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Using experimental decay of modern forms to reconstruct the early evolution and morphology of fossil enteropneusts

Published online by Cambridge University Press:  04 June 2015

Karma Nanglu ,
Jean-Bernard Caron  and
Christopher B. Cameron
Karma Nanglu
Affiliation:
Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Ontario M5S 2J7, Canada, and Department of Natural History Palaeobiology, Royal Ontario Museum, Toronto, Ontario M5S 2C6, Canada. E-mail: [email protected]
Jean-Bernard Caron
Affiliation:
Department of Natural History Palaeobiology, Royal Ontario Museum, Toronto, Ontario M5S 2C6, Canada. Departments of Ecology and Evolutionary Biology and Earth Sciences, University of Toronto, Toronto, Ontario M5S 2J7, Canada
Christopher B. Cameron
Affiliation:
Département de sciences biologiques, Université de Montréal C.P. 6128, Succursale Centre-ville, Montreal, Quebec H3C 3J7, Canada
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Abstract

Decay experiments are becoming a more widespread tool in evaluating the fidelity of the fossil record. Character interpretations of fossil specimens stand to benefit from an understanding of how decay can result in changes in morphology and, potentially, total character loss. We performed a decay experiment for the Class Enteropneusta to test the validity of anatomical interpretations of the Burgess Shale enteropneust Spartobranchus tenuis and to determine how the preservation of morphological features compares with the sequence of character decay in extant analogues. We used three species of enteropneust (Saccoglossus pusillus, Harrimania planktophilus, and Balanoglossus occidentalis) representing the two major families of Enteropneusta. Comparisons between decay sequences suggest that morphological characters decay in a consistent and predictable manner within Enteropneusta, and do not support the hypothesis of stemward slippage. The gill bars and nuchal skeleton were the most decay resistant, whereas the gill pores and pre-oral ciliary organ were unequivocally the most decay prone. Decay patterns support the identification of the nuchal skeleton, gill bars, esophageal organ, trunk, and proboscis in Spartobranchus tenuis and corroborate a harrimaniid affinity. Bias due to the taphonomic loss of taxonomically informative characters is unlikely. The morphologically simple harrimaniid body plan can be seen, therefore, to be plesiomorphic within the enteropneusts. Discrepancies between the sequence of decay in a laboratory setting and fossil preservation also exist. These discrepancies are highlighted not to discredit the use of modern decay studies but rather to underline their non-actualistic nature. Paleoenvironmental variables besides decay, such as the timeframe between death and early diagenesis as well as postmortem transport, are discussed relative to decay data. These experiments reinforce the strength of a comprehensive understanding of decay sequences as a benchmark against which to describe fossil taxa and understand the conditions leading to fossilization.

Type
Articles
Information
Paleobiology , Volume 41 , Issue 3 , June 2015 , pp. 460 - 478
Copyright
Copyright © 2015 The Paleontological Society. All rights reserved. 

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References

Literature Cited

Alessandrello, A., Bracchi, G., and Riou, B.. 2004. Polychaete, sipunculan and enteropneust worms from the lower Callovian (Middle Jurassic) of La Voulte-sur-Rhône (Ardèche, France). Atti della Società italiana di Scienze naturali e del Museo Civico di Storia naturale di Milano 32:3–14.Google Scholar
Allison, P. A. 1986. Soft-bodied animals in the fossil record: the role of decay in fragmentation during transport. Geology 14:979–981.2.0.CO;2>CrossRefGoogle Scholar
Allison, P. A. 1988. The role of anoxia in the decay and mineralization of proteinaceous macro-fossils. Paleobiology 14:139–154.CrossRefGoogle Scholar
Allison, P. A., and Brett, C. E.. 1995. In situ benthos and paleo-oxygenation in the Middle Cambrian Burgess Shale, British Columbia, Canada. Geology 23:1079–1082.2.3.CO;2>CrossRefGoogle Scholar
Arduini, P., Pinna, G., and Teruzzi, G.. 1981. Megaderaion sinemuriense ng. n.sp, a new fossil enteropneust of the Sinemurian of Osteno in Lombardy. Atti della Societa Italiana di Scienze Naturali e dei Museo Civico di Storia Naturalie di Milano 122:104–108.Google Scholar
Bechly, G., and Frickhinger, K. A.. 1999. The fossils of Solnhofen 2. Goldschneck, Korb, Germany.Google Scholar
Briggs, D. E. G., and Kear, A. J.. 1993a. Decay of Branchiostoma: implications for soft-tissue preservation in conodonts and other primitive chordates. Lethaia 26:275–287.CrossRefGoogle Scholar
Briggs, D. E. G., and Kear, A. J.. 1993b. Decay and preservation of polychaetes—taphonomic thresholds in soft-bodied organisms. Paleobiology 19:107–135.CrossRefGoogle Scholar
Briggs, D. E. G., and Kear, A. J.. 1994. Decay and mineralization of shrimps. Palaios 9:431–456.CrossRefGoogle Scholar
Briggs, D. E. G., Kear, A. J., Baas, M., Leeuw, J. W., and Rigby, S.. 1995. Decay and composition of the hemichordate Rhabdopleura: implications for the taphonomy of graptolites. Lethaia 28:15–23.CrossRefGoogle Scholar
Butterfield, N. J. 2002. Leanchoilia guts and the interpretation of three-dimensional structures in Burgess Shale-type fossils. Paleobiology 28:155–171.2.0.CO;2>CrossRefGoogle Scholar
Cameron, C. B. 2002. Particle retention and flow in the pharynx of the enteropneust worm Harrimania planktophilus: the filter feeding pharynx may have evolved prior to the chordates. Biological Bulletin 202:192–200.CrossRefGoogle Scholar
Cameron, C. B. 2005. A phylogeny of the hemichordates based on morphological characters. Canadian Journal of Zoology 83:196–215.CrossRefGoogle Scholar
Cameron, C. B., Swalla, B. J., and Garey, J. R.. 2000. Evolution of the chordate body plan: new insights from phylogenetic analysis of deuterostome phyla. Proceedings of the National Academy of Sciences USA 97:4469–4474.CrossRefGoogle ScholarPubMed
Cannon, J. T., Swalla, B. J., and Halanych, K. M.. 2013. Hemichordate molecular phylogeny reveals a novel cold-water clade of harrimaniid acorn worms. Biological Bulletin 225:194–204.CrossRefGoogle ScholarPubMed
Caron, J. B., and Jackson, D. A.. 2006. Taphonomy of the Greater Phyllopod Bed community, Burgess Shale. Palaios 21:451–465.CrossRefGoogle Scholar
Caron, J. B., Conway Morris, S., and Cameron, C. B.. 2013. Tubicolous enteropneusts from the Cambrian period. Nature 495:503–506.CrossRefGoogle ScholarPubMed
Casenove, D., Oji, T., and Goto, T.. 2011. Experimental taphonomy of benthic chaetognaths: implications for the decay process of Paleozoic chaetognath fossils. Paleontological Research 15:146–153.CrossRefGoogle Scholar
Chen, J. Y., Dzik, J., Edgecombe, G. D., Ramsköld, L., and Zhou, G. Q.. 1995. A possible Ealy Cambrian chordate. Nature 377:720–722.CrossRefGoogle Scholar
Chen, A., and Huang, D.. 2008. Gill rays of the primitive vertebrate Yunnanozoon from Early Cambrian: a first record. Frontiers of Biology in China 3:241–244.CrossRefGoogle Scholar
Conway Morris, S.. 2009. The Burgess Shale animal Oesia is not a chaetognath: a reply to Szaniawski. Acta Palaeontologica Polonica 54:175–179.CrossRefGoogle Scholar
Conway Morris, S., and Caron, J. B.. 2012. Pikaia gracilens Walcott, a stem-group chordate from the Middle Cambrian of British Columbia. Biological Reviews 87:480–512.CrossRefGoogle Scholar
Darroch, S. A. F., Laflamme, M., Schiffbauer, J. D., and Briggs, D. E. G.. 2012. Experimental formation of a microbial death mask. Palaios 27:293–303.CrossRefGoogle Scholar
Deland, C., Cameron, C. B., Bullock, T. H., Rao, K. P., and Ritter, W. E.. 2010. A taxonomic revision of the family Harrimaniidae (Hemichordata: Enteropneusta) with descriptions of seven species from the Eastern Pacific. Zootaxa 2408:1–30.CrossRefGoogle Scholar
Donoghue, P. C. J., and Purnell, M.. 2009. Distinguishing heat from light in debate over controversial fossils. BioEssays 31:178–189.CrossRefGoogle ScholarPubMed
Gabbott, S. E., Xian-guang, H., Norry, M. J., and Siveter, D. J.. 2004. Preservation of Early Cambrian animals of the Chengjiang biota. Geology 32:901–904.CrossRefGoogle Scholar
Gabbot, S. E., Zalasiewicz, J., and Collins, D.. 2008. Sedimentation of the Phyllopod Bed within the Cambrian Burgess Shale Formation of British Columbia. Journal of the Geologic Society 165:307–318.CrossRefGoogle Scholar
Gaines, R. R., Briggs, D. E. G., and Yuanlong, Z.. 2008. Cambrian Burgess Shale-type deposits share a common mode of fossilization. Geology 36:755–788.CrossRefGoogle Scholar
Gaines, R. R., Hammarlund, E. U., Hou, X., Qi, C., Gabbott, S. E., Zhao, Y., Peng, J., and Canfield, D. E.. 2012. Mechanism for Burgess Shale-type preservation. PNAS 109:5180–5184.CrossRefGoogle ScholarPubMed
Gonzalez, P., and Cameron, C. B.. 2009. The gill slits and pre-oral ciliary organ of Protoglossus (Hemichordata: Enteropneusta) are filter feeding structures. Biological Journal of the Linnean Society 98:896–906.CrossRefGoogle Scholar
Halanych, K. M., Cannon, J. T., Mahon, A. R., Swalla, B. J., and Smith, C. R.. 2013. Modern Antarctic acorn worms form tubes. Nature Communications 4, doi: 10.1038/ncomms3738.CrossRefGoogle ScholarPubMed
Maletz, J. 2014. Hemichordata (Pterobranchia, Enteropneusta) and the fossil record. Palaeogeography, Palaeclimatology, Palaeoecology 398:16–27.CrossRefGoogle Scholar
Mitchell, C. E., Melchin, J. M., Cameron, C. B., and Maletz, J.. 2013. Phylogeny of the tube-building Hemichordata reveals that Rhabdopleura is an extant graptolite. Lethaia 46:34–56.CrossRefGoogle Scholar
Osborn, K. J., Kuhnz, L. A., Priede, I. G., Urata, M., Gebruk, A. V., and Holland, N. D.. 2012. Diversification of acorn worms (Hemichordata, Enteropneusta) revealed in the deep sea. Proceedings of the Royal Society of London B 279:1646–1654.Google ScholarPubMed
Sansom, R. S., and Wills, M. A.. 2013. Fossilization causes organisms to appear erroneously primitive by distorting evolutionary trees. Scientific Reports 3:2545.CrossRefGoogle ScholarPubMed
Sansom, R. S., Gabbott, S. E., and Purnell, M. A.. 2010a. Non-random decay of chordate characters causes bias in fossil interpretation. Nature 463:797–800.CrossRefGoogle ScholarPubMed
Sansom, R. S., Gabbott, S. E., and Purnell, M. A.. 2010b. Decay of vertebrate characters in hagfish and lamprey (Cyclostomata) and the implications for the vertebrate fossil record. Proceedings of the Royal Society of London B 278:1150–1157.Google ScholarPubMed
Sansom, R. S., Gabbott, S. E., and Purnell, M. A.. 2013. Atlas of vertebrate decay: a visual and taphonomic guide to fossil interpretation. Palaeontology 56:457–474.CrossRefGoogle Scholar
Shabica, C. W., and Hay, A. A.. 1997. Richardson’s guide to the fossil fauna of Mazon Creek. Northeastern Illinois University, Chicago.Google Scholar
Shu, D., Zhang, X., and Chen, L.. 1996. Reinterpretation of Yunnanozoon as the earliest known hemichordate. Nature 380:428–430.CrossRefGoogle Scholar
Swalla, B. J., and Smith, A. B.. 2008. Deciphering deuterostome phylogeny: molecular, morphological and palaeontological perspectives. Philosophical Transactions of the Royal Society B of London 363:1557–1568.CrossRefGoogle ScholarPubMed
Szaniawski, H. 2005. Cambrian chaetognaths recognized in Burgess Shale fossils. Acta Palaeontologica Polonica 50:1–8.Google Scholar
Szaniawski, H. 2009. Fossil chaetognaths from the Burgess Shale: a reply to Conway Morris. Acta Palaeontologica Polonica 54:361–364.CrossRefGoogle Scholar
Urata, M., and Yamaguchi, M.. 2004. The development of the enteropneust hemichordate Balanoglossus misakiensis Kuwano. Zoological Science 21:533–540.CrossRefGoogle ScholarPubMed
Wilson, L. A., and Butterfield, N. J.. 2013. Sediment effects on preservation of Burgess Shale-type compression fossils. Palaios 29:145–153.CrossRefGoogle Scholar