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The post-embryonic development of Remipedia (Crustacea)—additional results and new insights

  • Stefan Koenemann
  • Jørgen Olesen
  • Frederike Alwes
  • Thomas M. Iliffe
  • Mario Hoenemann
  • Petra Ungerer
  • Carsten Wolff
  • Gerhard ScholtzEmail author
Original Article

Abstract

The post-embryonic development of a species of the enigmatic crustacean group Remipedia is described in detail for the first time under various aspects. Applying a molecular approach, we can clearly prove the species identity of the larvae as belonging to Pleomothra apletocheles. We document the cellular level of several larval stages and the differentiation of segments, limbs, and the general body morphology applying the techniques of confocal laser scanning microscopy and scanning electron microscopy. In addition, we document the swimming behavior and the peculiar movements of the naupliar appendages. A comparison of our results with published data on other Crustacea and their larval development tentatively supports ideas about phylogenetic affinities of the Remipedia to the Malacostraca.

Keywords

Arthropod evolution Nauplius larva Anamorphic development Swimming behavior Limb formation 

Notes

Acknowledgments

Collection expeditions to Abaco were funded by grants from the Biodiversity Surveys and Inventories Program, NSF (DEB-0315903) (T.M.I.), and German Research Foundation (DFG KO 3483/1-1) (S.K.). Collection of specimens was carried out under Bahamas Department of Fisheries marine resource collection permit (T.M.I.). SEM pictures were made at the Zoologisk Museum, Statens Naturhistoriske Museum, Københavns Universitet funded by Synthesys DK-TAF-3371. Logistical assistance for field work in Abaco was provided by Nancy Albury (Friends of the Environment, Abaco). In addition to T. Iliffe and M. Hoenemann, other March 2006 Abaco expedition team members included Renee Bishop, Brett Gonzalez, Lara Hinderstein, Brian Kakuk, Gregg Stanton, Tamara Thomsen, and Ute Wollermann, while August 2006 collections were carried out by B. Kakuk and T. Iliffe.

Supplementary material

427_2009_273_MOESM1_ESM.mpg (7 mb)
ESM 1 The movie shows the movements of the appendages of an orthonauplius (first part) and a metanauplius (second part) of the remipede crustacean P. apletocheles video-recorded in a Petri dish with cave water. Please note the impressive flexibility of the mandibles (third pair of appendages) (compare with Fig. 6). (MPG 7.02 MB).

References

  1. Addis A, Biagi F, Floris A, Puddu E, Carcupino M (2007) Larval development of Lightiella magdalenina (Crustacea, Cephalocarida). Mar Biol 152:1432–1793CrossRefGoogle Scholar
  2. Alwes F, Scholtz G (2006) Stages and other aspects of the embryology of the parthenogenetic Marmorkrebs (Decapoda, Reptantia, Astacida). Dev Genes Evol 216:169–184PubMedCrossRefGoogle Scholar
  3. Anderson DT (1973) Embryology and phylogeny in annelids and arthropods. Pergamon, OxfordGoogle Scholar
  4. Ax P (1999) Das System der Metazoa II. Ein Lehrbuch der phylogenetischen Systematik. Gustav Fischer Verlag, StuttgartGoogle Scholar
  5. Benesch R (1969) Zur Ontogenie und Morphologie von Artemia salina L. Zool Jb Anat 86:307–458Google Scholar
  6. Boxshall GA (1997) Comparative limb morphology in major crustacean groups: the coxa-basis joint in postmandibular limbs. In: Fortey RA, Thomas RH (eds) Arthropod relationships. Chapman & Hall, London, pp 156–167Google Scholar
  7. Boxshall GA (2004) The evolution of arthropod limbs. Biol Rev 79:253–300PubMedCrossRefGoogle Scholar
  8. Brusca RC, Brusca GJ (1990) Invertebrates. Sinauer, SunderlandGoogle Scholar
  9. Carapelli A, Liò P, Nardi F, van der Wath E, Frati F (2007) Phylogenetic analysis of mitochondrial protein coding genes confirms the reciprocal paraphyly of Hexapoda and Crustacea. BMC Evol Biol 7(suppl. 2):S8PubMedCrossRefGoogle Scholar
  10. Cook CE, Qiaoyun Y, Akam M (2005) Mitochondrial genomes suggest that hexapods and crustaceans are mutually paraphyletic. Proc R Soc Lond B 272:1295–1304CrossRefGoogle Scholar
  11. Dahms H-U (1989) Short note. First record of a lecithotrophic nauplius among Harpacticoida (Crustacea, Copepoda) collected from the Weddell Sea (Antarctica). Pol Biol 10:221–224CrossRefGoogle Scholar
  12. Dohle W, Gerberding M, Hejnol A, Scholtz G (2004) Cell lineage, segment differentiation, and gene expression in crustaceans. In: Scholtz G (ed) Evolutionary developmental biology of Crustacea. Crustacean Issues 15.A.A. Balkema, Lisse, pp 95–133Google Scholar
  13. Edgecombe GD (2004) Morphological data, extant Myriapoda, and the myriapod stem-group. Contrib Zool 73:207–252Google Scholar
  14. Fanenbruck M, Harzsch S (2005) A brain atlas of Godzilliognomus frondosus Yager, 1989 (Remipedia, Godzilliidae) and comparison with the brain of Speleonectes tulumensis Yager, 1987 (Remipedia, Speleonectidae): implications for arthropod relationships. Arthrop Struct Dev 34:343–378CrossRefGoogle Scholar
  15. Fanenbruck M, Harzsch S, Wägele JW (2004) The brain of the Remipedia (Crustacea) and an alternative hypothesis on their phylogenetic relationships. Proc Natl Acad Sci USA 101:3868–3873PubMedCrossRefGoogle Scholar
  16. 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
  17. Giribet G, Richter S, Edgecombe GD, Wheeler WC (2005) The position of crustaceans within the arthropoda—evidence from nine molecular loci and morphology. In: Koenemann S, Jenner RA (eds) Crustacea and arthropod relationships. Crustacean Issues 16. CRC, Boca Raton, pp 307–352Google Scholar
  18. Gruner HE (1993) Klasse Crustacea. In: Gruner HE (ed) Lehrbuch der Speziellen Zoologie. Band I. 4. Teil: Arthropoda (ohne Insecta). Gustav Fischer Verlag, Jena Stuttgart, pp 448–1009Google Scholar
  19. Hejnol A, Scholtz G (2004) Clonal analysis of Distal-less and engrailed expression patterns during early morphogenesis of uniramous and biramous crustacean limbs. Dev Genes Evol 214:473–485PubMedGoogle Scholar
  20. Høeg JT, Lagersson NC, Glenner H (2004) The complete cypris larva and its significance in thecostracan phylogeny. In: Scholtz G (ed) Evolutionary developmental biology of Crustacea. Crustacean Issues 15.A.A. Balkema, Lisse, pp 197–215Google Scholar
  21. Koenemann S, Schram FR, Bloechl A, Hoenemann M, Iliffe TM, Held C (2007a) Post-embryonic development of remipede crustaceans. Evol Dev 9:117–121PubMedGoogle Scholar
  22. Koenemann S, Schram FR, Hoenemann M, Iliffe TM (2007b) Phylogenetic analysis of Remipedia (Crustacea). Org Divers Evol 7:33–51CrossRefGoogle Scholar
  23. Koenemann S, Schram FR, Iliffe TM, Hinderstein LM, Bloechl A (2007c) Behavior of Remipedia in the laboratory, with supporting field observations. J Crust Biol 27:534–542CrossRefGoogle Scholar
  24. Koenemann S, Ziegler M, Iliffe TM (2008) Pleomothra fragilis n. sp. (Remipedia) from the Bahamas, with remarks on morphologic reductions and postnaupliar development. J Crust Biol 28:128–136CrossRefGoogle Scholar
  25. Kohlhage K, Yager J (1994) An analysis of swimming in remipede crustaceans. Phil Trans R Soc Lond B 346:213–221CrossRefGoogle Scholar
  26. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163PubMedCrossRefGoogle Scholar
  27. Lauterbach K-E (1983) Zum Problem der Monophylie der Crustacea. Verh naturwiss Ver Hamburg 26:293–320Google Scholar
  28. Maas A, Waloszek D (2001) Larval development of Euphausia superba Dana, 1852 and a phylogenetic analysis of the Euphausiacea. Hydrobiologia 448:143–169CrossRefGoogle Scholar
  29. Moura G, Christoffersen ML (1996) The system of the mandibulate arthropods: Tracheata and Remipedia as sister groups; Crustacea non-monophyletic. J Comp Biol 1(3/4):95–113Google Scholar
  30. Motoh H (1981) Studies on the fisheries biology of the giant tiger prawn, Penaeus monodon in the Philippines. SEAFDEC Tech Rep 7:128Google Scholar
  31. Müller KJ, Walossek D (1986) Arthropod larvae from the upper Cambrian of Sweden. Trans R Soc Edinb Earth Sci 77:157–179Google Scholar
  32. Olesen J (2004) On the ontogeny of the Branchiopoda (Crustacea):contribution of development to phylogeny and classification. In: Scholtz G (ed) Evolutionary developmental biology of Crustacea. Crustacean Issues 15.A.A. Balkema, Lisse, pp 217–269Google Scholar
  33. Olesen J (2007) Monophyly and phylogeny of the Branchiopoda (Crustacea), with focus on morphology and homologies of branchiopod phyllopodous limbs. J Crust Biol 27:165–183CrossRefGoogle Scholar
  34. Olesen J, Walossek D (2000) Limb ontogeny and trunk segmentation in Nebalia species. Zoomorphology 120:47–64CrossRefGoogle Scholar
  35. Olesen J, Grygier MJ (2004) Larval development of Japanese ‘conchostracans’: part 2, larval development of Caenestheriella gifuensis (Crustacea, Branchiopoda, Spinicaudata, Cyzicidae), with notes on homologies and evolution of certain naupliar appendages within the Branchiopoda. Arthrop Struct Dev 33:453–469CrossRefGoogle Scholar
  36. Pabst T, Scholtz G (2009) The development of phyllopodous limbs in Leptostraca and Branchiopoda. J Crust Biol 29:1–12CrossRefGoogle Scholar
  37. Regier JC, Shultz JW, Kambic RE (2005) Pancrustacean phylogeny: hexapods are terrestrial crustaceans and maxillopods are not monophyletic. Proc Acad Sci 272:395–401Google Scholar
  38. Richter S, Scholtz G (2001) Phylogenetic analysis of the Malacostraca (Crustacea). J Zool Syst Evol Res 39:113–36CrossRefGoogle Scholar
  39. Richter S (2002) The Tetraconata concept: hexapod–crustacean relationships and the phylogeny of Crustacea. Org Divers Evol 2:217–237CrossRefGoogle Scholar
  40. Sanders HL (1963) The Cephalocarida. Functional morphology, larval development, comparative external anatomy. Mem Conn Acad Arts Sci 15:1–80Google Scholar
  41. Sars GO (1898) On the propagation and early development of Euphausiidæ. Arch Math Naturvid 20:1–41Google Scholar
  42. Scholtz G (1990) The formation, differentiation and segmentation of the post-naupliar germ band of the amphipod Gammarus pulex L. (Crustacea, Malacostraca, Peracarida). Proc R Soc Lond B 239:163–211CrossRefGoogle Scholar
  43. Scholtz G (1997) Cleavage, germ band formation and head segmentation: the ground pattern of the Euarthropoda. In: Fortey RA, Thomas RH (eds) Arthropod relationships. Chapman & Hall, London, pp 317–332Google Scholar
  44. Scholtz G (2000) Evolution of the nauplius stage in malacostracan crustaceans. J Zool Syst Evol Res 38:175–187CrossRefGoogle Scholar
  45. Scholtz G (2002) Phylogeny and evolution. In: Holdich D (ed) Biology of freshwater crayfish. Blackwell Science, Oxford, pp 30–52Google Scholar
  46. Scholtz G (2004) Baupläne versus ground patterns, phyla versus monophyla: aspects of patterns and processes in evolutionary developmental biology. In: Scholtz G (ed) Evolutionary developmental biology of Crustacea. Crustacean Issues 15.A.A. Balkema, Lisse, pp 3–16Google Scholar
  47. Scholtz G, Wolff C (2002) Cleavage pattern, gastrulation, and germ disc formation of the amphipod crustacean Orchestia cavimana. Contrib Zool 71:9–28Google Scholar
  48. Scholtz G, Mittmann B, Gerberding M (1998) The pattern of Distal-less expression in the mouthparts of crustaceans, myriapods and insects: new evidence for a gnathobasic mandible and the common origin of Mandibulata. Int J Dev Biol 42:801–810PubMedGoogle Scholar
  49. Schram FR (1986) Crustacea. Oxford Univ Press, New YorkGoogle Scholar
  50. Schram FR, Hof CHJ (1998) Fossils and the interrelationships of major crustacean groups. In: Edgecombe G (ed) Arthropod fossils and phylogeny. Columbia Univ Press, New York, pp 233–302Google Scholar
  51. Schram FR, Koenemann S (2004) Shrimp cocktail: are crustaceans monophyletic? In: Cracraft J, Donoghue MJ (eds) Assembling the tree of life. Oxford Univ Press, Oxford, pp 319–329Google Scholar
  52. Spears T, Abele LG (1997) Crustacean phylogeny inferred from 18S rDNA. In: Fortey RA, Thomas RH (eds) Arthropod Relationships. Chapman & Hall, New York, pp 169–187Google Scholar
  53. Walossek D (1993) The upper Cambrian Rehbachiella and the phylogeny of Branchiopoda and Crustacea. Fossils Strata 32:1–202Google Scholar
  54. Walossek D, Høeg JT, Shirley TC (1996) Larval development of the rhizocephalan cirripede Briarosaccus tenellus (Maxillopoda: Thecostraca) reared in the laboratory: a scanning electron microscopy study. Hydrobiologia 328:9–47CrossRefGoogle Scholar
  55. Waloszek D (2003) Cambrian “Orsten”-type preserved arthropods and the phylogeny of Crustacea. In: Legakis A, Sfenthourakis S, Polymeni R, Thessalou-Legaki M (eds) The new panorama of animal evolution. Pensoft, Sofia, pp 69–87Google Scholar
  56. Williams TA (1998) Distal-less expression in crustaceans and the patterning of branched limbs. Dev Genes Evol 207:427–434PubMedCrossRefGoogle Scholar
  57. Wills MA (1998) A phylogeny of recent Crustacea derived from morphological characters. In: Fortey RA, Thomas RH (eds) Arthropod relationships. Chapman & Hall, New York, pp 189–209Google Scholar
  58. Wolff C, Scholtz G (2008) The clonal composition of biramous and uniramous arthropod limbs. Proc R Soc B 275:1023–1028PubMedCrossRefGoogle Scholar
  59. Yager J (1981) Remipedia, a new class of Crustacea from a marine cave in the Bahamas. J Crust Biol 1:328–333CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Stefan Koenemann
    • 1
  • Jørgen Olesen
    • 2
  • Frederike Alwes
    • 3
  • Thomas M. Iliffe
    • 4
  • Mario Hoenemann
    • 1
  • Petra Ungerer
    • 3
  • Carsten Wolff
    • 3
  • Gerhard Scholtz
    • 3
    Email author
  1. 1.Institute for Animal Ecology and Cell BiologyUniversity of Veterinary Medicine HannoverHannoverGermany
  2. 2.Natural History Museum of DenmarkCopenhagen UniversityCopenhagenDenmark
  3. 3.Institut für Biologie/Vergleichende ZoologieHumboldt-Universität zu BerlinBerlinGermany
  4. 4.Department of Marine BiologyTexas A&M University at GalvestonGalvestonUSA

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