Marine Biodiversity

, Volume 47, Issue 4, pp 1045–1055 | Cite as

Genetic diversity of the Acropora-associated hydrozoans: new insight from the Red Sea

  • Davide Maggioni
  • Simone Montano
  • Roberto Arrigoni
  • Paolo Galli
  • Stefania Puce
  • Daniela Pica
  • Michael L. Berumen
Red Sea Biodiversity


To date, four nominal species and several other unidentified species of Zanclea hydrozoans are known to live symbiotically with scleractinians, and recent surveys reported this association also in the Red Sea. Previous molecular studies showed that each coral genus involved in this association hosts only one species or molecular clade of Zanclea, with the only exception being the genus Acropora, which hosts at least two Zanclea species. Moreover, some of the detected genetic lineages were morphologically undistinguishable in the polyp stage, suggesting the presence of cryptic species. In this study, we investigated the morphology and genetic diversity of Acropora-associated Zanclea specimens collected in previous studies in Egypt and Israel, as well as new samples collected in Saudi Arabia. Based on the current data, all the analysed samples were morphologically identical to Zanclea gallii, a species associated with Acropora corals from the Maldives. However, molecular analyses separated the samples collected in the Red Sea from all other coral-associated hydroids. Therefore, phylogenetic reconstructions, haplotype networks, genetic distance analyses and distribution data allowed us to identify a previously unknown cryptic species of Acropora-associated hydroid, here named Zanclea gallii IIa, following a recently proposed molecular nomenclature.


Symbiosis Zanclea Integrative taxonomy Cryptic species Biodiversity Coral reefs Molecular nomenclature 



This research was undertaken in accordance with the policies and procedures of the King Abdullah University of Science and Technology (KAUST). Permissions relevant for KAUST to undertake the research have been obtained from the applicable governmental agencies in the Kingdom of Saudi Arabia. The authors wish to thank the members of the Reef Ecology Lab at King Abdullah University of Science and Technology and, in particular, Tullia Terraneo (KAUST) and Malek Amr Gusti (KAUST) for logistic support. Many thanks go to the staff of the iDive and Open Ocean Science Centre in Dahab, especially to Inga Dehnert and Hans Lange for their help in the field activities. We also want to thank all the staff of the Interuniversity Institute for Marine Sciences (IUI) in Eilat for their logistic support. Finally, we thank the two anonymous reviewers for their constructive comments. This project was partly supported by funding from KAUST (award # FCC/1/1973-07 and baseline research funds to MLB) and University of Milano-Bicocca (baseline research fund to PG). The samples from Eilat were collected during the project ‘HyDRa’ (ASSEMBLE grant no. 227799).

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  1. Alamaru A, Brokovich E, Loya Y (2016) Four new species and three new records of benthic ctenophores (Family: Coeloplanidae) from the Red Sea. Mar Biodivers 46:261–279. doi: 10.1007/s12526-015-0362-4 CrossRefGoogle Scholar
  2. Appeltans W, Ahyong ST, Anderson G et al (2012) The magnitude of global marine species diversity. Curr Biol 22:2189–2202. doi: 10.1016/j.cub.2012.09.036 CrossRefPubMedGoogle Scholar
  3. Arrigoni R, Berumen ML, Huang D, Terraneo TI, Benzoni F (2016) Cyphastrea (Cnidaria: Scleractinia: Merulinidae) in the Red Sea: phylogeny and a new reef coral species. Invertebr Syst. doi: 10.1071/IS16035
  4. Bailey G (2010) The Red Sea, coastal landscapes, and hominin dispersals. In: Petraglia MD, Rose JI (eds) The evolution of human populations in Arabia. Springer, Dordrecht, pp 15–37. doi: 10.1007/978-90-481-2719-1_2
  5. Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48. doi: 10.1093/oxfordjournals.molbev.a026036 CrossRefPubMedGoogle Scholar
  6. Baum DA, Shaw KL (1995) Genealogical perspectives on the species problem. In: Hoch PC, Stephenson AG (eds) Experimental and molecular approaches to plant biosystematics. Monographs in systematics, vol 53. Missouri Botanical Garden, St. Louis, pp 289–303Google Scholar
  7. Bergmann T, Hadrys H, Breves G, Schierwater B (2009) Character-based DNA barcoding: a superior tool for species classification. Berl Munch Tierarztl Wochenschr 122:446–450. doi: 10.2376/0005-9366-122-446 PubMedGoogle Scholar
  8. Berumen ML, Hoey AS, Bass WH et al (2013) The status of coral reef ecology research in the Red Sea. Coral Reefs 32:737–748. doi: 10.1007/s00338-013-1055-8 CrossRefGoogle Scholar
  9. Bo M, Di Camillo CG, Puce S et al (2011) A tubulariid hydroid associated with anthozoan corals in the Mediterranean Sea. Ital J Zool 78:487–496. doi: 10.1080/11250003.2011.568015 CrossRefGoogle Scholar
  10. Boero F, Bouillon J, Gravili C (2000) A survey of Zanclea, Halocoryne and Zanclella (Cnidaria, Hydrozoa, Anthomedusae, Zancleidae) with description of new species. Ital J Zool 67:93–124. doi: 10.1080/11250000009356301 CrossRefGoogle Scholar
  11. Bouchet P, Lozouet P, Maestrati P, Heros V (2002) Assessing the magnitude of species richness in tropical marine environments: exceptionally high numbers of molluscs at a New Caledonia site. Biol J Linn Soc 75:421–436. doi: 10.1046/j.1095-8312.2002.00052.x CrossRefGoogle Scholar
  12. Campbell AC (1987) Echinoderms of the Red Sea. Pergamon Press, OxfordCrossRefGoogle Scholar
  13. Churchill CK, Valdés Á, Foighil DÓ (2014) Molecular and morphological systematics of neustonic nudibranchs (Mollusca: Gastropoda: Glaucidae: Glaucus), with descriptions of three new cryptic species. Invertebr Syst 28:174–195. doi: 10.1071/IS13038 CrossRefGoogle Scholar
  14. Cunningham CW, Buss LW (1993) Molecular evidence for multiple episodes of paedomorphosis in the family Hydractiniidae. Biochem Syst Ecol 21:57–69. doi: 10.1016/0305-1978(93)90009-G CrossRefGoogle Scholar
  15. DiBattista JD, Howard Choat J, Gaither MR et al (2016a) On the origin of endemic species in the Red Sea. J Biogeogr 43:13–30. doi: 10.1111/jbi.12631 CrossRefGoogle Scholar
  16. DiBattista JD, Roberts MB, Bouwmeester J et al (2016b) A review of contemporary patterns of endemism for shallow water reef fauna in the Red Sea. J Biogeogr 43:423–439. doi: 10.1111/jbi.12649 CrossRefGoogle Scholar
  17. Eshel G, Cane MA, Blumenthal MB (1994) Modes of subsurface, intermediate, and deep water renewal in the Red Sea. J Geophys Res Oceans 99:15941–15952. doi: 10.1029/94JC01131 CrossRefGoogle Scholar
  18. Fisk DA, Harriott VJ (1990) Spatial and temporal variation in coral recruitment on the Great Barrier Reef: implications for dispersal hypotheses. Mar Biol 107:485–490. doi: 10.1007/BF01313433 CrossRefGoogle Scholar
  19. 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. Mol Mar Biol Biotechnol 3:294–299PubMedGoogle Scholar
  20. Fontana S, Keshavmurthy S, Hsieh HJ et al (2012) Molecular evidence shows low species diversity of coral-associated hydroids in Acropora corals. PLoS One 7:e50130. doi: 10.1371/journal.pone.0050130 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Fontaneto D, Flot JF, Tang CQ (2015) Guidelines for DNA taxonomy, with a focus on the meiofauna. Mar Biodivers 45:433–451. doi: 10.1007/s12526-015-0319-7 CrossRefGoogle Scholar
  22. Furby KA, Bouwmeester J, Berumen ML (2013) Susceptibility of central Red Sea corals during a major bleaching event. Coral Reefs 32:505–513. doi: 10.1007/s00338-012-0998-5 CrossRefGoogle Scholar
  23. Gegenbaur C (1856) Versuch eines Systemes der Medusen, mit Beschreibung neuer oder wenig gekannter Formen; zugleich ein Beitrag zur Kenntniss der Fauna des Mittelmeeres. Z Wiss Zool 8:202–273Google Scholar
  24. Gittenberger A, Gittenberger E (2011) Cryptic, adaptive radiation of endoparasitic snails: sibling species of Leptoconchus (Gastropoda: Coralliophilidae) in corals. Org Divers Evol 11:21–41. doi: 10.1007/s13127-011-0039-1 CrossRefGoogle Scholar
  25. Goldstein PZ, DeSalle R (2011) Integrating DNA barcode data and taxonomic practice: determination, discovery, and description. Bioessays 33:135–147. doi: 10.1002/bies.201000036 CrossRefPubMedGoogle Scholar
  26. Gravili C, Camillo CG, Piraino S, Boero F (2013) Hydrozoan species richness in the Mediterranean Sea: past and present. Mar Ecol 34:41–62. doi: 10.1111/maec.12023 CrossRefGoogle Scholar
  27. Guinot DA (1967) La faune carcinologique (Crustacea Brachyura) de l’océan Indien occidental et de la Mer Rouge. Catalogue, remarques biogéographiques et bibliographie. Mém Inst Fondam Afrique Noire 77:235–252Google Scholar
  28. Guzner B, Novoplansky A, Chadwick NE (2007) Population dynamics of the reef-building coral Acropora hemprichii as an indicator of reef condition. Mar Ecol Prog Ser 333:143–150. doi: 10.3354/meps333143 CrossRefGoogle Scholar
  29. Harriott VJ (1992) Recruitment patterns of scleractinian corals in an isolated sub-tropical reef system. Coral Reefs 11:215–219. doi: 10.1007/BF00301996 CrossRefGoogle Scholar
  30. Hirose M, Hirose E (2012) A new species of Zanclea (Cnidaria: Hydrozoa) associated with scleractinian corals from Okinawa, Japan. J Mar Biol Assoc UK 92:877–884. doi: 10.1017/S0025315411001238 CrossRefGoogle Scholar
  31. Hudson RR, Coyne JA (2002) Mathematical consequences of the genealogical species concept. Evolution 56:1557–1565. doi: 10.1554/0014-3820(2002)056[1557:MCOTGS]2.0.CO;2 CrossRefPubMedGoogle Scholar
  32. Hughes TP, Bellwood DR, Connolly SR (2002) Biodiversity hotspots, centres of endemicity, and the conservation of coral reefs. Ecol Lett 5:775–784. doi: 10.1046/j.1461-0248.2002.00383.x CrossRefGoogle Scholar
  33. Johnson SB, Warén A, Tunnicliffe V et al (2015) Molecular taxonomy and naming of five cryptic species of Alviniconcha snails (Gastropoda: Abyssochrysoidea) from hydrothermal vents. Syst Biodivers 13:278–295. doi: 10.1080/14772000.2014.970673 CrossRefGoogle Scholar
  34. Jörger KM, Schrödl M (2013) How to describe a cryptic species? Practical challenges of molecular taxonomy. Front Zool 10:59. doi: 10.1186/1742-9994-10-59 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Jörger KM, Schrödl M (2014) How to use CAOS software for taxonomy? A quick guide to extract diagnostic nucleotides or amino acids for species descriptions. Spixiana 37:21–26Google Scholar
  36. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. doi: 10.1093/molbev/mst010 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Knowlton N (2000) Molecular genetic analyses of species boundaries in the sea. Hydrobiologia 420:73–90. doi: 10.1023/A:1003933603879 CrossRefGoogle Scholar
  38. Lanfear R, Calcott B, Ho SY, Guindon S (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol 29:1695–1701. doi: 10.1093/molbev/mss020 CrossRefPubMedGoogle Scholar
  39. Linnaeus C (1758) Systema Naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Editio decima, reformata. Holmiae, StockholmGoogle Scholar
  40. Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, Van Woesik R (2001) Coral bleaching: the winners and the losers. Ecol Lett 4:122–131. doi: 10.1046/j.1461-0248.2001.00203.x CrossRefGoogle Scholar
  41. Maggioni D, Montano S, Seveso D, Galli P (2016) Molecular evidence for cryptic species in Pteroclava krempfi (Hydrozoa, Cladocorynidae) living in association with alcyonaceans. Syst Biodivers 14:484–493. doi: 10.1080/14772000.2016.1170735 CrossRefGoogle Scholar
  42. Marshall PA, Baird AH (2000) Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa. Coral Reefs 19:155–163. doi: 10.1007/s003380000086 CrossRefGoogle Scholar
  43. Medlin L, Elwood HJ, Stickel S, Sogin ML (1988) The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71:491–499. doi: 10.1016/0378-1119(88)90066-2 CrossRefPubMedGoogle Scholar
  44. Millard NAH, Bouillon J (1974) A collection of hydroids from Moçambique, East Africa. Ann S Afr Mus 65:1–40Google Scholar
  45. Montano S, Seveso D, Galli P, Obura DO (2010) Assessing coral bleaching and recovery with a colour reference card in Watamu Marine Park, Kenya. Hydrobiologia 655:99–108. doi: 10.1007/s10750-010-0407-4 CrossRefGoogle Scholar
  46. Montano S, Maggioni D, Galli P, Seveso D, Puce S (2013) Zanclea–coral association: new records from Maldives. Coral Reefs 32:701. doi: 10.1007/s00338-013-1023-3 CrossRefGoogle Scholar
  47. Montano S, Galli P, Maggioni D, Seveso D, Puce S (2014) First record of coral-associated Zanclea (Hydrozoa, Zancleidae) from the Red Sea. Mar Biodivers 44:581–584. doi: 10.1007/s12526-014-0207-6 CrossRefGoogle Scholar
  48. Montano S, Arrigoni R, Pica D, Maggioni D, Puce S (2015a) New insights into the symbiosis between Zanclea (Cnidaria, Hydrozoa) and scleractinians. Zool Scr 44:92–105. doi: 10.1111/zsc.12081 CrossRefGoogle Scholar
  49. Montano S, Maggioni D, Arrigoni R, Seveso D, Puce S, Galli P (2015b) The hidden diversity of Zanclea associated with scleractinians revealed by molecular data. PLoS One 10:e0133084. doi: 10.1371/journal.pone.0133084 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Montano S, Seveso D, Galli P, Puce S, Hoeksema BW (2015c) Mushroom corals as newly recorded hosts of the hydrozoan symbiont Zanclea sp. Mar Biol Res 11:773–779. doi: 10.1080/17451000.2015.1009467 CrossRefGoogle Scholar
  51. Montano S, Galli P, Hoeksema BW (2016a) First record from the Atlantic: a Zanclea-scleractinian association at St. Eustatius, Dutch Caribbean. Mar Biodivers 1–2. doi: 10.1007/s12526-015-0432-7
  52. Montano S, Maggioni D, Galli P, Hoeksema BW (2016b) A cryptic species in the Pteroclava krempfi species complex (Hydrozoa, Cladocorynidae) revealed in the Caribbean. Mar Biodivers 1–7. doi: 10.1007/s12526-016-0555-5
  53. Morard R, Escarguel G, Weiner AK et al (2016) Nomenclature for the nameless: a proposal for an integrative molecular taxonomy of cryptic diversity exemplified by planktonic foraminifera. Syst Biol 65:925–940. doi: 10.1093/sysbio/syw031 CrossRefPubMedGoogle Scholar
  54. Pantos O, Bythell JC (2010) A novel reef coral symbiosis. Coral Reefs 29:761–770. doi: 10.1007/s00338-010-0622-5 CrossRefGoogle Scholar
  55. Pantos O, Hoegh-Guldberg O (2011) Shared skeletal support in a coral-hydroid symbiosis. PLoS One 6:e20946. doi: 10.1371/journal.pone.0020946 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Pearson RG (1981) Recovery and recolonization of coral reefs. Mar Ecol Prog Ser 4:105–122CrossRefGoogle Scholar
  57. Pica D, Bastari A, Vaga CF, Di Camillo CG, Montano S, Puce S (in press) Hydroid diversity of Eilat Bay with the description of a new Zanclea species. Mar Biol Res. doi: 10.1080/17451000.2016.1236202
  58. Puce S, Cerrano C, Boyer M, Ferretti C, Bavestrello G (2002) Zanclea (Cnidaria: Hydrozoa) species from Bunaken Marine Park (Sulawesi Sea, Indonesia). J Mar Biol Assoc UK 82:943–954. doi: 10.1017/S0025315402006434 CrossRefGoogle Scholar
  59. Puce S, Cerrano C, Di Camillo CG, Bavestrello G (2008a) Hydroidomedusae (Cnidaria: Hydrozoa) symbiotic radiation. J Mar Biol Assoc UK 88:1715–1721. doi: 10.1017/S0025315408002233 CrossRefGoogle Scholar
  60. Puce S, Di Camillo CG, Bavestrello G (2008b) Hydroids symbiotic with octocorals from the Sulawesi Sea, Indonesia. J Mar Biol Assoc UK 88:1643–1654. doi: 10.1017/S0025315408001094 CrossRefGoogle Scholar
  61. Raitsos DE, Pradhan Y, Brewin RJ, Stenchikov G, Hoteit I (2013) Remote sensing the phytoplankton seasonal succession of the Red Sea. PLoS One 8:e64909. doi: 10.1371/journal.pone.0064909 CrossRefPubMedPubMedCentralGoogle Scholar
  62. Randall JE (1994) Twenty-two new records of fishes from the Red Sea. Fauna Saudi Arabia 14:259–275Google Scholar
  63. Renner SS (2016) A return to Linnaeus’s focus on diagnosis, not description: the use of DNA characters in the formal naming of species. Syst Biol. doi: 10.1093/sysbio/syw032 PubMedGoogle Scholar
  64. Ronquist F, Teslenko M, van der Mark P et al (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 CrossRefPubMedPubMedCentralGoogle Scholar
  65. Rüppell E (1835) Description d’un nouveau genre de mollusques de la classe des Gastéropodes Pectinibranches. Trans Zool Soc Lond 1:259–260CrossRefGoogle Scholar
  66. Sammarco PW, Carleton JH (1981) Damselfish territoriality and coral community structure: reduced grazing, coral recruitment, and effects on coral spat. In: Proceedings of the 4th International Coral Reef Symposium, Manila, Philippines, May 1981, vol 2, pp 525–535Google Scholar
  67. Sarkar IN, Thornton JW, Planet PJ, Figurski DH, Schierwater B, DeSalle R (2002) An automated phylogenetic key for classifying homeoboxes. Mol Phylogenet Evol 24:388–399. doi: 10.1016/S1055-7903(02)00259-2 CrossRefPubMedGoogle Scholar
  68. Sarkar IN, Planet PJ, Desalle ROB (2008) CAOS software for use in character‐based DNA barcoding. Mol Ecol Resour 8:1256–1259. doi: 10.1111/j.1755-0998.2008.02235.x CrossRefPubMedGoogle Scholar
  69. Scarpa F, Cossu P, Lai T, Sanna D, Curini-Galletti M, Casu M (2016) Meiofaunal cryptic species challenge species delimitation: the case of the Monocelis lineata (Platyhelminthes: Proseriata) species complex. Contrib Zool 85:123–145Google Scholar
  70. Schindel DE, Miller SE (2010) Provisional nomenclature: the on-ramp to taxonomic names. In: Polaszek A (ed) Systema Naturae 250: the Linnaean Ark. CRC Press, Boca Raton, Florida, pp 109–116. doi: 10.1201/EBK1420095012-c10 CrossRefGoogle Scholar
  71. Schuchert P (2014) High genetic diversity in the hydroid Plumularia setacea: a multitude of cryptic species or extensive population subdivision? Mol Phylogenet Evol 76:1–9. doi: 10.1016/j.ympev.2014.02.020 CrossRefPubMedGoogle Scholar
  72. Seveso D, Montano S, Pica D et al (2015) Pteroclava krempfi-octocoral symbiosis: new information from the Indian Ocean and the Red Sea. Mar Biodivers 46:483–487. doi: 10.1007/s12526-015-0368-y CrossRefGoogle Scholar
  73. Shenkar N (2012) Ascidian (Chordata, Ascidiacea) diversity in the Red Sea. Mar Biodivers 42:459–469. doi: 10.1007/s12526-012-0124-5 CrossRefGoogle Scholar
  74. Shipman C, Gosliner T (2015) Molecular and morphological systematics of Doto Oken, 1851 (Gastropoda: Heterobranchia), with descriptions of five new species and a new genus. Zootaxa 3973:57–101. doi: 10.11646/zootaxa.3973.1.2 CrossRefPubMedGoogle Scholar
  75. Sofianos SS, Johns WE (2003) An oceanic general circulation model (OGCM) investigation of the Red Sea circulation: 2. Three‐dimensional circulation in the Red Sea. J Geophys Res Oceans 108:3066. doi: 10.1029/2001JC001185 CrossRefGoogle Scholar
  76. Stella JS, Pratchett MS, Hutchings PA, Jones GP (2011) Coral-associated invertebrates: diversity, ecological importance and vulnerability to disturbance. Oceanogr Mar Biol 49:43–104Google Scholar
  77. Sukumaran J, Holder MT (2010) DendroPy: a Python library for phylogenetic computing. Bioinformatics 26:1569–1571. doi: 10.1093/bioinformatics/btq228 CrossRefPubMedGoogle Scholar
  78. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  79. Terraneo TI, Berumen ML, Arrigoni R et al (2014) Pachyseris inattesa sp. n. (Cnidaria, Anthozoa, Scleractinia): a new reef coral species from the Red Sea and its phylogenetic relationships. ZooKeys 433:1–30. doi: 10.3897/zookeys.433.8036 CrossRefGoogle Scholar
  80. Tornabene L, Ahmadia GN, Williams JT (2013) Four new species of dwarfgobies (Teleostei: Gobiidae: Eviota) from the Austral, Gambier, Marquesas and Society Archipelagos, French Polynesia. Syst Biodivers 11:363–380. doi: 10.1080/14772000.2013.819822 CrossRefGoogle Scholar
  81. van der Meij SE, Fransen CH, Pasman LR, Hoeksema BW (2015) Phylogenetic ecology of gall crabs (Cryptochiridae) as associates of mushroom corals (Fungiidae). Ecol Evol 5:5770–5780. doi: 10.1002/ece3.1808 CrossRefPubMedPubMedCentralGoogle Scholar
  82. Wallace CC (1983) A comparison of two consecutive spring–summer juvenile coral recruitment seasons on a reef front. Bull Mar Sci 33:783Google Scholar
  83. Wallace CC (1985) Reproduction, recruitment and fragmentation in nine sympatric species of the coral genus Acropora. Mar Biol 88:217–233. doi: 10.1007/BF00392585 CrossRefGoogle Scholar
  84. Wallace CC, Bull GD (1982) Patterns of juvenile coral recruitment on a reef front during a spring-summer spawning period. In: Proceedings of the 4th International Coral Reef Symposium, Manila, Philippines, May 1981, vol 2, pp 345–350Google Scholar
  85. Zielske S, Haase M (2015) Molecular phylogeny and a modified approach of character-based barcoding refining the taxonomy of New Caledonian freshwater gastropods (Caenogastropoda, Truncatelloidea, Tateidae). Mol Phylogenet Evol 89:171–181. doi: 10.1016/j.ympev.2015.04.020 CrossRefPubMedGoogle Scholar
  86. Zietara MS, Arndt A, Geets A, Hellemans B, Volckaert FA (2000) The nuclear rDNA region of Gyrodactylus arcuatus and G. branchicus (Monogenea: Gyrodactylidae). J Parasitol 86:1368–1373. doi: 10.1645/0022-3395(2000)086[1368:TNRROG]2.0.CO;2 CrossRefGoogle Scholar
  87. Zou S, Li Q, Kong L, Yu H, Zheng X (2011) Comparing the usefulness of distance, monophyly and character-based DNA barcoding methods in species identification: a case study of Neogastropoda. PLoS One 6:e26619. doi: 10.1371/journal.pone.0026619 CrossRefPubMedPubMedCentralGoogle Scholar
  88. Zwickl DJ (2006) GARLI: genetic algorithm for rapid likelihood inference. Home page at: Accessed 31 July 2016

Copyright information

© Senckenberg Gesellschaft für Naturforschung and Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Dipartimento di Biotecnologie e BioscienzeUniversità degli Studi di Milano-BicoccaMilanItaly
  2. 2.MaRHE CenterUniversità degli Studi di Milano-BicoccaMagoodhoo Island, Faafu AtollRepublic of Maldives
  3. 3.Red Sea Research Center, Division of Biological and Environmental Sciences and EngineeringKing Abdullah University of Science and TechnologyThuwalSaudi Arabia
  4. 4.Dipartimento di Scienze della Vita e dell’AmbienteUniversità Politecnica delle MarcheAnconaItaly

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