Advertisement

Parasitology Research

, Volume 113, Issue 2, pp 653–668 | Cite as

The Gyrodactylus (Monogenea, Gyrodactylidae) parasite fauna of freshwater sand gobies (Teleostei, Gobioidei) in their centre of endemism, with description of seven new species

  • Maarten P. M. VanhoveEmail author
  • Alcibiades N. Economou
  • Stamatis Zogaris
  • Sofia Giakoumi
  • Davor Zanella
  • Filip A. M. Volckaert
  • Tine Huyse
Original Paper

Abstract

While Gobioidei comprises showcases of (adaptive) radiation, the scientific interest they yielded did not ensure full understanding of goby biodiversity. Even in a well-studied region like Europe, wide knowledge gaps remain. Sand gobies represent one of the few clades whose monogenean parasites have been thoroughly studied. However, in the Balkans, part of the sand gobies' centre of endemism, these parasites were unstudied. We focus on Greek and Croatian freshwater gobies. From five sand goby species, the first parasites are reported, describing seven new Gyrodactylus species. Economidichthys pygmaeus harbours Gyrodactylus benedeni sp. n. and Gyrodactylus dorlodoti sp. n. Its congener E. trichonis hosts G. meelkopae sp. n. Knipowitschia milleri was found to host G. charon sp. n., K. thessala is infected by G. bios sp. n., and K. croatica by G. douglasadamsi sp. n. and G. hellemansi sp. n. Gyrodactylus bubyri was found on its type host K. caucasica. A diverse parasite fauna is expected for a region known for its biodiversity and endemism. The contribution of parasites to species richness in such hotspots is overlooked. The observed species richness per host is rather low compared to the better-studied eastern Atlantic sand gobies. Host vicariance is considered to mediate parasite specificity in this fauna. Some new flatworm species display unique morphological features, such as the remarkable size of the marginal hook sickle proper compared to its foot in the Economidichthys parasites, or a characteristically kinked marginal hook sickle in G. douglasadamsi sp. n. These features reflect their hosts' endemism in the Balkans.

Keywords

Type Host Gill Filament Parasite Fauna Male Copulatory Organ Apical Spine 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

We thank D. Mrdak, V. Pešić (University of Montenegro), E. Kalogianni, L. Vardakas, Y. Chatzinikolaou, V. Tachos, D. Kommatas, N. Koutsikos and Y. Kapakos (HCMR) for help with sampling; L. Schoofs, L. Arckens, E. Meelkop, J. Nys, J. Aerts and L. Minerva (KU Leuven) for (help with) the use of a ZEISS microscope; B. Geens for help with collecting part of the Gyrodactylus data; A. Vidalis (Biodiversity East) for providing Fig. 1; and W.A. Boeger (Universidade Federal do Paraná, Brazil), J. Cable (Cardiff University, Wales, United Kingdom), A. Pariselle (Institut de Recherche pour le Développement, France), M. Ondračková (Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic) and I. Přikrylová (Masaryk University, Czech Republic) for useful suggestions on monogenean work. M.P.M.V and T.H. benefited from a PhD and a postdoctoral fellowship, respectively, of the Research Council – Flanders (FWO – Vlaanderen). Fieldwork was partly financed by a travel grant to M.P.M.V. from BeNCoRe (Belgian Network for Coastal Research; ENCORA coordination action contract number FP6-2004-Global-3–518120). M.P.M.V. is currently supported by ECIP - Centre of excellence, GAČR No. GBP505/12/G112.

References

  1. Agorreta A, San Mauro D, Schliewen U, Van Tassell JL, Kovačić M, Zardoya R, Rüber L (2013) Molecular phylogenetics of Gobioidei and phylogenetic placement of European gobies. Mol Phylogenet Evol 69(3):619–633. doi: 10.1016/j.ympev.2013.07.017 Google Scholar
  2. Bakke TA, Cable J, Harris PD (2007) The biology of gyrodactylid monogeneans: the “Russian-doll Killers”. Adv Parasit 64:161–276CrossRefGoogle Scholar
  3. Barson M, Přikrylová I, Vanhove MPM, Huyse T (2010) Parasite hybridization in African Macrogyrodactylus spp. (Monogenea, Platyhelminthes) signals historical host distribution. Parasitology 137:1585–1595PubMedCrossRefGoogle Scholar
  4. Blakeslee AMH, Byers JE, Lesser MP (2008) Solving cryptogenic histories using host and parasite molecular genetics: the resolution of Littorina littorea’s North American origin. Mol Ecol 17:3684–3696PubMedCrossRefGoogle Scholar
  5. Boeger WA, Kritsky DC (2003) Parasites, fossils and geologic history: historical biogeography of the South American freshwater croakers, Plagioscion spp. (Teleostei, Sciaenidae). Zool Scr 32(1):3–11CrossRefGoogle Scholar
  6. Brooks DR, Hoberg EP (2001) Parasite systematics in the 21st century: opportunities and obstacles. Trends Parasitol 17(6):273–275PubMedCrossRefGoogle Scholar
  7. Brooks DR, McLennan DA (1993) Parascript. Parasites and the language of evolution. Smithsonian Institution Press, Washington, DCGoogle Scholar
  8. Choudhury A, Dick TA (2001) Sturgeons (Chondrostei: Acipenseridae) and their metazoan parasites: patterns and processes in historical biogeography. J Biogeogr 28(11–12):1411–1439CrossRefGoogle Scholar
  9. Criscione CD, Cooper B, Blouin MS (2006) Parasite genotypes identify source populations of migratory fish more accurately than fish genotypes. Ecology 87(4):823–828PubMedCrossRefGoogle Scholar
  10. Daoulas C, Economou AN, Psarras T, Barbieri-Tseliki R (1993) Reproductive strategies and early development of three freshwater gobies. J Fish Biol 42:749–776CrossRefGoogle Scholar
  11. de Meeûs T, Michalakis Y, Renaud F (1998) Santa Rosalia revisited: or why are there so many kinds of parasites in ‘the garden of early delights’? Parasitol Today 14:10–13PubMedCrossRefGoogle Scholar
  12. Dmitrieva EV, Skidan N (2005) Gyrodactylus leopardinus sp. n. (Monogenea) – a parasite of Pomatoschistus marmoratus (Gobiidae) from the Sea of Azov. Vestn Zool 39(3):17–22Google Scholar
  13. Dunn RR, Harris NC, Colwell RK, Koh LP, Sodhi NS (2009) The sixth mass coextinction: are most endangered species parasites and mutualists? P Roy Soc B-Biol Sci 276:3037–3045CrossRefGoogle Scholar
  14. Dupont F, Lambert A (1986) Study of communities of Monogenea Dactylogyridae parasites of the Cyprinidae in Lake Mikri Prespa (northern Greece). Description of 3 new species from an endemic Barbus: Barbus cyclolepis prespensis Karaman, 1924. Ann Parasitol Hum Comp 61(6):597–616 [in French]PubMedGoogle Scholar
  15. Economidis PS (1995) Endangered freshwater fishes of Greece. Biol Conserv 72:201–211CrossRefGoogle Scholar
  16. Economou AN, Miller PJ, Economidis PS (2004a) Economidichthys pygmaeus. In: Miller PJ (ed) The freshwater fishes of Europe – Gobiidae 2. AULA-Verlag GmbH, Wiebelsheim, pp 443–458Google Scholar
  17. Economou AN, Miller PJ, Economidis PS (2004b) Economidichthys trichonis. In: Miller PJ (ed) The freshwater fishes of Europe – Gobiidae 2. AULA-Verlag GmbH, Wiebelsheim, pp 459–468Google Scholar
  18. Economou AN, Giakoumi S, Vardakas L, Barbieri R, Stoumboudi M, Zogaris S (2007) The freshwater ichthyofauna of Greece – an update based on a hydrographic basin survey. Mediterr Mar Sci 8:91–166Google Scholar
  19. Ergens R (1985) Order Gyrodactylidea Bychowsky, 1937. In: Gusev AV (ed) Key to the parasites of the freshwater fish fauna of the USSR, vol 2. Nauka, Leningrad, pp 269–347Google Scholar
  20. Eschmeyer WN (ed) (2013) Genera, species, references. Catalog of Fishes. http://research.calacademy.org/research/ichthyology/catalog/fishcatmain.asp. Accessed 27 July 2013
  21. Fishelson L (1989) Bisexuality and pedogenesis in gobies (Gobiidae, Teleostei) and other fish, or, why so many little fish in tropical seas. Senck Marit 20(3–4):147–169Google Scholar
  22. García-Vásquez A, Shinn AP, Bron JE (2012) Development of a light microscopy stain for the sclerites of Gyrodactylus von Nordmann, 1832 (Monogenea) and related genera. Parasitol Res 110:1639–1648PubMedCrossRefGoogle Scholar
  23. Geets A, Malmberg G, Ollevier F (1998) Gyrodactylus longidactylus sp. nov., a monogenean from Pomatoschistus lozanoi (de Buen) (Gobiidae) from the North Sea. Syst Parasitol 41:63–70CrossRefGoogle Scholar
  24. Gillardin C, Vanhove MPM, Pariselle A, Huyse T, Volckaert FAM (2012) Ancyrocephalidae (Monogenea) of Lake Tanganyika: II. Description of the first Cichlidogyrus spp. parasites from Tropheini fish hosts (Teleostei, Cichlidae). Parasitol Res 110(1):305–313PubMedCrossRefGoogle Scholar
  25. Harris PD, Shinn AP, Cable J, Bakke TA (2004) Nominal species of the genus Gyrodactylus von Nordmann 1832 (Monogenea: Gyrodactylidae), with a list of principal host species. Syst Parasitol 59:1–27PubMedCrossRefGoogle Scholar
  26. Harris PD, Shinn AP, Cable J, Bakke TA, Bron JE (2008) GyroDb: gyrodactylid monogeneans on the web. Trends Parasitol 24:109–111PubMedCrossRefGoogle Scholar
  27. Huyse T, Malmberg G (2004) Molecular and morphological comparisons between Gyrodactylus ostendicus n. sp. (Monogenea: Gyrodactylidae) on Pomatoschistus microps (Krøyer) and G. harengi Malmberg, 1957 on Clupea harengus membras L. Syst Parasitol 58:105–113PubMedCrossRefGoogle Scholar
  28. Huyse T, Volckaert FAM (2002) Identification of a host-associated species complex using molecular and morphometric analyses, with the description of Gyrodactylus rugiensoides n. sp. (Gyrodactylidae, Monogenea). Int J Parasitol 32:907–919PubMedCrossRefGoogle Scholar
  29. Huyse T, Volckaert FAM (2005) Comparing host and parasite phylogenies: Gyrodactylus flatworms jumping from goby to goby. Syst Biol 54(5):710–718PubMedCrossRefGoogle Scholar
  30. Huyse T, Audenaert V, Volckaert FAM (2003) Speciation and host–parasite relationships in the parasite genus Gyrodactylus (Monogenea, Platyhelminthes) infecting gobies of the genus Pomatoschistus (Gobiidae, Teleostei). Int J Parasitol 33(14):1679–1689PubMedCrossRefGoogle Scholar
  31. Huyse T, Malmberg G, Volckaert FAM (2004a) Four new species of Gyrodactylus von Nordmann, 1832 (Monogenea, Gyrodactylidae) on gobiid fishes: combined DNA and morphological analyses. Syst Parasitol 59:103–120PubMedCrossRefGoogle Scholar
  32. Huyse T, Van Houdt J, Volckaert FAM (2004b) Paleoclimatic history and vicariant speciation in the “sand goby” group (Gobiidae, Teleostei). Mol Phylogenet Evol 32:324–336PubMedCrossRefGoogle Scholar
  33. Huyse T, Pampoulie C, Audenaert V, Volckaert FAM (2006) First report of Gyrodactylus spp. (Platyhelminthes: Monogenea) in the western Mediterranean sea: molecular and morphological descriptions. J Parasitol 92(4):682–690PubMedCrossRefGoogle Scholar
  34. Ishimatsu A, Gonzales TT (2011) Mudskippers: front runners in the modern invasion of land. In: Patzner RA, Van Tassell JL, Kovačić M, Kapoor BG (eds) The biology of Gobies. Science Publishers, Enfield, pp 609–638Google Scholar
  35. Justine J-L, Beveridge I, Boxshall GA, Bray RA, Miller TL, Moravec F, Trilles J-P, Whittington ID (2012) An annotated list of fish parasites (Isopoda, Copepoda, Monogenea, Digenea, Cestoda, Nematoda) collected from Snappers and Bream (Lutjanidae, Nemipteridae, Caesionidae) in New Caledonia confirms high parasite biodiversity on coral reef fish. Aquat Biosyst 8:22PubMedCentralPubMedCrossRefGoogle Scholar
  36. Koh LP, Dunn RR, Sodhi NS, Colwell RK, Proctor HC, Smith VS (2004) Species coextinctions and the biodiversity crisis. Science 305:1632–1634PubMedCrossRefGoogle Scholar
  37. Kottelat M, Freyhof J (2007) Handbook of European freshwater fishes. Kottelat, Cornol and Freyhof, BerlinGoogle Scholar
  38. Kovačić M, Patzner RA (2011) North-Eastern Atlantic and Mediterranean gobies. In: Patzner RA, Van Tassell JL, Kovačić M, Kapoor BG (eds) The biology of gobies. Science Publishers, Enfield, pp 177–206Google Scholar
  39. Kryštufek B, Reed JM (2004) Pattern and process in Balkan biodiversity – an overview. In: Griffiths HI, Kryštufek B, Reed JM (eds) Balkan biodiversity: pattern and process in the European hotspot. Kluwer Academic Publishers, Dordrecht, pp 1–8CrossRefGoogle Scholar
  40. Kuris AM, Hechinger RF, Shaw JC, Whitney KL, Aguirre-Macedo L, Boch CA, Dobson AP, Dunham EJ, Fredensborg BL, Huspeni TC, Lorda J, Mababa L, Mancini FT, Mora AB, Pickering M, Talhouk NL, Torchin ME, Lafferty KD (2008) Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454:515–518PubMedCrossRefGoogle Scholar
  41. Kvach Y, Skóra KE (2007) Metazoa parasites of the invasive round goby Apollonia melanostoma (Neogobius melanostomus) (Pallas) (Gobiidae: Osteichthyes) in the Gulf of Gdańsk, Baltic Sea, Poland: a comparison with the Black Sea. Parasitol Res 100:767–774PubMedCrossRefGoogle Scholar
  42. Kvach Y, Winkler HM (2011) The colonization of the invasive round goby Neogobius melanostomus by parasites in new localities in the southwestern Baltic Sea. Parasitol Res 109:769–780PubMedCrossRefGoogle Scholar
  43. Larmuseau MHD, Huyse T, Vancampenhout K, Van Houdt JKJ, Volckaert FAM (2010) High molecular diversity in the rhodopsin gene in closely related goby fishes: a role for visual pigments in adaptive speciation? Mol Phylogenet Evol 55:689–698PubMedCrossRefGoogle Scholar
  44. Larmuseau MHD, Vanhove MPM, Huyse T, Volckaert FAM, Decorte R (2011) Signature of selection on the rhodopsin gene in the marine radiation of American seven-spined gobies (Gobiidae, Gobiosomatini). J Evol Biol 24(7):1618–1625PubMedCrossRefGoogle Scholar
  45. Littlewood DTJ (2011) Systematics as a cornerstone of parasitology: overview and preface. Parasitology 138:1633–1637PubMedCrossRefGoogle Scholar
  46. Longshaw M, Pursglove M, Shinn AP (2003) Gyrodactylus quadratidigitus n. sp. (Monogenea: Gyrodactylidae), a parasite of the leopard-spotted goby Thorogobius ephippiatus (Lowe) from the south-western coast of the UK. Syst Parasitol 55:151–157PubMedCrossRefGoogle Scholar
  47. Lundberg JG, Kottelat M, Smith GR, Stiassny M, Gill T (2000) So many fishes, so little time: an overview of recent ichthyological discoveries in fresh waters. Ann Missouri Bot Gard 87:26–62CrossRefGoogle Scholar
  48. MacKenzie K (2002) Parasites as biological tags in population studies of marine organisms: an update. Parasitology 124:S153–S163PubMedCrossRefGoogle Scholar
  49. Malavasi S, Gkenas C, Leonardos I, Torricelli P, McLennan DA (2012) The phylogeny of a reduced ‘sand goby’ group based on behavioural and life history characters. Zool J Linn Soc-London 165:916–924CrossRefGoogle Scholar
  50. Malmberg G (1957) On the occurrence of Gyrodactylus on Swedish fishes. Skr Söd Sver Fiskför Asskr 1956:19–76 [in Swedish]Google Scholar
  51. Marcogliese DJ (2004) Parasites: small players with crucial roles in the ecological theater. EcoHealth 1:151–164CrossRefGoogle Scholar
  52. McDowall RM (2000) Biogeography of the southern cool-temperate galaxioid fishes: evidence from metazoan macroparasite faunas. J Biogeogr 27(5):1221–1229CrossRefGoogle Scholar
  53. Mierzejewska K, Martyniak A, Kakareko T, Dzika E, Stańczak K, Hliwa P (2011) Gyrodactylus proterorhini Ergens, 1967 (Monogenoidea, Gyrodactylidae) in gobiids from the Vistula River – the first record of the parasite in Poland. Parasitol Res 108:1147–1151PubMedCrossRefGoogle Scholar
  54. Miller PJ (1979) Adaptiveness and implications of small size in teleosts. Sym Zool S 44:263–306Google Scholar
  55. Miller PJ (1990) The endurance of endemism – the Mediterranean fresh-water gobies and their prospects for survival. J Fish Biol 37:145–156CrossRefGoogle Scholar
  56. Miller PJ (2004) Knipowitschia croatica. In: Miller PJ (ed) The freshwater fishes of Europe – Gobiidae 2. AULA-Verlag GmbH, Wiebelsheim, pp 365–369Google Scholar
  57. Miller PJ, Economidis PS (2004) Knipowitschia thessala. In: Miller PJ (ed) The freshwater fishes of Europe – Gobiidae 2. AULA-Verlag GmbH, Wiebelsheim, pp 423–429Google Scholar
  58. Miller PJ, Madurell T, Economou AN (2004) Knipowitschia milleri. In: Miller PJ (ed) The freshwater fishes of Europe – Gobiidae 2. AULA-Verlag GmbH, Wiebelsheim, pp 399–404Google Scholar
  59. Muterezi Bukinga F, Vanhove MPM, Van Steenberge M, Pariselle A (2012) Ancyrocephalidae (Monogenea) of Lake Tanganyika: III. Cichlidogyrus infecting the world’s biggest cichlid and the non-endemic tribes Haplochromini, Oreochromini and Tylochromini (Teleostei, Cichlidae). Parasitol Res 111(5):2049–2061PubMedCrossRefGoogle Scholar
  60. Nieberding C, Morand S, Libois R, Michaux JR (2004) A parasite reveals cryptic phylogeographic history of its host. P Roy Soc B-Biol Sci 271(1557):2559–2568CrossRefGoogle Scholar
  61. Ondračková M, Dávidová M, Blažek R, Gelnar M, Jurajda P (2009) The interaction between an introduced fish host and local parasite fauna: Neogobius kessleri in the middle Danube River. Parasitol Res 105:201–208PubMedCrossRefGoogle Scholar
  62. Osmanov SO (1971) Parasites of Uzbekistan’s fishes. FAN, Tashkent [In Russian]Google Scholar
  63. Palm HW, Rückert S (2009) A new approach to visualize ecosystem health by using parasites. Parasitol Res 105:539–553PubMedCrossRefGoogle Scholar
  64. Pariselle A, Morand S, Deveney M, Pouyaud L (2003) Parasite species richness of closely related hosts: historical scenario and “genetic” hypothesis. In: Combes C, Jourdan J (eds) Hommage à Louis Euzet—Taxonomie, écologie et évolution des métazoaires parasites. Taxonomy, ecology and evolution of metazoan parasites. Presses Universitaires de Perpignan, Perpignan, pp 147–166Google Scholar
  65. Pariselle A, Boeger WA, Snoeks J, Bilong Bilong CF, Morand S, Vanhove MPM (2011) The monogenean parasite fauna of cichlids: a potential tool for host biogeography. Int J Evol Biol 2011:471480PubMedCentralPubMedCrossRefGoogle Scholar
  66. Paugy D, Guégan JF, Agnèse JF (1990) Three simultaneous and independent approaches to the characterization of a new species of Labeo (Teleostei, Cyprinidae) from West Africa. Can J Zool 68:1124–1131CrossRefGoogle Scholar
  67. Poulin R (2002) The evolution of monogenean diversity. Int J Parasitol 32:245–254PubMedCrossRefGoogle Scholar
  68. Přikrylová I, Blažek R, Vanhove MPM (2012) An overview of the Gyrodactylus (Monogenea: Gyrodactylidae) species parasitizing African catfishes, and their morphological and molecular diversity. Parasitol Res 110:1185–1200PubMedCrossRefGoogle Scholar
  69. Pugachev ON, Gerasev PI, Gussev AV, Ergens R, Khotenowsky I (2009) Guide to Monogenoidea of freshwater fish of Palaearctic and Amur Regions. Ledizione-Ledi Publishing, MilanGoogle Scholar
  70. Raeymaekers JAM, Huyse T, Maelfait H, Hellemans B, Volckaert FAM (2008) Community structure, population structure and topographical specialisation of Gyrodactylus (Monogenea) ectoparasites living on sympatric stickleback species. Folia Parasit 55:187–196CrossRefGoogle Scholar
  71. Rüber L, Van Tassell JL, Zardoya R (2003) Rapid speciation and ecological divergence in the American seven-spined gobies (Gobiidae, Gobiosomatini) inferred from a molecular phylogeny. Evolution 57(7):1584–1598PubMedGoogle Scholar
  72. Ryan PA (1991) The success of the Gobiidae in tropical Pacific insular streams. New Zeal J Zool 18:25–30CrossRefGoogle Scholar
  73. Shinn AP, Hansen H, Olstad K, Bachmann L, Bakke TA (2004) The use of morphometric characters to discriminate specimens of laboratory-reared and wild populations of Gyrodactylus salaris and G. thymalli (Monogenea). Folia Parasit 51:239–252CrossRefGoogle Scholar
  74. Shinn AP, Harris PD, Cable J, Bakke TA, Paladini G, Bron JE (eds) (2010) GyroDb. http://www.gyrodb.net, version (06/2010)
  75. Stork NE, Lyal CHC (1993) Extinction or ‘co-extinction’ rates? Nature 366:307CrossRefGoogle Scholar
  76. Sures B (2004) Environmental parasitology: relevancy of parasites in monitoring environmental pollution. Trends Parasitol 20(4):170–177PubMedCrossRefGoogle Scholar
  77. Taylor MS, Hellberg ME (2005) Marine radiations at small geographic scales: speciation in neotropical reef gobies (Elacatinus). Evolution 59:374–385PubMedGoogle Scholar
  78. Thacker CE (2013) Phylogenetic placement of the European sand gobies in Gobionellidae and characterization of gobionellid lineages (Gobiiformes: Gobioidei). Zootaxa 3619(3):369–382CrossRefGoogle Scholar
  79. Thacker CE, Roje DM (2011) Phylogeny of Gobiidae and identification of gobiid lineages. Syst Biodivers 9(4):329–347CrossRefGoogle Scholar
  80. Thompson JN (1999) The evolution of species interactions. Science 284:2116–2118PubMedCrossRefGoogle Scholar
  81. Timm RM, Clauson BL (1987) Coevolution: Mammalia. In: Parker SP (ed) (1988) McGraw-Hill yearbook of science & technology. McGraw-Hill, New York, pp 212–214Google Scholar
  82. Vanhove MPM (2012) Species flocks and parasite evolution. Towards a co-phylogenetic analysis of monogenean flatworms of cichlids and gobies. PhD thesis, University of LeuvenGoogle Scholar
  83. Vanhove MPM, Kovačić M, Koutsikos NE, Zogaris S, Vardakas LE, Huyse T, Economou AN (2011a) First record of a landlocked population of marine Millerigobius macrocephalus (Perciformes: Gobiidae): observations from a unique spring-fed karstic lake (Lake Vouliagmeni, Greece) and phylogenetic positioning. Zool Anz 250(3):195–204CrossRefGoogle Scholar
  84. Vanhove MPM, Snoeks J, Volckaert FAM, Huyse T (2011b) First description of monogenean parasites in Lake Tanganyika: the cichlid Simochromis diagramma (Teleostei, Cichlidae) harbours a high diversity of Gyrodactylus species (Platyhelminthes, Monogenea). Parasitology 138(3):364–380PubMedCrossRefGoogle Scholar
  85. Vanhove MPM, Economou AN, Zogaris S, Larmuseau MHD, Giakoumi S, Kalogianni E, Volckaert FAM, Huyse T (2012) Phylogenetics and biogeography of the Balkan "sand gobies" (Teleostei, Gobiidae): vulnerable species in need of taxonomic revision. Biol J Linn Soc 105(1):73–91CrossRefGoogle Scholar
  86. Vanhove MPM, Van Steenberge M, Dessein S, Volckaert FAM, Snoeks J, Huyse T, Pariselle A (2013) Biogeographical implications of Zambezian Cichlidogyrus species (Platyhelminthes: Monogenea: Ancyrocephalidae) parasitizing Congolian cichlids. Zootaxa 3608(5):398–400CrossRefGoogle Scholar
  87. Windsor DA (1998) Most of the species on Earth are parasites. Int J Parasitol 28:1939–1941PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Maarten P. M. Vanhove
    • 1
    • 2
    • 3
    Email author
  • Alcibiades N. Economou
    • 2
  • Stamatis Zogaris
    • 2
  • Sofia Giakoumi
    • 2
  • Davor Zanella
    • 4
  • Filip A. M. Volckaert
    • 1
  • Tine Huyse
    • 1
    • 5
  1. 1.Laboratory of Biodiversity and Evolutionary Genomics, Department of BiologyUniversity of LeuvenLeuvenBelgium
  2. 2.Institute of Marine Biological Resources and Inland WatersHellenic Centre for Marine ResearchAnavyssosGreece
  3. 3.Department of Botany and Zoology, Faculty of ScienceMasaryk UniversityBrnoCzech Republic
  4. 4.Department of Zoology, Faculty of ScienceUniversity of ZagrebZagrebCroatia
  5. 5.Department of BiologyRoyal Museum for Central AfricaTervurenBelgium

Personalised recommendations