birth place for the nursery. Overall, the jumbo squid life cycle, especially at early ontogeny stage, is susceptible to the variation of oceanography, particularly the ENSO. For instance, during normal and cold years, intensive offshore transport carries paralarvae far away from the coast into the large open sea area, but during warm years, a weak current retains the paralarvae near the shelf. Therefore, considering higher plasticity of the squid and specificity of the study region, it is important for future studies to assess how and where the squid might move as the climate changes. ACKNOWLEDGEMENTS This work was funded by the National Science Foundation of China (NSFC 41306127 and NSFC41276156), the National Science Foundation of Shanghai (No.13ZR1419700), the Innovation Program of Shanghai Municipal Education Commission (No.13YZ091), the PhD Programs Foundation of Ministry of Education of China (No.20133104120001) and the Shanghai Universities First-class Disciplines Project (Fisheries A). Yong Chen’s involvement is supported by the SHOU International Center for Marine Sciences (No. 3606120001). REFERENCES Anderson, C.I.H. and Rodhous, P.G. (2001) Life cycles, oceanography and variability ommastrephid squid in variable oceanographic environments. Fish. Res. 54:133–143. Arkhipkin, A.I. (2005) Statolith as ‘balck boxes’(life recorders) in squid. Mar. Freshw. Res. 56:573–583. Arkhipkin, A.I., Campana, S.E., FitzGerald, J. and Thorrold, S.R. (2004) Spatial and temporal variation in elemental

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Table 1. Summary information of sampled Dosidicus gigas squid. ID

Catch date

Location

Coordinates

03 30 SC10-3 SC10-10 71 B10-2 SC07-11 SC10-21 72 D8-8 61b 70b 124b 140b A208 A77 C0923 D107 D12 D42 D94 E176 E202 E32 E54 G198 G267 G288 G422 G54 K154 K18 K203 K228 K242 K80 61a 88a 294a 301a 316a 321a 164b 6b 23b 35b 38b 49b 69b 75b F91 G173

2009:08:17 2009:08:19 2009:08:18 2009:08:18 2009:08:09 2009:07:26 2009:08:15 2009:08:18 2009:08:09 2009:07:29 2008:09:20 2008:09:20 2008:09:13 2008:09:13 2009:09:13 2009:10:01 2009:09:23 2008:02:11 2008:01:10 2008:01:21 2008:02:04 2008:12:14 2008:11:30 2009:01:25 2008:11:24 2010:01:16 210:03:10 2009:12:20 2009:11:15 2010:02:05 2010:10:25 2010:06:15 2010:08:10 2010:11:30 2010:11:10: 2010:06:20 2008:05:01 2008:05:07 2008:05:12 2008:05:12 2008:05:12 2008:05:09 2008:05:12 2007:01:20 2007:01:21 2007:01:25 2007:01:25 2008:05:14 2008:05:01 2008:05:07 2010:06:17 2010:05:15

Costa Rica Costa Rica Costa Rica Costa Rica Costa Rica Costa Rica Costa Rica Costa Rica Costa Rica Costa Rica Peru Peru Peru Peru Peru Peru Peru Peru Peru Peru Peru Peru Peru Peru Peru Peru Peru Peru Peru Peru Peru Peru Peru Peru Peru Peru Chile Chile Chile Chile Chile Chile Chile Chile Chile Chile Chile Chile Chile Chile Chile Chile

8°550 N, 94°550 W 8°350 N, 94°190 W 9°210 N, 94°520 W 9°210 N, 94°520 W 7°460 N, 91°480 W 9°300 N, 95°300 W 6°360 N, 95°020 W 9°210 N, 94°520 W 7°460 N, 96°300 W 8°300 N, 94°520 W 10°320 S, 83°140 W 10°320 S, 83°140 W 10°390 S, 82°290 W 10°390 S, 82°290 W 11°120 S, 83°170 W 10°590 S, 82°410 W 10°450 S, 83°100 W 13°220 S, 83°280 W 12°540 S, 82°560 W 13°060 S, 82°460 W 13°030 S, 83°040 W 13°200 S, 83°290 W 11°540 S, 83°040 W 12°450 S, 83°450 W 12°000 S, 83°050 W 14°430 S, 83°330 W 16°270 S, 79°260 W 15°020 S, 80°350 W 11°290 S, 82°310 W 14°070 S, 83°100 W 16°070 S, 82°140 W 16°250 S, 80°160 W 10°520 S, 81°550 W 15°390 S, 81°030 W 14°310 S, 82°090 W 15°520 S, 79°490 W 23°000 S, 75°000 W 22°000 S, 77°500 W 22°000 S, 75°000 W 22°000 S, 75°000 W 23°000 S, 75°000 W 24°000 S, 75°300 W 22°000 S, 75°000 W 24°000 S, 77°000 W 26°000 S, 76°000 W 37°300 S, 80°000 W 37°300 S, 80°000 W 21°000 S, 75°000 W 23°000 S, 75°000 W 22°000 S, 77°500 W 26°41S, 75°290 W 28°27S, 75°490 W

ML (mm)

Sex

Maturity stage

Spot 1 age (days)

Spot 2 age (days)

263 259 348 285 274 271 250 310 295 374 258 291 278 275 311 294 989 383 454 343 325 275 303 434 302 353 435 333 450 403 405 243 223 502 359 529 381 449 391 401 341 372 402 391 425 368 309 373 361 517 493 490

♂ ♀ ♀ ♂ ♀ ♀ ♀ ♂ ♂ ♀ ♀ ♀ ♀ ♀ ♀ ♂ ♀ ♂ ♀ ♂ ♀ ♀ ♀ ♀ ♀ ♀ ♀ ♂ ♀ ♀ ♀ ♂ ♀ ♀ ♀ ♀ ♀ ♂ ♀ ♀ ♂ ♀ ♀ ♀ ♀ ♀ ♀ ♂ ♂ ♀ ♀ ♀

Mature Immature Mature Mature Immature Mature Mature Mature Mature Mature Immature Immature Immature Immature Immature Immature Mature Mature Mature Immature Immature Immature Immature Mature Immature Mature Immature Immature Immature Immature Immature Immature Immature Immature Mature Mature Immature Immature Immature Immature Immature Immature Immature Immature Immature Immature Immature Immature Immature Immature Immature Immature

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

18 21 20 22 24 24 23 21 19 25 26 26 27 25 24 22 28 23 27 23 25 24 27 23 22 28 29 24 25 26 27 23 24 28 26 27 28 24 28 26 23 25 29 30 29 27 27 25 24 25 26 25


Jumbo flying squid natal origins

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Table 1. (Continued)

ID

Catch date

G561 L210 L216 L241 M11 M14 SB12

2010:04:30 2007:06:09 2007:06:10 2007:06:11 2008:02:24 2008:02:24 2010:06:05

Location

Coordinates 27°48S, 75°310 W 29°30S, 76°300 W 28°58S, 77°180 W 27°00S, 76°000 W 21°34S,81°210 W 21°34S,81°210 W 28°45S, 76°140 W

Chile Chile Chile Chile Chile Chile Chile

ML (mm)

Sex

Maturity stage

Spot 1 age (days)

Spot 2 age (days)

406 395 390 454 553 531 426

♂ ♀ ♂ ♀ ♀ ♀ ♀

Immature Immature Mature Immature Mature Mature Immature

0 0 0 0 0 0 0

24 29 22 29 28 27 27

ML, mantle length; BW, body weight; ♀, female; ♂, male; Dates are given as yyyy:mm:dd.

Table 2. Analysis of variance of signatures in the embryonic and paralarval statoliths (N and PN) for Dosidicus gigas. Embryonic statolith Element/Ca Li/Ca (lmol mol1) Na/Ca (mmol mol1) Mg/Ca (lmol mol1) K/Ca (lmol mol1) Mn/Ca (lmol mol1) Co/Ca (lmol mol1) Ni/Ca (lmol mol1) Cu/Ca (lmol mol1) Zn/Ca (lmol mol1) Sr/Ca (mmol mol1) Ba/Ca (lmol mol1) Pb/Ca (lmol mol1) U/Ca (lmol mol1)

Range 0.82–3.62 8.74–13.3 80–1235 87–1360 0–21.8 0–0.87 0–16.1 0–23.6 0–136 13.9–18.8 8.75–56.4 0–7.94 0–0.24

Paralarval statolith

Mean SD

Range

1.23–5.80 9.12–13.9 74–484 56–971 0–15.1 0–0.78 0–7.67 0–7.19 0–24.3 13.0–17.8 8.56–42.8 0–2.65 0–0.07

1.84 10.6 415 468 7.66 0.16 2.53 2.61 15.3 16.3 17.3 0.47 0.037

0.49 1.12 271 237 4.79 0.19 3.51 4.21 26.6 1.13 9.42 1.17 0.042

Mean SD

F

P

17.638 13.885 30.563 6.631 28.816 4.039 5.913 8.101 10.945 3.852 2.536 3.514 9.840

0.000* 0.000* 0.000* 0.011* 0.000* 0.047* 0.017* 0.005* 0.001* 0.052 0.114 0.063 0.002*

2.28 11.3 210 365 3.85 0.10 1.25 0.98 3.66 15.9 14.7 0.17 0.018

0.65 1.15 86 194 2.60 0.16 1.98 1.20 4.52 1.03 7.81 0.37 0.016

*Implies a significant difference.

ANOVA also showed that Ba within the embryonic and paralarval statoliths from Peru were both similar to Chile, but significantly lower than those in Costa Rica (Table 4). The values of Mg/Ca and Mn/Ca both in the embryonic and paralarval statoliths from Costa Rica were the highest and those from Chile were the lowest (Table 4). In the SDA of the multi-elemental signatures within embryonic statoliths, the results indicated that only Na, Mg and Ba made significant contributions to the determination of origins of samples (SDA, P < 0.05), and squid from different locations could be distinguished from each other using the first two functions, which explained 75.9% and 24.1% of the variations, respectively (Fig. 2). However, for paralarval statoliths, only K, Zn and Ba were responsible for all the contributions to the classification (SDA, P < 0.05), with discriminant function 1 (DF1) explaining the most variations (Fig. 2). © 2015 John Wiley & Sons Ltd, Fish. Oceanogr., 24:4, 335–346.

Although there was considerable overlap, squid from different locations could be separated, with final cross-validated classification rates of 61% and 52.5% for embryonic and paralarval statoliths, respectively (Table 5, Fig. 2). Overall, Ba contributed the greatest variation among the three sampling locations at the two functions, which can be seen from the values of the canonical coefficients (Table 6, Fig. 2). Hemispherical variation in signatures Multi-elemental signatures within embryonic and paralarval statoliths from the northern (Costa Rica) and southern hemisphere (Peru and Chile) used in the SDA showed that the final correct cross-validated classification rates were 84.7% and 88.1%, respectively, with a total Wilks’k value of 0.665 and 0.529 (P < 0.001) (Table 7). This suggested that elemental signatures have significant hemispherical differences,

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Table 3. Analysis of variance comparing elemental signature concentrations within embryonic and paralarval statoliths for Dosidicus gigas among the three regions. Embryonic statolith

Paralarval statolith

MS

MS

Signature

Regions

Error

F

Li/Ca Na/Ca Mg/Ca K/Ca Mn/Ca Co/Ca Ni/Ca Cu/Ca Zn/Ca Sr/Ca Ba/Ca Pb/Ca U/Ca

0.224 4.623 203 425 30 265 55.969 0.042 1.184 11.034 250.567 0.746 730.554 1.603 0.003

0.240 1.127 68 701 57 320 21.761 0.035 12.731 17.941 726.281 1.291 65.798 1.350 0.002

0.935 4.102 2.961 0.528 2.572 1.186 0.093 0.615 0.345 0.578 11.103 1.187 1.718

P

Regions

Error

F

P

0.399 0.022* 0.060 0.593 0.085 0.314 0.911 0.544 0.710 0.564 0.000* 0.313 0.189

0.506 1.503 10 267 33 226 10.639 0.017 0.225 0.124 98.296 1.337 564 0.058 0

0.416 1.320 7266 37 929 6.625 0.026 4.018 1.494 17.685 1.044 43.078 0.142 0.000

1.215 1.139 1.413 0.876 1.606 0.659 0.056 0.083 5.558 1.281 13.101 0.409 0.899

0.304 0.327 0.252 0.422 0.210 0.521 0.946 0.920 0.006* 0.286 0.000* 0.666 0.413

*Implies significant difference. Table 4. Elemental signature concentrations within embryonic and paralarval statoliths for Dosidicus gigas from the three different regions. Mean SD value of embryonic statolith Signature/Ca Li/Ca (lmol mol1) Na/Ca (mmol mol1) Mg/Ca (lmol mol1) K/Ca (lmol mol1) Mn/Ca (lmol mol1) Co/Ca (lmol mol1) Ni/Ca (lmol mol1) Cu/Ca (lmol mol1) Zn/Ca (lmol mol1) Sr/Ca (mmol mol1) Ba/Ca (lmol mol1) Pb/Ca (lmol mol1) U/Ca (lmol mol1)

Costa Rica 1.67 9.87 455 406 9.84 0.11 2.93 1.37 18.3 16.4 a 28.3 0.96 0.026 a

0.27 0.69 396 245 5.11 0.06 2.51 1.01 37.3 0.65 16.2 2.46 0.021

Peru 1.84 10.5 490 497 8.21 0.14 2.53 3.12 12.0 16.4 b 14.8 0.30 0.048

ab

0.50 0.93 223 281 5.44 0.15 3.53 4.56 10.8 0.96 5.80 0.53 0.054

Chile 1.92 11.0 312 461 6.09 0.21 2.35 2.57 17.7 16.1 b 15.3 0.46 0.029 b

0.54 1.30 233 179 3.33 0.25 3.96 4.66 33.9 1.43 4.69 0.81 0.032

Mean SD value of paralarval statolith Costa Rica 2.60 11.3 249 342 4.73 0.080 1.26 1.06 a 7.63 16.3 a 24.4 0.17 0.020

1.30 1.17 125 246 3.09 0.050 1.74 0.73 7.33 0.72 12.6 0.15 0.018

Peru 2.20 11.1 209 336 4.14 0.080 1.34 0.91 b 3.20 15.9 b 12.4 0.13 0.15

0.39 1.14 60.5 179 2.92 010 2.11 0.89 3.68 0.86 3.98 0.16 0.017

Chile 2.25 11.6 194 407 3.15 0.13 1.15 1.03 b 2.46 15.7 b 13.1 0.23 0.021

0.44 1.15 89.4 189 1.80 0.23 2.00 1.64 2.79 1.26 5.19 0.57 0.014

The results from Tukey’s HSD with a significant difference (P < 0.05) indicated by letters (a, b).

despite considerable overlaps as shown by the PCA scatter-plots (Fig. 3). DISCUSSION Elemental signatures of squid statoliths were used as markers for natal origin based on the assumption that spatial variation in chemical and physical properties of ambient waters could be reflected in the elemental composition, which was verified for fish otolith (Bath et al., 2000). For instance, the ontogenetic variation

in the Sr/Ca ratio of the Japanese common squid Todarodes pacificus statoliths showed significant differences between the Subarctic and Tsushima groups (Ikeda et al., 2003). Arkhipkin et al. (2004) reported that the combined elemental signatures in the whole statolith of the Patagonian longfin squid Loligo gahi varied significantly in different geographical and spawning groups. However, Ashford et al. (2006) argued that distinguishing populations using a whole-structure elemental analysis carried the risk of wrongly grouping a single stock into multiple stocks because studied © 2015 John Wiley & Sons Ltd, Fish. Oceanogr., 24:4, 335–346.


Figure 2. Discriminant function plots of embryonic and paralarval statolith to compare multi-elemental signatures among sampling locations using elements/Ca for Dosidicus gigas. Diamond: Costa Rica; Square: Peru; Triangle: Chile; Ellipses represents 95% confidence interval around centroids of each group.

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Table 5. Cross-validated classification rate on the basis of discriminant function analysis scores of multi-elemental signatures within embryonic and paralarval statolith for Dosidicus gigas from different regions. Cross-validated classification rate Statolith Embryonic

Paralarval

Region Costa Rica Peru Chile Costa Rica Peru Chile

Costa Rica %

Peru %

Chile %

Final %

60.0 3.8 8.7 60.0 7.7 8.7

30.0 65.4 34.8 40.0 53.8 43.5

10.0 30.8 56.5 0.0 38.5 47.8

61.0

52.5

Table 6. Standardized canonical discriminant function (DF) coefficients for Function 1 and Function 2 for each signature/Ca used in discriminant function analysis for Dosidicus gigas among the three sampling regions. Coefficients represent the relative contribution of each signature/Ca to each DF. Statolith

Signature

Embryonic

Na/Ca Mg/Ca Ba/Ca K/Ca Zn/Ca Ba/Ca

Paralarval

animals were separated for much of their life history but aggregated to spawn. In this case, the difference in elemental signature from different specimens did not result from different populations but rather from the different water properties that each group experienced. Instead, the elemental signatures of hard structures formed during the early stages subsequent to spawning provide strong evidence of natal origin and can be used to define populations. Dosidicus gigas, like other Ommastrephids, has a typical statolith microstructure composed of nucleus (N), postnuclear zone (PN), dark zone (DZ) and peripheral zone (PZ), which generally corresponds to major ontogenetic stages (Arkhipkin, 2005). The N is the area within the hatching increment (natal ring) associated with the embryonic stage, and the PN is the area next to the natal ring corresponding to the © 2015 John Wiley & Sons Ltd, Fish. Oceanogr., 24:4, 335–346.

DF1

DF2

0.625 0.300 0.808 0.554 0.597 0.961

0.508 0.864 0.541 0.821 0.329 0.302

paralarval phase (Liu et al., 2011). Therefore, in this study, the estimated age of embryonic statolith is zero (Table 1) because there was no growth increment deposit before Ommastrephidae squid hatching (Arkhipkin, 2005). The age of paralarval statolith (Table 1) are similar to previous findings reported by Liu (2012). According to this hypothesis, we analysed the elemental signatures in the statoliths formed in these two early stages to investigate the structure and natal origin of the D. gigas population. The cephalopod embryonic stage occurs before hatching when the capsule membrane of the embryo acts as an efficient shield preventing metals from being absorbed (Bustamante et al., 2002). During this stage, the elemental signature of the statolith’s nucleus is perhaps more likely to depend on brood squid and is less affected by external environmental factors because the composition of embryo foods from yolks is influenced by genetic factors (Zumholz, 2005). This hypothesis was supported in Kalish (1990), Yatsu et al. (1998) and Zumholz et al. (2007), who hypothesized

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Table 7. Cross-validated classification rate and values of Wilks’k on the basis of discriminant function analysis scores of multielemental signatures within embryonic and paralarval statolith for Dosidicus gigas from different hemisphere. Cross-validated classification rate Statolith

Hemisphere

Northern %

Southern %

Final %

Wilks’k

P

Embryonic

Northern Southern Northern Southern

60.0 10.2 70.0 8.2

40.0 89.8 30.0 91.8

84.7

0.655

0.000

88.1

0.529

0.000

Paralarval

Figure 3. Factorial Score plots of embryonic and paralarval statolith to compare multi-elemental signatures among sampling hemisphere using elements/Ca for Dosidicus gigas.

that the element values in statoliths at the embryonic period might not be because of ambient water but rather to the yolk sac. For this reason, in this study we can distinguish the adult D. gigas geographical population by analysing the nuclear statolith formed at the embryonic stage. An analogous study was completed for the California market squid Doryteuthis opalescens by Warner et al. (2009) who believed that spatial

differences of statolith’s core elemental signatures were distinct enough to identify populations. Squid at the paralarval stage, which follows the embryonic stage, have a poor swimming ability and tend to disperse with ocean currents. Information extracted from the elemental signatures of statoliths formed in this stage reflects the environment they experience. As expected, based on the assumption the SDA when using paralarval statolith showed a lower correct reclassification rate than that for embryonic statoliths (Table 5). Paralarval individuals with different dispersal patterns, even if they come from the same origin, might undermine the ability to use elemental signatures in paralarval statolith to separate populations. Thus, elemental signatures in zone N (embryonic statolith) were considered to be a better natural tag than those in zone PN (paralarval statolith), although both of them could be used as a proxy for distinguishing different geographical groups. Based on the SDA results, squid from the Costa Rican, Peruvian and Chilean waters could be separated, to some extent, by multi-elemental signature analyses especially for embryonic statoliths. Ba contributed the most variation to separate Costa Rican individuals from Peru and Chile (Fig. 2), which can be seen from significantly higher Ba/Ca in the statoliths from the Costa Rican waters (Table 4), coupled with the values of canonical coefficients (Table 6). However, this significantly higher Ba value was not found in the whole statolith reported by Liu et al. (2013). This is because the elemental signatures in whole statoliths for D. gigas were mean values representing the integrated information they experienced. Additionally, although there was considerable overlap (Fig. 2), squid from Peru and Chile could be separated from each other most clearly by Mg in embryonic statoliths and by K and Zn in paralarval statoliths (Table 5). Nesis (1983) proposed that D. gigas spawns in the eastern tropical Pacific and then migrates to feed at a higher latitude in both hemispheres, which mean that the squid from the southern and northern hemisphere © 2015 John Wiley & Sons Ltd, Fish. Oceanogr., 24:4, 335–346.


share the same natal origin. However, PCA and SDA analysis using data from the northern group (Costa Rica) and the southern group (Peru and Chile) show that they were significantly separated. This gave us a clearly contrasting view that squid from the southern and northern hemispheres should have different natal origins. Such a conclusion is consistent with Clarke and Paliza (2000) who defined D. gigas as ‘northern’ and ‘southern’ migration-based stocks, although its intra-specific structures are complicated and no consensus has been reached by scientists to date. These two migration-based populations were later verified by Sandoval-Castellanos et al. (2007, 2010) and Staaf et al. (2010) using a molecular method, and they believed that the two distinct genetic groups were separated by the equatorial currents and counter currents as well as a prominent oxygen minimum zone (OMZ) in the equator area. The scenario is consistent with the discriminant function plots (Fig. 3), which suggest that squid from the northern hemisphere experience significantly different oceanographic environments from those in the southern hemisphere, and the factorial score plots (Fig. 2), which indicate that squid from Peru and Chile suffer an analogous oceanographic environment during their early ontogeny. In the eastern Pacific Ocean, the surface oceanography is characterized by two low velocity boundary current systems (the California Current and the Humboldt Current), three equatorial currents (the South Equatorial Current, the Equatorial Counter Current and the North Equatorial Current) and several upwelling regions (the Gulf of Tehuantepec, the Costa Rica Dome and the Coast of Peru), properties of which are greatly influenced by the El Ni~ no-Southern Oscillation (ENSO) (Anderson and Rodhouse, 2001; Fernandez-Alamo and F€arber-Lorda, 2006; Lavın et al., 2006; Radenac et al., 2012). However, our study area in the northern hemisphere is mainly influenced by the Costa Rica Dome with a prevalence of strong upwelling, and the southern hemisphere is controlled by the Humboldt Current with a prevalence of winddriven upwelling (Fiedler and Talley, 2006). Oceanographic conditions (e.g., temperature, salinity and currents) coupled with biological parameters (especially spawning ground and food availability) have been shown to be related to jumbo flying squid movements and abundances (Rodhouse, 2001; Waluda et al., 2004b; Sandoval-Castellanos et al., 2010). Thus, the high variability of the environmental conditions in the Eastern Pacific affects the population structure and geographical distribution of D. gigas, mainly in the early stages that are dispersed by the prevailing currents. © 2015 John Wiley & Sons Ltd, Fish. Oceanogr., 24:4, 335–346.

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LA-ICP-MS analysis results showed that Ba/Ca both in embryonic and paralarval statoliths differed significantly between the two hemispheric samples. Ba/Ca was considered as an indicator element for upwelling events or nutrient distribution in cephalopods (Zumholz et al., 2007). For example, Arkhipkin et al. (2004) suggested that intensification of upwelling must have been responsible for the elevated levels of Ba in L. gahi statoliths collected from the shelf waters around the Falkland Islands. Based on this hypothesis, the significantly higher Ba/Ca in D. gigas from the northern hemisphere further proves that they must experience a strong upwelling water mass during their embryonic phase. The Costa Rica Dome is one of the most dominant water masses in the northern tropical Pacific Ocean with a prevalence of strong upwelling, and is supposed to be a spawning ground for D. gigas based on the observed aggregation of mature adult squid and the occurrence of paralarvae (Vecchione, 1999; Ichii et al., 2002; Chen et al., 2013). Thus, the Costa Rica Dome might be the spawning ground of sampled squid from the northern hemisphere, although a previous study defined the water off Mexico as the northern population natal origin (Staaf et al., 2013). A substantially higher Ba/Ca ratio was also observed in paralarval statoliths from Costa Rica (P < 0.05), indicating that paralarvae remained in the vicinity of the Costa Rica Dome for nutrients, which might be a result of the existence of special oceanographic features. In the vicinity of the Costa Rica Dome, the eastward-flowing, low energy, Equatorial Counter Current provides a mechanism for paralarval retention and heightened productivity in the area providing abundant food for paralarval squid (Anderson and Rodhous, 2001). Additionally, we found no difference in the correct classification rate in the SDA between embryonic and paralarval statolith, which directly confirmed the hypothesis that paralarvae occurred in the same waters with spent adults in the Costa Rican waters. Thus, the sampling locations adjacent to the Costa Rica Dome are not only putative spawning grounds but also nursery grounds, as strong upwelling brings nutrients to the surface water to provide enough food for paralarval squid. Significantly lower Ba/Ca ratios in embryonic statoliths for squid from Peru and Chile compared to those from Costa Rica indicated that the southern population experienced a relatively weak upwelling current. Meanwhile, a higher misclassification rate in the SDA between Peru and Chile revealed that D. gigas from the two places might have a similar natal origin. The Humboldt Current, the dominant current in the

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southeastern Pacific Ocean, is slow and broad, which must be responsible for the elemental signatures incorporated for the squid from both places (Chavez et al., 2008). Such a conclusion is consistent with the ~ez et al. (2011), who genetic view presented by Iban concluded that there was a single, large population in the Humboldt Current System. Moreover, they suggested that demographic population expansion in the currents is consistent with the oceanographic changes associated with the last glacial–interglacial transition. Sandoval-Castellanos et al. (2007) recommended that currents may partially explain the population interchange between Chile and Peru. They believed that the Chile population may have originated in the Peruvian waters and migrates to Chile by the countercurrents of the Peru Currents. Previous studies inferred that the jumbo squid in the southern hemisphere might spawn in tropical waters off the coast of northern Peru (Tafur et al., 2001; Sakai et al., 2008), where higher primary production provides nourishing and plentiful food for paralarval squid (Fiedler and Talley, 2006; Montecino and Lange, 2009). The differences in cross-validation between embryonic and paralarval statoliths, in this study, are mostly attributed to misclassification rates for Peruvian and Chilean squids rather than Costa Rican individuals, which can be seen from the variation in the correct classification rate for each of the separated groups (Table 5). This at least made us conclude that, unlike the Costa Rican Dome waters, the paralarvae of D. gigas from the Peruvian and Chilean waters were advected away from their natal source by oceanic currents. If the coastal water of northern Peru was indeed the spawning ground as concluded above, the paralarvae from the southern hemisphere must drift northward by the Humboldt Current rather than stay on the spawning ground for food. This conclusion is consistent with the view proposed by Anderson and Rodhouse (2001). In addition, they also suggested that juvenile squid are ultimately carried to the west of the South Equatorial Current and adults who remain in this tropical area grow to a small size, but others migrate southward to further south of Peru and Chile. In conclusion, all measured signatures were significantly different between embryonic and paralarval statoliths, except for Sr, Ba and Pb. Na and Ba within embryonic statoliths and Zn and Ba within paralarval statoliths where significant differences were found in the three regions. A significantly higher Ba/Ca ratio in the statoliths collected from Costa Rica was found, compared with those from Peru and Chile, which might result from the prevalence of strong upwelling

in Costa Rica, and a similar Ba/Ca between Peru and Chile might be influenced by the Humboldt Current. Elemental signatures in embryonic statoliths were considered to be a better natural tag than those in paralarval statoliths, although both of them could be used as a proxy for distinguishing different groups. The paralarvae of the same populations followed different dispersal trajectories, which might be responsible for their differences. We prefer to believe that the northern (Costa Rica) and southern (Peru and Chile) groups potentially have different natal origins and migration patterns. The northern population was putative spawning adjacent to the Costa Rica Dome, and the Equatorial Counter Current meant that the paralarvae remained in the spawning ground for food. In contrast, the southern population might spawn in the coastal waters off northern Peru, and the paralarvae would be carried northward rather than stay at the birth place for the nursery. Overall, the jumbo squid life cycle, especially at early ontogeny stage, is susceptible to the variation of oceanography, particularly the ENSO. For instance, during normal and cold years, intensive offshore transport carries paralarvae far away from the coast into the large open sea area, but during warm years, a weak current retains the paralarvae near the shelf. Therefore, considering higher plasticity of the squid and specificity of the study region, it is important for future studies to assess how and where the squid might move as the climate changes. ACKNOWLEDGEMENTS This work was funded by the National Science Foundation of China (NSFC 41306127 and NSFC41276156), the National Science Foundation of Shanghai (No.13ZR1419700), the Innovation Program of Shanghai Municipal Education Commission (No.13YZ091), the PhD Programs Foundation of Ministry of Education of China (No.20133104120001) and the Shanghai Universities First-class Disciplines Project (Fisheries A). Yong Chen’s involvement is supported by the SHOU International Center for Marine Sciences (No. 3606120001). REFERENCES Anderson, C.I.H. and Rodhous, P.G. (2001) Life cycles, oceanography and variability ommastrephid squid in variable oceanographic environments. Fish. Res. 54:133–143. Arkhipkin, A.I. (2005) Statolith as ‘balck boxes’(life recorders) in squid. Mar. Freshw. Res. 56:573–583. Arkhipkin, A.I., Campana, S.E., FitzGerald, J. and Thorrold, S.R. (2004) Spatial and temporal variation in elemental



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