, 98:889 | Cite as

Sperm carriers in Silurian sea scorpions

  • Carsten KamenzEmail author
  • Andreas Staude
  • Jason A. Dunlop
Original Paper


Invasion of the land by arachnids required adaptations of numerous organs, such as gills evolving into lungs, as well as mechanisms facilitating sperm transfer in a terrestrial environment. Many modern arachnids use spermatophores for this purpose, i.e. sperm transmitters detached from the body. Exceptionally preserved Silurian (423 Ma) fossils of Eurypterus tetragonophthalmus Fischer, 1839 (Chelicerata: Eurypterida) preserve so-called ‘horn organs’ which we here demonstrate as being equivalent to the spermatophore-producing parts of the genital tract in certain modern arachnids. This clarifies a long-running debate about sexing eurypterids based on the shape of the median abdominal (or genital) appendage. To our knowledge this is also the oldest direct evidence for spermatophore-mediated sperm transfer in the fossil record and suggests that eurypterids had evolved mating techniques using spermatophores as early as the Silurian, a valuable prerequisite for life on land. Spermatophores are absent in sea spiders (Pycnogonida) and horseshoe crabs (Xiphosura); thus the shared presence of sclerotized sperm-transfer devices in eurypterids and arachnids is a novel character, newly elucidated here, which offers explicit support for (Eurypterida + Arachnida). For this clade the name Sclerophorata n. nov. is proposed. Arachnida can be further defined by fusion of the originally paired genital opening.


Fossil Silurian Eurypterida Arachnida Spermatophore Evolution 



We thank Jeremy Huff, Simon Braddy, James Lamsdell, Lorenzo Prendini, Jonas Hagström, Stefan Bengtson, Jan Bergström, Estefania Rodriguez, Matthew Frenkel and Rebecca Rudolph for valuable discussion, access to material and technical support, and the reviewers for helpful comments. CK was supported by the Kalbfleisch fellowship and Gerstner scholarship of the AMNH.


  1. Alberti G, Gegner A, Witalinski W (2000) Fine structure of the spermatophore and spermatozoa in inseminated females of Pergamasus mites (Acari: Gamasida: Pergamasidae). J Morph 245:1–18PubMedCrossRefGoogle Scholar
  2. Alexander AJ (1957) Courtship and mating in the scorpion, Opistophthalmus latimanus. Proc Zool Soc Lond 128:529–544Google Scholar
  3. Alexander AJ (1959) Courtship and mating in the buthid scorpion. Proc Zool Soc Lond 133:145–169Google Scholar
  4. Braddy SJ (2001) Eurypterid palaeoecology: palaeobiological, ichnological and comparative evidence for a ‘mass–moult–mate’ hypothesis. Palaeogeog Paleoclim Palaeoecol 172:115–132CrossRefGoogle Scholar
  5. Braddy SJ, Dunlop JA (1997) The functional morphology of mating in the Silurian eurypterid Baltoeurypterus tetragonophthalmus (Fischer, 1839). Zool J Linn Soc 121:435–461CrossRefGoogle Scholar
  6. Briggs DEG, Dalingwater JE, Selden PA (1991) Biomechanics of locomotion in fossil arthropods. In: Rayner JMV, Wooton RJ (eds) Biomechanics and evolution. Cambridge University Press, Cambridge, pp 37–56Google Scholar
  7. Cloudsley-Thompson JL (1988) Evolution and adaptation of terrestrial arthropods. Springer-Verlag, BerlinCrossRefGoogle Scholar
  8. Dubinin VB (1962) Subphylum Chelicerophora. Chelicerate arthropods (trans. 1991). In: Rohdendorf BB (ed) Arthropoda, Tracheata, Chelicerata. Fundamentals of paleontology, vol 9. Smithsonian, Washington, pp 577–814Google Scholar
  9. Dunlop JA (2010) Geological history and phylogeny of Chelicerata. Arth Struc Develop 39:124–142CrossRefGoogle Scholar
  10. Franke OF (1979) Spermatophores of some North American scorpions (Arachnida, Scorpiones). J Arachnol 7:19–32Google Scholar
  11. Gaskell WH (1908) The origin of vertebrates. Longmans, LondonGoogle Scholar
  12. Holm G (1898) Über die Organisation des Eurypterus fischeri Eichw. Mem Acad Imp Sci St-Pétersbourg 8:1–57Google Scholar
  13. Jacob A, Gantenbein I, Braunwalder ME, Nentwig W, Kropf C (2004) Morphology and function of male genitalia (spermatophores) in Euscorpius italicus (Euscorpiidae, Scorpiones): complex spermatophore structures enable safe sperm transfer. J Morphol 260:72–84PubMedCrossRefGoogle Scholar
  14. Jeram AJ (1990) Book-lungs in a Lower Carboniferous scorpion. Nature 343:360–361CrossRefGoogle Scholar
  15. Kamenz C, Prendini L (2008) An atlas of book lung fine structure in the order Scorpiones (Arachnida). Bull Am Mus Nat Hist 316:359ppGoogle Scholar
  16. Kamenz C, Dunlop JA, Scholtz G, Kerp H, Hass H (2008) Microanatomy of early Devonian book lungs. Biol Lett 4:212–215PubMedCrossRefGoogle Scholar
  17. Karaman I (2005) Evidence of spermatophores in Cyphophthalmi (Arachnida, Opiliones). Rev Suisse Zool 112:3–11Google Scholar
  18. Kraus O (1976) Zur phylogenetischen Stellung und Evolution der Chelicerata. Entomol Germ 3:1–12Google Scholar
  19. Lamsdell JC, Braddy SJ (2009) Cope’s rule and Romer’s theory: patterns of diversity and gigantism in eurypterids and Palaeozoic vertebrates. Biol Lett 6:265–269PubMedCrossRefGoogle Scholar
  20. Legg G (1971) The comparative and functional morphology of the genitalia of the British Pseudoscorpiones. Thesis, University of ManchesterGoogle Scholar
  21. Legg G (1973) Spermatophore formation in the pseudoscorpion Chthonius ischnocheles (Chthoniidae). J Zool Lond 170:367–394CrossRefGoogle Scholar
  22. Manning PL, Dunlop JA (1995) The respiratory organs of eurypterids. Palaeontology 38:287–297Google Scholar
  23. Parker GA (1984) Sperm competition and the evolution of animal mating strategies. In: Smith RL (ed) Sperm competition and the evolution of animal mating systems. Academic, Orlando, pp 1–60Google Scholar
  24. Peretti AV, Battan-Horenstein M (2003) Comparative analysis of the male reproductive system in Bothriuridae scorpions: structures associated with the paraxial organs and the presence of sperm packages (Chelicerata, Scorpiones). Zool Anz 242:21–31CrossRefGoogle Scholar
  25. Proctor HC (1998) Indirect sperm transfer in arthropods: behavioral and evolutionary trends. Ann Rev Entomol 43:153–174CrossRefGoogle Scholar
  26. Schaller F (1971) Indirect sperm transfer by soil arthropods. Ann Rev Entomol 16:407–446CrossRefGoogle Scholar
  27. Schaller F (1979) Significance of sperm transfer and formation of spermatophores in arthropod phylogeny. In: Gupta AP (ed) Arthropod phylogeny. Van Nostrand Reinhold, New York, pp 587–608Google Scholar
  28. Selden PA (1981) Functional morphology of the prosoma of Baltoeurypterus tetragonophthalmus (Fischer) (Chelicerata: Eurypterida). Trans R Soc Edinburgh, Earth Sci 72:9–48Google Scholar
  29. Selden PA, Jeram AJ (1989) Palaeophysiology of terrestrialisation in the Chelicerata. Trans R Soc Edinburgh, Earth Sci 80:303–310Google Scholar
  30. Shultz JW (2007) A phylogenetic analysis of the arachnid orders based on morphological characters. Zool J Linn Soc 150:221–265CrossRefGoogle Scholar
  31. Størmer L (1944) On the relationships and phylogeny of fossil and recent Arachnomorpha. Skrifter utgitt av det Norske Videnskaps-Akademi. Mat. Naturv. Klasse 5: pp 158Google Scholar
  32. Størmer L, Kjellesvig-Waering EN (1969) Sexual dimorphism in eurypterids. In: Westermann GEG (ed) Sexual dimorphism in fossil Metazoa and taxonomic implications. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart, pp 201–214Google Scholar
  33. Tetlie OE (2006) Two new Silurian species of Eurypterus (Chelicerata: Eurypterida) from Norway and Canada and the phylogeny of the genus. J Syst Palaeont 4:397–412CrossRefGoogle Scholar
  34. Tetlie OE (2007) Distribution and dispersal history of Eurypterida (Chelicerata). Palaeogeog Paleoclim Palaeoecol 252:557–574CrossRefGoogle Scholar
  35. Thomas RH, Zeh DW (1984) Sperm transfer and utilization strategies in arachnids: ecological and morphological constraints. In: Smith RL (ed) Sperm competition and the evolution of animal mating systems. Academic, Orlando, pp 179–221Google Scholar
  36. Vrech DE, Peretti AV, Mattoni CI (2011) Sperm package morphology in the scorpions and its relation to phylogeny. Zool J Linn Soc 161:463–483CrossRefGoogle Scholar
  37. Warren E (1939) The genital system of Hypoctonus formosus (Butler) (Thelyphonidae). Ann Natal Mus 9:307–344Google Scholar
  38. Weygoldt P (1970) Vergleichende Untersuchungen zur Fortpflanzungsbiologie der Pseudoscorpione II. Zool Syst Evolutionsforsch 8:241–259CrossRefGoogle Scholar
  39. Weygoldt P (1972) Spermatophorenbau und Samenübertragung bei Uropygen (Mastigoproctus brasilianus C. L. Koch) und Amblypygen (Charinus brasilianus Weygoldt und Admetus pumilio C. L. Koch) (Chelicerata, Arachnida). Z Morph Tiere 71:23–51CrossRefGoogle Scholar
  40. Weygoldt P (1978) Paarungsverhalten und Spermatophorenmorphologie bei Geißelskorpionen: Thelyphonellus amazonicus Butler und Typopeltis crucifer Pocock (Arachnida, Uropygi). Zoomorphologie 89:145–156CrossRefGoogle Scholar
  41. Weygoldt P (1988) Sperm transfer and spermatophore morphology in the whip scorpion Thelyphonus linganus (Arachnida: Uropygi: Thelyphonidae). J Zool Lond 215:189–196CrossRefGoogle Scholar
  42. Weygoldt P (1990) Arthropoda-Chelicerata: Sperm transfer. In: Adiyodi KG, Adiyodi RG (eds) Reproductive biology of invertebrates, vol 4. Part B. Oxford, New Delhi, pp 77–119Google Scholar
  43. Weygoldt P, Paulus HF (1979) Untersuchungen zur Morphologie, Taxonomie und Phylogenie der Chelicerata. Z Zool Systematik Evolut-forsch 17(85–116):177–200Google Scholar
  44. Weygoldt P, Weisemann A, Weisemann K (1972) Morphologisch-histologische Untersuchungen an den Geschlechtsorganen der Amblypygi unter besonderer Berücksichtigung von Tarantula marginemaculata C. L. Koch (Arachnida). Z Morph Tiere 73:209–247CrossRefGoogle Scholar
  45. Wills LJ (1964) The ventral anatomy of the Upper Carboniferous eurypterid Anthraconectes Meek and Worthen. Palaeontology 7:474–507Google Scholar
  46. Wills LJ (1965) A supplement to Gerhard Holm’s ‘Über die Organisation des Eurypterus fischeri Eichw’ with special reference to the organs of sight, respiration and reproduction. Ark Zool 18:93–145Google Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Carsten Kamenz
    • 1
    Email author
  • Andreas Staude
    • 2
  • Jason A. Dunlop
    • 3
  1. 1.American Museum of Natural HistoryNew YorkUSA
  2. 2.Federal Institute for Materials Research and Testing (BAM)BerlinGermany
  3. 3.Museum für Naturkunde, Leibniz Institute for Research on Evolution and BiodiversityHumboldt University BerlinBerlinGermany

Personalised recommendations