Acute vision in the giant Cambrian predator Anomalocaris and the origin of compound eyes

Journal name:
Nature
Volume:
480,
Pages:
237–240
Date published:
DOI:
doi:10.1038/nature10689
Received
Accepted
Published online

Until recently1, intricate details of the optical design of non-biomineralized arthropod eyes remained elusive in Cambrian Burgess-Shale-type deposits, despite exceptional preservation of soft-part anatomy in such Konservat-Lagerstätten2, 3. The structure and development of ommatidia in arthropod compound eyes support a single origin some time before the latest common ancestor of crown-group arthropods4, but the appearance of compound eyes in the arthropod stem group has been poorly constrained in the absence of adequate fossils. Here we report 2–3-cm paired eyes from the early Cambrian (approximately 515 million years old) Emu Bay Shale of South Australia, assigned to the Cambrian apex predator Anomalocaris. Their preserved visual surfaces are composed of at least 16,000 hexagonally packed ommatidial lenses (in a single eye), rivalling the most acute compound eyes in modern arthropods. The specimens show two distinct taphonomic modes, preserved as iron oxide (after pyrite) and calcium phosphate, demonstrating that disparate styles of early diagenetic mineralization can replicate the same type of extracellular tissue (that is, cuticle) within a single Burgess-Shale-type deposit. These fossils also provide compelling evidence for the arthropod affinities of anomalocaridids, push the origin of compound eyes deeper down the arthropod stem lineage, and indicate that the compound eye evolved before such features as a hardened exoskeleton. The inferred acuity of the anomalocaridid eye is consistent with other evidence that these animals were highly mobile visual predators in the water column5, 6. The existence of large, macrophagous nektonic predators possessing sharp vision—such as Anomalocaris—within the early Cambrian ecosystem probably helped to accelerate the escalatory ‘arms race’ that began over half a billion years ago7, 8.

At a glance

Figures

  1. Anomalocaris eyes from the Emu Bay Shale.
    Figure 1: Anomalocaris eyes from the Emu Bay Shale.

    ad, Eye pair, SAM P45920a, level 10.4m. a, b, Overview and camera lucida drawing. Scale bars, 5mm. Grey fill in b represents visual surface, the proximal part in the upper eye extrapolated from the lower eye. c, Detail of ommatidial lenses located by horizontal white box in a. Scale bar, 1mm. d, More complete eye, showing transition between visual surface and eye stalk (white arrows). Scale bar, 2mm. e, Detail of ommatidial lenses in counterpart SAM P45920b. Scale bar, 0.3mm. es, eye stalk; I.c., Isoxys communis; us, undetermined structure; vs, visual surface. Tilted white box in a represents area analysed using SEM-EDS, with elemental maps shown in Fig. 2a.

  2. SEM-EDS analyses of Anomalocaris eyes.
    Figure 2: SEM-EDS analyses of Anomalocaris eyes.

    a, SAM P45920a. Scale bar, 1mm; see Fig. 1a for area analysed. b, SAM P46330b. Scale bar, 0.3mm; see Supplementary Fig. 1e for area analysed. Accelerating voltage of 20kV. Each map depicts the relative abundance of each element, with brighter colours indicating greater abundance. SEM, backscattered electron image of area analysed. Al, aluminium (green); Ca, calcium (cyan); Fe, iron (red); O, oxygen (dark blue); P, phosphorus (purple); S, sulphur (yellow); Si, silicon (pink). The visual surface of SAM P45920a in a contains elevated amounts of iron, oxygen and sulphur, indicative of limonite after pyrite; the matrix (at left of each image) shows high levels of silicon and aluminium, reflecting muscovite and aluminosilicate clay minerals. The lenses of SAM P46330b in b contain elevated amounts of calcium and phosphorus, indicative of calcium phosphate.

  3. The early evolution of compound eyes, and the position of anomalocaridids (Radiodonta), in the arthropod stem group.
    Figure 3: The early evolution of compound eyes, and the position of anomalocaridids (Radiodonta), in the arthropod stem group.

    Numbers refer to the inclusiveness of the monophyletic group that can be confidently inferred to possess compound eyes: (1) based on extant taxa alone; (2) based on discovery of Schinderhannes19; and (3) based on new data herein. Phylogeny after ref. 19.

References

  1. Lee, M. S. Y. et al. Modern optics in exceptionally preserved eyes of Early Cambrian arthropods from Australia. Nature 474, 631634 (2011)
  2. Briggs, D. E. G., Erwin, D. H. & Collier, F. J. The Fossils of the Burgess Shale (Smithsonian Institution, 1994)
  3. Hou, X.-G. et al. The Cambrian Fossils of Chengjiang, China: The Flowering of Early Animal Life (Blackwell, 2004)
  4. Harzsch, S. & Hafner, G. Evolution of eye development in arthropods: phylogenetic aspects. Arthropod Struct. Dev. 35, 319340 (2006)
  5. Briggs, D. E. G. Giant predators from the Cambrian of China. Science 264, 12831284 (1994)
  6. Vannier, J. & Chen, J.-. Early Cambrian food chain: new evidence from fossil aggregates in the Maotianshan Shale Biota, SW China. Palaios 20, 326 (2005)
  7. Marshall, C. R. Explaining the Cambrian “explosion” of animals. Annu. Rev. Earth Planet. Sci. 34, 355384 (2006)
  8. Bush, A. M. & Bambach, R. K. Paleoecologic megatrends in marine Metazoa. Annu. Rev. Earth Planet. Sci. 39, 241269 (2011)
  9. Van Roy, P. & Briggs, D. E. G. A giant Ordovician anomalocaridid. Nature 473, 510513 (2011)
  10. Whittington, H. B. & Briggs, D. E. G. The largest Cambrian animal, Anomalocaris, Burgess Shale, British Columbia. Phil. Trans. R. Soc. Lond. B 309, 569609 (1985)
  11. Butterfield, N. J. Leanchoilia guts and the interpretation of three-dimensional structures in Burgess Shale-type fossils. Paleobiology 28, 155171 (2002)
  12. Nedin, C. Anomalocaris predation on nonmineralized and mineralized trilobites. Geology 27, 987990 (1999)
  13. Chen, J.-Y., Ramsköld, L. & Zhou, G.-Q. Evidence for monophyly and arthropod affinity of Cambrian giant predators. Science 264, 13041308 (1994)
  14. Bergström, J. in Darwin’s Heritage Today. Proceedings of the Darwin 200 International Conference 29–42 (Higher Education, 2010)
  15. Hou, X.-G., Bergström, J. & Ahlberg, P. Anomalocaris and other large animals in the Lower Cambrian Chengjiang fauna of southwest China. GFF 117, 163183 (1995)
  16. Usami, Y. Theoretical study on the body form and swimming pattern of Anomalocaris based on hydrodynamic simulation. J. Theor. Biol. 238, 1117 (2006)
  17. Collins, D. The “evolution” of Anomalocaris and its classification in the arthropod class Dinocarida (nov.) and order Radiodonta (nov.). J. Paleontol. 70, 280293 (1996)
  18. Daley, A. C., Budd, G. E., Caron, J.-B., Edgecombe, G. D. & Collins, D. The Burgess Shale anomalocaridid Hurdia and its significance for early euarthropod evolution. Science 323, 15971600 (2009)
  19. Kühl, G., Briggs, D. E. G. & Rust, J. A great-appendage arthropod with a radial mouth from the Lower Devonian Hunsrück Slate, Germany. Science 323, 771773 (2009)
  20. Ma, X.-Y., Hou, X.-G. & Bergström, J. Morphology of Luolishania longicruris (Lower Cambrian, Chengjiang Lagerstätte, SW China) and the phylogenetic relationships within lobopodians. Arthropod Struct. Dev. 38, 271291 (2009)
  21. Gehling, J. G., Jago, J. B., Paterson, J. R., García-Bellido, D. C. & Edgecombe, G. D. The geological context of the lower Cambrian (series 2) Emu Bay Shale Lagerstätte and adjacent stratigraphic units, Kangaroo Island, South Australia. Aust. J. Earth Sci. 58, 243257 (2011)
  22. McKirdy, D. M. et al. Paleoredox status and thermal alteration of the lower Cambrian (Series 2) Emu Bay Shale Lagerstätte, South Australia. Aust. J. Earth Sci. 58, 259272 (2011)
  23. Gabbott, S. E., Hou, X.-G., Norry, M. J. & Siveter, D. J. Preservation of Early Cambrian animals of the Chengjiang biota. Geology 32, 901904 (2004)
  24. Gaines, R. R., Briggs, D. E. G. & Zhao, Y. Cambrian Burgess Shale-type deposits share a common mode of fossilization. Geology 36, 755758 (2008)
  25. Nedin, C. The Emu Bay Shale, a Lower Cambrian fossil Lagerstätten, Kangaroo Island, South Australia. Mem. Assoc. Austral. Palaeontol. 18, 3140 (1995)
  26. Cronin, T. W. & Porter, M. L. Exceptional variation on a common theme: the evolution of crustacean compound eyes. Evol. Edu. Outreach 1, 463475 (2008)
  27. Wehner, R. in Comparative Physiology and Evolution of Vision in Invertebrates: C 287616 (Springer, 1981)
  28. Harzsch, S. Neurophylogeny: architecture of the nervous system and a fresh view on arthropod phylogeny. Integr. Comp. Biol. 46, 162194 (2006)
  29. Vannier, J., García-Bellido, D. C., Hu, S.-X. & Chen, A.-L. Arthropod visual predators in the early pelagic ecosystem: evidence from the Burgess Shale and Chengjiang biotas. Proc. R. Soc. Lond. B 276, 25672574 (2009)
  30. Hu, S.-X. et al. Diverse pelagic predators from the Chengjiang Lagerstätte and the establishment of modern-style pelagic ecosystems in the early Cambrian. Palaeogeogr. Palaeoclimatol. Palaeoecol. 254, 307316 (2007)

Download references

Author information

Affiliations

  1. Division of Earth Sciences, School of Environmental and Rural Science, University of New England, Armidale, New South Wales 2351, Australia

    • John R. Paterson
  2. Departamento de Geología Sedimentaria y Cambio Ambiental, Instituto de Geociencias (CSIC-UCM), José Antonio Novais 2, Madrid 28040, Spain

    • Diego C. García-Bellido
  3. South Australian Museum, North Terrace, Adelaide, South Australia 5000, Australia

    • Michael S. Y. Lee &
    • James B. Jago
  4. School of Earth and Environmental Sciences, University of Adelaide, South Australia 5005, Australia

    • Michael S. Y. Lee
  5. Department of Biological Sciences, Macquarie University, New South Wales 2109, Australia

    • Glenn A. Brock
  6. School of Natural and Built Environments, University of South Australia, Mawson Lakes, South Australia 5095, Australia

    • James B. Jago
  7. Department of Palaeontology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK

    • Gregory D. Edgecombe

Contributions

All authors directly contributed to excavation and interpretation of fossil specimens, analysis, and writing the manuscript. J.R.P. and D.C.G.-B. conducted the digital photography and camera lucida drawings; G.A.B. and J.R.P. conducted the SEM-EDS analyses.

Competing financial interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to:

Author details

Supplementary information

PDF files

  1. Supplementary Information (450K)

    This file contains Supplementary Methods, Supplementary Figures 1-2 with legends, Supplementary Table 1 and additional references.

Additional data