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Urchins in the meadow: paleobiological and evolutionary implications of cidaroid predation on crinoids

Published online by Cambridge University Press:  08 April 2016

Tomasz K. Baumiller
Affiliation:
Museum of Paleontology, University of Michigan, Ann Arbor, Michigan 48109-1079. E-mail: [email protected]
Rich Mooi
Affiliation:
Department of Invertebrate Zoology and Geology, California Academy Sciences, San Francisco, California 94103. E-mail: [email protected]
Charles G. Messing
Affiliation:
Nova Southeastern Oceanographic Center, Dania, Florida 33004. E-mail: [email protected]

Abstract

Deep-sea submersible observations made in the Bahamas revealed interactions between the stalked crinoid Endoxocrinus parrae and the cidaroid sea urchin Calocidaris micans. The in situ observations include occurrence of cidaroids within “meadows” of sea lilies, close proximity of cidaroids to several upended isocrinids, a cidaroid perched over the distal end of the stalk of an upended isocrinid, and disarticulated crinoid cirri and columnals directly underneath a specimen of C. micans. Guts of two C. micans collected from the crinoid meadow contain up to 70% crinoid material. Two of three large museum specimens of another cidaroid species, Histocidaris nuttingi, contain 14–99% crinoid material.

A comparison of cidaroid gut contents with local sediment revealed significant differences: sediment-derived material consists of single crinoid ossicles often abraded and lacking soft tissue, whereas crinoid columnals, cirrals, brachials, and pinnulars found in the cidaroids are often articulated, linked by soft tissue, and unabraded. Furthermore, articulated, multi-element fragments often show a mode of fracture characteristic of fresh crinoid material. Taken together, these data suggest that cidaroids prey on live isocrinids.

We argue that isocrinid stalk-shedding, whose purpose has remained a puzzle, and the recently documented rapid crawling of isocrinids are used in escaping benthic predators: isocrinids sacrifice and shed the distal stalk portion when attacked by cidaroids and crawl away, reducing the chance of a subsequent encounter. If such predation occurred throughout the Mesozoic and Cenozoic (possibly since the mid-Paleozoic), several evolutionary trends among crinoids might represent strategies to escape predation by slow-moving benthic predators.

Type
Articles
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Ausich, W. I. 1977. The functional morphology and evolution of Pisocrinus (Crinoidea: Silurian). Journal of Paleontology 51:672686.Google Scholar
Ausich, W. I., and Baumiller, T. K. 1993. Taphonomic method for determining muscular articulations in fossil crinoids. Palaios 8:477484.Google Scholar
Ausich, W. I., Kammer, T. W., and Baumiller, T. K. 1994. Demise of the Middle Paleozoic crinoid fauna: a single extinction event or rapid faunal turnover? Paleobiology 20:345361.Google Scholar
Baumiller, T. K. 1994. Patterns of dominance and extinction in the record of Paleozoic crinoids. Pp. 193198in David, B., Guille, A., Feral, J. P., and Roux, M., eds. Echinoderms through time (Echinoderms Dijon). Balkema, Rotterdam.Google Scholar
Baumiller, T. K. 2003. Experimental and biostratinomic disarticulation of crinoids: taphonomic implications. Pp. 243248in Feral, J.-P. F. and David, B., eds. Echinoderm research 2001. Balkema, Rotterdam.Google Scholar
Baumiller, T. K., and Ausich, W. I. 1992. The broken-stick model as a null hypothesis for crinoid stalk taphonomy and as a guide to the distribution of connective tissue in fossils. Paleobiology 18:288298.Google Scholar
Baumiller, T. K., and Hagdorn, H. 1995. Taphonomy as a guide to functional morphology of Holocrinus, the first post-Paleozoic crinoid. Lethaia 28:221228.Google Scholar
Baumiller, T. K., and Messing, C. G. 2007. Stalked crinoid locomotion and its ecological and evolutionary implications. Palaeontologia Electronica 10(1):10.Google Scholar
Baumiller, T. K., LaBarbera, M., and Woodley, J. W. 1991. Ecology and functional morphology of the isocrinid Cenocrinus asterius (Linnaeus) (Echinodermata: Crinoidea): in situ and laboratory experiments and observations. Bulletin of Marine Science 48:731748.Google Scholar
Baumiller, T. K., Llewellyn, G., Messing, C. G., and Ausich, W. I. 1995. Taphonomy of isocrinid stalks: influence of decay and autotomy. Palaios 10:8795.Google Scholar
Birenheide, R., and Motokawa, T. 1994. Morphological basis and mechanics of arm movement in the stalked crinoids Metacrinus rotundus (Echinodermata, Crinoidea). Marine Biology 121:273283.CrossRefGoogle Scholar
Bottjer, D. J., and Jablonski, D. 1988. Paleoenvironmental patterns in the evolution of post-Paleozoic benthic marine invertebrates. Palaios 3:540560.Google Scholar
Brett, C. E., and Walker, S. E. 2002. Predators and predation in Paleozoic marine environments. In Kowalewski, M. and Kelley, P. H., eds. The fossil record of predation. Paleontological Society Special Papers 8:93118.Google Scholar
Brun, E. 1972. Food and feeding habits of Luidia ciliaris (Echinodermata: Asteroidea). Journal of the Marine Biological Association of the United Kingdom 52:255286.Google Scholar
Burns, C., and Mooi, R. 2003. Eocene-Oligocene echinoderm faunas of the Pacific Northwest—a preliminary report. Pp. 88106in Prothero, D. R., Ivany, L. C., and Nesbitt, E. A., eds. From greenhouse to icehouse: the marine Eocene-Oligocene transition. Columbia University Press, New York.Google Scholar
De Ridder, C., and Lawrence, J. M. 1982. Food and feeding mechanisms: Echinoidea. Pp. 57115in Jangoux, M. and Lawrence, J. M., eds. Echinoderm nutrition. Balkema, Rotterdam.Google Scholar
Donovan, S. K. 1984. Stem morphology of the Recent crinoid Chladocrinus (Neocrinus) decorus. Palaeontology 27:825841.Google Scholar
Emson, R. H., and Wilkie, I. C. 1980. Fission and autotomy in echinoderms. Oceanography and Marine Biology: An Annual Review 18:155250.Google Scholar
Fabricius, K. E. 1994. Spatial patterns in shallow-water crinoid communities on the Central Great Barrier Reef. Australian Journal of Marine and Freshwater Research 45:12251236.Google Scholar
Fishelson, L. 1974. Ecology of Northern Red Sea crinoids and their epi- and endozoic fauna. Marine Biology 26:183192.Google Scholar
Grimmer, J. C., Holland, N. D., and Hayami, I. 1985. Fine structure of the stalk of an isocrinid sea lily (Metacrinus rotundus). Zoomorphology 105:3950.Google Scholar
Hagdorn, H., and Campbell, H. J. 1993. Paracomatula triadica sp. nov.—an early comatulid crinoid from the Otapirian (Late Triassic) of New Caledonia. Alcheringa 17:117.Google Scholar
Halpern, J. A. 1970. A monographic revision of the goniasterid sea stars of the North Atlantic. . University of Miami, Miami.Google Scholar
Hess, H., Ausich, W. I., Brett, C. E., and Simms, M. J. 1999. Fossil crinoids. Cambridge University Press, Cambridge.Google Scholar
Holterhoff, P. F., and Baumiller, T. K. 1996. Phylogeny of the proto-articulates (ampelocrinids + basal articulates): implications for the Permo-Triassic extinction and re-radiation of the Crinoidea. Paleontological Society Special Publication 8.Google Scholar
Lane, N. G. 1978. Historical review of classification of Crinoidea. Pp. T348T359in Ubaghs, G. et al. Echinodermata2, Crinoidea. Part T ofMoore, R. C. and Teichert, C., eds. Treatise on invertebrate paleontology. Geological Society of America, Boulder, Colo., and University of Kansas, Lawrence.Google Scholar
Lane, N. G. 1984. Predation and survival among inadunate crinoids. Paleobiology 10:453458.Google Scholar
Lane, N. G., and Macurda, D. B. 1975. New evidence for muscular articulations in Paleozoic crinoids. Paleobiology 1:5962.Google Scholar
Lawrence, J. M. 1982. Digestion. Pp. 283316in Jangoux, M. and Lawrence, J. M., eds. Echinoderm nutrition. Balkema, Rotterdam.Google Scholar
Llewellyn, G., and Messing, C. G. 1993. Compositional and taphonomic variation in modern crinoid-rich sediments from deep-water margin of a carbonate bank. Palaios 8:554573.Google Scholar
Macurda, D. B. Jr. 1973. Ecology of comatulid crinoids at Grand Bahama Island. Hydro-lab Underwater Research Program Bulletin 2:924.Google Scholar
Macurda, D. B. Jr., and Meyer, D. L. 1983. Sea lilies and featherstars. American Scientist 71:354365.Google Scholar
Malzahn, E. 1968. Uber neue Funde von Janassa bituminosa (Schloth.) im niederrheinischen Zechstein. Geologisches Jahrbuch 85:6796.Google Scholar
McClintock, J. B., Baker, B. J., Baumiller, T. K., and Messing, C. G. 1999. Lack of chemical defenses in two species of stalked crinoids: support for the predation hypothesis for Mesozoic bathymetric restriction. Journal of Experimental Marine Biology and Ecology 232:17.Google Scholar
McIntosh, G. C. 1983. Review of the Devonian cladid inadunate crinoids: suborder Dendrocrinina. . University of Michigan, Ann Arbor.Google Scholar
Messing, C. G. 1994. In situ stalk growth and sediment production rates in a living stalked crinoid (Chladocrinus decorus) (Echinodermata). Geological Society of America Abstracts with Programs 26(7):A428.Google Scholar
Messing, C. G., RoseSmyth, M. C., Mailer, S. R., and Miller, J. E. 1988. Relocation movement in a stalked crinoid (Echinodermata). Bulletin of Marine Science 42:480487.Google Scholar
Messing, C. G., Meyer, D. L., Siebeck, U. E., Jermiin, L. S., Vaney, D. I., and Rouse, G. W. 2004. A modern, soft-bottom, shallow-water tropical crinoid fauna, with a comparison between living Comatula rotalaria and fossil Uintacrinus socialis (Echinodermata: Crinoidea). P. 596in Heinzeller, T. and Nebelsick, J. H., eds. Echinoderms: München. Balkema, Rotterdam.Google Scholar
Messing, C. G., David, J., Roux, M., Améziane, N., and Baumiller, T. K. 2007. In situ stalk growth rates in tropical western Atlantic sea lilies (Echinodermata: Crinoidea). Journal of Experimental Marine Biology and Ecology 353:211220.Google Scholar
Meyer, D. L. 1985. Evolutionary implications of predation on Recent comatulid crinoids from the Great Barrier Reef. Paleobiology 11:154164.Google Scholar
Meyer, D. L., and Ausich, W. I. 1983. Biotic interactions among Recent and fossil crinoids. Pp. 377427in Tevesz, M. F. S. and McCall, P. L., eds. Biotic interactions in recent and fossil benthic communities. Plenum, New York.Google Scholar
Meyer, D. L., and Macurda, D. B. Jr. 1977. Adaptive radiation of comatulid crinoids. Paleobiology 3:7482.Google Scholar
Meyer, D. L., and Meyer, K. B. 1986. Biostratinomy of Recent crinoids (Echinodermata) at Lizard Island, Great Barrier Reef, Australia. Palaios 1:294302.Google Scholar
Meyer, D. L., LaHaye, C. A., Holland, N. D., Arenson, A. C., and 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 78:179184.Google Scholar
Milsom, C. V. 1994. Saccocoma: a benthic crinoid from the Jurassic Solnhofen Limestone, Germany. Palaeontology 37:121129.Google Scholar
Milsom, C. V., and Sharpe, T. 1995. Jurassic lagoon: salt or soup? Geology Today 11:2226.Google Scholar
Milsom, C. V., Simms, M. J., and Gale, A. S. 1994. Phylogeny and paleobiology of Marsupites and Uintacrinus. Palaeontology 37:595607.Google Scholar
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 61:28732879.Google Scholar
Motokawa, T. 1984. Connective tissue catch in echinoderms. Biological Review 59:255270.Google Scholar
Moy-Thomas, J. A., and Miles, R. S. 1971. Paleozoic fishes. W. B. Saunders, Philadelphia.Google Scholar
Nichols, D. 1994. Reproductive seasonality in the comatulid crinoid Antedon bifida (Pennant) from the English Channel. Philosophical Transactions of the Royal Society of London B 343:113134.Google Scholar
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 19:237240.Google Scholar
Oji, T., and Okamoto, T. 1994. Arm autotomy and arm branching pattern as anti-predatory adaptations in stalked and stalkless crinoids. Paleobiology 20:2739.Google Scholar
Rasmussen, H. W. 1978. Articulata. Pp. T813T928in Ubaghs, G. et al. Echinodermata 2, Crinoidea. Part T ofMoore, R. C. and Teichert, C., eds. Treatise on invertebrate paleontology. Geological Society of America, Boulder, Colo., and University of Kansas, Lawrence.Google Scholar
Roux, M. 1977. The stalk-joint of Recent Isocrinidae (Crinoidea). Bulletin of the British Museum (Natural History) (Zoology) 32:4564.Google Scholar
Schneider, C. 2001. Heaps of echinoids in a Pennsylvanian echinoderm lagerstätten: implications for fossilized behavior. PaleoBios 21(Suppl. to No. 2):113.Google Scholar
Schneider, J. A. 1988. Frequency of arm regeneration of comatulid crinoids in relation to life habit. Pp. 531538in Burke, R. D., Mladenov, P. V., Lambert, P., and Parsley, R. L., eds. Echinoderm biology. Balkema, Rotterdam.Google Scholar
Shaw, G. D., and Fontaine, A. R. 1990. The locomotion of the comatulid Florometra serratissima (Echinodermata: Crinoidea) and its adaptive significance. Canadian Journal of Zoology 68:942950.Google Scholar
Signor, P. W. III, and Brett, C. E. 1984. The mid-Paleozoic precursor to the Mesozoic marine revolution. Paleobiology 10:229245.Google Scholar
Simms, M. J. 1999. Systematics, phylogeny and evolutionary history. Pp. 3140in Hess, H., Ausich, W. I., Brett, C. E., and Simms, M. J., eds. Fossil crinoids. Cambridge University Press, Cambridge.Google Scholar
Simms, M. J., and Sevastopulo, G. D. 1993. The origin of articulate crinoids. Palaeontology 36:91109.Google Scholar
Sloan, N. A., and Campbell, A. C. 1982. Perception of food. Pp. 323in Jangoux, M. and Lawrence, J. M., eds. Echinoderm nutrition. Balkema, Rotterdam.Google Scholar
Smith, A. B. 1984. Echinoid palaeobiology. George Allen and Unwin, Boston.Google Scholar
Smith, A. B. 2005. The Echinoid Directory. http://www.nhm.ac.uk/research-curation/projects/echinoid-directory/index [accessed 5/25/2007]Google Scholar
Smith, A. B., and Hollingworth, N. T. J. 1990. Tooth structure and phylogeny of the Upper Permian echinoid Miocidaris keyserlingi. Proceedings of the Yorkshire Geological Society 48:4760.Google Scholar
Smith, A. B., and Wright, C. W. 1989. British Cretaceous echinoids, Part 1. General introduction and Cidaroida. Monograph of the Palaeontographical Society No. 578, part of Vol. 141:1101.Google Scholar
Thomas, G. E., and Gruffydd, L. D. 1971. The types of escape reactions elicited in the scallop Pecten maximus by selected sea-star species. Marine Biology 10:8793.Google Scholar
Vail, L. 1987. Diel patterns of emergence of crinoids (Echinodermata) from within a reef at Lizard Island, Great Barrier Reef, Australia. Marine Biology 93:551560.Google Scholar
Vermeij, G. J. 1977. The Mesozoic marine revolution: evidence from snails, predators, and grazers. Paleobiology 3:245258.Google Scholar
Waters, J. A., and Maples, C. G. 1991. Mississippian pelmatozoan community reorganization: a predation-mediated faunal change. Paleobiology 17:400410.Google Scholar
Wilkie, I. C. 1984. Variable tensility in echinoderm collagenous tissue: a review. Marine Behaviour and Physiology 11:134.Google Scholar
Wilkie, I. C. 2005. Mutable collagenous tissue: overview and biotechnological perspective. Pp. 221250in Matranaga, V., ed. Echinodermata. Springer, Berlin.Google Scholar
Wilkie, I. C., Dolan, S., Lewis, J., and Blake, D. R. 2007. “Autotomy”: a terminological inexactitude. Pain 128:283294.Google Scholar
Zangerl, R., and Richardson, E. S. Jr. 1963. The paleoecological history of the two Pennsylvanian black shales. Fieldiana (Geology) Memoirs 4:1352.Google Scholar