Marine Biology

, 165:123 | Cite as

Marine connectivity dynamics: clarifying cosmopolitan distributions of marine interstitial invertebrates and the meiofauna paradox

  • José CercaEmail author
  • Günter Purschke
  • Torsten H. Struck
Student Review


Many interstitial species were first described as widely distributed, often cosmopolitan or amphi-oceanic, contrasting with descriptions of a sedentary life style and the general absence of pelagic dispersal stages. These inconsistencies became known as the “meiofauna paradox”. In this review, we present a literature review investigating these inconsistencies and address the assumptions of the meiofauna paradox. We break the paradox down to two aspects including species distribution and dispersal. Focusing on distribution, we demonstrate that wide distributions are seldom given and false records likely stem from biological phenomena like stasis or recent speciation. These phenomena account for morphological similarity, ultimately represented by the pronounced occurrence of cryptic species with restricted distribution ranges. Additionally, taxonomic artefacts such as the erroneous application of taxonomic keys contribute to the report of widely distributed species. Considering dispersal, we point out the mismatch between traditional assumptions of meiofaunal sedentarism and growing experimental and empirical evidences suggesting higher dispersal potential. These evidences include not only indications for dispersal by pelagic stages, but further consider ecological and life-history traits in shaping distribution ranges. We conclude that the meiofauna paradox sensu stricto most likely does not exist and provide a roadmap for future research, suggesting a focus on morphological similarity and marine connectivity. Meiofaunal research should concentrate on evolutionary factors resulting in morphological similarity, improving the taxonomic resolution of species complexes and conducting more sophisticated experimental experiments to meiofaunal dispersal. In all cases, meiofaunal research will benefit from high-throughput sequencing such as genome scanning approaches, metagenomics or metatranscriptomics.



The authors are indebted to two anonymous reviewers and Diego Fontaneto whose comments have considerably improved the original manuscript. JC is grateful to Zeca Afonso (among other thinkers) for inspiration (“Em cada esquina um amigo; Em cada rosto igualdade”). This is NHM Evolutionary Genomics Lab contribution No. 10.

Compliance with ethical standards

Ethical approval

All authors have approved the submitted manuscript

Conflict of interest

The authors declare that they have no conflict of interest.

Human animal rights statement

This article does not contain any studies with animals performed by any of the authors.

Supplementary material

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Supplementary material 1 (XLSX 200 kb)
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Supplementary material 2 (XLSX 43 kb)
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Supplementary material 3 (XLSX 138 kb)
227_2018_3383_MOESM4_ESM.pdf (82 kb)
Supplementary material 4 (PDF 81 kb)


  1. Andrade SCS, Norenburg JL, Solferini VN (2011) Worms without borders: genetic diversity patterns in four Brazilian Ototyphlonemertes species (Nemertea, Hoplonemertea). Mar Biol 158:2109–2124. CrossRefGoogle Scholar
  2. Ansari KGMT, Pattnaik AK, Rastogi G, Bhadury P (2015a) An inventory of free-living marine nematodes from Asia’s largest coastal lagoon, Chilika, India. Wetl Ecol Manag 23:881–890. CrossRefGoogle Scholar
  3. Ansari KGMT, Lyla PS, Khan SA (2015b) New distributional records of free-living marine nematodes from Indian waters I. Chromadorids. Indian J Geo Mar Sci 44:756–765Google Scholar
  4. Ansari KGMT, Lyla PS, Khan SA (2016) New distributional records of free-living marine nematodes from Indian waters II. Monhysterids. Indian J Geo-Marine Sci 45:342–351Google Scholar
  5. Ansari KGMT, Lyla PS, Ajmal Khan S (2017) New distributional records of free-living marine nematodes from Indian waters III. Microlaimids and Laptolaimids. Indian J Geo Mar Sci 46:155–162Google Scholar
  6. Armonies W (1990) Short-term changes of meiofaunal abundance in intertidal sediments. Helgoländer Meeresuntersuchungen 386:375–386CrossRefGoogle Scholar
  7. Armonies W (1994) Drifting meio- and macrobenthic invertebrates on tidal flats in Königshafen: a review. Helgoländer Meeresuntersuchungen 48:299–320. CrossRefGoogle Scholar
  8. Arroyo NL, Aarnio K, Bonsdorff E (2006) Drifting algae as a means of re-colonizing defaunated sediments in the Baltic Sea. A short-term microcosm study. Hydrobiologia 554:83–95. CrossRefGoogle Scholar
  9. Atherton S, Jondelius U (2018) Microstomum (Platyhelminthes, Macrostomorpha, Microstomidae) from the Swedish west coast: two new species and a population description. Eur J Taxon. CrossRefGoogle Scholar
  10. Baco AR, Etter RJ, Ribeiro PA, von der Heyden S, Beerli P, Kinlan BP (2016) A synthesis of genetic connectivity in deep-sea fauna and implications for marine reserve design. Mol Ecol 25:3276–3298. PubMedCrossRefGoogle Scholar
  11. Baldrighi E, Aliani S, Conversi A, Lavaleye M, Borghini M, Manini E (2013) From microbes to macrofauna: an integrated study of deep benthic communities and their response to environmental variables along the Malta Escarpment (Ionian Sea). Sci Mar 77:625–639. CrossRefGoogle Scholar
  12. Barnes DKA (2002) Invasions by marine life on plastic debris. Nature 416:808–809. PubMedCrossRefGoogle Scholar
  13. Bhadury P, Austen MC, Bilton DT, Lambshead PJD, Rogers AD, Smerdon GR (2006) Molecular detection of marine nematodes from environmental samples: overcoming eukaryotic interference. Aquat Microb Ecol 44:97–103. CrossRefGoogle Scholar
  14. Bhaud M, Duchêne J (1995) Change from planktonic to benthic development: is life cycle evolution an adaptive answer to the constraints of dispersal? Oceanol Acta 19:335–346Google Scholar
  15. Bik HM, Thomas WK, Lunt DH, Lambshead PJD (2010) Low endemism, continued deep-shallow interchanges, and evidence for cosmopolitan distributions in free-living marine nematodes (order Enoplida). BMC Evol Biol 10:389. PubMedPubMedCentralCrossRefGoogle Scholar
  16. Bik HM, Sung W, De Ley P, Baldwin JG, Sharma J, Rocha-Olivares A, Thomas WK (2012) Metagenetic community analysis of microbial eukaryotes illuminates biogeographic patterns in deep-sea and shallow water sediments. Mol Ecol 21:1048–1059. PubMedCrossRefGoogle Scholar
  17. Boeckner MJ, Sharma J, Proctor HC (2009) Revisiting the meiofauna paradox: dispersal and colonization of nematodes and other meiofaunal organisms in low- and high-energy environments. Hydrobiologia 624:91–106. CrossRefGoogle Scholar
  18. Boissin E, Egea E, Féral JP, Chenuil A (2015) Contrasting population genetic structures in Amphipholis squamata, a complex of brooding, self-reproducing sister species sharing life history traits. Mar Ecol Prog Ser 539:165–177. CrossRefGoogle Scholar
  19. Brenzinger B, Haszprunar G, Schrödl M (2013) At the limits of a successful body plan—3D microanatomy, histology and evolution of Helminthope (Mollusca: Heterobranchia: Rhodopemorpha), the most worm-like gastropod. Front Zool 10:37. PubMedPubMedCentralCrossRefGoogle Scholar
  20. Callens M, Gheerardyn H, Ndraro SGM, De Troch M, Vanreusel A (2012) Harpacticoid copepod colonization of coral fragments in a tropical reef lagoon (Zanzibar, Tanzania). J Mar Biol Assoc UK 92:1535–1545. CrossRefGoogle Scholar
  21. Carugati L, Corinaldesi C, Dell A, Danovaro R (2015) Marine genomics metagenetic tools for the census of marine meiofaunal biodiversity: an overview. Mar Genom 24:11–20. CrossRefGoogle Scholar
  22. Casu M, Curini-Galletti M (2004) Sibling species in interstitial flatworms: a case study using Monocelis lineata (Proseriata: Monocelididae). Mar Biol 145:669–679. CrossRefGoogle Scholar
  23. Casu M, Curini-Galletti M (2006) Genetic evidence for the existence of cryptic species in the mesopsammic flatworm Pseudomonocelis ophiocephala (Rhabditophora: Proseriata). Biol J Linn Soc 87:553–576. CrossRefGoogle Scholar
  24. Casu M, Lai T, Sanna D, Cossu P, Curini-Galletti M (2009) An integrative approach to the taxonomy of the pigmented European Pseudomonocelis meixner, 1943 (Platyhelminthes: Proseriata). Biol J Linn Soc 98:907–922. CrossRefGoogle Scholar
  25. Chatterjee T, Troch M De (2000) Halacaridae (Acari) from Gazi Bay (Kenya): description and biogeography of three new and two known species. Hydrobiologia 427:177–194. CrossRefGoogle Scholar
  26. Christiansen FB, Fenchel TM (1979) Evolution of marine invertebrate reproductive patterns. Theor Popul Biol 16:267–282. PubMedCrossRefGoogle Scholar
  27. Clausen C (2000) Gastrotricha macrodasyida from the Tromsø region, northern Norway. Sarsia 85:357–384. CrossRefGoogle Scholar
  28. Colborn J, Crabtree RE, Shaklee JB, Pfeiler E, Bowen BW (2001) The evolutionary enigma of bonefishes (Albula spp.): cryptic species and ancient separations in a globally distributed shorefish. Evolution (N Y) 55:807–820. CrossRefGoogle Scholar
  29. Commito JA, Tita G (2002) Differential dispersal rates in an intertidal meiofauna assemblage. J Exp Mar Bio Ecol 268:237–256. CrossRefGoogle Scholar
  30. Cowen RK, Gawarkiewicz G, Pineda J, Thorrold SR, Werner FE (2007) Population connectivity in marine systems. Oceanography 20:14–21. CrossRefGoogle Scholar
  31. Cristoni C, Colangelo MA, Ceccherelli VU (2004) Spatial scale and meiobenthic copepod recolonisation: testing the effect of disturbance size in a seagrass habitat. J Exp Mar Bio Ecol 298:49–70. CrossRefGoogle Scholar
  32. Curini-Galletti M, Puccinelli I (1998) The Gyratrix hermaphroditus species complex (Kalyptorhynchia: Polycystididae) in marine habitats of eastern Australia. Hydrobiologia 383:287–298. CrossRefGoogle Scholar
  33. Cuvelier D, Beesau J, Ivanenko VN, Zeppilli D, Sarradin PM, Sarrazin J (2014) First insights into macro- and meiofaunal colonisation patterns on paired wood/slate substrata at Atlantic deep-sea hydrothermal vents. Deep Res Part I Oceanogr Res Pap 87:70–81. CrossRefGoogle Scholar
  34. da Fonsêca-Genevois V, Somerfield PJ, Neves MHB, Coutinho R, Moens T (2006) Colonization and early succession on artificial hard substrata by meiofauna. Mar Biol 148:1039–1050. CrossRefGoogle Scholar
  35. Dal Zotto M (2015) Antygomonas caeciliae, a new kinorhynch from the Mediterranean Sea, with report of mitochondrial genetic data for the phylum. Mar Biol Res 11:689–702. CrossRefGoogle Scholar
  36. Dal Zotto M, Todaro MA (2016) Kinorhyncha from Italy, a revision of the current checklist and an account of the recent investigations. Zool Anz 265:90–107. CrossRefGoogle Scholar
  37. Danielopol DAN, Wouters K (1992) Evolutionary (Paleo)biology of marine interstitial ostracoda. Geobios 25:207–211CrossRefGoogle Scholar
  38. Dawson MN (2001) Phylogeography in coastal marine animals: a solution from California? J Biogeogr 28:723–736CrossRefGoogle Scholar
  39. De Ley P, De Ley IT, Morris K, Abebe E, Mundo-Ocampo M, Yoder M, Heras J, Waumann D, Rocha-Olivares A, Jay Burr AH, Baldwin JG, Thomas WK (2005) An integrated approach to fast and informative morphological vouchering of nematodes for applications in molecular barcoding. Philos Trans R Soc B Biol Sci 360:1945–1958. CrossRefGoogle Scholar
  40. de Meester N, Derycke S, Bonte D, Moens T (2011) Salinity effects on the coexistence of cryptic species: a case study on marine nematodes. Mar Biol 158:2717–2726. CrossRefGoogle Scholar
  41. De Meester N, Derycke S, Moens T (2012) Differences in time until dispersal between cryptic species of a marine nematode species complex. PLoS One 7:1–8. CrossRefGoogle Scholar
  42. De Meester N, Derycke S, Rigaux A, Moens T (2015) Active dispersal is differentially affected by inter- and intraspecific competition in closely related nematode species. Oikos 124:561–570. CrossRefGoogle Scholar
  43. Delogu V, Casu M, Curini-Galletti M (2008) The genera Parotoplana Meixner, 1938 and Parotoplanella Ax, 1956 (Platyhelminthes: Proseriata) in southern Spain. J Nat Hist 42:157–176. CrossRefGoogle Scholar
  44. Denis F, Ravallec R, Pavillon J-F, Van Wormhoudt A (2009) Genetic differentiation of Atlantic populations of the intertidal copepod Tigriopus brevicornis. Sci Mar 73:579–587. CrossRefGoogle Scholar
  45. Derycke S, Remerie T, Vierstraete A, Backeljau T, Vanfleteren JR, Vincx M, Moens T (2005) Mitochondrial DNA variation and cryptic speciation within the free-living marine nematode Pellioditis marina. Mar Ecol Prog Ser 300:91–103. CrossRefGoogle Scholar
  46. Derycke S, Backeljau T, Vlaeminck C, Vierstraete A, Vanfleteren J, Vincx M, Moens T (2006) Seasonal dynamics of population genetic structure in cryptic taxa of the Pellioditis marina complex (Nematoda: Rhabditida). Genetica 128:307–321. PubMedCrossRefGoogle Scholar
  47. Derycke S, Van Vynckt R, Vanoverbeke J, Vincx M, Moens T (2007a) Colonization patterns of Nematoda on decomposing algae in the estuarine environment: community assembly and genetic structure of the dominant species Pellioditis marina. Limnol Oceanogr 52:992–1001. CrossRefGoogle Scholar
  48. Derycke S, Backeljau T, Vlaeminck C, Vierstraete A, Vanfleteren J, Vincx M, Moens T (2007b) Spatiotemporal analysis of population genetic structure in Geomonhystera disjuncta (Nematoda, Monhysteridae) reveals high levels of molecular diversity. Mar Biol 151:1799–1812. CrossRefGoogle Scholar
  49. Derycke S, Remerie T, Backeljau T, Vierstraete A, Vanfleteren J, Vincx M, Moens T (2008) Phylogeography of the Rhabditis (Pellioditis) marina species complex: evidence for long-distance dispersal, and for range expansions and restricted gene flow in the northeast Atlantic. Mol Ecol 17:3306–3322. PubMedCrossRefGoogle Scholar
  50. Derycke S, Sheibani Tezerji R, Rigaux A, Moens T (2012) Investigating the ecology and evolution of cryptic marine nematode species through quantitative real-time PCR of the ribosomal ITS region. Mol Ecol Resour 12:607–619. PubMedCrossRefGoogle Scholar
  51. Derycke S, Backeljau T, Moens T (2013) Dispersal and gene flow in free-living marine nematodes. Front Zool 10:1. PubMedPubMedCentralCrossRefGoogle Scholar
  52. Derycke S, De Meester N, Rigaux A, Creer S, Bik H, Thomas W, Moens T (2016) Coexisting cryptic species of the Litoditis marina complex (Nematoda) show differential resource use and have distinct microbiomes with high intraspecific variability. Mol Ecol. PubMedCrossRefGoogle Scholar
  53. Di Domenico M, Martínez A, Lana P, Worsaae K (2014) Molecular and morphological phylogeny of Saccocirridae (Annelida) reveals two cosmopolitan clades with specific habitat preferences. Mol Phylogenet Evol 75:202–218. PubMedCrossRefGoogle Scholar
  54. Dujardin F (1851) Sur un petit animal marin, l’Echinodère, formant un type intermédiaire entre les Crustacés et les Vers. Ann Sci Nat Zool 3:158–160Google Scholar
  55. Dunn CW, Giribet G, Edgecombe GD, Hejnol A (2014) Animal phylogeny and its evolutionary implications. Annu Rev Ecol Syst 45:371–395. CrossRefGoogle Scholar
  56. Eder B, Schrödl M, Jörger KM (2011) Systematics and redescription of the European meiofaunal slug Microhedyle glandulifera (Kowalevsky, 1901) (Heterobranchia: Acochlidia): Evidence from molecules and morphology. J Molluscan Stud 77:388–400. CrossRefGoogle Scholar
  57. Fenchel TM (1978) The ecology of micro- and meiobenthos. Annu Rev Ecol Syst 9:99–121CrossRefGoogle Scholar
  58. Fonseca VG, Carvalho GR, Nichols B, Quince C, Johnson HF, Neill SP, Lambshead JD, Thomas WK, Power DM, Creer S (2014) Metagenetic analysis of patterns of distribution and diversity of marine meiobenthic eukaryotes. Glob Ecol Biogeogr 23:1293–1302. CrossRefGoogle Scholar
  59. Fontaneto D, Kaya M, Herniou EA, Barraclough TG (2009) Extreme levels of hidden diversity in microscopic animals (Rotifera) revealed by DNA taxonomy. Mol Phylogenet Evol 53:182–189. PubMedCrossRefGoogle Scholar
  60. Fontaneto D, Flot JF, Tang CQ (2015) Guidelines for DNA taxonomy, with a focus on the meiofauna. Mar Biodivers 45:433–451. CrossRefGoogle Scholar
  61. Futuyma DJ (2010) Evolutionary constraint and ecological consequences. Evolution (N Y) 64:1865–1884. CrossRefGoogle Scholar
  62. Gallucci F, Moens T, Vanreusel A, Fonseca G (2008) Active colonisation of disturbed sediments by deep-sea nematodes: evidence for the patch mosaic model. Mar Ecol Prog Ser 367:173–183. CrossRefGoogle Scholar
  63. Garlitska L, Neretina T, Schepetov D, Mugue N, De Troch M, Baguley JG, Azovsky A (2012) Cryptic diversity of the “cosmopolitan” harpacticoid copepod Nannopus palustris: genetic and morphological evidence. Mol Ecol 21:5336–5347. PubMedCrossRefGoogle Scholar
  64. Garraffoni ARS, Balsamo M (2017) Is the ubiquitous distribution real for marine gastrotrichs? Detection of areas of endemism using Parsimony Analysis of Endemicity (PAE). Proc Biol Soc Wash 130:197–210. CrossRefGoogle Scholar
  65. Gaylord B, Gaines SD (2000) Temperature or transport? Range limits in marine species mediated solely by flow. Am Nat 155:769–789. PubMedCrossRefGoogle Scholar
  66. George KH (2013) Faunistic research on metazoan meiofauna from seamounts—a review. Meiofauna Mar 20:1–32Google Scholar
  67. George KH, Schminke HK (2002) Harpacticoida (Crustacea, Copepoda) of the Great Meteor Seamount, with first conclusions as to the origin of the plateau fauna. Mar Biol 141:887–895. CrossRefGoogle Scholar
  68. Gerlach SA (1977) Means of meiofauna dispersal. In: Sterrer W, Ax P (eds) The meiofauna species in time and space. Mikrofauna Meeresbod, vol 61, pp 89–103Google Scholar
  69. Giard A (1904) Sur une faunule charactéristique des sables à diatomées d’Ambleteuse. C R Séanc Soc Biol Paris 56:107–165Google Scholar
  70. Giere O (2009) Meiobenthology: the microscopic motile fauna of aquatic sediments, 2nd edn. Springler-Verlag, Berlin HeidelbergGoogle Scholar
  71. Gobin JF, Warwick RM (2006) Geographical variation in species diversity: a comparison of marine polychaetes and nematodes. J Exp Mar Bio Ecol 330:234–244. CrossRefGoogle Scholar
  72. Golombek A, Tobergte S, Nesnidal MP, Purschke G, Struck TH (2013) Mitochondrial genomes to the rescue—diurodrilidae in the myzostomid trap. Mol Phylogenet Evol 68:312–326PubMedCrossRefGoogle Scholar
  73. Golombek A, Tobergte S, Struck TH (2015) Elucidating the phylogenetic position of Gnathostomulida and first mitochondrial genomes of Gnathostomulida, Gastrotricha and Polycladida (Platyhelminthes). Mol Phylogenet Evol 86:49–63. PubMedCrossRefGoogle Scholar
  74. Gruber-Vodicka HR, Dirks U, Leisch N, Baranyi C, Stoecker K, Bulgheresi S, Heindl NR, Horn M, Lott C, Loy A, Wagner M, Ott J (2011) Paracatenula, an ancient symbiosis between thiotrophic Alphaproteobacteria and catenulid flatworms. Proc Natl Acad Sci 108:12078–12083. PubMedCrossRefGoogle Scholar
  75. Guilini K, Soltwedel T, van Oevelen D, Vanreusel A (2011) Deep-sea nematodes actively colonise sediments, irrespective of the presence of a pulse of organic matter: results from an in situ experiment. PLoS One. PubMedPubMedCentralCrossRefGoogle Scholar
  76. Gwyther J, Fairweather PG (2005) Meiofaunal recruitment to mimic pneumatophores in a cool-temperate mangrove forest: spatial context and biofilm effects. J Exp Mar Bio Ecol 317:69–85. CrossRefGoogle Scholar
  77. Hagerman GM, Rieger RM (1981) Dispersal of benthic meiofauna by wave and current action in Bogue sound, North Carolina, USA. Mar Ecol 2:245–270. CrossRefGoogle Scholar
  78. Hansen TF, Houle D (2004) Evolvability, stabilizing selection, and the problem of stasis. In: Pigliucci M, Preston K (eds) Phenotypic integration: studying the ecology and evolution of complex phenotypes. Oxford University Press, New York, pp 130–154Google Scholar
  79. Hellberg ME (2009) Gene flow and isolation among populations of marine animals. Annu Rev Ecol Evol Syst 40:291–310. CrossRefGoogle Scholar
  80. Higgins RP, Thiel H (1988) Introduction to the study of meiofauna. Smithsonian Institution Press, WashingtonGoogle Scholar
  81. Hooper GJ, Davenport J (2006) Epifaunal composition and fractal dimensions of intertidal marine macroalgae in relation to emersion. J Mar Biol Assoc UK 86:1297–1304. CrossRefGoogle Scholar
  82. Hutchings P, Kupriyanova E (2018) Cosmopolitan polychaetes—fact or fiction? Personal and historical perspectives. Invertebr Syst 32:1–9. CrossRefGoogle Scholar
  83. Johannesson K (1988) The paradox of Rockall: why is a brooding gastropod (Littorina saxatilis) more widespread than one having a planktonic larval dispersal stage (L. littorea)? Mar Biol 99:507–513. CrossRefGoogle Scholar
  84. Johnson MS, Black R (2006) Islands increase genetic subdivision and disrupt patterns of connectivity of intertidal snails in a complex archipelago. Evolution (N Y) 60:2498–2506. CrossRefGoogle Scholar
  85. Jokiel PL (1990) Long-distance dispersal by rafting: reemergence of an old hypothesis. Endeavour 14:66–73CrossRefGoogle Scholar
  86. Jörger KM, Schrödl M (2013) How to describe a cryptic species? Practical challenges of molecular taxonomy. Front Zool 10:59. PubMedPubMedCentralCrossRefGoogle Scholar
  87. Jörger KM, Norenburg JL, Wilson NG, Schrödl M (2012) Barcoding against a paradox? Combined molecular species delineations reveal multiple cryptic lineages in elusive meiofaunal sea slugs. BMC Evol Biol 12:245. PubMedPubMedCentralCrossRefGoogle Scholar
  88. Jörger KM, Neusser TP, Brenzinger B, Schrödl M (2014) Exploring the diversity of mesopsammic gastropods: how to collect, identify, and delimitate small and elusive sea slugs? Am Malacol Bull 32:290–307. CrossRefGoogle Scholar
  89. Jouin-Toulmond C, Gambi MC (2007) Description of Saccocirrus goodrichi sp. nov. (Annelida: Polychaeta: Saccocirridae), a new Mediterranean species and new data on the chaetae of S. papillocercus and S. major. Cah Biol Mar 48:381–390Google Scholar
  90. Junkins R, Kelaher B, Levinton J (2006) Contributions of adult oligochaete emigration and immigration in a dynamic soft-sediment community. J Exp Mar Bio Ecol 330:208–220. CrossRefGoogle Scholar
  91. Kajihara H, Ikoma M, Yamasaki H, Hiruta SF (2015) Trilobodrilus itoi sp. nov., with a re-description of T. nipponicus (Annelida: Dinophilidae) and a molecular phylogeny of the genus. Zool Sci 32:405–417. PubMedCrossRefGoogle Scholar
  92. Kånneby T, Bernvi DC, Jondelius U (2015) Distribution, delimitation and description of species of Archaphanostoma (Acoela). Zool Scr 44:218–231. CrossRefGoogle Scholar
  93. Karanovic I, Tanaka H, Tsukagoshi A (2016) Congruence between male upper lip morphology and molecular phylogeny in Parapolycope (Ostracoda), with two new species from Korea Congruence between male upper lip morphology and molecular phylogeny in Parapolycope (Ostracoda), with two new species from. Invertebr Syst 30:231–254CrossRefGoogle Scholar
  94. Kelly RP, Palumbi SR (2010) Genetic structure among 50 species of the northeastern pacific rocky intertidal community. PLoS One. CrossRefPubMedPubMedCentralGoogle Scholar
  95. Kieneke A, Nikoukar H (2017) Integrative morphological and molecular investigation of Turbanella hyalina Schultze, 1853 (Gastrotricha: Macrodasyida), including a redescription of the species. Zool Anz 267:168–186. CrossRefGoogle Scholar
  96. Kieneke A, Martínez Arbizu PM, Fontaneto D (2012) Spatially structured populations with a low level of cryptic diversity in European marine Gastrotricha. Mol Ecol 21:1239–1254. PubMedCrossRefGoogle Scholar
  97. Klautau M, Russo CAM, Lazoski C, Boury-esnault N, Thorpe JP, Sole-cava AM, Klautau M, Russo CAM, Lazoski C, Boury-esnault N, John P, Solt-cava AM (1999) Does cosmopolitanism result from overconservative systematics? A case study using the marine sponge Chondrilla nucula. Evolution (N Y) 53:1414–1422Google Scholar
  98. Knowlton N (1993) Sibling species in the sea. Annu Rev Ecol Syst 24:189–216CrossRefGoogle Scholar
  99. Kritzer JP, Sale PF (2004) Metapopulation ecology in the sea: from Levins’ model to marine ecology and fisheries science. Fish Fish 5:131–140. CrossRefGoogle Scholar
  100. Kyle CJ, Boulding EG (2000) Comparative population genetic structure of marine gastropods (Littorina spp.) with and without pelagic larval dispersal. Mar Biol 137:835–845. CrossRefGoogle Scholar
  101. Leasi F, Norenburg JL (2014) The necessity of DNA taxonomy to reveal cryptic diversity and spatial distribution of meiofauna, with a focus on Nemertea. PLoS One. PubMedPubMedCentralCrossRefGoogle Scholar
  102. Leasi F, Norenburg JL (2016) At least some meiofaunal species are not everywhere. Indication of geographic, ecological and geological barriers affecting the dispersion of species of Ototyphlonemertes (Nemertea, Hoplonemertea). Mol Ecol 25:1381–1397. PubMedCrossRefGoogle Scholar
  103. Leasi F, Todaro MA (2007) The Muscular system of Musellifer delamarei and other chaetonotidans with implication for the phylogeny and systematisation of the Paucitubulatina (Gastrotricha). Biol J Linn Soc 94:379–398CrossRefGoogle Scholar
  104. Leasi F, Todaro MA (2009) Meiofaunal cryptic species revealed by confocal microscopy: the case of Xenotrichula intermedia (Gastrotricha). Mar Biol 156:1335–1346. CrossRefGoogle Scholar
  105. Leasi F, Tang CQ, De Smet WH, Fontaneto D (2013) Cryptic diversity with wide salinity tolerance in the putative euryhaline Testudinella clypeata (Rotifera, Monogononta). Zool J Linn Soc 168:17–28. CrossRefGoogle Scholar
  106. Leray M, Knowlton N (2015) DNA barcoding and metabarcoding of standardized samples reveal patterns of marine benthic diversity. Proc Natl Acad Sci 2014:201424997. CrossRefGoogle Scholar
  107. Leray M, Knowlton N (2016) Censusing marine eukaryotic diversity in the twenty-first century. Philos Trans R Soc B Biol Sci 371:20150331. CrossRefGoogle Scholar
  108. Lester SE, Ruttenberg BI (2005) The relationship between pelagic larval duration and range size in tropical reef fishes: a synthetic analysis. Proc Biol Sci 272:585–591. PubMedPubMedCentralCrossRefGoogle Scholar
  109. Lester SE, Ruttenberg BI, Gaines SD, Kinlan BP (2007) The relationship between dispersal ability and geographic range size. Ecol Lett 10:745–758. PubMedCrossRefGoogle Scholar
  110. Lins L, Vanreusel A, van Campenhout J, Ingels J (2013) Selective settlement of deep-sea canyon nematodes after resuspension—an experimental approach. J Exp Mar Bio Ecol 441:110–116. CrossRefGoogle Scholar
  111. Lovén S (1844) Chaetoderma, ett nytt masksläkte n.g. Öfvers K Vetenskaps-Akad Förh 1:116 + pl.112Google Scholar
  112. Mcfarlane CBA, Drolet D, Barbeau MA, Hamilton DJ, Ollerhead J (2013) Dispersal of marine benthic invertebrates through ice rafting. Ecology 94:250–256CrossRefGoogle Scholar
  113. Méndez N, Linke-Gamenick I, Forbes VE (2000) Variability in reproductive mode and larval development within the Capitella capitata species complex. Invertebr Reprod Dev 38:131–142. CrossRefGoogle Scholar
  114. Mevenkamp L, Van Campenhout J, Vanreusel A (2016) Experimental evidence for selective settlement of meiofauna from two distinct environments after sediment suspension. J Exp Mar Bio Ecol 474:195–203. CrossRefGoogle Scholar
  115. Meyer-Wachsmuth I, Curini Galletti M, Jondelius U (2014) Hyper-cryptic marine meiofauna: species complexes in Nemertodermatida. PLoS One. PubMedPubMedCentralCrossRefGoogle Scholar
  116. Muenter L, Kieneke A (2017) Novel myo-anatomical insights to the Xenotrichula intermedia species complex (Gastrotricha: Paucitubulatina): Implications for a pan-European species and reconsideration of muscle homology among Paucitubulatina. Proc Biol Soc Wash 130:165–185. CrossRefGoogle Scholar
  117. Neusser TP, Heß M, Schrödl M (2009) Tiny but complex - interactive 3D visualization of the interstitial acochlidian gastropod Pseudunela cornuta (Challis, 1970). Front Zool. PubMedPubMedCentralCrossRefGoogle Scholar
  118. Neusser TP, Jörger KM, Schrödl M (2011) Cryptic species in tropic sands—interactive 3D anatomy, molecular phylogeny and evolution of meiofaunal Pseudunelidae (Gastropoda, Acochlidia). PLoS One. PubMedPubMedCentralCrossRefGoogle Scholar
  119. Norris RD, Hull PM (2012) The temporal dimension of marine speciation. Evol Ecol 26:393–415. CrossRefGoogle Scholar
  120. Packmor J, Riedl T (2016) Records of Normanellidae Lang, 1944 (Copepoda, Harpacticoida) from Madeira island support the hypothetical role of seamounts and oceanic islands as “stepping stones” in the dispersal of marine meiofauna. Mar Biodivers 46:861–877. CrossRefGoogle Scholar
  121. Palmer M (1988) Dispersal of marine meiofauna: a review and conceptual model explaining passive transport and active emergence with implications for recruitment. Mar Ecol Prog Ser 48:81–91. CrossRefGoogle Scholar
  122. Palmer MA, Gust G (1985) Dispersal of meiofauna in a turbulent tidal creek. J Mar Res 43:179–210. CrossRefGoogle Scholar
  123. Pietsch A, Westheide W (1985) Ultrastructural investigations of presumed photoreceptors as a means of discrimination and identificafion of closely related species of the genus Microphtbalmus (Polychaeta, Hesionidae). Zoomorphology 105:265–276CrossRefGoogle Scholar
  124. Prasath D, Balasubramaniam J, Marimuthu P, Jayaraj KA (2017) New record of two free-living marine nematode species, Sphaerolaimus balticus and Sphaerolaimus islandicus (Nematoda: Sphaerolaimaidae) from Sipphighat mangrove region, South Andaman. Indian J Geo Mar Sci 46:1105–1109Google Scholar
  125. Pugh PJA (1996) Using artificial substrata to monitor how cryptofaunal acari colonize littoral algae on sub-antarctic south Georgia. Acarologia 37:188–200Google Scholar
  126. Radziejewska T, Gruszka P, Rokicka-Praxmajer J (2006) A home away from home: a meiobenthic assemblage in a ship’s ballast water tank sediment. Oceanologia 48:259–265Google Scholar
  127. Randsø PV, Domenico MD, Herranz M, Lorenzen ED, Sørensen MV (2018) Population genetic structure of the intertidal kinorhynch Echinoderes marthae (Kinorhyncha; Cyclorhagida; Echinoderidae) across the São Sebastião Channel, Brazil. Proc Biol Soc Wash 131:36–46. CrossRefGoogle Scholar
  128. Remane A (1933) Verteilung und organisation der benthonischen mikrofauna der Kieler Bucht. Wissenschaftliche Meeresuntersuchungen 21:161–221Google Scholar
  129. Rinaldo A, Garraffoni S, Araújo TQ (2017) Phylogeny of Pseudostomella Swedmark, 1956 (Gastrotricha: Macrodasyida) base on morphological data and first insights on the historical biogeography of Thaumastodermatidae. Proc Biol Soc Wash 130:222–238. CrossRefGoogle Scholar
  130. Rocha-Olivares A, Fleeger JW, Foltz DW (2001) Decoupling of molecular and morphological evolution in deep lineages of a meiobenthic Harpacticoid Copepod. Mol Biol Evol 18:1088–1102. PubMedCrossRefGoogle Scholar
  131. Ronce O (2007) How does it feel to be like a rolling stone? Ten questions about dispersal evolution. Annu Rev Ecol Evol Syst 38:231–253. CrossRefGoogle Scholar
  132. Rundell RJ, Leander BS (2014) Molecular examination of kalyptorhynch diversity (Platyhelminthes: Rhabdocoela), including descriptions of five meiofaunal species from the north-eastern Pacific Ocean. J Mar Biol Assoc UK 94:499–514. CrossRefGoogle Scholar
  133. Sahraean N, Van Campenhout J, Rigaux A, Mosallanejad H, Leliaert F, Moens T (2017) Lack of population genetic structure in the marine nematodes Ptycholaimellus pandispiculatus and Terschellingia longicaudata in beaches of the Persian Gulf, Iran. Mar Ecol. CrossRefGoogle Scholar
  134. Sánchez N, Yamasaki H, Pardos F, Sørensen MV, Martínez A (2016) Morphology disentangles the systematics of a ubiquitous but elusive meiofaunal group (Kinorhyncha: Pycnophyidae). Cladistics 32:479–505. CrossRefGoogle Scholar
  135. Sands CJ, Convey P, Linse K, McInnes SJ (2008) Assessing meiofaunal variation among individuals utilising morphological and molecular approaches: an example using the Tardigrada. BMC Ecol 8:7. PubMedPubMedCentralCrossRefGoogle Scholar
  136. Sanford E, Kelly MW (2011) Local adaptation in marine invertebrates. Annu Rev Mar Sci 3:509–537. CrossRefGoogle Scholar
  137. Scarpa F, Cossu P, Sanna D, Lai T, Norenburg JL, Curini-Galletti M, Casu M (2015) An 18S and 28S-based clock calibration for marine Proseriata (Platyhelminthes). J Exp Mar Bio Ecol 463:22–31. CrossRefGoogle Scholar
  138. Schmidt H, Westheide W (1999) Genetic relationships (RAPD-PCR) between geographically separated populations of the “cosmopolitan” interstitial polychaete Hesionides gohari (Hesionidae) and the evolutionary origin of the freshwater species Hesionides riegerorum. Biol Bull 196:216–226. PubMedCrossRefGoogle Scholar
  139. Schmidt H, Westheide W (2000) Are the meiofaunal polychaetes Hesionides arenaria and Stygocapitella subterranea true cosmopolitan species?—results of RAPD-PCR investigations. Zool Scr 29:17–27. CrossRefGoogle Scholar
  140. Schratzberger M, Rees HL, Boyd SE (2000) Effects of simulated deposition of dredged material on structure of nematode assemblages—the role of burial. Mar Biol 136:519–530CrossRefGoogle Scholar
  141. Scotese CR (2002) PALEOMAP project website. Accessed May 2017
  142. Sedlacek L, Thistle D (2006) Emergence on the continental shelf: differences among species and between microhabitats. Mar Ecol Prog Ser 311:29–36CrossRefGoogle Scholar
  143. Shanks AL, Walters K (1997) Holoplankton, meroplankton, and meiofauna associated with marine snow. Mar Ecol Prog Ser 156:75–86CrossRefGoogle Scholar
  144. Smythe AB (2015) Evolution of feeding structures in the marine nematode order Enoplida. Integr Comp Biol 55:228–240. PubMedCrossRefGoogle Scholar
  145. Sponer R, Roy MS (2002) Phylogeographic analysis of the brooding brittle star Amphipholis squamata (Echinodermata) along the coast of New Zealand reveals high cryptic genetic variation and cryptic dispersal potential. Evolution (N Y) 56:1954–1967Google Scholar
  146. Sterrer W (1973) Plate tectonics as a mechanism for dispersal and speciation in interstitial sand fauna. Neth J Sea Res 7:200–222CrossRefGoogle Scholar
  147. Sterrer W, Sørensen MV (2006) Chirognathia dracula gen. et spec. nov. (Gnathostomulida) from the west coast of North America. Mar Biol Res 2:296–302. CrossRefGoogle Scholar
  148. Struck TH, Koczula J, Stateczny D, Meyer C, Purschke G (2017) Two new species in the annelid genus Stygocapitella (Orbiniida, Parergodrilidae) with comments on their biogeography. Zootaxa 4286:301–332. CrossRefGoogle Scholar
  149. Struck TH, Feder JL, Bendiksby M, Birkeland S, Cerca J, Gusarov VI, Kistenich S, Larsson K-H, Liow LH, Nowak MD, Stedje B, Bachmann L, Dimitrov D (2018a) Cryptic species—more than terminological chaos: a reply to heethoff. Trends Ecol Evol 33:310–312. PubMedCrossRefGoogle Scholar
  150. Struck TH, Feder JL, Bendiksby M, Birkeland S, Cerca J, Gusarov VI, Kistenich S, Larsson K-H, Liow LH, Nowak MD, Stedje B, Bachmann L, Dimitrov D (2018b) Finding evolutionary processes hidden in cryptic species. Trends Ecol Evol. CrossRefPubMedGoogle Scholar
  151. Suatoni E, Vicario S, Rice S, Snell T, Caccone A (2006) An analysis of species boundaries and biogeographic patterns in a cryptic species complex: the rotifer—Brachionus plicatilis. Mol Phylogenet Evol 41:86–98. PubMedCrossRefGoogle Scholar
  152. Swift HF, Daglio LG, Dawson MN (2016) Three routes to crypsis: stasis, convergence, and parallelism in the Mastigias species complex (Scyphozoa, Rhizostomeae). Mol Phylogenet Evol 99:103–115. PubMedCrossRefGoogle Scholar
  153. Tanaka H, Ohtsuka S (2016) Historical biogeography of the genus Polycopissa (Ostracoda: Myodocopa: Cladocopina), with the description and DNA barcode of the second Indo-Pacific species from the Seto Inland Sea. Mar Biodivers 46:625–640. CrossRefGoogle Scholar
  154. Taylor DJ, Finston TL, Hebert PDN (1998) Biogeography of a widespread freshwater crustacean: pseudocongruence and cryptic endemism in the North American Daphnia laevis complex. Evolution (N Y) 52:1648–1670Google Scholar
  155. Teasdale M, Vopel K, Thistle D (2004) The timing of benthic copepod emergence. Limnol Oceanogr 49:884–889CrossRefGoogle Scholar
  156. Thistle D (2003) Harpacticoid copepod emergence at a shelf site in summer and winter: implications for hydrodynamic and mating hypotheses. Mar Ecol Prog Ser 248:177–185. CrossRefGoogle Scholar
  157. Thomas MC, Lana PC (2011) A new look into the small-scale dispersal of free-living marine nematodes. Zoologia 28:449–456. CrossRefGoogle Scholar
  158. Todaro MA, Fleeger JW, Hu YP, Hrincevich AW, Foltz DW (1996) Are meiofaunal species cosmopolitan? Morphological and molecular analysis of Xenotrichula intermedia (Gastrotricha: Chaetonotida). Mar Biol 125:735–742CrossRefGoogle Scholar
  159. Todaro MA, Telford MJ, Lockyer AE, Littlewood DTJ (2006) Interrelationships of the Gastrotricha and their place among the Metazoa inferred from 18S rRNA genes. Zool Scr 35:251–259. CrossRefGoogle Scholar
  160. Todaro MA, Leasi F, Hochberg R (2014) A new species, genus and family of marine Gastrotricha from Jamaica, with a phylogenetic analysis of Macrodasyida based on molecular data. Syst Biodivers 12:473–488. CrossRefGoogle Scholar
  161. Tulchinsky AY, Norenburg JL, Turbeville JM (2012) Phylogeography of the marine interstitial nemertean Ototyphlonemertes parmula (Nemertea, Hoplonemertea) reveals cryptic diversity and high dispersal potential. Mar Biol 159:661–674. CrossRefGoogle Scholar
  162. Ullberg J, Ólafsson E (2003a) Effects of biological disturbance by Monoporeia affinis (Amphipoda) on small-scale migration of marine nematodes in low-energy soft sediments. Mar Biol 143:867–874. CrossRefGoogle Scholar
  163. Ullberg J, Ólafsson E (2003b) Free-living marine nematodes actively choose habitat when descending from the water column. Mar Ecol Prog Ser 250:141–149. CrossRefGoogle Scholar
  164. Van Campenhout J, Derycke S, Moens T, Vanreusel A (2014) Differences in life-histories refute ecological equivalence of cryptic species and provide clues to the origin of bathyal Halomonhystera (Nematoda). PLoS One. CrossRefPubMedPubMedCentralGoogle Scholar
  165. van Oppen MJH, Klerk H, Olsen JL, Stam WT (1996) Hidden diversity in marine algae: some examples of genetic variation below the species level. J Mar Biol Assoc UK 76:239–242CrossRefGoogle Scholar
  166. Van Steenkiste NWL, Herbert ER, Leander BS (2018) Species diversity in the marine microturbellarian Astrotorhynchus bifidus sensu lato (Platyhelminthes: Rhabdocoela) from the Northeast Pacific Ocean. Mol Phylogenet Evol 120:259–273. PubMedCrossRefGoogle Scholar
  167. Villora-Moreno S, de Grimaldi SZ (1993) Redescription and ecology of Batillipes phreaticus Renaud-Debyser, 1959 (Arthrotardigrada, Batillipedidae) in the gulf of Valencia (western mediterranean). Cah Biol Mar 34:387–399Google Scholar
  168. von Soosten C, Schmidt H, Westheide W (1998) Genetic variability and relationships among geographically widely separated populations of Petitia amphophthalma (Polychaeta: Syllidae). Results from RAPD-PCR investigations. Mar Biol 131:659–669. CrossRefGoogle Scholar
  169. Wada S, Kameda Y, Chiba S (2013) Long-term stasis and short-term divergence in the phenotypes of microsnails on oceanic islands. Mol Ecol 22:4801–4810. PubMedCrossRefGoogle Scholar
  170. Wares JP, Gianes SD, Cunningham CW (2001) A comparative study of asymmetric migration events across a marine biogeographic boundary. Evolution (N Y) 55:295–306Google Scholar
  171. Westheide W (1977) The geographical distribution of interstitial polychaetes. Mikrofauna Meeresb 61:287–302Google Scholar
  172. Westheide W (1991) The meiofauna of the galapagos: a review. In: James Mathew J (ed) Galápagos marine invertebrates. Springler, New York, pp 37–69CrossRefGoogle Scholar
  173. Westheide W (2005) Meiofauna geographic distribution: vicariance and dispersal. Meiofauna Mar 14:201–207Google Scholar
  174. Westheide W, Hass-Cordes E (2001) Molecular taxonomy: description of a cryptic Petitia species (Polychaeta: Syllidae) from the island of Mahe (Seychelles, Indian Ocean) using RAPD markers and ITS2 sequences. J Zool Syst Evol Res 39:103–111CrossRefGoogle Scholar
  175. Westheide W, Rieger RM (1987) Systematics of the amphiatlantic Microphthalmus listensis species-group (Polychaeta: Hesionidae): facts and concepts for reconstruction of phylogeny and speciation. Zeitschrift für Zool Syst und Evol 25:12–39CrossRefGoogle Scholar
  176. White TA, Stefanni S, Stamford J, Hoelzel AR (2009) Unexpected panmixia in a long-lived, deep-sea fish with well-defined spawning habitat and relatively low fecundity. Mol Ecol 18:2563–2573. PubMedCrossRefGoogle Scholar
  177. Yamasaki H, Hiruta SF, Kajihara H, Dick MH (2014) Two Kinorhynch species (Cyclorhagida, Echinoderidae, Echinoderes) show different distribution patterns across Tsugaru Strait, Northern Japan. Zool Sci 31:421–429. PubMedCrossRefGoogle Scholar
  178. Zawierucha K, Grzelak K, Kotwicki L, Michalczyk Ł, Kaczmarek Ł (2013) Batillipes pennaki Marcus, 1946, a new addition to the Thai Tardigrade fauna, with an overview of literature on the species. Pak J Zool 45:801–808Google Scholar
  179. Zeppilli D, Vanreusel A, Danovaro R (2011) Cosmopolitanism and biogeography of the genus Manganonema (Nematoda: Monhysterida) in the deep sea. Animals 1:291–305. PubMedCrossRefGoogle Scholar
  180. Zeppilli D, Sarrazin J, Leduc D, Arbizu PM, Fontaneto D, Fontanier C, Gooday AJ, Kristensen RM, Ivanenko VN, Sørensen MV, Vanreusel A, Thébault J, Mea M, Allio N, Andro T, Arvigo A, Castrec J, Danielo M, Foulon V, Fumeron R, Hermabessiere L, Hulot V, James T, Langonne-Augen R, Le Bot T, Long M, Mahabror D, Morel Q, Pantalos M, Pouplard E, Raimondeau L, Rio-Cabello A, Seite S, Traisnel G, Urvoy K, Van Der Stegen T, Weyand M, Fernandes D (2015) Is the meiofauna a good indicator for climate change and anthropogenic impacts? Mar Biodivers 45:505–535. CrossRefGoogle Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Frontiers of Evolutionary Zoology Research Group, Natural History MuseumUniversity of OsloOsloNorway
  2. 2.Fachbereich Biologie/ChemieUniversität OsnabrückOsnabrückGermany

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