Abstract
Sepioteuthis lessoniana is a crucial squid species in fisheries and plays a critical role in marine ecosystems. At least two taxa of the squid species have been identified in the waters around Japan; however, the basic biological information of these taxa is limited. In this study, the taxa composition of Sepioteuthis was examined using molecular evidence, and the life-history traits and statolith shape of these taxa were analyzed to elucidate the potential population structure. A total of 142 squid samples were collected from six locations around Nagasaki (southwestern Japan) where high taxonomic diversity has been found previously. Three taxa (Sepioteuthis sp. 1, sp. 2, and sp. 2A) were identified based on the mitochondrial cytochrome oxidase c subunit I (COI) gene, among which Sepioteuthis sp. 2A was defined for the first time. Sepioteuthis sp. 2 was predominant in the region (average occurrence rate 84%), whereas Sepioteuthis sp. 1 was rare, with only two individuals found near Goto Islands. The mantle length composition, mantle length–body weight relationship, age structure, and average growth rates were similar between Sepioteuthis sp. 2 and sp. 2A. However, Sepioteuthis sp. 2 mainly hatched during summer (June–July), whereas Sepioteuthis sp. 2A hatched during winter (December–February). The statolith shapes of the squids were similar between the taxa, although slight differences were noted in the wing regions. The three taxa largely overlapped in a principal component analysis bi-plot based on variations extracted from five life-history traits. These results suggest that at least three taxa of Sepioteuthis inhabited the region, although few differences were found between them in life-history traits or statolith shapes that might be substantially influenced by regional oceanographic conditions. This study provides essential information on the population structure and connectivity of the squid, which is crucial in the context of conservation and management measures for fisheries.
Similar content being viewed by others
References
Abaunza P, Murta AG, Campbell N, Cimmaruta R, Comesaña AS, Dahle G, Gallo E, García Santamaría MT, Gordo LS, Iversen SA, MacKenzie K, Magoulas A, Mattiucci S, Molloy J, Nascetti G, Pinto AL, Quinta R, Ramos P, Ruggi A, Sanjuan A, Santos AT, Stransky C, Zimmermann C (2008) Stock identity of horse mackerel (Trachurus trachurus) in the Northeast Atlantic and Mediterranean Sea: integrating the results from different stock identification approaches. Fish Res 89:196–209
Anderson CIH, Rodhouse PG (2001) Life cycles, oceanography and variability: ommastrephid squid in variable oceanographic environments. Fish Res 54:133–143
Aoki M, Imai H, Naruse T, Ikeda Y (2008) Low genetic diversity of oval squid, Sepioteuthis cf. lessoniana (Cephalopoda: Loliginidae), in Japanese waters inferred from a mitochondrial DNA non-coding region. Pac Sci 62:403–411
Arkhipkin AI (2003) Towards identification of the ecological lifestyle in nektonic squid using statolith morphometry. J Molluscan Stud 69:171–178
Arkhipkin AI (2005) Statoliths as ‘black boxes’ (life recorders) in squid. Mar Freshw Res 56:573–583
Arkhipkin AI, Bizikov VA (2000) Role of the statolith in functioning of the acceleration receptor system in squids and sepioids. J Zool 250:21–55
Arkhipkin AI, Shcherbich ZN (2012) Thirty years’ progress in age determination of squid using statoliths. J Mar Bio Ass UK 92:1389–1398
Arkhipkin AI, Jereb P, Ragonese S (2000) Growth and maturation in two successive seasonal groups of the short-finned squid, Illex coindetii, from the Strait of Sicily (central Mediterranean) ICES. J Mar Sci 57:31–41
Arkhipkin AI, Campana SE, FitzGerald J, Thorrold SR (2004) Spatial and temporal variation in elemental signatures of statoliths from the Patagonian longfin squid (Loligo gahi). Can J Fish Aquat Sci 61:1212–1224
Arkhipkin AI, Rodhouse PGK, Pierce GJ, Sauer W, Sakai M, Allcock L, Arguelles J, Bower JR, Castillo G, Ceriola L, Chen C-S, Chen XJ, Diaz-Santana M, Downey N, González AF, Amores JG, Green CP, Guerra A, Hendrickson LC, Ibáñez C, Ito K, Jereb P, Kato Y, Katugin ON, Kawano M, Kidokoro H, Kulik VV, Laptikhovsky VV, Lipinski MR, Liu BL, Mariátegui L, Marin W, Medina A, Miki K, Miyahara K, Moltschaniwskyj N, Moustahfi H, Nabhitabhata J, Nanjo N, Nigmatullin CM, Ohtani T, Pecl G, Perez JAA, Piatkowski U, Saikliang P, Salinas-Zavala CA, Steer M, Tian YJ, Ueta Y, Vijai D, Wakabayashi T, Yamaguchi T, Yamashiro C, Yamashita N, Zeidberg LD (2015) World squid fisheries. Rev Fish Sci Aquat 23:92–252
Barcellos DD, Gasalla MA (2015) Morphology and morphometry of Doryteuthis plei (Cephalopoda: Loliginidae) statoliths from the northern shelf off São Paulo, southeastern Brazil. J Natu His 49:1305–1317
Begg G, Brown R (2000) Stock identification of haddock Melanogramus aeglefinus on Georges Bank based on otolith shape analysis. Trans Am Fish Soci 129:935–945
Begg GA, Waldman JR (1999) An holistic approach to fish stock identification. Fish Res 43:35–44
Begg G, Overholtz WJ, Munroe NJ (2000) The use of internal otolith morphometrics for identification of haddock (Melanogram aelefinus) stocks on Georges Bank. Fish Bull 99:1–14
Bettencourt V, Guerra A (2000) Growth increments and biomineralization process in cephalopod statoliths. J Exp Mar Bio Ecol 248:191–205
Boyle PR, Ngoile MAK (1993) Assessment of maturity state and seasonality of reproduction in Loligo forbesi (Cephalopoda: Loliginidae) from Scottish waters. In: Okutani T et al (eds) Recent advances in cephalopod fisheries biology. Tokai University Press, Tokyo, pp 37–48
Cadrin SX (2005) Morphometric landmarks. In: Cadrin SX et al (eds) Stock identification methods. Elsevier, San Diego, pp 153–172
Campana SE (2005) Otolith science entering the 21st century. Mar Freshw Res 56:485–495
Campana SE, Casselman JM (1993) Stock discrimination using otolith shape analysis. Can J Fish Aquat Sci 50:1062–1083
Campana SE, Thorrold SR (2001) Otoliths, increments, and elements: keys to a comprehensive understanding of fish populations? Can J Fish Aquat Sci 58:30–38
Cañás L, Stransky C, Schlickeisen J, Sampedro MP, Fariña AC (2012) Use of the otolith shape analysis in stock identification of anglerfish (Lophius piscatorius) in the Northeast Atlantic. ICES J Mar Sci 69:250–256
Carvalho GR, Nigmatullin CM (1998) Species identification and stock struckture analysis within the genus Illex. In: Rodhouse PG et al (eds) Squid recruitment dynamics: the genus Illex as a model, the commercial species and influences on variability. FAO Fisheries Technical Paper 376, Food and Agriculture Organization, Rome, pp 199–232
Castonguay M, Simard P, Gagnon P (1991) Usefulness of Fourier analysis of otolith shape for Atlantic mackerel (Scomber scombrus) stock discrimination. Can J Fish Aquat Sci 48:296–302
Chen C-S, Chen J-Y, Lin C-W (2015) Variation in life-history traits for micro-cohorts of Sepioteuthis lessoniana in the waters off northern Taiwan. Fish Sci 81:53–64
Cheng SH, Anderson FE, Bergman A, Mahardika GN, Muchlisin ZA, Dang BT, Calumpong HP, Mohamed KS, Sasikumar G, Venkatesan V, Barber PH (2014) Molecular evidence for co-occurring cryptic lineages within the Sepioteuthis cf. lessoniana species complex in the Indian and Indo-West Pacific Oceans. Hydrobiologia 725:165–188
Ching T-Y, Chen C-S, Wang C-H (2019) Spatiotemporal variations in life-history traits and statolith trace elements of Sepioteuthis lessoniana populations around northern Taiwan. J Mar Biol Ass UK 99:203–201
Clarke MR (1978) The cephalopod statolith: an introduction to its form. J Mar Biol Ass UK 58:701–712
Crampton JS (1995) Elliptic Fourier shape analysis of fossil bivalves: some practical considerations. Lethaia 28:179–186
Fang Z, Chen X, Su H, Staples K, Chen Y (2018) Exploration of statolith shape variation in jumbo flying squid, Dosidicus gigas, based on wavelet analysis and machine learning methods for stock classification. Bull Mar Sci 19:1465–1482
Forsythe JW (2004) Accounting for the effect of temperature on squid growth in nature: from hypothesis to practice. Mar Freshw Res 55:331–339
Forsythe JW (1993) A working hypothesis on how seasonal temperature change may impact the field growth of young cephalopods. In: Okutani T et al (eds) Recent advances in cephalopod fisheries biology. Tokai University Press, Tokyo, pp 133–143
Gillanders BM (2005) Using elemental chemistry of fish otoliths to determine connectivity between estuarine and coastal habitats. Estuar Coast Shelf Sci 64:47–57
Green CP, Robertson SG, Hamer PA, Virtue P, Jackson GD (2015) Combining statolith element composition and Fourier shape data allows discrimination of spatial and temporal stock structure of arrow squid (Nototodarus gouldi). Can J Fish Aquat Sci 72:1609–1618
Hatfield MCE (2000) Do some like it hot? Temperature as a possible determinant of variability in the growth of the Patagonian squid, Loligo gahi (Cephalopoda: Loliginidae). Fish Res 47:27–40
Hsiao C-D, Shen K-N, Ching T-Y, Wang Y-H, Ye J-J, Tsai S-Y, Wu S-C, Chen C-H, Wang C-H (2016) The complete mitochondrial genome of the cryptic “lineage A” big-fin reef squid, Sepioteuthis lessonaina (Cephalopoda: Loliginidae) in Indo-West Pacific. Mitochondrial DNA Part A 27:2433–2434
Imai H, Aoki M (2012) Genetic diversity and genetic heterogeneity of bigfin reef squid "Sepioteuthis lessoniana" species complex in northwestern Pacific Ocean. In: Caliskan M (ed) Analysis of genetic variation in animals. InTech, Croatia, pp 151–166
Iwata H, Ukai Y (2002) SHAPE: A computer program package for quantitative evaluation of biological shape based on elliptic Fourier descriptors. J Hered 93:384–385
Izuka T, Segawa S, Okutani T, Numachi K (1994) Evidence on the existence of three species in the oval squids Sepioteuthis lessoniana complex in Ishigaki Island, Okinawa, Southwestern Japan, by isozyme analysis. Jpn J Malacol 53:217–228
Izuka T, Segawa S, Okutani T (1996a) Biochemical study of the population heterogeneity and distribution of the oval squid Sepioteuthis lessoniana complex in southwestern Japan. Am Malacol Bull 12:129–135
Izuka T, Segawa S, Okutani T (1996b) Identification of three species in oval squid, Sepioteuthis lessoniana complex by chromatophore arrangements on the funnel. Jpn J Malacol 55:139–142
Jackson GD (1990) Age and growth of the tropical nearshore loliginid aquid Sepioteuthis lessoniana determined from statolith growth-ring analysis. Fish Bull 88:113–118
Jackson GD, Moltschaniwskyj NA (2001) Temporal variation in growth rates and reproductive parameters in the small near-shore tropical squid Loliolus noctiluca; is cooler better? Mar Ecol Prog Ser 218:167–177
Jackson GD, Moltschaniwskyj NA (2002) Spatial and temporal variation in growth rates and maturity in the Indo-Pacific squid Sepioteuthis lessoniana (Cephalopoda: Loliginidae). Mar Biol 140:747–754
Jereb P, Roper CFE (2010) Cephalopods of the world: an annotated and illustrated catalogue of cephalopod species known to date, volume 2. Myopsid and Oegopsid Squids. FAO Species Catalogue for Fishery Purposes, Food and Agriculture Organization, Rome
L’Abée-Lund JH (1988) Otolith shape discriminates between juvenile Atlantic salmon, Salmo salar, and brown trout, Salmo trutta. J Fish Biol 33:899–903
Lombarte A, Lleonart J (1993) Otolith size changes related with body growth, habitat depth and temperature. Environ Biol Fishes 37:297–306
McKeown NJ, Arkhipkin AI, Shaw PW (2015) Integrating genetic and otolith microchemistry data to understand population structure in the Patagonian Hoki (Macruronus magellanicus). Fish Res 164:1–7
Moreno A, Azevedo M, Pereira J, Pierce GJ (2007) Growth strategies in the squid Loligo vulgaris from Portuguese waters. Mar Biol Res 3:49–59
Morimoto A, Isoda Y, Tameishi T, Moriwaki S (2009) Seasonal variation in Tsushima warm current paths over the shelf off the San’in coast, Japan. Cont Shelf Res 29:1437–1447
Okutani T (1984) Life history of the oval squid, Sepioteuthis lessoniana. Saibai Giken 13:69–75 (In Japanese)
Onitsuka G, Yanagi T, Yoon J-H (2007) A numerical study on nutrient source in the suface layer of the Japan Sea using a coupled physical-ecosystem model. J Geophys Res 112:C05042
Pecl GT (2001) Flexible reproductive strategies in tropical and temperate Sepioteuthis squids. Mar Biol 138:93–101
Segawa S, Hirayana S, Okutani T (1993) Is Sepioteuthis lessoniana in Okinawa a single species? In: Okutani T et al (eds) Recent advances in cephalopod fisheries biology. Tokai University Press, Tokyo, pp 513–521
Semmens JM, Pecl GT, Gillanders BM, Waluda CM, Shea EK, Jouffre D, Ichii T, Zumholz K, Katugin ON, Leporati SC, Shaw PW (2007) Approaches to resolving cephalopod movement and migration patterns. Rev Fish Biol Fish 17:401–423
Shen K-N, Yen T-C, Chen C-H, Ye J-J, Hsiao C-D (2016) The complete mitochondrial genome of the cryptic “lineage B” big-fin reef squid, Sepioteuthis lessonaina (Cephalopoda: Loliginidae) in Indo-West Pacific. Mitochondrial DNA Part A 27:2100–2101
Stransky C, Murta AG, Schlickeiesn J, Zimmermann C (2008) Otolith shape analysis as a tool for stock separation of horse mackerel (Trachurus trachurus) in the Northeast Atlantic and Mediterranean. Fish Res 89:59–166
Swearer SE, Forrester GE, Steele MA, Brooks AJ, Lea DW (2003) Spatio-temporal and interspecific variation in otolith trace-elemental fingerprints in a temperate estuarine fish assemblage. Estuar Coast Shelf Sci 56:1111–1123
Sweeney MJ, Roper CFE, Mangold KM, Clarke MR, Boletzky SV (1992) “Larval” and juvenile cephalopods: a manual fortheir identification. Smithson Contrib Zool 513:1–28
Takahashi T, Nakata H, Hirano K, Matsuoka K, Iwataki M, Yamaguchi H, Kasuya T (2009) Upwelling of oxygen-depleted water (Sumishio) in Omura Bay, Japan. Oceanography 65:113–120
Thorpe JP, Solé-Cava AM, Watts PC (2000) Exploited marine invertebrates: genetics and fisheries. Hydrobiologia 420:165–184
Tomano S, UetaY KN, Umino T (2015a) Stock identification and spawning depth of oval squid Sepioteuthis spp. in Tanega-shima Island inferred by DNA markers. Aqua Sci 63:39–47 (In Japanese with English abstract)
Tomano S, Sanchez G, Ueno K, Ueta Y, Ohara K, Umino T (2015b) Microsatellite DNA variation of oval squid, Sepioteuthis sp. 2 reveals a single fishery stock on the coastline of mainland Japan. Fish Sci 81:839–847
Tomano S, Sanchez G, Kawai K, Kasaoka N, Ueta Y, Umino T (2016) Contribution of Sepioteuthis sp. 1 and Sepioteuthis sp. 2 to oval squid fishery stocks in western Japan. Fish Sci 82:585–596
Tuset VM, Lozano IJ, González JA, Pertusa JF, García-Díaz MM (2003) Shape indices to identify regional differences in otolith morphology of comber, Serranus cabrilla (L., 1758). J App Ichthyol 19:88–93
Wang K-Y, Chang K-Y, Liao C-H, Lee M-A, Lee K-T (2013) Growth strategies of the swordtip squid, Uroteuthis edulis, in response to environmental changes in the southern East China Sea. A cohort analysis. Bull Mar Sci 89:677–698
Ward RD (2000) Genetics in fisheries management. Hydrobiologia 420:191–201
Xavier JC, Allcock AL, Cherel Y (2015) Future challenges in cephalopod research. J Mar Biol Ass UK 95:999–1015
Yamaguchi T, Takayama K, Hirose N, Matsuyama M (2020) Relationship between empirical water temperature and spring characteristics of swordtip squid (Uroteuthis edulis) caught in the eastern Tsushima Strait. Mar Biol Res 16:93–102
Acknowledgements
We are grateful to the staff of Nagasaki Kakuyo High School and Nomozaki Sanwa Fishery Cooperative Association for their assistance with the squid sample collection. The critical suggestions and discussion provided by Professor Yutaka Natsukari at Nagasaki University are highly appreciated. We also thank the Marine Biology Lab at Nagasaki University for offering essential funds and assistance to T-YC during her PhD program for both Nagasaki University and National Taiwan Ocean University. This manuscript was edited by Wallace Academic Editing. Constructive comments from two anonymous referees and the Editor were highly appreciated.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Ching, TY., Chen, CS., Yagishita, N. et al. Variations in life-history traits and statolith shape for Sepioteuthis spp. in the waters off southwestern Japan. Fish Sci 87, 173–185 (2021). https://doi.org/10.1007/s12562-020-01485-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12562-020-01485-3