Lifting the curtain on the freshwater mussel diversity of the Italian Peninsula and Croatian Adriatic coast

Abstract

Freshwater mussels of the order Unionida have been dramatically declining globally. Despite their ecological importance, conservation of these animals has been hindered by unresolved taxonomy and a lack of data on the distribution and status of populations, especially in southern Europe. Although the Italian Peninsula has been noted as a centre of endemism and one of the major refugia of the glacial ages for several taxa, few studies have been performed on the genetic diversity of Unionida. Most importantly, the taxonomic status of several freshwater mussel populations of the Italian Peninsula is still unresolved. Here we present the first comprehensive dataset for the Unionida of the region spanning Italy and the coastal Croatian region (west of the Dinaric Alps). In total, 191 specimens were collected (85 Anodonta, 64 Unio, 17 Microcondylaea bonellii and 25 Sinanodonta woodiana) from 34 sites across the Italian Peninsula and coastal Croatian river basins for molecular identification (COI, 16S and 28S). Genetic analyses were performed to understand major phylogenetic and phylogeographic patterns. Seven species were detected: three Anodonta species (A. anatina, A. cygnea and A. exulcerata), two Unio species (U. mancus and U. elongatulus), Microcondylaea bonellii, and the invasive Sinanodonta woodiana. The presence of three endemic species (A. exulcerata, U. elongatulus and M. bonellii) confirms the importance of the region as a centre of endemism for freshwater mussels. The Apennine Mountains act as an important biogeographic barrier.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  1. Albrecht C, Lohfink D, Schultheiß R (2006) Dramatic decline and loss of mollusc diversity in long-lived lakes in Greece. Tentacle 14:11–13

    Google Scholar 

  2. Albrecht C, Bodon M, Cianfanelli S, Giusti F, Manganelli G (2011) Microcondylaea bonellii. The IUCN Red List of Threatened Species 2011: e.T155595A4805631. http://dx.doi.org/10.2305/IUCN.UK.2011-2.RLTS.T155595A4805631.en. Downloaded on 21 November 2016

  3. Araujo R, Gómez I, Machordom A (2005) The identity and biology of Unio mancus Lamarck, 1819 (=U. elongatulus) (Bivalvia: Unionidae) in the Iberian Peninsula. J Molluscan Stud 71:25–31. doi:10.1093/mollus/eyi002

    Article  Google Scholar 

  4. Araujo R, Toledo C, Machordom A (2009) Redescription of Unio gibbus Spengler, 1793, A West Palaearctic freshwater mussel with hookless glochidia. Malacologia 51:131–141. doi:10.4002/040.051.0109

    Article  Google Scholar 

  5. Badino G (1982) Unio elongatulus Pfeiffer (Bivalvia): variabilité biométrique et génétique des populations du Piémont (Italie du nord). Malacologia 22:673–677

    Google Scholar 

  6. Benejam L, Angermeier PL, Munné A, García-Berthou E (2010) Assessing effects of water abstraction on fish assemblages in Mediterranean streams. Freshw Biol 55:628–642. doi:10.1111/j.1365-2427.2009.02299.x

    Article  Google Scholar 

  7. Bogdanowicz W, Hulva P, Černá Bolfíková B, Buś MM, Rychlicka E, Sztencel-Jabłonka A, Cistrone L, Russo D (2015) Cryptic diversity of Italian bats and the role of the Apennine refugium in the phylogeography of the western Palaearctic. Zool J Linn Soc 174:635–648. doi:10.1111/zoj.12248

    Article  Google Scholar 

  8. Boggero A, Pierri C, Alber R, Austoni M, Barbone E, Bartolozzi L, Bertani I, Campanaro A, Cattaneo A, Cianferoni F, Colangelo P, Corriero G, Martin Dörr A, Elia AC, Ficetola GF, Fontaneto D, Gaino E, Goretti E, Kamburska L, La Porta G, Lauceri R, Lorenzoni M, Ludovisi A, Manca M, Morabito G, Nonnis Marzano F, Oggioni A, Riccardi N, Rossetti G, Tagliolato P, Thaler B, Ungaro N, Volta P, Zaupa S, Rosati I, Fiore N, Basset A, Marchetto A (2016) A geographic distribution data set of biodiversity in Italian freshwaters. Biogeographia 31:55–72. doi:10.21426/B631132737

    Google Scholar 

  9. Campanella L, Gatta T, Ravera O (2005) Relationship between anti-oxidant capacity and manganese accumulation in the soft tissues of two freshwater molluscs: Unio pictorum mancus (Lamellibranchia, Unionidae) and Viviparus ater (Gastropoda, Prosobranchia). J Limnol 64:153. doi:10.4081/jlimnol.2005.153

    Article  Google Scholar 

  10. Canestrelli D, Aloise G, Cecchetti S, Nascetti G (2010) Birth of a hotspot of intraspecific genetic diversity: notes from the underground. Mol Ecol 19:5432–5451. doi:10.1111/j.1365-294X.2010.04900.x

    Article  PubMed  Google Scholar 

  11. Cappelletti C, Cianfanelli S, Beltrami ME, Ciutti F (2009) Sinanodonta woodiana (Lea, 1834) (Bivalvia: Unionidae): a new non-indigenous species in Lake Garda (Italy). Aquat Invasions 4:685–688. doi:10.3391/ai.2009.4.4.15

    Article  Google Scholar 

  12. Carella F, Villari G, Maio N, De Vico G (2016) Disease and disorders of freshwater unionid mussels: a brief overview of recent studies. Front Physiol 7:489. doi:10.3389/fphys.2016.00489

    Article  PubMed  PubMed Central  Google Scholar 

  13. Cianfanelli S, Lori E, Bodon M (2007) Non-indigenous freshwater molluscs and their distribution in Italy. In: Gherardi F (ed) Biological invaders in inland waters: profiles, distribution, and threats. Springer, Berlin

    Google Scholar 

  14. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659. doi:10.1046/j.1365-294x.2000.01020.x

    CAS  Article  PubMed  Google Scholar 

  15. Colomba MS, Liberto F, Reitano A et al (2013) On the presence of Dreissena polymorpha Pallas, 1771 and Sinanodonta woodiana woodiana (Lea, 1834) in Sicily (Bivalvia). Biodivers J 4:571–580

    Google Scholar 

  16. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772. doi:10.1038/nmeth.2109

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  17. De Vico G, Maio N, Castagnolo L (2007) Prime segnalazione di Anodonta (Sinanodonta) woodiana (Lea, 1834) (Mollusca: Bivalvia: Unionidae) per il Sud Italia. Notiziario SIM 25:23–25

    Google Scholar 

  18. Donrovich SW, Douda K, Plechingerová V, Rylková K, Horký P, Slavík O, Liu H-Z, Reichard M, Lopes-Lima M, Sousa R (2017) Invasive Chinese pond mussel Sinanodonta woodiana threatens native mussel reproduction by inducing cross-resistance of host fish. Aquat Conserv Mar Freshw Ecosyst. doi:10.1002/aqc.2759

    Google Scholar 

  19. Fenoglio S, Bo T, Cucco M, Mercalli L, Malacarne G (2010) Effects of global climate change on freshwater biota: a review with special emphasis on the Italian situation. Ital J Zool 77:374–383. doi:10.1080/11250000903176497

    Article  Google Scholar 

  20. Fochetti R (2012) Italian freshwater biodiversity: status, threats and hints for its conservation. Ital J Zool 79:2–8. doi:10.1080/11250003.2011.620636

    Article  Google Scholar 

  21. Froufe E, Sobral C, Teixeira A, Sousa R, Varandas S, Aldridge DC, Lopes-Lima M (2014) Genetic diversity of the pan-European freshwater mussel Anodonta anatina (Bivalvia: Unionoida) based on CO1: new phylogenetic insights and implications for conservation. Aquat Conserv Mar Freshw Ecosyst 24:561–574. doi:10.1002/aqc.2456

    Article  Google Scholar 

  22. Froufe E, Gonçalves DV, Teixeira A, Sousa R, Varandas S, Ghamizi M, Zieritz A, Lopes-Lima M (2016a) Who lives where? Molecular and morphometric analyses clarify which Unio species (Unionida, Mollusca) inhabit the southwestern Palearctic region. Org Divers Evol 16:597–611. doi:10.1007/s13127-016-0262-x

    Article  Google Scholar 

  23. Froufe E, Prié V, Faria J, Ghamizi M, Gonçalves DV, Gürlek ME, Karaouzas I, Kebapçi U, Sereflisan H, Sobral C, Sousa R, Teixeira A, Varandas S, Zogaris S, Lopes-Lima M (2016b) Phylogeny, phylogeography, and evolution in the Mediterranean region: news from a freshwater mussel (Potomida, Unionida). Mol Phylogenet Evol 100:322–332. doi:10.1016/j.ympev.2016.04.030

    Article  PubMed  Google Scholar 

  24. Froufe E, Gan HM, Lee YP, Carneiro J, Varandas S, Teixeira A, Zieritz A, Sousa R, Lopes-Lima M (2016c) The male and female complete mitochondrial genome sequences of the Endangered freshwater mussel Potomida littoralis (Cuvier, 1798) (Bivalvia: Unionidae). Mitochondrial DNA Part A 27:3571–3572. doi:10.3109/19401736.2015.1074223

    CAS  Article  Google Scholar 

  25. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Geist J, Söderberg H, Karlberg A, Kuehn R (2010) Drainage-independent genetic structure and high genetic diversity of endangered freshwater pearl mussels (Margaritifera margaritifera) in northern Europe. Conserv Genet 11:1339–1350. doi:10.1007/s10592-009-9963-4

    Article  Google Scholar 

  27. Gherardi F, Bertolino S, Bodon M, Casellato S, Cianfanelli S, Ferraguti M, Lori E, Mura G, Nocita A, Riccardi N, Rossetti G, Rota E, Scalera R, Zerunian S, Tricarico E (2008) Animal xenodiversity in Italian inland waters: distribution, modes of arrival, and pathways. Biol Invasions 10:435–454. doi:10.1007/s10530-007-9142-9

    Article  Google Scholar 

  28. Giovannotti M, Nisi-Cerioni P, Caputo V (2010) Mitochondrial DNA sequence analysis reveals multiple Pleistocene glacial refugia for Podarcis muralis (Laurenti, 1768) in the Italian Peninsula. Ital J Zool 77:277–288. doi:10.1080/11250000903143885

    CAS  Article  Google Scholar 

  29. Giusti F, Castagnolo L, Farina LM, Renzoni A (1975) The reproductive cycle and the glochidium of Anodonta cygnea L. from Lago Trasimeno (Central Italy). Monit Zool Ital 9:99–118

    Google Scholar 

  30. Gómez A, Lunt D (2007) Refugia within refugia: patterns of phylogeographic concordance in the Iberian Peninsula. In: Weiss S, Ferrand N (eds) Phylogeography in Southern European Refugia: evolutionary perspectives on the origin and conservation of European biodiversity. Springer, Dordrecht, pp 155–188

    Google Scholar 

  31. Graf DL, Cummings KS (2017) The MUSSEL project database. http://musselproject.uwsp.edu/db/. Accessed 05 June 2017

  32. Guidi P, Frenzilli G, Benedetti M, Bernardeschi M, Falleni A, Fattorini D, Regoli F, Scarcelli V, Nigro M (2010) Antioxidant, genotoxic and lysosomal biomarkers in the freshwater bivalve (Unio pictorum) transplanted in a metal polluted river basin. Aquat Toxicol 100:75–83. doi:10.1016/j.aquatox.2010.07.009

    CAS  Article  PubMed  Google Scholar 

  33. Haas F (1969) Superfamilia Unionacea. Das Tierrich, vol 88. Walter de Gruyter, Berlin

    Google Scholar 

  34. Hall T (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  35. Hewitt GM (1999) Post-glacial re-colonization of European biota. Biol J Linn Soc 68:87–112. doi:10.1111/j.1095-8312.1999.tb01160.x

    Article  Google Scholar 

  36. Killeen I, Aldridge D (2011) Anodonta cygnea. The IUCN Red List of Threatened Species 2011: e.T156066A4907255. Downloaded on 22 November 2016

  37. Klenovšek D, Govedič M, Vaupotič M (2012) Record of the China mussel Sinanodonta woodiana (Lea, 1834) (Bivalvia: Unionidae) in Slovenia. Nat Slov 14:35–37

    Google Scholar 

  38. Lajtner J, Crnčan P (2011) Distribution of the invasive bivalve Sinanodonta woodiana (Lea, 1834) in Croatia. Aquat Invasions 6(suppl 1):S119–S124

    Article  Google Scholar 

  39. Lajtner J, Crnčan P (2014) Spreading of the invasive bivalve Sinanodonta woodiana (Lea, 1834) in Croatia. Book of Abstracts of the 1st Croatian Symposium on invasive species (ed. S. Jelaska), 24. November 2014, Zagreb, Croatia

  40. Lopes-Lima M (2014a) Anodonta cygnea. The IUCN Red List of Threatened Species 2014: e.T156066A21400900. http://dx.doi.org/10.2305/IUCN.UK.2014-1.RLTS.T156066A21400900.en. Downloaded on 21 November 2016

  41. Lopes-Lima M (2014b) Anodonta anatina. The IUCN Red List of Threatened Species 2014: e.T155667A21400363. http://dx.doi.org/10.2305/IUCN.UK.2014-1.RLTS.T155667A21400363.en. Downloaded on 21 November 2016

  42. Lopes-Lima M, Seddon MB (2014) Unio mancus. The IUCN Red List of Threatened Species 2014: e.T22737A42466471. http://dx.doi.org/10.2305/IUCN.UK.2014-3.RLTS.T22737A42466471.en. Downloaded on 21 November 2016

  43. Lopes-Lima M, Teixeira A, Froufe E, Lopes A, Varandas S, Sousa R (2014) Biology and conservation of freshwater bivalves: past, present and future perspectives. Hydrobiologia 735:1–13. doi:10.1007/s10750-014-1902-9

    Article  Google Scholar 

  44. Lopes-Lima M, Froufe E, Do VT, Ghamizi M, Mock KE, Kebapçi Ü, Klishko O, Kovitvadhi S, Kovitvadhi U, Paulo OS, Pfeiffer JM, Raley M, Riccardi N, Şereflişan H, Sousa R, Teixeira A, Varandas S, Wu X, Zanatta DT, Zieritz A, Bogan AE (2017a) Phylogeny of the most species-rich freshwater bivalve family (Bivalvia: Unionida: Unionidae): defining modern subfamilies and tribes. Mol Phylogenet Evol 106:174–191. doi:10.1016/j.ympev.2016.08.021

    Article  PubMed  Google Scholar 

  45. Lopes-Lima M, Sousa R, Geist J, Aldridge DC, Araujo R, Bergengren J, Bespalaja Y, Bódis E, Burlakova L, Van Damme D, Douda K, Froufe E, Georgiev D, Gumpinger C, Karatayev A, Kebapçi U, Killeen I, Lajtner J, Larsen BM, Lauceri R, Legakis A, Lois S, Lundberg S, Moorkens E, Motte G, Nagel KO, Ondina P, Outeiro A, Paunovic M, Prié V, von Proschwitz T, Riccardi N, Rudzīte M, Rudzītis M, Scheder C, Seddon M, Şereflişan H, Simić V, Sokolova S, Stoeckl K, Taskinen J, Teixeira A, Thielen F, Trichkova T, Varandas S, Vicentini H, Zajac K, Zajac T, Zogaris S (2017b) Conservation status of freshwater mussels in Europe: state of the art and future challenges. Biol Rev 92:572–607. doi:10.1111/brv.12244

    Article  PubMed  Google Scholar 

  46. Machordom A, Araujo R, Erpenbeck D, Ramos M-Á (2003) Phylogeography and conservation genetics of endangered European Margaritiferidae (Bivalvia: Unionoidea). Biol J Linn Soc 78:235–252. doi:10.1046/j.1095-8312.2003.00158.x

    Article  Google Scholar 

  47. Magri D (2008) Patterns of post-glacial spread and the extent of glacial refugia of European beech (Fagus sylvatica). J Biogeogr 35:450–463. doi:10.1111/J.1365-2699.2007.01803.X

    Article  Google Scholar 

  48. Manganelli G, Bodon M, Favilli L, Castagnolo L, Giusti F (1998) Checklist delle specie della fauna d’Italia, molluschi terrestri e d’acqua dolce. Boll Malacol 33:151–156

    Google Scholar 

  49. Mezzasalma M, Dall’asta A, Loy A, Cheylan M, Lymberakis P, Zuffi MA, Tomovi_c L, Odierna G, Guarino FM (2015) A sisters’ story: comparative phylogeography and taxonomy of Hierophis viridiflavus and H. gemonensis (Serpentes, Colubridae). R Swed Acad Sciences 44:495–508

    Google Scholar 

  50. Mienis H (2012) Additional information concerning the conquest of Europe by the invasive chinese pond mussel Sinanodonta woodiana, 36. News from Austria, Belgium, France, Greece, Hungary and Italy. Ellipsaria 16:12–13

    Google Scholar 

  51. Nagel KO, Badino G (2001) Population genetics and systematics of European Unionoidea. In: Bauer G, Wächtler B (eds) Ecology and evolution of the freshwater mussels Unionoida. Springer, Berlin, pp 51–80

    Google Scholar 

  52. Nagel K-O, Badino G, Alessandria B (1996) Population genetics of European anodontinae (Bivalvia: Unionidae). J Molluscan Stud 62:343–357. doi:10.1093/mollus/62.3.343

    Article  Google Scholar 

  53. Nagel K-O, Castagnolo L, Cencetti E, Moro GA (2007) Notes on reproduction, growth and habitat of Microcondylaea bonellii (Mollusca: Bivalvia: Unionidae) in the Torrente Versa (Italy). Mollusca 25:41–49

    Google Scholar 

  54. Naimo TJ, Damschen ED, Rada RG, Monroe EM (1998) Nonlethal evaluation of the physiological health of unionid mussels: methods for biopsy and glycogen analysis. J North Am Benthol Soc 17:121–128

    Article  Google Scholar 

  55. Palumbi SR, Martin AP, Romano S, McMillan WO, Stice L, Grabowski G (1991) The Simple Fool’s Guide to PCR, Version 2.0. Published and distributed by the authors, Honolulu

  56. Panini E, Sicuro B, Daprà F, Forneris G (2008) Preliminary considerations for freshwater mussel reproduction and possible application for extensive rearing in Italy. J Conch 39:709–716

    Google Scholar 

  57. Paunović M, Csány B, Simic V, Stojanovic B, Cakic P (2006) Distribution of Anodonta (Sinanodonta) woodiana (Lea 1834 in inland waters of Serbia. Aquat Invasions 1:154–160

    Article  Google Scholar 

  58. Polettini AE, Fortaner S, Farina M, Groppi F, Manenti S, Libralato G, Sabbioni E (2015) Uptake from water, internal distribution and bioaccumulation of selenium in Scenedesmus obliquus, Unio mancus and Rattus norvegicus: part A. Bull Environ Contam Toxicol 94:84–89. doi:10.1007/s00128-014-1407-2

    CAS  Article  PubMed  Google Scholar 

  59. Pou-Rovira Q, Araujo R, Boix D, Clavero M, Feo C, Ordeix M, Zamora L (2009) Presence of the alien chinese pond mussel Anodonta woodiana (Lea, 1834) (Bivalvia, Unionidae) in the Iberian Peninsula. Graellsia 65:67–70. doi:10.3989/graellsia.2009.v65.i1.137

    Article  Google Scholar 

  60. Prié V, Puillandre N (2014) Molecular phylogeny, taxonomy, and distribution of French Unio species (Bivalvia, Unionidae). Hydrobiologia 735:95–110. doi:10.1007/s10750-013-1571-0

    Article  Google Scholar 

  61. Prié V, Puillandre N, Bouchet P (2012) Bad taxonomy can kill: molecular reevaluation of Unio mancus Lamarck, 1819 (Bivalvia: Unionidae) and its accepted subspecies. Knowl Manag Aquat Ecosyst 8:1–18. doi:10.1051/kmae/2012014

    Google Scholar 

  62. Rambaut A, Suchard MA, Xie D, Drummond AJ (2014) Tracer v1. 6 Computer Program and Documentation Distributed by the Author. http://beast.bio.ed.ac.uk/Tracer

  63. Ravera O, Sprocati AR (1997) Population dynamics, production, assimilation and respiration of two fresh water mussels: Unio mancus, Zhadin and Anodonta cygnea Lam. Mem Ist Ital Di Idrobiol 56:113–130

    Google Scholar 

  64. Ravera O, Beone GM, Trincherini PR, Riccardi N (2007) Seasonal variations in metal content of two Unio pictorum mancus (Mollusca, Unionidae) populations from two lakes of different trophic state. J Limnol 66:28–39. doi:10.4081/jlimnol.2007.28

    Article  Google Scholar 

  65. Reischütz A, Reischütz N, Reischütz PL (2014) Helleniká pantoía, 36. Noch einmal zur Molluskenfauna des Pamvotis-Sees (Epirus, Griechenland). Nachrichtenblatt der Ersten Vor Malakol Gesellschaft 21:83–86

    Google Scholar 

  66. Renda W, Niero I (2014) Nuove segnalazioni di Sinanodonta woodiana woodiana (Lea, 1834) (Mollusca: Bivalvia: Unionidae) per il sud Italia. Not SIM 32:14–16

    Google Scholar 

  67. Riccardi N, Froufe E, Lopes-Lima M, Mazzoli C (2016) When and how? Freshwater mussel recolonization in Lake Orta. J Limnol 75(s2):120–130. doi:10.4081/jlimnol.2016.1286

    Google Scholar 

  68. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. doi:10.1093/sysbio/sys029

    Article  PubMed  PubMed Central  Google Scholar 

  69. Sabbioni E, Polettini AE, Fortaner S, Farina M, Groppi F, Manenti S, Libralato G (2015) Uptake from water, internal distribution and bioaccumulation of selenium in Scenedesmus obliquus, Unio mancus and Rattus norvegicus: part B. Bull Environ Contam Toxicol 94:90–95. doi:10.1007/s00128-014-1406-3

    CAS  Article  PubMed  Google Scholar 

  70. Salvi D, Harris D, Kaliontzopoulou A, Carretero MA, Pinho C (2013) Persistence across Pleistocene ice ages in Mediterranean and extra-Mediterranean refugia: phylogeographic insights from the common wall lizard. BMC Evol Biol 13:147. doi:10.1186/1471-2148-13-147

    Article  PubMed  PubMed Central  Google Scholar 

  71. Sambrook J, Fritsch EFMT (1989) Molecular cloning. A Laboratory Manual. Cold Spring Harbor Laboratory Press, Plainview

    Google Scholar 

  72. Sàrkàny-Kiss A (1986) Anodonta woodiana (Lea, 1834) a new species in Romania (Bivalvia, Unionacea). Trav Mus Hist Nat Grigore Antipa 28:15–17

    Google Scholar 

  73. Schmitt T (2007) Molecular biogeography of Europe: pleistocene cycles and postglacial trends. Front Zool 4:11. doi:10.1186/1742-9994-4-11

    Article  PubMed  PubMed Central  Google Scholar 

  74. Sicuro B, Mioletti S, Abete C, Amedeo S, Panini E, Forneris G (2010) Potential utilisation of farmed freshwater mussels (Anodonta anatina and Unio mancus) in Italy. Cuba J Agric Sci 44:409–414

    Google Scholar 

  75. Sicuro B, Panini E, Forneris G (2015) A floating cage system for rearing freshwater mussels Anodonta anatina and Unio mancus in Piedmont region (NW Italy). Iran J Fish Sci 14:754–766

    Google Scholar 

  76. Sousa R, Novais A, Costa R, Strayer DL (2014) Invasive bivalves in fresh waters: impacts from individuals to ecosystems and possible control strategies. Hydrobiologia 735:233–251

    Article  Google Scholar 

  77. Taberlet P, Fumagalli L, Wust-Saucy AG, Cosson JF (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol. doi:10.1046/j.1365-294x.1998.00289.x

    Google Scholar 

  78. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. doi:10.1093/molbev/mst197

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  80. Tomović J, Zorić K, Simić V, Kostić M, Kljajić Z, Lajtner J, Paunović M (2013) The first record of the Chinese pond mussel Sinanodonta woodiana (Lea, 1834) in Montenegro. Arch Biol Sci 65:1525–1533

    Article  Google Scholar 

  81. Vilaça ST, Biosa D, Zachos F, Iacolina L, Kirschning J, Alves PC, Paule L, Gortazar C, Mamuris Z, Jędrzejewska B, Borowik T, Sidorovich VE, Kusak J, Costa S, Schley L, Hartl GB, Apollonio M, Bertorelle G, Scandura M (2014) Mitochondrial phylogeography of the European wild boar: the effect of climate on genetic diversity and spatial lineage sorting across Europe. J Biogeogr 41:987–998. doi:10.1111/jbi.12268

    Article  Google Scholar 

  82. Volta P, Jepsen N (2008) The recent invasion of Rutilus rutilus (L.) (Pisces: Cyprinidae) in a large South-Alpine lake: Lago Maggiore. J Limnol 67:163. doi:10.4081/jlimnol.2008.163

    Article  Google Scholar 

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

    Google Scholar 

  84. Walker JM, Curole JP, Wade DE, Chapman EG, Bogan AE, Watters GT, Hoeh WR (2006) Taxonomic distribution and phylogenetic utility of gender-associated mitochondrial genomes in the unionoida (Bivalvia). Malacologia 48:265–282

    Google Scholar 

  85. Whiting MF (2002) Mecoptera is paraphyletic: multiple genes and phylogeny of Mecoptera and Siphonaptera. Zool Scr 31:93–104. doi:10.1046/j.0300-3256.2001.00095.x

    Article  Google Scholar 

  86. Yurishinets V, Korniushin A (2001) The new species in the fauna of Ukraine Anodonta woodiana woodiana (Lea, 1834) (Bivalvia, Unionidae), its diagnostics and possible ways of introduction. Vestn Zool 35:79–84

    Google Scholar 

  87. Zieritz A, Aldridge DC (2011) Sexual, habitat-constrained and parasite-induced dimorphism in the shell of a freshwater mussel (Anodonta anatina, Unionidae). J Morphol 272:1365–1375. doi:10.1002/jmor.10990

    Article  PubMed  Google Scholar 

  88. Zieritz A, Hoffman JI, Amos W, Aldridge DC (2010) Phenotypic plasticity and genetic isolation-by-distance in the freshwater mussel Unio pictorum (Mollusca: Unionoida). Evol Ecol 24:923–938

    Article  Google Scholar 

Download references

Acknowledgements

This work was partially supported by the Portuguese Foundation for Science and Technology (FCT) under grants SFRH/BPD/108445/2015 (EF) and SFRH/BD/115728/2016 (MLL). Cindy Bogan reviewed a draft of this manuscript. We are grateful to the two anonymous reviewers for their helpful remarks and suggestions that improved the quality of the manuscript; and to the Göteborg Natural History Museum for the loan of Swedish tissue samples.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Elsa Froufe.

Additional information

This article belongs to the Topical Collection: Coastal and marine biodiversity.

Communicated by Robert Cowie.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Froufe, E., Lopes-Lima, M., Riccardi, N. et al. Lifting the curtain on the freshwater mussel diversity of the Italian Peninsula and Croatian Adriatic coast. Biodivers Conserv 26, 3255–3274 (2017). https://doi.org/10.1007/s10531-017-1403-z

Download citation

Keywords

  • Unionida
  • Italy
  • Croatia
  • Biogeography
  • Genetic diversity
  • Conservation