Abstract
Shape descriptors of sagittal otoliths were applied to the identification of four sympatric species of the genus Sebastes (Sebastes schlegeli, S. hubbsi, S. nudus and S. thompsoni) inhabiting the coastal reefs of the Bohai Sea and the Yellow Sea, northwest Pacific. Canonical discriminate analysis of standard length-corrected otolith shape variables (a combination of shape indices and elliptic Fourier coefficients) was demonstrated to be a useful tool for species identification with a high overall classification success of 96.6 %. An otolith morphological tree based on hierarchical average linkage cluster analysis indicated the closest proximity was between S. hubbsi and S. nudus. The otolith morphological affinities coincide well with the phylogenetic relationships reported among these species, which indicates the potential to use otolith morphology to establish phylogenetic relationships in this genus. In addition, ecomorphological comparisons suggest that the otolith shapes might be influenced by several ecological and environmental components such as depth, body color and substrate type. Among the environmental factors, depth could be the most comprehensive factor associated with the inter-specific variations of otolith morphology.
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References
Aguirre H, Lombarte A (1999) Ecomorphological comparisons of sagittae in Mullus barbatus and M. surmuletus. J Fish Biol 55(1):105–114
Aleev YG (1969) Function and gross morphology in fish. Israel Program for Scientific Translations, Jerusalem
An HS, Park JY, Kim M-J, Lee EY, Kim KK (2009) Isolation and characterization of microsatellite markers for the heavily exploited rockfish Sebastes schlegeli, and cross-species amplification in four related Sebastes spp. Conserv Genet 10(6):1969–1972
Arellano R, Hamerlynck O, Vincx M, Mees J, Hostens K, Gijselinck W (1995) Changes in the ratio of the sulcus acusticus area to the sagitta area of Pomatoschistus minutus and P. lozanoi (Pisces, Gobiidae). Mar Biol 122(3):355–360
Boehlert GW, Kusakari M, Shimizu M (1986) Energetics during embryonic development in kurosoi, Sebastes schlegeli hilgendorf. J Exp Mar Biol Ecol 101(3):239–256
Bunke C, Hanel R, Trautner J (2013) Phylogenetic relationships among north Atlantic redfish (genus sebastes) as revealed by mitochondrial DNA sequence analyses. J Appl Ichthyol 29(1):82–92
Campana SE, Neilson JD (1985) Microstructure of fish otoliths. Can J Fish Aquat Sci 42(5):1014–1032
Chen L (1985) A study of the Sebastes inermis species complex with delimitation of subgenus Mebarus (Pisces, scorpaenidae). J Taiwan Mus 38:23–37
Chen L (1986) Meristic variation in Sebastes (Scorpaenidae), with an analysis of character association and bilateral pattern and their significance in species separation. US Department of Commerce, National Oceanic and Atmospheric Administration, National Marine Fisheries Service
Cruz A, Lombarte A (2004) Otolith size and its relationship with colour patterns and sound production. J Fish Biol 65(6):1512–1525
Denton E (1990) Light and vision at depths greater than 200 metres. Light and life in the sea:127–148
Gauldie R, Nelson D (1988) Aragonite twinning and neuroprotein secretion are the cause of daily growth rings in fish otoliths. Comp Biochem Physiol A Physiol 90(3):501–509
Herler J (2007) Microhabitats and ecomorphology of coral - and coral rock - associated gobiid fish (teleostei: gobiidae) in the northern red sea. Mar Ecol 28(s1):82–94
Hyde JR, Vetter RD (2007) The origin, evolution, and diversification of rockfishes of the genus Sebastes (Cuvier). Mol Phylogenet Evol 44(2):790–811
Ingram T, Shurin JB (2009) Trait-based assembly and phylogenetic structure in northeast Pacific rockfish assemblages. Ecology 90(9):2444–2453
Iwata H, Ukai Y (2002) SHAPE: a computer program package for quantitative evaluation of biological shapes based on elliptic fourier descriptors. J Hered 93(5):384–385
Jin X (2006) Fauna Sinica, Osteichthyes, Scorpaeniformes. Science Press, Beijing (in Chinese)
Kai Y, Nakabo T (2013) Taxonomic review of the Sebastes pachycephalus complex (scorpaeniformes: scorpaenidae). Zootaxa 3637(5):541–560
Kai Y, Nakayama K, Nakabo T (2003) Molecular phylogenetic perspective on speciation in the genus Sebastes (scorpaenidae) from the northwest pacific and the position of Sebastes within the subfamily sebastinae. Ichthyol Res 50(3):239–244
Kai Y, Nakayama K, Nakabo T (2011) Genetic and morphological divergence within the Sebastes pachycephalus complex (scorpaeniformes: scorpaenidae). Ichthyol Res 58(4):333–343
Kendall AW Jr (2000) An historical review of sebastes taxonomy and systematics. Mar Fish Rev 62(2):1–23
Lenarz W (1986) The rockfish fishery, a California perspective. Rockfish: a focus for research. In: Proceedings of a California Sea Grant Workshop. University of California, Davis
Lleonart J, Salat J, Torres GJ (2000) Removing allometric effects of body size in morphological analysis. J Theor Biol 205(1):85–93
Lombarte A, Cruz A (2007) Otolith size trends in marine fish communities from different depth strata. J Fish Biol 71(1):53–76
Lombarte A, Lleonart J (1993) Otolith size changes related with body growth, habitat depth and temperature. Environ Biol Fish 37(3):297–306
Lombarte A, Popper AN (1994) Quantitative analyses of postembryonic hair cell addition in the otolithic endorgans of the inner ear of the European hake, Merluccius merluccius (gadiformes, teleostei). J Comp Neurol 345(3):419–428
Lombarte A, Palmer M, Matallanas J, Gómez-Zurita J, Morales-Nin B (2010) Ecomorphological trends and phylogenetic inertia of otolith sagittae in nototheniidae. Environ Biol Fish 89(3–4):607–618
Love MS, Yoklavich MM, Thorsteinson LK (2002) The rockfishes of the northeast Pacific. Press, Univ of California
Matsubara K (1936) Studies on the scorpaenoid fishes of Japan. III. On the external and internal characters of Sebastichthys longispinis Mihi and Sebastichthys brevispinis, nom. nov., compared. J Imp Fish Inst 31:79–96
Monteiro LR, Beneditto APMD, Guillermo LH, Rivera LA (2005) Allometric changes and shape differentiation of sagitta otoliths in sciaenid fishes. Fish Res 74(1):288–299
Nagasawa T (2001) Early life history of rockfishes (genus Sebastes) in the sea of Japan. Bull Jpn Sea Natl Fish Res Inst 51:1–132
Nelson JS (2006) Fishes of the World. John Wiley & Sons
Orr JW, Brown MA, Baker DC (2000) Guide to rockfishes (Scorpaenidae) of the genera Sebastes, Sebastolobus, and Adelosebastes of the Northeast Pacific Ocean. US Department of Commerce, National Oceanic and Atmospheric Administration, National Marine Fisheries Service, Alaska Fisheries Science Center
Parin N (2003) An annotated catalogue of fish-like vertebrates and fishes of the seas of Russia and adjacent countries: part 3. Orders perciformes (excluding suborders gobioidei, zoarcoidei and stichaeoidei) and tetraodontiformes. J Ichthyol 43(1):S1
Rocha L, Bowen B (2008) Speciation in coral- reef fishes. J Fish Biol 72(5):1101–1121
Rocha-Olivares A, Rosenblatt RH, Vetter RD (1999a) Molecular evolution, systematics, and zoogeography of the rockfish subgenus sebastomus (sebastes, scorpaenidae) based on mitochondrial cytochrome b and control region sequences. Mol Phylogenet Evol 11(3):441–458
Rocha-Olivares A, Kimbrell CA, Eitner BJ, Vetter RD (1999b) Evolution of a mitochondrial cytochrome b gene sequence in the species-rich genus sebastes (teleostei, scorpaenidae) and its utility in testing the monophyly of the subgenus sebastomu. Mol Phylogenet Evol 11(3):426–440
Rocha-Olivares A, Rosenblatt RH, Vetter RD (1999c) Cryptic species of rockfishes (sebastes: scorpaenidae) in the southern hemisphere inferred from mitochondrial lineages. J Hered 90(3):404–411
Rogers PH, Cox M (1988) Underwater sound as a biological stimulus. In: Sensory biology of aquatic animals. Springer, pp 131–149
Sadighzadeh Z, Tuset VM, Valinassab T, Dadpour MR, Lombarte A (2012) Comparison of different otolith shape descriptors and morphometrics for the identification of closely related species of Lutjanus spp. from the Persian Gulf. Mar Biol Res 8(9):802–814
Stransky C, MacLellan SE (2005) Species separation and zoogeography of redfish and rockfish (genus Sebastes) by otolith shape analysis. Can J Fish Aquat Sci 62(10):2265–2276
Tuset VM, Lombarte A, Assis CA (2008) Otolith atlas for the western Mediterranean, north and central eastern Atlantic. Sci Mar 72(S1):7–198
Tuset VM, Piretti S, Lombarte A, González JA (2010) Using sagittal otoliths and eye diameter for ecological characterization of deep-sea fish: Aphanopus carbo and A. intermedius from NE Atlantic waters. Sci Mar 74(4):807–814
Tuset VM, Parisi-Baradad V, Lombarte A (2013) Application of otolith mass and shape for discriminating scabbardfishes Aphanopus spp. In the north- eastern Atlantic ocean. J Fish Biol 82(5):1746–1752
Venerus LA, Ciancio JE, Riva-Rossi C, Gilbert-Horvath EA, Gosztonyi AE, Garza JC (2013) Genetic structure and different color morphotypes suggest the occurrence and bathymetric segregation of two incipient species of Sebastes off Argentina. Naturwissenschaften:1–14
Vignon M, Morat F (2010) Environmental and genetic determinant of otolith shape revealed by a non-indigenous tropical fish. Mar Ecol Prog Ser 411:231–241
Volpedo A, Echeverrı́a DD (2003) Ecomorphological patterns of the sagitta in fish on the continental shelf off Argentine. Fish Res 60(2):551–560
Volpedo AV, Tombari A, Echeverría DD (2008) Eco-morphological patterns of the sagitta of Antarctic fish. Polar Biol 31(5):635–640
Warrant E (2000) The eyes of deep–sea fishes and the changing nature of visual scenes with depth. Philos Trans R Soc Lond Ser B Biol Sci 355(1401):1155–1159
Wourms JP (1991) Reproduction and development of Sebastes in the context of the evolution of piscine viviparity. Environ Biol Fish 30(1–2):111–126
Yamada U, Shirai S, Irie T, Tokimura M, Deng S, Zheng Y, Li C, Kim Y, Kim Y (1995) Names and illustrations of fishes from the east China sea and the yellow sea. Overseas Fish Cooperation Found Tokyo:1–288
Zhang H, Zhang Y, Zhang Z, Gao T (2013) DNA barcodes of eight species in genus Sebastes. Biochem Syst Ecol 48:45–50
Acknowledgments
We greatly acknowledge the financial support of the Public Science and Technology Research Funds Projects of Ocean (Grant No. 201305030) and the Specialized Research Fund for the Doctoral Program of Higher Education (Grant No. 20120132130001). We thank Professor X. Q. Zeng for his great assistance in taking photographs of otoliths. All the four Sebastes species in this study are economic edible fish and not evaluated in the IUCN red list of threatened species. Although animal ethics approval is not required, all Sebastes experimental procedures were performed following the general animal ethical guidelines of Institutional Animal Ethical Committee (IAEC).
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Zhuang, L., Ye, Z. & Zhang, C. Application of otolith shape analysis to species separation in Sebastes spp. from the Bohai Sea and the Yellow Sea, northwest Pacific. Environ Biol Fish 98, 547–558 (2015). https://doi.org/10.1007/s10641-014-0286-z
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DOI: https://doi.org/10.1007/s10641-014-0286-z