Skip to main content
Log in

The ontogeny of the 300 million year old xiphosuran Euproops danae (Euchelicerata) and implications for resolving the Euproops species complex

  • Original Article
  • Published:
Development Genes and Evolution Aims and scope Submit manuscript

Abstract

Xiphosurans have often been considered as archaic appearing cheliceratan arthropods, with a rich fossil record. We describe here parts of the post-embryonic ontogeny of the 300 million year old xiphosuran Euproops danae (Xiphosura sensu stricto, Euchelicerata), from the Mazon Creek Lagerstätte (Upper Carboniferous), USA. Recently, the ontogeny of a closely related species, Euproops sp. from the Upper Carboniferous Piesberg quarry, Osnabrück, Germany (informally called ‘Piesproops’), has been reconstructed. This analysis has drawn characters into question that were used to differentiate E. danae from another species occurring at the same time, Euproops rotundatus from the British Middle Coal Measures. More precisely, early post-embryonic stages of Piesproops resemble E. danae; later stages resemble E. rotundatus. Based on this earlier study, the here-described reinvestigation of E. danae has been performed as the ontogenetic sequence itself may yield more reliable characters for differentiating species of Euproops. We could identify eight different growth stages for E. danae. This ontogenetic sequence shows a comparable growth to that of Piesproops, but differs markedly in the development of the opisthosomal flange. This character may serve as a basis for reliably differentiating these species. Additionally, analysing the ontogeny of further species may offer the basis for identifying heterochronic shifts in the evolution of xiphosurans.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Anderson LI (1994) Xiphosurans from the Westphalian D of the Radstock Basin, Somerset Coalfield, the South Wales Coalfield and Mazon Creek, Illinois. Proc Geol Assoc 105(4):265–275. https://doi.org/10.1016/S0016-7878(08)80179-4

    Article  Google Scholar 

  • Anderson LI, Selden PA (1997) Opisthosomal fusion and phylogeny of Palaeozoic Xiphosura. Lethaia 30:19–31

    Article  Google Scholar 

  • Anger K (2001) The biology of decapod crustacean larvae. Crust Iss 14:1–420

    Google Scholar 

  • Bellinger RG, Pienkowski RL (1987) Developmental polymorphism in the red-legged grasshopper, Melanoplus femurrubrum (DeGeer) (Orthoptera: Acrididae). Environ Entomol 16(1):120–125. https://doi.org/10.1093/ee/16.1.120

    Article  Google Scholar 

  • Block W, Baust JG, Franks F, Johnston IA, Bale J (1990) Cold tolerance of insects and other arthropods [and discussion]. Phil T Roy Soc B 326(1237):613–633. https://doi.org/10.1098/rstb.1990.0035

    Article  Google Scholar 

  • Brauckmann C (1982) Der Schwertschwanz Euproops (Xiphosurida, Limulina, Euproopacea) aus dem Ober-Karbon des Piesbergs bei Osnabrück. Osnabrücker Naturwiss Mitt 9:17–26

    Google Scholar 

  • Budd GE (1999) A nectaspid arthropod from the Early Cambrian Sirius Passet Fauna, with a description of retrodeformation based on functional morphology. Palaeontology 42(1):99–122. https://doi.org/10.1111/1475-4983.00064

    Article  Google Scholar 

  • Carmichael RH, Rutecki D, Valiela I (2003) Abundance and population structure of the Atlantic horseshoe crab Limulus polyphemus in Pleasant Bay, Cape Cod. Mar Ecol Prog Ser 246:225–239

    Article  Google Scholar 

  • Chen J, Waloszek D, Maas A (2004) A new ‘great-appendage’ arthropod from the Lower Cambrian of China and homology of chelicerate chelicerae and raptorial antero-ventral appendages. Lethaia 15:3–20

    Google Scholar 

  • Chiu HMC, Morton B (2001) Growth and allometry of two horseshoe crab species, Tachypleus tridentatus and Carcinoscorpius rotundicauda (Xiphosura), in Hong Kong. Asian Mar Biol 18:129–141

    Google Scholar 

  • Dunlop JA, Penney D, Tetlie OE, Anderson LI (2008) How many species of fossil arachnids are there? J Arachnol 36(2):267–272. https://doi.org/10.1636/CH07-89.1

    Article  Google Scholar 

  • Feist R, Lerosey-Aubril R, Johnson R (2010) Coaptative devices, enrollment, and life habits in Paralejurus, a particular case in scutelluid trilobites. Palaeobio Palaeoenv 90(2):125–137. https://doi.org/10.1007/s12549-010-0025-1

    Article  Google Scholar 

  • Fields PG (1992) The control of stored-product insects and mites with extreme temperatures. J Stored Prod Res 28(2):89–118. https://doi.org/10.1016/0022-474X(92)90018-L

    Article  Google Scholar 

  • Fisher DC (1977) Functional significance of spines in the Pennsylvanian horseshoe crab Euproops danae. Paleobiology 3(02):175–195. https://doi.org/10.1017/S009483730000525X

    Article  Google Scholar 

  • Fisher DC (1979) Evidence for subaerial activity of Euproops danae (Merostomata, Xiphosurida). In: Nitecki MH (ed) Mazon Creek fossils. Academic Press, New York, pp 379–447. https://doi.org/10.1016/B978-0-12-519650-5.50022-9

    Chapter  Google Scholar 

  • Haug C, Haug JT (2014) Defensive enrolment in mantis shrimp larvae. Contr Zool 83(3):185–194

    Google Scholar 

  • Haug JT, Haug C, Kutschera V, Mayer G, Maas A, Liebau S, Castellani C, Wolfram U, Clarkson ENK, Waloszek D (2011) Autofluorescence imaging, an excellent tool for comparative morphology. J Microsc 244(3):259–272. https://doi.org/10.1111/j.1365-2818.2011.03534.x

    Article  PubMed  Google Scholar 

  • Haug C, Van Roy P, Leipner A, Funch P, Rudkin DM, Schöllmann L, Haug JT (2012a) A holomorph approach to xiphosuran evolution—a case study on the ontogeny of Euproops. Dev Genes Evol 222(5):253–268. https://doi.org/10.1007/s00427-012-0407-7

    Article  PubMed  Google Scholar 

  • Haug JT, Mayer G, Haug C, Briggs DEG (2012b) A carboniferous non-onychophoran lobopodian reveals long-term survival of a Cambrian morphotype. Curr Biol 22(18):1673–1675. https://doi.org/10.1016/j.cub.2012.06.066

    Article  CAS  PubMed  Google Scholar 

  • Haug C, Nyborg T, Vega FJ (2013) An exceptionally preserved upogebiid (Decapoda: Reptantia) from the Eocene of California. Bol Soc Geol Mexic 65:235–248

    Google Scholar 

  • Hauschke N, Wilde V (2004) Palaeogene limulids (Xiphosura) from Saxony-Anhalt (Germany) – systematics and palaeobiogeography. Hallesch Jb Geowiss B 18:161–168

    Google Scholar 

  • Hennig W (1966) Phylogenetic systematics. University of Illinois Press, Urbana

    Google Scholar 

  • Hu M, Kwan BKY, Wang Y, Cheung SG, Shin PKS (2015) Population structure and growth of juvenile horseshoe crabs Tachypleus tridentatus and Carcinoscorpius rotundicauda (Xiphosura) in southern China. In: Carmichael R, Botton M, Shin P, Cheung S (eds) Changing global perspectives on horseshoe crab biology, conservation and management. Springer International Publishing, Cham, pp 167–180. https://doi.org/10.1007/978-3-319-19542-1_8

    Chapter  Google Scholar 

  • Lamsdell JC (2013) Revised systematics of Palaeozoic ‘horseshoe crabs’ and the myth of monophyletic Xiphosura. Zool J Linn Soc Lond 167(1):1–27. https://doi.org/10.1111/j.1096-3642.2012.00874.x

  • Lamsdell JC (2016) Horseshoe crab phylogeny and independent colonizations of fresh water: ecological invasion as a driver for morphological innovation. Palaeontology 59(2):181–194. https://doi.org/10.1111/pala.12220

    Article  Google Scholar 

  • Lamsdell JC, McKenzie SC (2015) Tachypleus syriacus (Woodward)—a sexually dimorphic Cretaceous crown limulid reveals underestimated horseshoe crab divergence times. Org Divers Evol 15:681–693

  • Loveland RE, Botton ML (1992) Size dimorphism and the mating system in horseshoe crabs, Limulus polyphemus L. Animal Behav 44(5):907–916. https://doi.org/10.1016/S0003-3472(05)80586-X

    Article  Google Scholar 

  • Müller KJ, Walossek D (1987) Morphology, ontogeny, and life habit of Agnostus pisiformis from the Upper Cambrian of Sweden. Fossils Strata 19:1–124

    Google Scholar 

  • Racheboeuf PR, Vannier J, Anderson LI (2002) A new three-dimensionally preserved xiphosuran chelicerate from the Montceau-Les-Mines Lagerstätte (Carboniferous, France). Palaeontology 45(1):125–147

    Article  Google Scholar 

  • Reisinger PWM, Tutter I, Welsch U (1991) Fine structure of the gills of the horseshoe crabs Limulus polyphemus and Tachypleus tridentatus and of the book lungs of the spider Eurypelma californicum. Zool Jahrb Anat 121:331–357

    Google Scholar 

  • Remy W (1975) The floral changes at the Carboniferous-Permian boundary in Europe and North America. In: Barlow JA (ed) The Age of the Dunkard - Proceedings of the First I. C. White Memorial Symposium, West Virginia Geological and Economic Survey, Morgantown, pp 305–352

  • Rudolf NR, Haug C, Haug JT (2016) Functional morphology of giant mole crab larvae: a possible case of defensive enrollment. Zool Lett 2:Art 17

    Article  Google Scholar 

  • Schultka S (2000) Zur Palökologie der Euproopiden im Nordwestdeutschen Oberkarbon. Mitt Mus Naturwiss Berl Geowiss R 3:87–98

    Google Scholar 

  • Shuster CN Jr, Sekiguchi K (2003) Growing up takes about ten years and eighteen stages. In: Shuster CN Jr, Barlow RB, Brockmann HJ (eds) The American Horseshoe Crab. Harvard University Press, Cambridge, pp 103–132

    Google Scholar 

  • Waterman TH (1954) Relative growth and the compound eye in Xiphosura. J Morph 95(1):125–158. https://doi.org/10.1002/jmor.1050950107

    Article  Google Scholar 

  • Waterston CD (1985) Chelicerata from the Dinantian of Foulden, Berwickshire, Scotland. Trans R Soc Edinb Earth Sci 76(01):25–33. https://doi.org/10.1017/S0263593300010269

    Article  Google Scholar 

  • Williams RB (1980) Comment on report of the committee of typification of species of Protozoa. Bull Zool Nomencl 37:137–140. https://doi.org/10.5962/bhl.part.5156

    Article  Google Scholar 

  • Williams RB (1986) Hapantotypes: a possible solution to some problems of parasite nomenclature. Parasitol Today 2(11):314–316. https://doi.org/10.1016/0169-4758(86)90128-6

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank Susan Butts, Jessica Utrup, Eric Lazo-Wasem, Daniel Drew and Lourdes Rojas for their help in the collections of the Yale Peabody Museum, New Haven, CT, USA. Derek Briggs, Yale University, Steffen Harzsch, University of Greifswald, and J. Matthias Starck, LMU Munich, are thanked for discussions and support. We are very grateful to Joachim T. Haug, LMU Munich, for continuous help with the imaging and fruitful discussions during the entire study. CH was kindly supported by a Bavarian Equal Opportunities scholarship of the LMU and is currently funded by the German Research Foundation (DFG HA 7066/3-1).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Carolin Haug.

Additional information

Communicated by Nico Posnien

Electronic supplementary material

Supplementary Fig. 1

Non-stereo versions of Fig. 1, otherwise identical with it. (GIF 131 kb)

High Resolution Image (TIFF 6848 kb)

Supplementary Fig. 2

Non-stereo versions of Fig. 2, otherwise identical with it. (GIF 418 kb)

High Resolution Image (TIFF 19600 kb)

Supplementary Fig. 3

Non-stereo versions of Fig. 3, otherwise identical with it. (GIF 463 kb)

High Resolution Image (TIFF 19438 kb)

Supplementary Fig. 4

Non-stereo versions of Fig. 5, otherwise identical with it. (GIF 313 kb)

High Resolution Image (TIFF 11423 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Haug, C., Rötzer, M.A.I.N. The ontogeny of the 300 million year old xiphosuran Euproops danae (Euchelicerata) and implications for resolving the Euproops species complex. Dev Genes Evol 228, 63–74 (2018). https://doi.org/10.1007/s00427-018-0604-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00427-018-0604-0

Keywords

Navigation