Abstract
Validation of species using independent lines of evidence is sometimes desirable when their identification using only one approach is difficult or questionable. The identification of anchovies (Engraulidae) are often challenging based on morphology because closely related species exhibit only slight morphological differentiation. This study utilized morphological characteristics and DNA barcodes for identification and validation of anchovies in the Persian Gulf and Oman Sea. Based on morphology, we identified eight species: Thryssa hamiltonii, T. setirostris, T. vitrirostris, T. whiteheadi, T. dussumieri, Encrasicholina punctifer, E. pseudoheteroloba and Stolephorus indicus. A 658 bp region of mitochondrial cytochrome oxidase subunit I (COI) was generated for 53 specimens from these eight species. From these sequences, we built a Maximum Likelihood phylogenetic tree. In this tree, each species forms a monophyletic group confirming our initial morphological identification. In addition, we provided (and registered in GenBank) the first barcode sequences for T. whiteheadi, an endemic species of this region. Interspecies genetic distances were comprised between 0.168 to 0.275. The largest genetic distance was found between T. vitrirostris and S. indicus and the smallest between T. dussumieri and T. whiteheadi. This study successfully identified eight species of anchovies in the Persian Gulf and Oman Sea based on both morphological and molecular characters.
References
Ajmal Khan, S., Lyla, P.S., Akbar John, B., Prasanna Kuamr, C., Murugan, S. & Jalal, K.C.A. (2010) DNA barcoding of Stolephorus indicus, Stolephorus commersonnii and Terapon jarbua of Parangipettai coastal waters. Biotechnology, 9 (3), 373–377.
https://doi.org/10.3923/biotech.2010.373.377
Al-Jufaili, S.M., Hermosa, G., Al-Shuaily, S.S. & Mujaini, A.A. (2010) Oman fish biodiversity. Journal of King Abdulaziz University, Marine Science, 21 (1), 3–51.
https://doi.org/10.4197/Mar.21-1.1
Bianchi, G. (1985) FAO species identification sheets for fishery purposes. Field guide to the commercial marine and brackish-water species of Pakistan. Prepared with the support of PAK/77/033 and FAO (FIRM) Regular Programme. FAO, Rome, 200 pp.
Bloom, D.D. & Lovejoy, N.R. (2012) Molecular phylogenetics reveals a pattern of biome conservatism in New World anchovies (family Engraulidae). Journal of Evolutionary Biology, 25 (4), 701–715.
https://doi.org/10.1111/j.1420-9101.2012.02464.x
Briggs, J.C. & Bowen, B.W. (2012) A realignment of marine biogeographic provinces with particular reference to fish distributions. Journal of Biogeography, 39 (1), 12–30.
https://doi.org/10.1111/j.1365-2699.2011.02613.x
Carpenter, K.E., Krupp, F., Jones, D.A. & Zajonz, U. (1997) FAO species identification guide for fishery purposes. The living marine resources of Kuwait, Eastern Saudi Arabia, Bahrain, Qatar, and the United Arab Emirates. FAO, Rome, 293 pp.
Dayrat, B. (2005) Towards integrative taxonomy. Biological Journal of the Linnean Society, 85 (3), 407–415.
https://doi.org/10.1111/j.1095-8312.2005.00503.x
Delfieh, P., Zohrehbakhsh, E., Owfi, F., Kazemian, M. & Delfieh, P. (2011) The overview study of Engraulididae and Pristigasteridae, two families of clupeiforms in the Persian Gulf and Oman Sea. Iranian Journal of Marine Biology, 3 (9), 41–52. [in Persian/abstract in English]
Di Dario, F. (2009) Chirocentrids as engrauloids: evidence from suspensorium, branchial arches, and infraorbital bones (Clupeomorpha, Teleostei). Zoological Journal of the Linnean Society, 156 (2), 363–383.
https://doi.org/10.1111/j.1096-3642.2008.00472.x
Ebach, M.C. & Holdrege, C. (2005) DNA barcoding is no substitute for taxonomy. Nature, 434 (7034), 1–697.
https://doi.org/10.1038/434697b
Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular marine biology and biotechnology, 3 (5), 294–299.
Frézal, L. & Leblois, R. (2008) Four years of DNA barcoding: Current advances and prospects. Infection, Genetics and Evolution, 8 (5), 727–736.
https://doi.org/10.1016/j.meegid.2008.05.005
Fricke, R., Eschmeyer, W.N. & Van der Laan, R. (2020) Eschmeyer’s catalog of fishes: genera, species, references. Available from: http://researcharchive. calacademy.org/research/catalog/ fishcatmain.asp. (accessed date 1 July 2019)
Fricke, R., Golani, D. & Appelbaum-Golani, B. (2015) First record of the Indian anchovy Stolephorus indicus (van Hasselt, 1823) (Clupeiformes: Engraulidae) in the Mediterranean Sea. BioInvasions Records, 4 (4), 293–297.
https://doi.org/10.3391/bir.2015.4.4.11
Ganias, K. (2014) Biology and Ecology of Sardines and Anchovies. CRC Press, Taylor & Francis Group, Boca Raton, Florida, 382 pp.
Hata, H. & Motomura, H. (2015) A new species of anchovy, Encrasicholina macrocephala (Clupeiformes: Engraulidae), from the northwestern Indian Ocean. Zootaxa, 3941 (1), 117–124.
https://doi.org/10.11646/zootaxa.3941.1.6
Hata, H. & Motomura, H. (2016) Two new species of the genus Encrasicholina (Clupeiformes: Engraulidae): E. intermedia from the western Indian Ocean and E. gloria from the Persian Gulf, Red Sea and Mediterranean. Raffles Bulletin of Zoology, 64, 79–88.
https://doi.org/urn:lsid:zoobank.org:pub:D6D1C4DE-58A2-4885-A199-D3CB0E3774A8
Hata, H. & Motomura, H. (2017) Validity of Encrasicholina pseudoheteroloba (Hardenberg 1933) and redescription of Encrasicholina heteroloba (Rüppell 1837), a senior synonym of Encrasicholina devisi (Whitley 1940) (Clupeiformes: Engraulidae). Ichthyological Research, 64 (1), 18–28.
https://doi.org/10.1007/s10228-016-0529-4
Hata, H., Motomura, H. & Ishimori, H. (2012) First Japanese record of an engraulid fish, Encrasicholina devisi (Clupeiformes), collected from Kagoshima Prefecture, southern Japan and comparisons with congeners. Japanese Journal of Ichthyology, 59 (2), 125–134.
https://doi.org/10.11369/jji.59.125
Hebert, P.D.N., Cywinska, A., Ball, S.L. & deWaard, J.R. (2003) Biological identifications through DNA barcodes. Proceedings of the Royal Society Series B: Biological Sciences, 270 (1512), 313–321.
https://doi.org/10.1098/rspb.2002.2218
Hubert, N., Hanner, R., Holm, E., Mandrak, N.E., Taylor, E., Burridge, M., Watkinson, D., Dumont, P., Curry, A., Bentzen, P., Zhang, J., April, J. & Bernatchez, L. (2008) Identifying Canadian freshwater fishes through DNA barcodes. PLoS ONE, 3 (6), e2490.
https://doi.org/10.1371/journal.pone.0002490
Kimura, M. (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16 (2), 111–120.
https://doi.org/10.1007/BF01731581
Lakra, W.S., Singh, M., Goswami, M., Gopalakrishnan, A., Lal, K.K., Mohindra, V., Sarkar, U.K., Punia, P.P., Singh, K.V., Bhatt, J.P. & Ayyappan. S. (2016) DNA barcoding Indian freshwater fishes. Mitochondrial DNA Part A: DNA Mapping, Sequencing, and Analysis, 27 (6), 4510–4517.
https://doi.org/10.3109/19401736.2015.1101540
Landi, M., Dimech, M., Arculeo, M., Biondo, G., Martins, R., Carneiro, M., Carvalho, G.R., Brutto, S.L. & Costa, F.O. (2014) DNA barcoding for species assignment: the case of Mediterranean marine fishes. PLoS ONE, 9 (9), e106135.
https://doi.org/10.1371/journal.pone.0106135
Lavoué, S., Miya, M. & Nishida, M. (2010) Mitochondrial phylogenomics of anchovies (family Engraulidae) and recurrent origins of pronounced miniaturization in the order Clupeiformes. Molecular Phylogenetics and Evolution, 56 (1), 480–485.
https://doi.org/10.1016/j.ympev.2009.11.022
Lefebure, T., Douady, C.J., Gouy, M. & Gibert, J. (2006) Relationship between morphological taxonomy and molecular divergence within Crustacea: proposal of a molecular threshold to help species delimitation. Molecular Phylogenetics and Evolution, 40 (2), 435–447.
https://doi.org/10.1016/j.ympev.2006.03.014
Ma, C., Ma, L., Ni, Y., Shen, A., Zhang, Y., Zhang, F. & Zhao, Y. (2010) Phylogenetic relationship of Thryssa inferred from morphologic characteristic and mitochondrial 16 S rRNA gene sequences. Journal of Fishery Sciences of China, 17 (3), 471–477.
Ma, C.Y., Ma, H.Y., Ni, Y., Wang, W. & Ma, L.B. (2015) Molecular identification of the genus Thryssa based on DNA barcoding. Genetics and Molecular Research, 14 (4), 18580–18586.
https://doi.org/10.4238/2015.December.28.5
Pappalardo, A.M. & Ferrito, V. (2015) DNA barcoding species identification unveils mislabeling of processed flatfish products in southern Italy markets. Fisheries Research, 164, 153–158.
https://doi.org/10.1016/j.fishres.2014.11.004
Psomadakis, P.N., Osmany, H.B. & Moazzam, M. (2015) FAO species identification guide for fishery purposes. The living marine resources of Pakistan. FAO, Rome, 386 pp.
Rajpoot, A., Kumar, V.P., Bahuguna, A. & Kumar, D. (2016) DNA barcoding and traditional taxonomy: An integrative approach. International Journal of Current Research, 8 (11), 42025–42031.
Randall, J.E. (1995) Coastal fishes of Oman. University of Hawaii Press, Honolulu, 432 pp.
Ribeiro, A.O., Caires, R.A., Mariguela, T.C., Pereira, L.H.G., Hanner, R. & Oliveira, C. (2012) DNA barcodes identify marine fishes of São Paulo State, Brazil. Molecular Ecology Resources, 12 (6), 1012–1020.
https://doi.org/10.1111/1755-0998.12007
Salarpour, A., Darvishi, M., Behzadi, S. & Seraji, F. (2008) Reproduction and feeding of buccaneer anchovy (Encrasicholina punctifer) from coastal waters of Qeshm Island, the Persian Gulf. Iranian Scientific Fisheries Journal, 17 (1), 45–54. [in Persian/abstract in English]
Santos, M., Hata, H., Belga, P.B., Lanzuela, N., Buccat, F.G.A., Villanueva, J.A., Villarao, M.C., Doyola, M.C., Deligero, R., Alcantara, M., Gatlabayan, L.V., Lopez, G., Parido, L. & Gapuz, A.V. (2017) Encrasicholina pseudoheteroloba. The IUCN red list of threatened species. Available from: http://dx.doi.org/10.2305/IUCN.UK.2017-3.RLTS.T103422139A103422186.en (accessed 5 February 2020)
Sembiring, A., Pertiwi, N.P.D., Mahardini, A., Wulandari, R., Kurniasih, E.M., Kuncoro, A.W., Cahyani, N.K.D., Anggoro, A.W. Ulfa, M., Madduppa, H., Carpenter, K.E., Barber, P.H. & Mahardika, G.N. (2015) DNA barcoding reveals targeted fisheries for endangered sharks in Indonesia. Fisheries Research, 164, 130–134.
https://doi.org/10.1016/j.fishres.2014.11.003
Sharawy, Z.Z., Abbas, E.M., Khafage, A.R., Galal-Khallaf, A., Ismail, R.F., Ahmed, H.O., Mohammed-Geba, K. & Kato, M. (2017) Descriptive analysis, DNA barcoding and condition index of Penaeids (Crustacea: Decapoda) from the Egyptian Mediterranean coast. Fisheries Research, 188, 6–16.
https://doi.org/10.1016/j.fishres.2016.12.007
Steinke, D., deWaard, J.R., Gomon, M.F., Johnson, J.W., Larson, H.K., Lucanus, O., Moore, G.I., Reader, S. & Ward, R.D. (2017) DNA barcoding the fishes of Lizard Island (Great Barrier Reef). Biodiversity Data Journal, 5, e12409.
https://doi.org/10.3897/BDJ.5.e12409
Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution, 30 (12), 2725–2729.
https://doi.org/10.1093/molbev/mst197
Thompson, J.D., Higgins, D.G. & Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22 (22), 4673–4680.
https://doi.org/10.1093/nar/22.22.4673
Tzeng, C-H. & Chiu, T-S. (2012) DNA barcode-based identification of commercially caught cutlassfishes (Family: Trichiuridae) with a phylogenetic assessment. Fisheries Research, 127–128, 176–181.
https://doi.org/10.1016/j.fishres.2012.01.022
Wang, H-Y., Dong, C.A. & Lin, H-C. (2017) DNA barcoding of fisheries catch to reveal composition and distribution of cutlassfishes along the Taiwan coast. Fisheries Research, 187, 103–109.
https://doi.org/10.1016/j.fishres.2016.11.015
Ward, R.D., Hanner, R. & Hebert, P.D. (2009) The campaign to DNA barcode all fishes, FISH-BOL. Journal of fish biology, 74 (2), 329–356.
https://doi.org/10.1111/j.1095-8649.2008.02080.x
Whitehead, P.J.P. (1985) FAO species catalogue. 7 (125), Clupeoid fishes of the world. An annotated and illustrated catalogue of the herrings, sardines, pilchards, sprats, anchovies and wolfherrings. Part 1. Chirocentridae, Clupeidae and Pristigasteridae. FAO Fisheries Synopsis, Rome, 303 pp.
Whitehead, P.J.P., Nelson, G.J. & Wongratana, T. (1988) FAO species catalogue. 7 (125). Clupeoid fishes of the world. An annotated and illustrated catalogue of the herrings, sardines, pilchards, sprats, anchovies and wolfherrings. Part 2. Engraulididae. FAO Fisheries Synopsis, Rome, pp. 305–579.
Wongratana, T. (1980 ) Systematics of clupeoid fishes of the Indo-Pacific region. Ph.D. thesis, Faculty of Science, University of London, London, 923 pp.
Wongratana, T. (1983) Diagnoses of 24 new species and proposal of a new name for a species of Indo-Pacific Clupeoid fishes. Japanese Journal of Ichthyology, 29 (4), 385–407.
https://doi.org/10.11369/jji1950.29.385
Zhang, J. (2011) Species identification of marine fishes in China with DNA barcoding. Evidence-based Complementary and Alternative Medicine, 2215 (978253), 1–10.
https://doi.org/10.1155/2011/978253
Zhang, J-B. & Hanner, R. (2011) DNA barcoding is a useful tool for the identification of marine fishes from Japan. Biochemical Systematics and Ecology, 39 (1), 31–42.
https://doi.org/10.1016/j.bse.2010.12.017