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Reconstructing predation intensity on crinoids using longitudinal and cross-sectional approaches

  • Tomasz K. Baumiller
  • Angela Stevenson
Regular Research Article
  • 11 Downloads

Abstract

Predation has been hypothesized as important to crinoid ecology, and numerous crinoid traits have been linked to predation. However, testing such hypotheses requires some assessment of predation intensity, or pressure. Although direct observations of predatory activity on crinoids are exceedingly rare in the Recent, and unobservable in the fossil record, evidence of predation exists in the form of sublethal damage, especially to their arms. Substantial data exist on the relative frequency, or prevalence, of such injuries, but estimating predation intensity in taxa with ephemeral injuries, such as crinoids, requires combining the prevalence of injuries with rates at which they heal (regenerate). An alternate, independent estimate of predation intensity involves gathering longitudinal data on the number of injuries incurred by particular individuals over a given time span. In this study, predation intensity on crinoids is explored experimentally using these two approaches. We demonstrate that for the two feather star species examined, Capillaster multiradiatus and Clarkcomanthus mirabilis, both methods produce reasonably consistent results and that predation intensity is slightly lower on the latter perhaps because it responds to tactile stimulation by crawling deeper into its perch, whereas the former shows no response.

Keywords

Regeneration rate Prevalence of injuries Feather stars 

Notes

Acknowledgements

This work would not have been possible without the dedicated efforts of Tadhg Ó Corcora in the field and Marine Conservation Philippines with logistics. The study was partly funded by the Challenger Society for Marine Sciences Stepping Stone Bursary to A. Stevenson. We appreciate the insightful comments from Charles Messing and Tatsuo Oji that helped improve this manuscript. This contribution is dedicated to the memory of Hans Hess.

References

  1. Aronson, R. B. (1987). Predation on fossil and Recent ophiuroids. Paleobiology, 13, 187–192.CrossRefGoogle Scholar
  2. Aronson, R. B. (1991). Predation, physical disturbance, and sublethal arm damage in ophiuroids: A Jurassic-Recent comparison. Marine Ecology Progress Series, 74, 91–97.CrossRefGoogle Scholar
  3. Baumiller, T. K. (2003). Experimental and biostratinomic disarticulation of crinoids: Taphonomic implications. In J.-P. Féral & B. David (Eds.), Echinoderm research 2001 (pp. 243–248). Lisse: Balkema.Google Scholar
  4. Baumiller, T. K. (2013a). Ephemeral injuries, regeneration frequencies and intensity of the injury-producing process. Marine Biology, 160, 3233–3239.  https://doi.org/10.1007/s00227-013-2302-9.CrossRefGoogle Scholar
  5. Baumiller, T. K. (2013b). Arm regeneration frequencies in Florometra serratissima (Crinoidea, Echinodermata): Impact of depth of habitat on rates of arm loss. Cahiers de Biologie Marine, 54, 571–576.Google Scholar
  6. Baumiller, T. K., & Fordyce, R. E. (2018). Rautangaroa, a new genus of feather star (Echinodermata: Crinoidea) from the Oligocene of New Zealand. Journal of Paleontology, 92(872), 882.  https://doi.org/10.1017/jpa.2018.17.CrossRefGoogle Scholar
  7. Baumiller, T. K., & Gahn, F. J. (2003). Chapter 10, predation on crinoids. In P. H. Kelley, M. Kowalewski, & T. A. Hansen (Eds.), Predator-prey interactions in the fossil record. Topics in geobiology (Vol. 20, pp. 263–278). New York: Springer.CrossRefGoogle Scholar
  8. Baumiller, T. K., & Gahn, F. J. (2004). Testing predation-driven evolution using Mid-Paleozoic crinoid arm regeneration. Science, 305, 1453–1455.CrossRefGoogle Scholar
  9. Baumiller, T. K., & Gahn, F. J. (2013). Reconstructing predation pressure on crinoids: Estimating arm-loss rates from regenerating arms. Paleobiology, 39, 40–51.CrossRefGoogle Scholar
  10. Baumiller, T. K., Mooi, R., & Messing, C. G. (2008). Urchins in the meadow: Paleobiological and evolutionary implications of cidaroid predation on crinoids. Paleobiology, 34, 22–34.CrossRefGoogle Scholar
  11. Baumiller, T. K., Salamon, M., Gorzelak, P., Mooi, R., Messing, C. G., & Gahn, F. J. (2010). Benthic predation drove early Mesozoic crinoid radiation. PNAS, 107, 5893–5896.CrossRefGoogle Scholar
  12. Brun, E. (1972). Food and feeding habits of Luidia ciliaris (Echinodermata: Asteroidea). Journal of the Marine Biological Association of the United Kingdom, 52, 225–236.CrossRefGoogle Scholar
  13. Clark, A. H. (1910). The origin of the crinoidal muscular articulation. American Journal of Science, 29, 40–44.CrossRefGoogle Scholar
  14. Emson, R. H., & Wilkie, I. C. (1980). Fission and autotomy in echinoderms. Oceanography and Marine Biology: An Annual Review, 18, 155–250.Google Scholar
  15. Foerste, A. F. (1893). The reproduction of arms in crinoids. American Geologist, 12, 270–271.Google Scholar
  16. Gahn, F. J., & Baumiller, T. K. (2005). Arm regeneration in Mississippian crinoids: Evidence of intense predation pressure in the Paleozoic? Paleobiology, 31, 151–164.CrossRefGoogle Scholar
  17. Gahn, F. J., & Baumiller, T. K. (2010). Evolutionary history of regeneration in crinoids (Echinodermata). Integrative and Comparative Biology, 50, 514a–514m.  https://doi.org/10.1093/icb/icq155.CrossRefGoogle Scholar
  18. Gorzelak, P., Salamon, M. A., & Baumiller, T. K. (2012). Predator-induced macroevolutionary trends in Mesozoic crinoids. PNAS, 109, 7004–7007.CrossRefGoogle Scholar
  19. Hall, J. (1861). Description of new species of Crinoidea from the Carboniferous rocks of the Mississippi Valley. Journal of the Boston Society of Natural History, 7, 261–328.Google Scholar
  20. Messing, C. G., & Tay, T. S. (2016). Extant Crinoidea (Echinodermata) of Singapore. Raffles Bulletin of Zoology Supplement, 34, 627–658 D.Google Scholar
  21. Meyer, D. L. (1985). Evolutionary implications of predation on Recent comatulid crinoids from the Great Barrier Reef. Paleobiology, 11, 154–164.CrossRefGoogle Scholar
  22. Meyer, D. L. (1988). Crinoids as renewable resources: Rapid regeneration of the visceral mass in a tropical reef-dwelling crinoid from Australia. In R. D. Burke, P. D. Mladenov, P. Lambert, & R. L. Parsley (Eds.), Echinoderm biology (pp. 519–522). Rotterdam: A. A. Balkema.Google Scholar
  23. Meyer, D. L., & Ausich, W. I. (1983). Biotic interactions among Recent and fossil crinoids. In M. F. S. Tevesz & P. L. McCall (Eds.), Biotic interactions in Recent and fossil benthic communities (pp. 377–427). New York: Plenum.CrossRefGoogle Scholar
  24. Meyer, D. L., LaHaye, C. A., Holland, N. D., Arenson, A. C., & Strickler, J. R. (1984). Time-lapse cinematography of feather stars (Echinodermata: Crinoidea) on the Great Barrier Reef, Australia: Demonstrations of posture changes, locomotion, spawning and possible predation by fish. Marine Biology, 78, 179–184.CrossRefGoogle Scholar
  25. Meyer, D. L., & Macurda, D. B., Jr. (1977). Adaptive radiation of comatulid crinoids. Paleobiology, 3, 74–82.CrossRefGoogle Scholar
  26. Meyer, D. L., & Oji, T. (1993). Eocene crinoids from Seymour Island, Antarctic Peninsula: Paleobiogeographic and paleoecologic implications. Journal of Paleontology, 67, 250–257.CrossRefGoogle Scholar
  27. Minckert, W. (1905). Über Regeneration bei Comatuliden nebst Ausführungen über die Auffassung und Bedeutung der syzygieen. Archiv fur Naturgeschichte, 71, 163–244.Google Scholar
  28. Mladenov, P. V. (1983). Rate of arm regeneration and potential causes of arm loss in the feather star Florometra serratissima (Echinodermata: Crinoidea). Canadian Journal of Zoology, 61, 2873–2879.CrossRefGoogle Scholar
  29. Nichols, D. (1996). Evidence for a sacrificial response to predation in the reproductive strategy of the comatulid crinoid Antedon bifida from the English Channel. Oceanologica Acta, 19, 237–240.Google Scholar
  30. Oji, T. (1996). Is predation intensity reduced with increasing depth? Evidence from the west Atlantic stalked crinoid Endoxocrinus parrae (Gervais) and implications for the Mesozoic marine revolution. Paleobiology, 22, 339–351.CrossRefGoogle Scholar
  31. Oji, T. (2001). Fossil record of echinoderm regeneration with special regard to crinoids. Microscopy Research and Technique, 55, 397–402.CrossRefGoogle Scholar
  32. Oji, T., & Okamoto, T. (1994). Arm autotomy and arm branching pattern as anti-predatory adaptations in stalked and stalkless crinoids. Paleobiology, 20, 27–39.CrossRefGoogle Scholar
  33. Roux, M. (1976). Aspects de la variabilité et de la croissance au sein d’une population de la pentacrine actuelle: Annacrinus wyville thompsoni Jeffreys (Crinoidea). Thalassia Jugoslavica, 12, 307–320.Google Scholar
  34. Schneider, J. A. (1988). Frequency of arm regeneration of comatulid crinoids in relation to life habit. In R. D. Burke, P. V. Mladenov, P. Lambert, & R. L. Parsley (Eds.), Echinoderm biology (pp. 531–538). Rotterdam: Balkema.Google Scholar
  35. Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9, 671–675.CrossRefGoogle Scholar
  36. Schoener, T. W. (1979). Inferring the properties of predation and other injury-producing agents from injury frequencies. Ecology, 60, 1110–1115.CrossRefGoogle Scholar
  37. Shibata, T. F., & Oji, T. (2005). Autotomy and arm number increase in Oxycomanthus japonicus (Echinodermata, Crinoidea). Invertebrate Biology, 122, 375–379.CrossRefGoogle Scholar
  38. Strimple, H. L., & Beane, B. H. (1966). Reproduction of lost arms on a crinoid from Le Grand, Iowa. Oklahoma Geology Notes, 26, 35–37.Google Scholar
  39. Syverson, V. J., Messing, C. J., Stanley, K., & Baumiller, T. K. (2015). Growth, injury, and population dynamics in the extant cyrtocrinid Holopus mikihe (Crinoidea, Echinodermata) near Roatán, Honduras. Bulletin of Marine Science, 91, 47–61.  https://doi.org/10.5343/bms.2014.1061.CrossRefGoogle Scholar
  40. Wachsmuth, C., & Springer, F. (1897). The North American Crinoidea Camerata. Harvard College Museum of Comparative Zoology Memoir, 20(21), 1–897.Google Scholar
  41. Weissmüller, A. (1998). Ein umfangreicher Fund von Encrinus liliiformis Lamarck im Oberen Muschelkalk (mo2) des Diemeltales (Nordhessen). Phillipia, 8, 245–270.Google Scholar
  42. Whitfield, R. P. (1904). Notice of a remarkable case of reproduction of lost parts shown on a fossil crinoid. Bulletin American Museum Natural History, 20, 471–472.Google Scholar

Copyright information

© Akademie der Naturwissenschaften Schweiz (SCNAT) 2018

Authors and Affiliations

  1. 1.Museum of Paleontology, Department of Earth and Environmental SciencesUniversity of MichiganAnn ArborUSA
  2. 2.Department of ZoologyUniversity of British ColumbiaVancouverCanada

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