, Volume 128, Issue 3, pp 247–262 | Cite as

Nephridial development and body cavity formation in Artemia salina (Crustacea: Branchiopoda): no evidence for any transitory coelom

  • Thomas BartolomaeusEmail author
  • Björn Quast
  • Markus Koch
Original Paper


The Ecdysozoa-hypothesis on the origin of arthropods questions the homology of segmentation in arthropods, onychophorans, and annelids. The implication of convergent gain of metamery in these groups seems to conflict particularly with the correspondence in the development of serial coelomic cavities and metanephridia. Ultrastructural studies of the mesoderm development in Onychophora revealed that main correspondence with the state in annelids concerns the involvement of epithelial lining cells of the embryonic coelomic cavities in the formation of the visceral and somatic musculature. The significance of this correspondence, however, remained unclear as comparable data on the state in arthropods were still missing. Developmental studies on selected representatives covering all major arthropod subgroups aim to fill in this gap. Data were raised by a combination of transmission electron microscopy and fluorescent stainings of the muscular system and nuclei for the anostracan crustacean Artemia salina. In this species, putative transitory coelomic cavities proved to be absent in all trunk segments. In the second antennal and second maxillary segments small, compact nephridial anlagen develop into a sacculus and excretory duct. The sacculus originates from the terminal cells of the nephridial duct, which is formed in advance. The lumen of the sacculus is inconspicuous in its earliest functional stage and later enlarges to a bulb; it accordingly represents no remnant of any primarily large coelomic cavity. The muscular system is entirely formed prior to and independent of coelomic or nephridial anlagen. Visceral and somatic mesoderm already separate in the caudal body region. Transitory segmental clusters of mesodermal cells are composed of somatic cells only and accordingly represent no “somites”. Our observations overall do not provide any support for the homology of coelomic cavities in annelids and arthropods.


Anostraca Nephridia Mesoderm Ultrastructure Ecdysozoa 



Our project on the mesoderm development in arthropods is supported within the priority programme “Deep Metazoan Phylogeny” of the German Research Foundation (DFG-project Ba 1520/9). We thank Alexander Suh (FU Berlin) for rearing the animals, and Jörn von Döhren (FU Berlin) for his help with the fluorescence staining. Suggestions on the manuscript by two anonymous referees are also gratefully acknowledged.


  1. Anderson DT (1967) Larval development and segment formation in the branchipod crustaceans Limnadia stanleyana King (Conchostraca) and Artemia salina (L.) (Anostraca). Aust J ZooI 15:47–91. doi: 10.1071/ZO9670047 CrossRefGoogle Scholar
  2. Anderson DT (1973) Embryology and phylogeny in annelids and arthropods. Pergamon Press, OxfordGoogle Scholar
  3. Arnaud F, Bamber RN (1987) The biology of Pycnogonida. Adv Mar Biol 24:1–96. doi: 10.1016/S0065-2881(08)60073-5 CrossRefGoogle Scholar
  4. Ax P (1996) Multicellular animals. a new approach to the phylogenetic order in nature, vol 1. Springer, HeidelbergGoogle Scholar
  5. Bartolomaeus T (1993) Die Leibeshöhlenverhältnisse und Nierenorgane der Bilateria—Ultrastruktur, Entwicklung und Evolution. Universität Göttingen, HabilitationsschriftGoogle Scholar
  6. Bartolomaeus T (1994) On the ultrastructure of the coelomic lining in annelids, echiurids and sipunculids. Microfauna Marina 9:171–220Google Scholar
  7. Bartolomaeus T, Quast B (2005) Structure and development of nephridia in Annelida and related taxa. Hydrobiologia 535/536:139–164. doi: 10.1007/s10750-004-1840-z CrossRefGoogle Scholar
  8. Bartolomaeus T, Ruhberg H (1999) Ultrastructure of the body cavity lining in embryos of Epiperipatus biolleyi (Peripatidae, Onychophora). Invertebr Biol 118:165–174. doi: 10.2307/3227057 CrossRefGoogle Scholar
  9. Benesch R (1969) Zur Ontogenie und Morphologie von Artemia salina L. Zool Jb Anat 86:307–458Google Scholar
  10. Cannon HG (1924) On the development of an estheriid crustacean. Philos Trans R Soc B 212:395–430. doi: 10.1098/rstb.1924.0010 CrossRefGoogle Scholar
  11. Criel GRJ (1991) Ontogeny of Artemia. In: Browne RA, Sorgeloos P, Trotman CNA (eds) Artemia biology. CRC Press, Boca Raton, pp 155–185Google Scholar
  12. Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, Seaver E, Rouse GW, Obst M, Edgecombe GD, Sörensen MV, Haddock SHD, Schmidt-Rhaesa A, Okusu A, Kristensen RM, Wheeler WC, Martindale MQ, Giribet G (2008) Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452:745–749. doi: 10.1038/nature06614 PubMedCrossRefGoogle Scholar
  13. Edgecombe GD (2004) Morphological data, extant Myriapoda, and the myriapod stem-group. Contrib Zool 73(3):207–252Google Scholar
  14. Fahrenbach WH, Arango CP (2007) Microscopic anatomy of Pycnogonida: II. Digestive system. III. Excretory system. J Morphol 268:917–935. doi: 10.1002/jmor.10553 PubMedCrossRefGoogle Scholar
  15. Fränsemeier L (1939) Zur Frage der Herkunft des metanauplialen Mesoderms und die Segmentbildung bei Artemia salina Leach. Z Wiss Zool 152:439–472Google Scholar
  16. Gilbert SF (1997) Arthropods: the crustaceans, spiders, and myriapods. In: Gilbert SF, Raunio AM (eds) Embryology: constructing the organism. Sinauer Ass, Sunderland, pp 237–257Google Scholar
  17. Giribet G (2003) Molecules, development and fossils in the study of metazoan evolution; Articulata versus Ecdysozoa revisited. Zoology 106:303–326. doi: 10.1078/0944-2006-00131 PubMedCrossRefGoogle Scholar
  18. Giribet G, Richter S, Edgecombe GD, Wheeler WC (2005) The position of crustaceans within Arthropoda–evidence from nine molecular loci and morphology. In: Koenemann S, Jenner RA (eds) Crustacea and arthropod relationships. Taylor & Francis, Boca Raton, pp 307–352Google Scholar
  19. Hessler RR, Elofsson R (1995) Segmental podocytic excretory glands in the thorax of Hutchinsoniella macracantha (Cephalocarida). J Crustac Biol 15:61–69. doi: 10.2307/1549011 CrossRefGoogle Scholar
  20. Hessler RR, Elofsson R (2007) An excretory organ in the Mystacocarida (Crustacea). Arthropod Struct Dev 36:171–181. doi: 10.1016/j.asd.2007.01.002 PubMedCrossRefGoogle Scholar
  21. Hinsch GW (1990) Morphology, histology, and ultrastructure of the maxillary glands in crustaceans: their probable function in morphogenesis. In: Gupta AP (ed) Morphogenetic hormones of arthropods. Embryonic and postembryonic sources, vol 1: 2. Rutgers Univ Press, New Brunsbrick, London, pp 473–494Google Scholar
  22. Hosfeld B, Schminke HK (1997) Discovery of segmental extranephridial podocytes in Harpacticoida (Copepoda) and Bathynellacea (Syncarida). J Crustac Biol 17:13–20. doi: 10.2307/1549456 CrossRefGoogle Scholar
  23. Kieneke A, Ahlrichs WH, Arbizu PM, Bartolomaeus T (2008) Ultrastructure of protonephridia in Xenotrichula carolinensis syltensis and Chaetonotus maximus (Gastrotricha: Chaetonotida): comparative evaluation of the gastrotrich excretory organs. Zoomorphology 127:1–20. doi: 10.1007/s00435-007-0051-3 CrossRefGoogle Scholar
  24. Kiernan DA, Hertzler PL (2006) Muscle development in dendrobranchiate shrimp, with comparison with Artemia. Evol Dev 8(6):537–549. doi: 10.1111/j.1525-142X.2006.00126.x PubMedCrossRefGoogle Scholar
  25. Klag J, Ksiazkiewicz Kapralska M (1989) Embryonic hemocytes and body cavity formation in Tetrodontophora bielanensis (Insecta, Collembola). In: Dallai R (ed) Third international seminar on Apterygota. University of Siena, Siena, pp 215–219Google Scholar
  26. Mallat J, Giribet G (2006) Further use of nearly complete 28S and 18S rRNA genes to classify Ecdysozoa: 37 more arthropods and a kinorhynch. Mol Phylogenet Evol 40:772–794. doi: 10.1016/j.ympev.2006.04.021 CrossRefGoogle Scholar
  27. Mayer G (2006) Origin and differentiation of nephridia in the Onychophora provide no support for the Articulata. Zoomorphology 125:1–12. doi: 10.1007/s00435-005-0006-5 CrossRefGoogle Scholar
  28. Mayer G, Koch M (2005) Ultrastructure and fate of the nephridial anlagen in the antennal segment of Epiperipatus biolleyi (Onychophora, Peripatidae)—evidence for the onychophoran antennae being modified legs. Arthropod Struct Dev 34:471–480. doi: 10.1016/j.asd.2005.03.004 CrossRefGoogle Scholar
  29. Mayer G, Ruhberg H, Bartolomaeus T (2004) When an epithelium ceases to exist—an ultrastructural study on the fate of the embryonic coelom in Epiperipatus biolleyi (Onychophora, Peripatidae). Acta Zool 85:163–170. doi: 10.1111/j.0001-7272.2004.00166.x CrossRefGoogle Scholar
  30. Mayer G, Ruhberg H, Bartolomaeus T (2005) Ultrastructure of mesoderm in embryos of Opisthopatus roseus (Onychophora, Peripathopsidae): revision of the “long germ band” hypothesis for Opisthopatus. J Morphol 263:60–70. doi: 10.1002/jmor.10289 PubMedCrossRefGoogle Scholar
  31. Nassonow HB (1887) Balanus and Artemia. Tr Lab Zool Muz Moskovskago Univ 3:15–86 (in Russian)Google Scholar
  32. Philippe H, Lartillot N, Brinkmann H (2005) Multigene analyses of bilaterian animals corroborate the monophyly of Ecdysozoa, Lophotrochozoa, and Protostomia. Mol Biol Evol 22(5):1246–1253. doi: 10.1093/molbev/msi111 PubMedCrossRefGoogle Scholar
  33. Podsiadlowski L, Braband A, Mayer G (2008) The complete mitochondrial genome of the onychophoran Epiperipatus biolleyi reveals a unique transfer RNA set and provides further support for the Ecdysozoa hypothesis. Mol Biol Evol 25(1):42–51. doi: 10.1093/molbev/msm223 PubMedCrossRefGoogle Scholar
  34. Ruppert EE (1991) Introduction of the aschelminth phyla. A consideration of mesoderm, body cavities and cuticle. In: Harrison FW, Ruppert EE (eds) Microscopic anatomy of Invertebrates. Wiley-Liss Inc., New York, pp 1–17Google Scholar
  35. Ruppert EE, Smith PR (1988) The functional organization of filtration nephridia. Biol Rev Camb Philos Soc 63:231–258. doi: 10.1111/j.1469-185X.1988.tb00631.x CrossRefGoogle Scholar
  36. Salvini-Plawen L von, Bartolomaeus T (1995) Mollusca—Mesenchymata with a coelom. In: Lanzavecchia G, Valvassori R, Candia Carnevali MD (eds) Body cavities: function and phylogeny. Selected symposia and monographs UZI 8. Mucchi, Modena, pp 75–92Google Scholar
  37. Schmidt-Rhaesa A (2007) The evolution of organ systems. Oxford University Press, OxfordCrossRefGoogle Scholar
  38. Scholtz G (2002) The Articulata hypothesis—or what is a segment? Org Divers Evol 2:197–215. doi: 10.1078/1439-6092-00046 CrossRefGoogle Scholar
  39. Scholtz G (2003) Is the taxon Articulata obsolete? Arguments in favour of a close relationship between annelids and arthropods. In: Legakis A, Sfenthourakis S, Polymeni R, Thessalou-Legaki M (eds) The new Panorama of animal evolution. Proceedings of the 18th inernational congress of zoology. Pensoft Publishers, Sofia, pp 489–501Google Scholar
  40. Schwalm FE (1997) Arthropods: the insects. In: Gilbert SF, Raunio AM (eds) Embryology: constructing the organism. Sinauer Ass, Sunderland, pp 259–278Google Scholar
  41. Seifert G (1979) Considerations about the evolution of excretory organs in terrestrial arthropods. In: Camatini M (ed) Myriapod biology. Academic Press, London, pp 353–372Google Scholar
  42. Seifert G (1995) Entomologisches Praktikum, 3rd edn. Thieme, StuttgartGoogle Scholar
  43. Telford MJ, Bourlat SJ, Economou A, Papillon D, Rota-Stabelli O (2008) The evolution of the Ecdysozoa. Philos Trans R Soc B 363:1529–1537. doi: 10.1098/rstb.2007.2243 CrossRefGoogle Scholar
  44. Tiegs OW (1947) The development and affinities of the Pauropoda, based on a study of Pauropus silvaticus. Q J Microsc Sci 88:165–267 (Part I), 275–336 (Part II)Google Scholar
  45. Tyson GE (1968) The fine structure of the maxillary gland of the brine shrimp, Artemia salina: the end-sac. Z Zellforsch 86:129–138. doi: 10.1007/BF00340363 PubMedCrossRefGoogle Scholar
  46. Warren HS (1938) The segmental excretory glands of Artemia salina Linn., var. principalis Simon. J Morphol 62:263–289. doi: 10.1002/jmor.1050620206 CrossRefGoogle Scholar
  47. Weisz PB (1947) The histological pattern of metameric development in Artemia salina. J Morphol 81:45–89. doi: 10.1002/jmor.1050810103 CrossRefGoogle Scholar
  48. Weygoldt P (1958) Die Embryonalentwicklung des Amphipoden Gammarus pulex pulex (L.). Zool Jb Anat 77(1):51–110Google Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Thomas Bartolomaeus
    • 1
    Email author
  • Björn Quast
    • 1
  • Markus Koch
    • 1
  1. 1.Systematik und Evolution der TiereFreie Universität BerlinBerlinGermany

Personalised recommendations