Cite this paper:
Jianzhong GUO, Dan LIU, Chi ZHANG, Yongjun TIAN, Zhixin LI. Using statolith shape analysis to identify five commercial Loliginidae squid species in Chinese waters[J]. Journal of Oceanology and Limnology, 2021, 39(3): 1160-1168

Using statolith shape analysis to identify five commercial Loliginidae squid species in Chinese waters

Jianzhong GUO1, Dan LIU1, Chi ZHANG1, Yongjun TIAN1,2,3, Zhixin LI1
1 Fisheries College, Ocean University of China, Qingdao 266003, China;
2 Frontiers Science Center for Deep Ocean Multispheres and Earth System(FDOMES), Ocean University of China, Qingdao 266100, China;
3 Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266071, China
Abstract:
Identification of squids in the family Loliginidae is a time-consuming exercise because of the highly overlapping distributions of species and their overall similarity (fin shape and size, sucker ring dentition, and color). Identifying squid based on statolith morphology is considered more accurate than identifying species based on beaks or gladius morphology. We report and compare the statolith shape of five commercially Loliginidae squid (Uroteuthis (Photololigo) duvaucelii, U. edulis, U. chinensis, Loliolus beka, L. japonica) to determine how well these structures discriminate species. Based on statolith morphology, variation in the lateral and dorsal domes enables an 84.8% success rate at classifying species. Environmental factors correlate with statolith shape, and for vertically migrating squid, statolith relative size decreases with increased depth of habitation. Statolith morphology can be used to effectively and accurately identify species of Loliginidae squid occurring in Chinese waters, and may prove valuable for identifying and managing squid resources.
Key words:    statolith shape analysis|Loliginidae squid|fishery management|Chinese waters   
Received: 2020-03-30   Revised: 2020-05-25
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Articles by Jianzhong GUO
Articles by Dan LIU
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Articles by Yongjun TIAN
Articles by Zhixin LI
References:
Anderson C I H, Rodhouse P G. 2001. Life cycles, oceanography and variability:ommastrephid squid in variable oceanographic environments. Fisheries Research, 54(1):133-143, https://doi.org/10.1016/S0165-7836(01)00378-2.
Arkhipkin A I, Bizikov V A. 2000. Role of the statolith in functioning of the acceleration receptor system in squids and sepioids. Journal of Zoology, 250(1):31-55, https://doi.org/10.1111/j.1469-7998.2000.tb00575.x.
Arkhipkin A I, Rodhouse P G K, Pierce G J, Sauer W, Sakai M, Allcock L, Arguelles J, Bower J R, Castillo G, Ceriola L, Chen C S, Chen X J, Diaz-Santana M, Downey N, González A F, Amores J G, Green C P, Guerra A, Hendrickson L C, Ibáñez C, Ito K, Jereb P, Kato Y, Katugin O N, Kawano M, Kidokoro H, Kulik V V, Laptikhovsky V V, Lipinski M R, Liu B L, Mariátegui L, Marin W, Medina A, Miki K, Miyahara K, Moltschaniwskyj N, Moustahfid H, Nabhitabhata J, Nanjo N, Nigmatullin C M, Ohtani T, Pecl G, Perez J A A, Piatkowski U, Saikliang P, Salinas-Zavala C A, Steer M, Tian Y J, Ueta Y, Vijai D, Wakabayashi T, Yamaguchi T, Yamashiro C, Yamashita N, Zeidberg L D. 2015. World squid fisheries. Reviews in Fisheries Science & Aquaculture, 23(2):92-252, https://doi.org/10.1080/23308249.2015.1026226.
Arkhipkin A I. 2003. Towards identification of the ecological lifestyle in nektonic squid using statolith morphometry.Journal of Molluscan Studies, 69(3):171-178, https://doi.org/10.1093/mollus/69.3.171.
Arkhipkin A I. 2005. Statoliths as ‘black boxes’ (life recorders) in squid. Marine and Freshwater Research, 56(5):573-583, https://doi.org/10.1071/MF04158.
Belkin I M. 2009. Rapid warming of large marine ecosystems.Progress in Oceanography, 81(1-4):207-213, https://doi.org/10.1016/j.pocean.2009.04.011.
Borges T C. 1995. Discriminate analysis of geographic variation in hard structures of Todarodes saguttatus(Lamarek 1798) from North Atlantic Ocean. ICES Marine Science Symposium, (199):433-440.
Breiman L. 2001. Random forests. Machine Learning, 45:5-32, https://doi.org/10.1023/A:1010933404324.
Cadrin S X, Kerr L A, Mariani S. 2014. Stock Identification Methods:Applications in Fishery Science. 2nd edn.Academic Press, London. p.1-10.
Cadrin S X, Silva V M. 2005. Morphometric variation of yellowtail flounder. ICES Journal of Marine Science, 62(4):683-694, https://doi.org/10.1016/j.icesjms.2005.02.006.
Chapela M J, Sotelo C G, Pérez-Martín R I. 2003. Molecular identification of cephalopod species by FINS and PCRRFLP of a cytochrome b gene fragment. European Food Research and Technology, 217(6):524-529, https://doi.org/10.1007/s00217-003-0788-y.
Chen X J, Wang G Y, Qian W G. 2013. Important Economic Resources and Fisheries of Cephalopod in Coast of China. Science Press, Beijing, China. p.67, 101-120. (in Chinese)
Clarke M R. 1978. The cephalopod statolithan-introduction to its form. Journal of the Marine Biological Association of the United Kingdom, 58(3):701-712, https://doi.org/10.1017/S0025315400041345.
Crandall K A, Bininda-Emonds O R P, Mace G M, Wayne R K. 2000. Considering evolutionary processes in conservation biology. Trends in Ecology & Evolution, 15(7):290-295, https://doi.org/10.1016/S0169-5347(00)01876-0.
de la Chesnais T, Fulton E A, Tracey S R, Pecl G T. 2019. The ecological role of cephalopods and their representation in ecosystem models. Reviews in Fish Biology and Fisheries, 29(2):313-334, https://doi.org/10.1007/s11160-019-09554-2.
Díaz-Santana-Iturrios M, Salinas-Zavala C A, GranadosAmores J, de la Cruz-Agüero J, García-Rodríguez F J. 2019. Taxonomic considerations of squids of the family Loliginidae (Cephalopoda:Myopsida) supported by morphological, morphometric, and molecular data.Marine Biodiversity, 49(5):2 401-2 409, https://doi.org/10.1007/s12526-019-00979-3.
Dommergues J L, Neige P, Boletzky S V. 2000. Exploration of morphospace using procrustes analysis in statoliths of cuttlefish and squid (Cephalopoda:Decabrachia)-evolutionary aspects of form disparity. The Veliger, 43(3):265-276.
Dong Z Z. 1988. Fauna Sinica, Phylum Mollusca, Class Cephalopoda. Science Press, Beijing, China. p.111-114.(in Chinese)
Dong Z Z. 1993. Morphological comparison of the several structures of cephalopods. Acta Zoologica Sinica, 39(4):348-354. (in Chinese with English abstract)
Du T F. 2016. Resources Assessment for Cephalopod in Offshore Water of China and Classification of Genus Level of Squids. Shanghai Ocean University, Shanghai, China. p.47. (in Chinese with English abstract)
Fang Z, Liu B L, Li J H, Su H, Chen X J. 2014. Stock identification of neon flying squid (Ommastrephes bartramii) in the North Pacific Ocean on the basis of beak and statolith morphology. Scientia Marina, 78(2):239-248, https://doi.org/10.3989/scimar.03991.06A.
Goud J, De Heij A. 2012. Mediterranean Sepiola aurantiaca Jatta, 1896, versus the NE Atlantic Sepiola pfefferi Grimpe, 1921 (Cephalopoda, Sepiolinae). Basteria, 76(1-3):1-11.
Green C P, Robertson S G, Hamer P A, Virtue P, Jackson G D, Moltschaniwskyj N A. 2015. Combining statolith element composition and Fourier shape data allows discrimination of spatial and temporal stock structure of arrow squid(Nototodarus gouldi). Canadian Journal of Fisheries and Aquatic Sciences, 72(11):1 609-1 618, https://doi.org/10.1139/cjfas-2014-0559.
Hanlon R T, Messenger J B. 1996. Cephalopod Behaviour.Cambridge University Press, Cambridge, England. 232p.
Ho S C. 2005. Taxonomic Study of the Taiwan Inshore Squids.Taiwan Ocean University, Keelung, China. 93p. (in Chinese with English abstract)
Hu F F, Chen X J, Liu B L, Li J H. 2017. Review on identification of cephalopods classification. Marine Fisheries, 39(1):110-120. (in Chinese with English abstract)
Jereb P, Roper C F E. 2006. Cephalopods of the Indian Ocean.A review. Part I. Inshore squids (Loliginidae) collected during the international Indian Ocean Expedition.Proceedings of the Biological Society of Washington, 119(1):91-136, https://doi.org/10.2988/0006-324x(2006) 119[91:cotioa]2.0.co;2.
Jereb P, Roper C F E. 2010. Cephalopods of the world. An annotated and illustrated catalogue of cephalopod species known to date. Volume 2. Myopsid and Oegopsid squids.In:FAO Species Catalogue for Fishery Purposes. Rome, FAO.p. 38-117.
Jiang L H, Kang L S, Wu C W, Chen M, Lü Z M. 2018. A comprehensive description and evolutionary analysis of 9 Loliginidae mitochondrial genomes. Hydrobiologia, 808(1):115-124, https://doi.org/10.1007/s10750-017-3377-y.
Jin Y, Liu B L, Chen X J, Staples K. 2018. Morphological beak differences of loliginid squid, Uroteuthis chinensis and Uroteuthis edulis, in the northern South China Sea.Journal of Oceanology and Limnology, 36(2):559-571, https://doi.org/10.1007/s00343-017-6285-0.
Jin Y, Liu B L, Li J H, Chen X J. 2017. Identification of three common Loliginidae squid species in the South China Sea by analyzing hard tissues with geometric outline method.Journal of Ocean University of China, 16(5):840-846, https://doi.org/10.1007/s11802-017-3218-7.
Libungan L A, Pálsson S. 2015. ShapeR:an R package to study otolith shape variation among fish populations. PLoS One, 10(3):e0121102, https://doi.org/10.1371/journal.pone.0121102.
Lombarte A, Cruz A. 2007. Otolith size trends in marine fish communities from different depth strata. Journal of Fish Biology, 71(1):53-76, https://doi.org/10.1111/j.1095-8649.2007.01465.x.
Lombarte A, Rufino M M, Sánchez P. 2006. Statolith identification of Mediterranean Octopodidae, Sepiidae, Loliginidae, Ommastrephidae and Enoploteuthidae based on warp analyses. Journal of the Marine Biological Association of the United Kingdom, 86(4):767-771, https://doi.org/10.1017/S0025315406013683.
Lombarte A, Sanchez P, Morales-Nin B. 1997. Intraspecific shape variability in statoliths of three cephalopod species.Vie et Milieu-Life and Environment, 47(2):165-169.
Moustahfid H. 2002. Age and growth of arrow squid Todarodes sagittatus (Cephalopoda:Ommastrephidae) sampled in summer in Atlantic Moroccan waters. Bulletin of Marine Science, 71(1):535-543.
Natsukari Y, Nakanose T, Oda K. 1988. Age and growth of loliginid squid Photololigo edulis (Hoyle, 1885). Journal of Experimental Marine Biology and Ecology, 116(2):177-190, https://doi.org/10.1016/0022-0981(88)90054-8.
Okutani T. 2015. Cuttlefishes and Squids of the World (New Edition). Tokai University Press, Tokyo, Japan. p.73-227.(in Japanese)
Pang Y M, Tian Y J, Fu C H, Wang B, Li J C, Ren Y P, Wan R. 2018. Variability of coastal cephalopods in overexploited China Seas under climate change with implications on fisheries management. Fisheries Research, 208:22-33, https://doi.org/10.1016/j.fishres.2018.07.004.
Parisi-Baradad V, Manjabacas A, Lombarte A, Olivella R, Chic O, Piera J, García-Ladona E. 2010. Automated Taxon Identification of Teleost fishes using an otolith online database-AFORO. Fisheries Research, 105(1):13-20, https://doi.org/10.1016/j.fishres.2010.02.005.
Pecl G T, Jackson G D. 2008. The potential impacts of climate change on inshore squid:biology, ecology and fisheries.Reviews in Fish Biology and Fisheries, 18(4):373-385, https://doi.org/10.1007/s11160-007-9077-3.
Pecl G T, Moltschaniwskyj N A, Tracey S R, Jordan A R. 2004.Inter-annual plasticity of squid life history and population structure:ecological and management implications.Oecologia, 139(4):515-524, https://doi.org/10.1007/s00442-004-1537-z.
Pérez-del-Olmo A, Montero F E, Fernández M, Barrett J, Raga J A, Kostadinova A. 2010. Discrimination of fish populations using parasites:random forests on a ‘predictable’ host-parasite system. Parasitology, 137(12):1 833-1 847, https://doi.org/10.1017/S0031182010000739.
Reig-Bolaño R, Marti-Puig P, Lombarte A, Soria J A, ParisiBaradad V. 2010. A new otolith image contour descriptor based on partial reflection. Environmental Biology of Fishes, 89(3-4):579-590, https://doi.org/10.1007/s10641-010-9700-3.
Ren Y, Hou R, Feng H, Wang L, Feng C L. 2015. DNA analysis methods in species identification. Shaanxi Journal of Agricultural Sciences, 61(10):61-64. (in Chinese)
Sin Y W, Yau C, Chu K H. 2009. Morphological and genetic differentiation of two loliginid squids, Uroteuthis(Photololigo) chinensis and Uroteuthis (Photololigo) edulis (Cephalopoda:Loliginidae), in Asia. Journal of Experimental Marine Biology and Ecology, 369(1):22-30, https://doi.org/10.1016/j.jembe.2008.10.029.
Smith P J, Robertson S G, Horn P L, Bull B, Anderson O F, Stanton B R, Oke C S. 2002. Multiple techniques for determining stock relationships between orange roughy, Hoplostethus atlanticus, fisheries in the eastern Tasman Sea. Fisheries Research, 58(2):119-140, https://doi.org/10.1016/s0165-7836(01)00389-7.
Strobl C, Malley J, Tutz G. 2009. An introduction to recursive partitioning:rationale, application, and characteristics of classification and regression trees, bagging, and random forests. Psychological Methods, 14(4):323-348, https://doi.org/10.1037/a0016973.
Vignon M, Morat F. 2010. Environmental and genetic determinant of otolith shape revealed by a non-indigenous tropical fish. Marine Ecology Progress Series, 411:231-241, https://doi.org/10.3354/meps08651.
Yang L L, Jiang Y Z, Liu Z L, Lin N, Li S F, Cheng J H. 2012.Analysis of beak morphology of Loligo beka in the East China Sea. Journal of Fishery Sciences of China, 19(4):586-593, https://doi.org/10.3724/SP.J.1118.2012.00586.(in Chinese with English abstract)
Zhang C, Ye Z J, Li Z G, Wan R, Ren Y P, Dou S Z. 2016.Population structure of Japanese Spanish mackerel Scomberomorus niphonius in the Bohai Sea, the Yellow Sea and the East China Sea:evidence from random forests based on otolith features. Fisheries Science, 82(2):251-256, https://doi.org/10.1007/s12562-016-0968-x.
Zhao B, Liu J H, Song J J, Cao L, Dou S Z. 2017. Evaluation of removal of the size effect using data scaling and elliptic Fourier descriptors in otolith shape analysis, exemplified by the discrimination of two yellow croaker stocks along the Chinese coast. Chinese Journal of Oceanology and Limnology, 35(6):1 482-1 492, https://doi.org/10.1007/s00343-017-6012-x.
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