Discovery and DNA analysis of the invasive freshwater mussel Sinanodonta lauta (Unionidae) in south Iran

Kazem Alwanzadegan; Hadise Kashiri; Ivan N. Bolotov; Ertan Ercan; Ainaz Shirangi; Edris Ghaderi

doi:10.22034/ijab.v11i2.1796

Authors

Kazem Alwanzadegan Department of Aquatic Ecology, Faculty of Fisheries and Environment, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran.
Hadise Kashiri
[email protected]
Department of Aquatic Ecology, Faculty of Fisheries and Environment, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran.
Ivan N. Bolotov N. Laverov Federal Center for Integrated Arctic Research of the Ural Branch of the Russian Academy of Sciences, Northern Dvina Emb. 23, 163000 Arkhangelsk, Russia.
Ertan Ercan Fisheries Faculty, Mugla Sitki Koçman University, Mugla, Turkey.
Ainaz Shirangi Basic Sciences Faculty, Gonbad Kavous University, Gonbad, Iran.
Edris Ghaderi Department of Aquatic Ecology, Faculty of Fisheries and Environment, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran.

Vol. 11 No. 2 (2023): April

Articles

March 24, 2023

Downloads

PDF

Abstract
How to Cite
Metrics
References
License

Some members of the genus Sinanodonta (Modell, 1944) are known as successful invaders of freshwater habitats. Here we report the first record of Sinanodonta lauta (Martens, 1877) from Iran and provide morphological and molecular data on this alien population. This species was observed in the Dez River and a fish farm in Khuzestan, south of Iran. The S. lauta introduction seems to be closely related to the introduction of Asian carps from East Asia. The individuals collected from the river exhibited two COI haplotypes, probably due to several introduction events of host fish. Based on our haplotype network, the alien individuals found in Iran is closer to the native ones from South Korea (two-three substitutions) compared to other native individuals reported from Japan and Russian Far East. The presence of 10-11 years old specimens in Dez River shows that the species can survive well in the natural environment of southern Iran. Further expansion and colonization of S. lauta in south Iran or beyond it are not unexpected due to some human-mediated dispersal events as well as waterways in the region.

Alwanzadegan, K., Kashiri, H., Bolotov, I. N., Ercan, E., Shirangi, A., & Ghaderi, E. (2023). Discovery and DNA analysis of the invasive freshwater mussel Sinanodonta lauta (Unionidae) in south Iran. International Journal of Aquatic Biology, 11(2), 86–97. https://doi.org/10.22034/ijab.v11i2.1796

Download Citation

Abbasi K., Mouludi-Saleh A., Eagderi S., Sarpanah A. (2020). Morphometric and meristic comparison of Garra rufa Heckel, 1843 populations in rivers of the Karkheh and Karun basins. Journal of Animal Environment, 12(4): 465-472. ?

Akaike H. (1973). Information theory and an extension of the maximum likelihood principle. In: Petrov B.N., Csáki F. (Ed.). Second International Symposium on Information Theory, Budapest: Akadémiai Kiadó, pp: 267-281.

Bauer W.G., Stewart D.T., Cespedes R.Q., Valverde S.A. (2021). Easy RH. DNA barcoding evidence of the tropical Invasive Lineage of Sinanodonta woodiana in Costa Rica. Neotropical Biodiversity. 5: 1-8.

Beran L. (2020). First records of Sinanodonta woodiana (Lea, 1834) and Corbicula fluminea (O. F. Müller, 1774) (Mollusca, Bivalvia) from the Adriatic part of Croatia. Folia Malacologica, 28(4): 295-302.

Bespalaya Y.V., Bolotov I.N., Aksenova O.V., Gofarov M.Y., Kondakov A.V., Vikhrev I.V., Vinarski M.V. (2018). DNA barcoding reveals invasion of two cryptic Sinanodonta mussel species (Bivalvia: Unionidae) into the largest Siberian river. Limnologica, 69: 94-102.

Bogan A.E., Al-Fanharawi A.A., Lopes-Lima M. (2021). First record of Sinanodonta woodiana and report for freshwater bivalves from Iraq (Mollusca: Bivalvia: Unionidae). Ecologica Montenegrina, 46: 52-60.

Böhm M., Dewhurst-Richman N.I., Seddon M., Ledger S.E.H., Albrecht C., Allen D., Bogan A.E., Corderio J., Cummings K.S., Cuttelod A., Darrigran G., Darwall W., Fehér Z., Gibson C., Graf D.L., Köhler F., Lopes-Limam M., Pastorino G., Perez K.E., Smith K., Damme D.V., Vinarski M.V., Proschwitz T.V., Rintelen T.V., Aldridge D.C., Aravind N.A., Budha P.B., Clavijo C., Tu D.V., Gargominy O., Ghamiz, M., Haase M., Hilton-Taylor C., Johnson P.D., Kebapç? Ü., Lajtner J., Lange C.N., Lepitzki D.A.W., Martínez-Ortí A., Moorkens E.A., Neubert E., Pollock C.M., Prié V., Radea C., Ramirez R., Ramos M.A., Santos S.B., Slapnik R., Son M.O., Stensgaard A.S., Collen B. (2020). The conservation status of the world’s freshwater molluscs. Hydrobiologia, 848: 3231-3254.

Bolotov I.N., Bespalaya Y.V., Gofarov M.Y., Kondakov A.V., Konopleva E.S., Vikhrev I.V. (2016). Spreading of the Chinese pond mussel, Sinanodonta woodiana, across Wallacea: One or more lineages invade tropical islands and Europe. Biochemical Systematics and Ecology, 67: 58-64.

Bolotov IN., Bespalaya Y.V., Vikhrev I.V., Aksenova O.V., Aspholm P.E., Gofarov M.Y., Klishko O.K., Kolosova Y.V., Kondakov A.V., Lyubas A.A., Paltser I.S., Konopleva I.S., Tumpeesuwan S., Bolotov N.I., Voroshilova I.S. (2015). Taxonomy and distribution of freshwater pearl mussels (Unionoida: Margaritiferidae) of the Russian Far East. PLoS One, 10(5): e0122408.

Douda K., ?adková Z. (2018). Water clearance efficiency indicates potential filter-feeding interactions between invasive Sinanodonta woodiana and native freshwater mussels. Biological Invasions, 20: 1093-1098.

Douda K., Velíšek J., Kolá?ová J., Rylková K., Slavík O., Horký P., Langrová I. (2017). Direct impact of invasive bivalve (Sinanodonta woodiana) parasitism on freshwater fish physiology: evidence and implications. Biological Invasions, 19: 989-999.

Douda K., Vrtílek M., Slavík O., Reichard M. (2012). The role of host specificity in explaining the invasion success of the freshwater mussel Anodonta woodiana in Europe. Biological Invasions, 14(1): 127-137.

Duggan I.C. 2010. The freshwater aquarium trade as a vector for incidental invertebrate fauna. Biological Invasions, 12: 3757-3770.

Eagderi S., Mouludi-Saleh A., Esmaeli H.R., Sayyadzadeh G., Nasri, M. (2022). Freshwater lamprey and fishes of Iran; a revised and updated annotated checklist-2022. Turkish Journal of Zoology, 46(6): 500-522.

Eagderi S., Mouludi-Saleh A., Nazlabadi S.A. (2019). First record of the rohu, Labeo rohita (Hamilton, 1822) (Cyprinidae) from Karun River, Tigris River drainage, Iran. Fishtaxa, 4(1): 18-20. ?

Ercan E., Gaygusuz O., Tarkan A.S., Reichard M., Smith C. (2012). The ecology of freshwater bivalves in the Lake Sapanca basin, Turkey. Turkish Journal of Zoology, 37: 730-738.

Eskandari G.H., Sabzalizade S., Dehghan Madise S., Mayahi Y. (2005). Fish populations structure in the Dez Dam Lake. Pajuhesh and Sazandegi, 74: 123-129.

Eskandari G.H., Safikhani H., Marmazi J. (2000). Ichthyofauna and some biological indices in Karoon, Dez and Bahmanshir Rivers (Southwest of Iran). Iranian Scientific Fisheries Journal, 8(3): 23-36.

Fornillos R.J.C., Que G.C.L., Mendoza R.V.D., Fontanilia I.K.C. (2020). Molecular identification of the Chinese pond mussel Sinanodonta woodiana (Lea, 1834) from Mindoro and Leyte Islands, Philippines. Science Diliman, 32(2): 77-96.

Hall T.A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41: 95e98.

Huber V., Geist J. (2019). Reproduction success of the invasive Sinanodonta woodiana (Lea 1834) in relation to native mussel species. Biological Invasions, 21: 3451-3465.

Huelsenbeck J.P., Ronquist F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17(8): 754-755.

Källersjö M., Von Proschwitz T., Lundberg S., Eldenäs P., Erséus C. (2005). Evaluation of ITS rDNA as a complement to mitochondrial gene sequences for phylogenetic studies in freshwater mussels: an example using Unionidae from north-western Europe. Zoologica Scripta, 34: 415e424.

Klishko O., Lopes-Lima M., Froufe E., Bogan A., Vasiliev L., Yanovich L. (2017). Taxonomic reassessment of the freshwater mussel genus Unio (Bivalvia: unionidae) in Russia and Ukraine based on morphological and molecular data. Zootaxa, 4286: 93-112.

Kondakov A.V., Bespalaya Y.V., Vikhrev I.V., Konopleva E.S., Gofarov M.Y., Tomilova A.A., Vinarski M.V., Bolotov I.N. (2020b). The Asian pond mussels rapidly colonize Russia: successful invasions of two cryptic species to the Volga and Ob rivers. Bioinvasions Records, 9(3): 504-518.

Kondakov A.V., Konopleva E.S., Vikhrev I.V., Bespalaya Y.V., Gofarov M.Y., Kabakov M.B., Tomilova A.A., Vinarski M.V., Bolotov I.N. (2020a). Phylogeographic affinities, distribution and population status of the non-native Asian pond mussels Sinanodonta lauta and S. woodiana in

Kazakhstan. Ecologica Montenegrina, 27: 22-34.

Kondakov A.V., Palatov D.M., Rajabov Z.P., Gofarov M.Y., Konopleva E.S., Tomilova A.A., Vikhrev I.V., Bolotov I.N. (2018). DNA analysis of a non-native lineage of Sinanodonta woodiana species complex (Bivalvia: Unionidae) from Middle Asia supports the Chinese origin of the European invaders. Zootaxa, 4462(4): 511-522.

Kraszewski A., Zdanowski B. (2001). The distribution and abundance of the Chinese mussel Anodonta woodiana (Lea, 1834) in the heated Konin Lakes. Archives of Polish Fisheries, 9: 253-265.

Leigh J.W., Bryant D. (2015). PopART: Full-feature software for haplotype network construction. Methods in Ecology and Evolution, 6: 1110-1116.

Liu J., Hayashi H., Inajuma Y., Ikematsu S., Shimatani Y., Minagawa T. (2014). Factors of Water Quality and Feeding Environment for a Freshwater mussel’s (Anodonta lauta) Survival in a Restored Wetland. Wetlands, 34(5): 865-876.

Lopes-Lim, M., Hattori A., Kondo T., Lee J.H., Kim S.K., Shirai A., Hayashi H., Usui T., Sakuma K., Toriya T., Sunamura Y., Ishikawa H., Hoshino N., Kusano Y., Kumaki H., Tanaka A., Sao K., Sano I., Miyazaki J.I., Gonçalves D.V., Klishko O., Konopleva E., Vikhrev I., Kondakov A.V., Gofarov M.Y., Bolotov I., Zieritz A., Bogan A.E., Froufe E. (2020). Freshwater mussels (Bivalvia: Unionidae) from the Rising Sun (Far East Asia): phylogeny, systematics and distribution. Molecular Phylogenetic and Evolution, 146: 106755.

Lopes-Lima M., Sousa R., Geist J., Aldridge D.C., Araujo R., Bergengren J., Bespalaya Y., Bódis E., Burlakova L., Damme D.V., Douda K., Froufe E., Georgiev D., Gumpinger C., Karatayev A., Kebapçi Ü., Killeen I., Lajtner J., Larsen B.M., Lauceri R., Legakis A., Lois S., Lundberg S., Moorkens E., Motte G., Nagel K.O., Ondina P., Outeiro A., Paunovic M., Prié V., Proschwitz T.V., Riccardi N., Rudz?te M., Rudz?tis M., Scheder C., Seddon M., ?erefli?an H., Simi? V., Sokolova S., Stoeckl K., Taskinen J., Teixeira A., Thielen F., Trichkova T., Varandas S., Vicentini H., Zajac K., Zajac T., Zogaris S. (2016). Conservation status of freshwater mussels in Europe: state of the art and future challenges. Biological Reviews, 92(1): 572-607.

Lydeard C., Cowie R.H., Ponder W.F., Bogan A.E., Bouchet P., Clark S.A., Cummings K.S., Frest T.J., Gargominy O., Herbert D.G., Hershler R., Perez K.E., Roth B., Seddon M., Strong E.E., Thompson F.G. (2004). The global decline of nonmarine mollusks. Bioscience, 54: 321-330.

Mohammadi Ruzbahani M., Roghanizadehgan N., Dehghan Madiseh, S. (2014). Assessment of Dez River water quality by Bmwp index. Journal of Wetland Ecobiology, 5(18): 55-66.

Posada D., Crandall K.A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics, 14: 817-818.

Prié V., Puillandre N. (2014). Molecular phylogeny, taxonomy, and distribution of French Unio species (Bivalvia, Unionidae). Hydrobiologia, 735: 95e110.

Rambaut A. (2008). FigTree v1.1.1: Tree figure drawing tool. Available: http://tree.bio.ed.ac.uk/software/.

Sambrook J., Fritschi E.F., Maniatis T. (1989). Molecular cloning: a laboratory manual. USA: Cold Spring Harbor Laboratory Press, New York. 1659 p.

Sano I., Shirai A., Kondo T., Miyazaki J.I. (2017). Phylogenetic relationships of Japanese Unionoida (Mollusca: bivalvia) based on mitochondrial 16S rDNA sequences. Journal of Water Resource and Protection, 9(5): 493-509.

Sárkány-Kiss A., Sîrbu I., Hulea O. (2000). Expansion of the adventive

species Anodonta woodiana (Lea, 1834) (Mollusca, Bivalvia, Unionoidea) in central and eastern Europe. Acta Oecologica, 7: 49-57.

Sayenko E.M., Soroka M., Kholin S.K. (2017). Comparison of the species Sinanodonta amurensis Moskvicheva, 1973 and Sinanodonta primorjensis Bogatov et Zatrawkin, 1988 (Bivalvia: Unionidae: Anodontinae) in view of variability of the mitochondrial DNA cox1 gene and conchological features. Biological Bulletin of the Russian Academy of Sciences, 44(3): 266-276.

Soroka M. (2010). Characteristics of mitochondrial DNA of unionid bivalves (Mollusca: Bivalvia: Unionidae). II. Comparison of complete sequences of maternally inherited mitochondrial genomes of Sinanodonta woodiana and Unio pictorum. Folia Malacologica, 18(4): 189-209.

Sousa R., Novais A., Costa R., Strayer D.L. (2014). Invasive bivalves in fresh waters: Impacts from individuals to ecosystems and possible control strategies. Hydrobiologia, 735: 233-251.

Stelbrink B., Von Rintelen T., Albrecht C., Clewing C., Nagap O. (2019). Forgotten for decades: Lake Lanao and the genetic assessment of its mollusc diversity. Hydrobiologia, 843: 31-49.

Swofford D.L. 2003. PAUP: Phylogenetic analysis using parsimony (and other methods), Version 4. Sunderland: Sinauer Associates.

Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30: 2725-2729.

Urba?ska M., Kamocki A., Kirschenstein M., O?go M. (2021). The Chinese pond mussel Sinanodonta woodiana demographically outperforms European native mussel. Scientific Reports, 11: 7058.

Vaughn C.C. (2018). Ecosystem services provided by freshwater mussels. Hydrobiologia, 810: 15-27.

Villesen P. (2007). FaBox: an online toolbox for matrix choice. Nucleic Acids Research, 22: 4673-4680.

Von Proschwitz T. (2008). The Chinese giant mussel – Sinanodonta woodiana (Lea, 1834) (Bivalvia, Unionidae)-an unwelcome addition to the Swedish fauna. Basteria, 72: 307-311.

Walker J.M., Bogan A.E., Bonfiglio E.A., Campbell D.C., Christian A.D., Curole J.P., Harris J.L., Wojtecki R.J., Hoeh W.R. (2007). Primers for amplifying the hypervariable, male-transmitted COII-COI junction region in amblemine freshwater mussels (Bivalvia: Unionoidea: Ambleminae). Molecular Ecology Notes, 7: 489-491.

Walker J.M., Curole J.P., Wade D.E., Chapman E.G., Bogan A.E., Watters G.T., Hoeh W.R. (2006). Taxonomic distribution and phylogenetic utility of gender-associated mitochondrial genomes in the Unionoida (Bivalvia). Malacologia, 48: 265-282.

Zare M., Keivani Y., Ebrahimi E., Banaduc D. (2019). Karun river fish fauna elements. 7th Aquatic Biodiversity International Conference. Romania: Sibiu, Transylvania. 39 p.

Zieritz A., Taha H., Lopes-Lima M., Pfeiffer J., Sing K.W., Sulaiman Z., McGowan S., Rahim K.A.A. (2020). Towards the conservation of Borneo’s freshwater mussels: rediscovery of the endemic Ctenodesma borneensis and first record of the non-native Sinanodonta lauta. Biodiversity Conservation, 29(7): 2235-2253.