Molecular characteristics and taxonomic status of morphologically similar barnacles (Amphibalanus) assessed using the cytochrome c oxidase 1 gene
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Abstract. Riani S, Prabowo RE, Nuryanto A. 2021. Molecular characteristics and taxonomic status of morphologically similar barnacles (Amphibalanus) assessed using the cytochrome c oxidase 1 gene. Biodiversitas 22: 1456-1466. Amphibalanus variegatus and A. reticulatus have similar external morphology. Morphological similarities can be a severe problem for direct species-level identification. The problem can be overcome through anatomy-based identification and validated through molecular barcoding. Molecular characterization using the cytochrome c oxidase 1 (COI) gene provides a useful tool for precise species identification. This study attempted to assess the molecular characteristics of morphologically similar barnacle (Amphibalanus) specimens collected at five localities in Indonesia to validate their taxonomic status. Forty-five barnacle specimens were collected during the field trips in Lampung, Jakarta, Semarang, Bali, and Lombok. The COI gene was amplified using LCO1490 and HCO2198 primers. The gene was sequenced using bidirectional sequencing at 1st base Asia. The specimens' taxonomic status was determined based on sequence identity, genetic distance, monophyly, nucleotide compositions, and nucleotides in a particular position. Shell shapes-based identification placed barnacle specimens into A. reticulatus. However, anatomical-based identification placed barnacle samples into two different anatomic groups, which was further validated by molecular data that two anatomic groups of Amphibalanus samples have significant differences in their COI gene. Based on the molecular characteristics, 43 samples were identified as A. reticulatus, while the two remaining samples were identified as A. variegatus.
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References
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Bekker EI, Karabanov DP, Galimov YR, Kotov AA. 2016. DNA barcoding reveals high cryptic diversity in the North Eurasian Moina species (Crustacea: Cladocera). PLoS One 11 (8): e0161737. DOI: 10.1371/journal.pone.0161737
Bilgin R, Utkan MA, Kalkan E, Karhan SU, Bekbolet M. 2015. DNA barcoding of twelve shrimp (Crustacea: Decapoda) from Turkish sea reveals cryptic diversity. Mediterr Mar Sci 16 (1): 36-45. DOI: 10.12681/mms.548
Bucklin A, Hopcroft RR, Kosobokova KN, Nigro LM, Ortman BD, Jennings RM, Sweetmann CJ. 2010. DNA barcoding of Arctic Ocean holozooplankton for species identification and recognition. Deep-Sea Research II 57: 40-48.
Camacho AI, Dorda BA, Rey I. 2011. Identifying cryptic speciation across groundwater populations: first COI sequences of Bathynellidae (Crustacea, Syncarida). Graellsia 67 (1): 7-12. DOI: 10.3989/graellsia.2011.v67.031
Candek K, Kuntner M. 2015. DNA barcoding gap: Reliable species identi?cation over morphological and geographical scales. Mol Ecol Resour 15 (2): 268-277. DOI: 10.1111/1755-0998.12304
Carlton JT, Newman WA, Pitombo FB. 2011. Barnacle Invasions: Introduced, Cryptogenic, and Range Expanding Cirripedia of North and South America . In: B.S. Galil et al. (eds.), In the Wrong Place - Alien Marine Crustaceans: Distribution, Biology and Impacts. Invading Nature - Springer Series in Invasion Ecology 6, 159. DOI 10.1007/978-94-007-0591-3_5
Chen HN, Tsang LM, Chong VC, Chan BK. 2014. Worldwide genetic differentiation in the common fouling barnacle, Amphibalanus amphitrite. Biofouling 30(9): 1067–1078.
Claridge MF, Dawah HA, Wilson MR. 1997. Species: The units of biodiversity. Chapman and Hall: London. pp 439.
da Silva JM, Creer S, dos Santos A, Costa AC, Cunha MR, Costa FO, Carvalho GR. 2011. Systematic and evolutionary insights derived from mtDNA COI barcode diversity in the Decapoda (Crustacea: Malacostraca). PLoSONE 6 (5): e19449. DOI: 10.1371/journal.pone.0019449
Excoffier L, and Lischer HEL. 2010. Arlequin Suite Ver 3.5: A New Series Of Programs To Perform Population Genetics Analyses Under Linux And Windows. Molecular Ecology Resources. vol 10(3):564–567. doi: https://doi.org/10.1111/j.1755-0998.2010.02847.x
Fertl D, Newman WA. Barnacles. In: Encyclopedia of marine mammals (Third Edition). Academic Press. pp. 75-78.
Folmer O, Black M, Lutz R, Vrijenhoek R. 1994. DNA Primers for Amplification of Mitochondrial Cytochrome C Oxidase Subunit I from Metazoan Invertebrates. Mol. Mar. Biol. Biotechnol. 3 (5): 294-299.
Hall TA. 2005. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95-98. DOI: 10.14601/Phytopathol_Mediterr-14998u1.29
Havermans C, Nagy ZT, Sonet G, De Broyer C, Martin P. 2011. DNA barcoding reveals new insights into the diversity of Antarctic species of Orchomene sensu lato (Crustacea: Amphipoda: Lysianassoidea). Deep-Sea Research II(58): 230-241.
Henry DP, McLaughlin PA. 1975. The barnacles of the Balanus amphitrite complex (Cirripedia, Thoracica). Zoologische Verhandelingen 141(1): 1–254.
Horikosi A, Okamoto K. 2005. The first finding of the introduced barnacle Amphibalanus variegatus (Darwin) in Tokyo Bay. Sessile Organisms 22(2): 47-50.
Hubert N, Meyer CP, Bruggeman HJ, Guerin F, Komeno RJL, Espiau B, Caussee R, Wiliams JT, Planes S. 2012. Cryptic diversity in Indo-Pacific coral reef fishes revealed by DNA barcoding provides new support to the center of overlap hypothesis. PloS One 7(3): e28987.
Jeffery NW, Elias-Guttierrez M, Adamowicz SJ. 2011. Species diversity and phylogeographical affinities of the Branchiopoda (Crustacea) of Churchill, Manitoba, Canada. PLoS One 6 (5): e18364. DOI: 10.1371/journal.pone.0018364
Jones DS. 2012 Australian barnacles (Cirripedia: Thoracica), distributions and biogeographical affinities. Integrative and comparative biology, 52(3): 366–387.
Jones DS, Hosie AM. 2016. A checklist of the barnacles (Cirripedia: Thoracica) of Singapore and neighbouring waters. Raffles Bulletin of Zoology 34: 241–311.
Karanovic I. 2015. Barcoding of ancient lake Ostracods (Crustacea) reveals cryptic speciation with extremely low distances. PLoS One 10 (3): e0121133. DOI: 10.1371/journal.pone.0121133
Ko HL, Wang YT, Chiu TS, Lee MA, Leu MY, Chang KZ, Chen WY, Shao KT. 2013. Evaluating the accuracy of morphological identification of larval fishes by applying DNA barcoding. PLoS ONE 8 (1): 253451. DOI: 10.1371/journal.pone.0053451.
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. 2018. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35 (6): 1547-1549. DOI: 10.1093/molbev/msy096
Kurniawaty, N., Hidayat, P. &Rauf, A. (2016).Characterization of three Species of thrips on banyan, nutmeg, and marine seruni plants based on COI gene. Biosaintifika 8(2): 185-192.
Kusbiyanto, Bhagawati D, Nuryanto A. 2020. DNA barcoding of crustacean larvae in Segara Anakan, Cilacap, Central Java, Indonesia using cytochrome c oxidase gene.Biodiversitas 21 (10): 4878-4887.
Lin X, Stur E, Ekrem T. 2015. Exploring genetic divergence in a species rich insect genus using 2790 DNA barcodes. PLoS One 10(9): e0138993. doi:10.1371/journal.pone.0138993
Nuryanto A, Pramono H, Sastranegara MH. 2017. Molecular identification of fish larvae from East Plawangan of Segara Anakan, Cilacap, Central Java, Indonesia. Biosaintifika 9 (1): 33-40. DOI: 10.15294/biosaintifika.v9i1.9191
Nuryanto A, Amalia G, Khairani D, Pramono H, Bhagawati D. 2018. Molecular characterization four giant gourami strains from Java dan Sumatra. Biodiversitas 19 (2): 528-539. DOI: 10.13057/biodiv/d190228
Nuryanto A, Komalawati N, Sugiharto. 2019. Genetic diversity assessment of Hemibagrus nemurus from rivers in Java Island, Indonesia using COI gene. Biodiversitas 20 (9): 2707-2717. DOI: 10.13057/biodiv/d200936
Palecanda S, Feller KD, Porter ML. 2020. Using larval barcoding to estimate stomatopod species richness at Lizard Island, Australia for conservation monitoring. Sci Rep 10: 10990. DOI: 10.1038/s41598-020-67696-x
Palero F, Genis-Armero R, Hall MR, Clark PF. 2016. DNA barcoding the phyllosoma of Scyllarides squammosus (H. Milne Edwards, 1837) (Decapoda: Achelata: Scyllaridae). Zootaxa 4139 (4): 481- 498. DOI: 10.11646/zootaxa.4139.4.2
Pereira LHG, Hanner R, Foresti F, Oliveira C. 2013. Can DNA barcoding accurately discriminate megadiverse Neotropical freshwater fish fauna? BMC Genet 12: 20.
Pitriana P, Valente L, von Rintelen R, Jones DS, Prabowo RE, von Rintelen K. 2020. An annotated checklist and integrative biodiversity discovery of barnacles (Crustacea, Cirripedia) from the Moluccas, East Indonesia. ZooKeys 945: 17-83.
Pitombo FB. 2004. Phylogenetic analysis of the Balanidae (Cirripedia, Balanomorpha). Zoologica Scripta 33(3): 361-276.
Pochai A, Kingtong S, Sukparangsi W, Khachonpisitsak S. 2017. The diversity of acorn barnacles (Cirripedia, Balanomorpha) across Thailand’s coasts: The Andaman Sea and the Gulf of Thailand. Zoosystematics and Evolution 93: 13–34.
Power AM, Klepal W, Zheden V, Jonker J, McEvilly P, von Byern J. 2010. Mechanisms of adhesion in adult barnacles. In: von Byern J., Grunwald I. (eds) Biological Adhesive Systems. Springer, Vienna, 153–168.
Puspasari I.A. 2001. Phylogeny of the balanus amphitrite complex (Cirripedia, Balanidae). PhD thesis, Chiba Univ.
Raupach MJ, Radulovici AE. 2015. Looking back on a decade barcoding crustaceans. Zookeys 539: 53-81. DOI: 10.3897/zookeys.539.6530
Ratnasingham S. 2016. BOLDSYSTEMS. Available from: http://www.boldsystems.org/ (accessed 20 October 20)
Ratnasingham S, Hebert PDN. 2007. The Barcode of Life Data System (http://www.barcodinglife.org). Molecular Ecology Notes 7: 355–364.
Riehl T, Brenke N, Brix S, Driskell A, Kaiser S, Brandt A. 2014. Field and laboratory methods for DNA studies on deep-sea isopod crustaceans. Polish Polar Res 35 (22): 203-224.
Shahdadi A, Sari A, Naderloo R. 2014. A checklist of the barnacles (Crustacea: Cirripedia: Thoracica) of the Persian Gulf and Gulf of Oman with nine new records. Zootaxa 3784 (3): 201-223.
Tang RWK, Yau C, Ng W-C. 2010. Identification of stomatopod larvae (Crustacea: Stomatopoda) from Hong Kong waters using DNA barcodes. Mol Ecol Res 10 (3): 439-448. DOI: 10.1111/j.1755-0998.2009.02794.x
Thirumaraiselvi R, Das S, Ramanadevi V, Thangaraj M. 2015. MtDNA barcode identification of Fisnfish larvae from Vellar Estuary, Tamilnadu, India. Notulae Scientia Biologicae 7(1),16-19
Thompson JG, Higgins DG, Gibson TJ. 1994. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignments through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22 (22): 4673-4680. DOI: 10.1093/nar/22.22.4673
von der Heyden, S., Berger, M., Toonen, R.J., van Herwerden, L., Juinio-Menez, M.A., Ravago-Gotanco, R., Fauvelot, C., and Bernardi, G. 2014. The Application of Genetics to Marine Management and Consrvation: Examples from the Indo-Pacific. Bull. Mar. Sci. 90 (1): 123-158.
Weis M, Macher JN, Seefeldt MA, Leese F. 2014. Molecular evidence for further overlooked species within the Gammarus fossarum complex (Crustacea: Amphipoda). Hydrobiol 721 (1): 165-184. DOI: 10.1007/s10750-013-1658-7.
Bhagawati D, Winarni ET, Nuryanto A. 2020. Molecular Barcoding Reveal the Existence of Mole Crabs Emerita emeritus in North Coast of Central Java. Biosaintifika 12 (1): 104-110.
Bekker EI, Karabanov DP, Galimov YR, Kotov AA. 2016. DNA barcoding reveals high cryptic diversity in the North Eurasian Moina species (Crustacea: Cladocera). PLoS One 11 (8): e0161737. DOI: 10.1371/journal.pone.0161737
Bilgin R, Utkan MA, Kalkan E, Karhan SU, Bekbolet M. 2015. DNA barcoding of twelve shrimp (Crustacea: Decapoda) from Turkish sea reveals cryptic diversity. Mediterr Mar Sci 16 (1): 36-45. DOI: 10.12681/mms.548
Bucklin A, Hopcroft RR, Kosobokova KN, Nigro LM, Ortman BD, Jennings RM, Sweetmann CJ. 2010. DNA barcoding of Arctic Ocean holozooplankton for species identification and recognition. Deep-Sea Research II 57: 40-48.
Camacho AI, Dorda BA, Rey I. 2011. Identifying cryptic speciation across groundwater populations: first COI sequences of Bathynellidae (Crustacea, Syncarida). Graellsia 67 (1): 7-12. DOI: 10.3989/graellsia.2011.v67.031
Candek K, Kuntner M. 2015. DNA barcoding gap: Reliable species identi?cation over morphological and geographical scales. Mol Ecol Resour 15 (2): 268-277. DOI: 10.1111/1755-0998.12304
Carlton JT, Newman WA, Pitombo FB. 2011. Barnacle Invasions: Introduced, Cryptogenic, and Range Expanding Cirripedia of North and South America . In: B.S. Galil et al. (eds.), In the Wrong Place - Alien Marine Crustaceans: Distribution, Biology and Impacts. Invading Nature - Springer Series in Invasion Ecology 6, 159. DOI 10.1007/978-94-007-0591-3_5
Chen HN, Tsang LM, Chong VC, Chan BK. 2014. Worldwide genetic differentiation in the common fouling barnacle, Amphibalanus amphitrite. Biofouling 30(9): 1067–1078.
Claridge MF, Dawah HA, Wilson MR. 1997. Species: The units of biodiversity. Chapman and Hall: London. pp 439.
da Silva JM, Creer S, dos Santos A, Costa AC, Cunha MR, Costa FO, Carvalho GR. 2011. Systematic and evolutionary insights derived from mtDNA COI barcode diversity in the Decapoda (Crustacea: Malacostraca). PLoSONE 6 (5): e19449. DOI: 10.1371/journal.pone.0019449
Excoffier L, and Lischer HEL. 2010. Arlequin Suite Ver 3.5: A New Series Of Programs To Perform Population Genetics Analyses Under Linux And Windows. Molecular Ecology Resources. vol 10(3):564–567. doi: https://doi.org/10.1111/j.1755-0998.2010.02847.x
Fertl D, Newman WA. Barnacles. In: Encyclopedia of marine mammals (Third Edition). Academic Press. pp. 75-78.
Folmer O, Black M, Lutz R, Vrijenhoek R. 1994. DNA Primers for Amplification of Mitochondrial Cytochrome C Oxidase Subunit I from Metazoan Invertebrates. Mol. Mar. Biol. Biotechnol. 3 (5): 294-299.
Hall TA. 2005. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95-98. DOI: 10.14601/Phytopathol_Mediterr-14998u1.29
Havermans C, Nagy ZT, Sonet G, De Broyer C, Martin P. 2011. DNA barcoding reveals new insights into the diversity of Antarctic species of Orchomene sensu lato (Crustacea: Amphipoda: Lysianassoidea). Deep-Sea Research II(58): 230-241.
Henry DP, McLaughlin PA. 1975. The barnacles of the Balanus amphitrite complex (Cirripedia, Thoracica). Zoologische Verhandelingen 141(1): 1–254.
Horikosi A, Okamoto K. 2005. The first finding of the introduced barnacle Amphibalanus variegatus (Darwin) in Tokyo Bay. Sessile Organisms 22(2): 47-50.
Hubert N, Meyer CP, Bruggeman HJ, Guerin F, Komeno RJL, Espiau B, Caussee R, Wiliams JT, Planes S. 2012. Cryptic diversity in Indo-Pacific coral reef fishes revealed by DNA barcoding provides new support to the center of overlap hypothesis. PloS One 7(3): e28987.
Jeffery NW, Elias-Guttierrez M, Adamowicz SJ. 2011. Species diversity and phylogeographical affinities of the Branchiopoda (Crustacea) of Churchill, Manitoba, Canada. PLoS One 6 (5): e18364. DOI: 10.1371/journal.pone.0018364
Jones DS. 2012 Australian barnacles (Cirripedia: Thoracica), distributions and biogeographical affinities. Integrative and comparative biology, 52(3): 366–387.
Jones DS, Hosie AM. 2016. A checklist of the barnacles (Cirripedia: Thoracica) of Singapore and neighbouring waters. Raffles Bulletin of Zoology 34: 241–311.
Karanovic I. 2015. Barcoding of ancient lake Ostracods (Crustacea) reveals cryptic speciation with extremely low distances. PLoS One 10 (3): e0121133. DOI: 10.1371/journal.pone.0121133
Ko HL, Wang YT, Chiu TS, Lee MA, Leu MY, Chang KZ, Chen WY, Shao KT. 2013. Evaluating the accuracy of morphological identification of larval fishes by applying DNA barcoding. PLoS ONE 8 (1): 253451. DOI: 10.1371/journal.pone.0053451.
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. 2018. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35 (6): 1547-1549. DOI: 10.1093/molbev/msy096
Kurniawaty, N., Hidayat, P. &Rauf, A. (2016).Characterization of three Species of thrips on banyan, nutmeg, and marine seruni plants based on COI gene. Biosaintifika 8(2): 185-192.
Kusbiyanto, Bhagawati D, Nuryanto A. 2020. DNA barcoding of crustacean larvae in Segara Anakan, Cilacap, Central Java, Indonesia using cytochrome c oxidase gene.Biodiversitas 21 (10): 4878-4887.
Lin X, Stur E, Ekrem T. 2015. Exploring genetic divergence in a species rich insect genus using 2790 DNA barcodes. PLoS One 10(9): e0138993. doi:10.1371/journal.pone.0138993
Nuryanto A, Pramono H, Sastranegara MH. 2017. Molecular identification of fish larvae from East Plawangan of Segara Anakan, Cilacap, Central Java, Indonesia. Biosaintifika 9 (1): 33-40. DOI: 10.15294/biosaintifika.v9i1.9191
Nuryanto A, Amalia G, Khairani D, Pramono H, Bhagawati D. 2018. Molecular characterization four giant gourami strains from Java dan Sumatra. Biodiversitas 19 (2): 528-539. DOI: 10.13057/biodiv/d190228
Nuryanto A, Komalawati N, Sugiharto. 2019. Genetic diversity assessment of Hemibagrus nemurus from rivers in Java Island, Indonesia using COI gene. Biodiversitas 20 (9): 2707-2717. DOI: 10.13057/biodiv/d200936
Palecanda S, Feller KD, Porter ML. 2020. Using larval barcoding to estimate stomatopod species richness at Lizard Island, Australia for conservation monitoring. Sci Rep 10: 10990. DOI: 10.1038/s41598-020-67696-x
Palero F, Genis-Armero R, Hall MR, Clark PF. 2016. DNA barcoding the phyllosoma of Scyllarides squammosus (H. Milne Edwards, 1837) (Decapoda: Achelata: Scyllaridae). Zootaxa 4139 (4): 481- 498. DOI: 10.11646/zootaxa.4139.4.2
Pereira LHG, Hanner R, Foresti F, Oliveira C. 2013. Can DNA barcoding accurately discriminate megadiverse Neotropical freshwater fish fauna? BMC Genet 12: 20.
Pitriana P, Valente L, von Rintelen R, Jones DS, Prabowo RE, von Rintelen K. 2020. An annotated checklist and integrative biodiversity discovery of barnacles (Crustacea, Cirripedia) from the Moluccas, East Indonesia. ZooKeys 945: 17-83.
Pitombo FB. 2004. Phylogenetic analysis of the Balanidae (Cirripedia, Balanomorpha). Zoologica Scripta 33(3): 361-276.
Pochai A, Kingtong S, Sukparangsi W, Khachonpisitsak S. 2017. The diversity of acorn barnacles (Cirripedia, Balanomorpha) across Thailand’s coasts: The Andaman Sea and the Gulf of Thailand. Zoosystematics and Evolution 93: 13–34.
Power AM, Klepal W, Zheden V, Jonker J, McEvilly P, von Byern J. 2010. Mechanisms of adhesion in adult barnacles. In: von Byern J., Grunwald I. (eds) Biological Adhesive Systems. Springer, Vienna, 153–168.
Puspasari I.A. 2001. Phylogeny of the balanus amphitrite complex (Cirripedia, Balanidae). PhD thesis, Chiba Univ.
Raupach MJ, Radulovici AE. 2015. Looking back on a decade barcoding crustaceans. Zookeys 539: 53-81. DOI: 10.3897/zookeys.539.6530
Ratnasingham S. 2016. BOLDSYSTEMS. Available from: http://www.boldsystems.org/ (accessed 20 October 20)
Ratnasingham S, Hebert PDN. 2007. The Barcode of Life Data System (http://www.barcodinglife.org). Molecular Ecology Notes 7: 355–364.
Riehl T, Brenke N, Brix S, Driskell A, Kaiser S, Brandt A. 2014. Field and laboratory methods for DNA studies on deep-sea isopod crustaceans. Polish Polar Res 35 (22): 203-224.
Shahdadi A, Sari A, Naderloo R. 2014. A checklist of the barnacles (Crustacea: Cirripedia: Thoracica) of the Persian Gulf and Gulf of Oman with nine new records. Zootaxa 3784 (3): 201-223.
Tang RWK, Yau C, Ng W-C. 2010. Identification of stomatopod larvae (Crustacea: Stomatopoda) from Hong Kong waters using DNA barcodes. Mol Ecol Res 10 (3): 439-448. DOI: 10.1111/j.1755-0998.2009.02794.x
Thirumaraiselvi R, Das S, Ramanadevi V, Thangaraj M. 2015. MtDNA barcode identification of Fisnfish larvae from Vellar Estuary, Tamilnadu, India. Notulae Scientia Biologicae 7(1),16-19
Thompson JG, Higgins DG, Gibson TJ. 1994. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignments through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22 (22): 4673-4680. DOI: 10.1093/nar/22.22.4673
von der Heyden, S., Berger, M., Toonen, R.J., van Herwerden, L., Juinio-Menez, M.A., Ravago-Gotanco, R., Fauvelot, C., and Bernardi, G. 2014. The Application of Genetics to Marine Management and Consrvation: Examples from the Indo-Pacific. Bull. Mar. Sci. 90 (1): 123-158.
Weis M, Macher JN, Seefeldt MA, Leese F. 2014. Molecular evidence for further overlooked species within the Gammarus fossarum complex (Crustacea: Amphipoda). Hydrobiol 721 (1): 165-184. DOI: 10.1007/s10750-013-1658-7.
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