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The arrangement of possible muscle fibres in the Ediacaran taxon Haootia quadriformis

2015; Royal Society; Volume: 282; Issue: 1803 Linguagem: Inglês

10.1098/rspb.2014.2949

1471-2954

Alexander Liu, Jack Matthews, Latha R. Menon, Duncan McIlroy, Martin D. Brasier,

Cephalopods and Marine Biology

You have accessMoreSectionsView PDF ToolsAdd to favoritesDownload CitationsTrack Citations ShareShare onFacebookTwitterLinked InRedditEmail Cite this article Liu Alexander G., Matthews Jack J., Menon Latha R., McIlroy Duncan and Brasier Martin D. 2015The arrangement of possible muscle fibres in the Ediacaran taxon Haootia quadriformisProc. R. Soc. B.2822014294920142949http://doi.org/10.1098/rspb.2014.2949SectionYou have accessComments and invited repliesThe arrangement of possible muscle fibres in the Ediacaran taxon Haootia quadriformis Alexander G. Liu Alexander G. Liu School of Earth Sciences, University of Bristol, Life Sciences Building, 24 Tyndall Avenue, Bristol BS8 1TQ, UK [email protected] Google Scholar Find this author on PubMed Search for more papers by this author , Jack J. Matthews Jack J. Matthews Department of Earth Sciences, University of Oxford, South Parks Road, Oxford OX1 3AN, UK Google Scholar Find this author on PubMed Search for more papers by this author , Latha R. Menon Latha R. Menon Department of Earth Sciences, University of Oxford, South Parks Road, Oxford OX1 3AN, UK Google Scholar Find this author on PubMed Search for more papers by this author , Duncan McIlroy Duncan McIlroy http://orcid.org/0000-0001-9521-499X Department of Earth Sciences, Memorial University of Newfoundland, 300 Prince Philip Drive, St John's, Newfoundland and Labrador, CanadaA1B 3X5 Google Scholar Find this author on PubMed Search for more papers by this author and Martin D. Brasier Martin D. Brasier Department of Earth Sciences, University of Oxford, South Parks Road, Oxford OX1 3AN, UK Department of Earth Sciences, Memorial University of Newfoundland, 300 Prince Philip Drive, St John's, Newfoundland and Labrador, CanadaA1B 3X5 Google Scholar Find this author on PubMed Search for more papers by this author Alexander G. Liu Alexander G. Liu School of Earth Sciences, University of Bristol, Life Sciences Building, 24 Tyndall Avenue, Bristol BS8 1TQ, UK [email protected] Google Scholar Find this author on PubMed , Jack J. Matthews Jack J. Matthews Department of Earth Sciences, University of Oxford, South Parks Road, Oxford OX1 3AN, UK Google Scholar Find this author on PubMed , Latha R. Menon Latha R. Menon Department of Earth Sciences, University of Oxford, South Parks Road, Oxford OX1 3AN, UK Google Scholar Find this author on PubMed , Duncan McIlroy Duncan McIlroy http://orcid.org/0000-0001-9521-499X Department of Earth Sciences, Memorial University of Newfoundland, 300 Prince Philip Drive, St John's, Newfoundland and Labrador, CanadaA1B 3X5 Google Scholar Find this author on PubMed and Martin D. Brasier Martin D. Brasier Department of Earth Sciences, University of Oxford, South Parks Road, Oxford OX1 3AN, UK Department of Earth Sciences, Memorial University of Newfoundland, 300 Prince Philip Drive, St John's, Newfoundland and Labrador, CanadaA1B 3X5 Google Scholar Find this author on PubMed Published:22 March 2015https://doi.org/10.1098/rspb.2014.2949Haootia quadriformis from Newfoundland, Canada, is one of the most unusual impressions of a soft-bodied macro-organism yet described from the late Ediacaran Period. Interpreted as a metazoan of cnidarian grade [1], the body impression of H. quadriformis possesses features interpreted as fibrous structures that represent possible evidence for muscular tissue. Evidence both in support of and against a relationship between H. quadriformis and the Staurozoa, one of the cnidarian groups to which Haootia was compared in Liu et al. [1], is outlined by Miranda et al. [2]. Our intention in our original paper was to illustrate the staurozoan body plan for comparative purposes, rather than suggest homology or direct ancestry. Nevertheless, fresh insights from workers with expertise in the biology of extant cnidarians are welcomed.We are pleased that the main points of our paper find support from the biological community: that recently discovered Haootia quadriformis probably preserves the impressions of muscle fibres in a macrofossil characterized by tetra-radial symmetry, and that these structures are consistent with a cnidarian body plan [2]. Histological images provided by Miranda et al. [2], plus their accompanying discussion, present a clear picture of muscular arrangements within modern stauromedusae. We concur that Haootia shows both similarities and differences with respect to stauromedusans.Miranda et al. [2] suggest that the organization of musculature described by us (see [1], fig. 3b) within the body of Haootia appears inconsistent with that observed in modern staurozoan taxa. While the argument for the presence of a radial (longitudinal) muscle arrangement is well reasoned (see [2], fig. 1s), a revisiting of the type material to determine the orientation of fibrous structures in Haootia leads us to conclude that they are essentially as published in our original paper. The paratype specimen (see [1], fig. 1f) has fibres from potential coronal muscles that extend in arcs almost to the base of the calyx, with no clear preservation of radial fibres running perpendicular to these. We would argue that this phenomenon contradicts the suggestion that coronal muscle may have been restricted to the margins of the Haootia body [2].The arrangement of musculature inferred by Liu et al. [1] does not preclude the presence of additional radial muscle bundles within the body of the organism. The holotype of H. quadriformis contains evidence for superposition of fibrous structures. We can clearly discern that the body sheet/calyx drapes parallel fibres observed in the stalk/peduncle, and that subsidiary branches appear to extend beneath the body (figure 1). In such cases, the fibres beneath the calyx are not expressed in the fossilized impression and are inferred to lie beyond the plane of preservation. It is therefore possible that both coronal and radial musculature were present in the calyx of Haootia (just as both are present in the arms of modern stauromedusae [2]), but only the outermost set is recorded in the cast of the body tissues so beautifully preserved in the Haootia impression. Figure 1. The disc, stalk and body of the Haootia quadriformis holotype. Image taken at The Rooms Provincial Museum, St John's. Note that although the outline of the stalk/peduncle can be seen beneath the body/calyx, the longitudinal fibres running along its length cannot be easily traced (white arrow). Similarly, fibres radiating from the smallest subsidiary branches are typically not seen to continue beneath the body (e.g. cross-hatched arrow). It is thus plausible that additional muscle bundles, perhaps in different arrangements from those preserved, were present in the original Haootia organism, but do not lie in the plane of preservation. Scale bar, 10 mm. (Online version in colour.)Download figureOpen in new tabDownload PowerPointIf one were to adopt a stauromedusan analogue for Haootia, the inferred coronal musculature would be in the 'calyx' rather than the radial disc. This proposed muscular arrangement (see [1], fig. 3b) would argue against a free-swimming mode of life, and adds support to a benthic mode of life for Haootia. We therefore take great interest in the suggestion that this arrangement of muscles is consistent with an organism capable of producing powerful body contractions, potentially involved in a pulsing feeding strategy [2]. We must keep in mind that some, or maybe most, Ediacaran body plans and feeding strategies may have been specifically adapted to Ediacaran conditions. Possible behavioural ecologies such as surface detritus feeding, which would be feasible for an organism with so flexible a body, still await analysis.The hypothetical models of muscle fibre arrangement proposed both by ourselves [1] and Miranda et al. [2] require further testing against the fossil material. The remarkably preserved holotype specimen of Haootia has now been collected (under permits issued by the Department of Tourism, Culture and Recreation, Government of Newfoundland and Labrador) and is housed at The Rooms Provincial Museum, St. John's, Newfoundland (specimen NFM F-994). While the fidelity of preservation restricts elements of the interpretation of this key fossil, the opportunity to apply controlled lighting conditions to the specimen following its removal from the outcrop offers the potential for further analysis (e.g. figure 1). We are confident that well-informed discussion of analogue taxa such as that offered by Miranda et al. will lead to a more complete understanding of Haootia, and its evolutionary significance. Similarly detailed consideration of the physiology of other extant cnidarian clades would be greatly beneficial for palaeontologists working on candidate early cnidarians.We would like to add in support of our discussion of Haootia that strata of similar age in Newfoundland also contain rare fossilized surface locomotion trails that are considered to have formed by contractile activities associated with a cnidarian body plan [3–6]. We have hitherto found no evidence that the basal disc of Haootia could contract or move, but having two independent lines of evidence for the presence of organisms with contractile tissues in the Ediacaran makes a more compelling case for the presence of cnidarian-grade organisms [1]. While we recognize the potential importance of a fossil cnidarian ancestor from somewhat well-dated strata for understanding the phylogeny of the Cnidaria, we would caution against the uncritical extension of such interpretations to other Ediacaran taxa. The preservation and morphology of many late Ediacaran macrofossils make them difficult to interpret, and further work is required before we can be confident in our understanding of these ancient and evolutionarily important organisms.Data accessibilityAdditional images are available from the Dryad Digital Repository: doi:10.5061/dryad.8m2q8.AcknowledgementThe staff of The Rooms Provincial Museum and the Newfoundland and Labrador Department of Tourism, Culture and Recreation are thanked for their role in the successful salvage and curation of the holotype specimen.Funding statementWe are grateful to two anonymous reviewers, and to NSERC (to D.M.) and the Natural Environment Research Council (grant no. NE/L011409/1 to A.G.L. and NE/J5000045/1 to J.J.M.) for financial support.FootnotesThe accompanying comment can be viewed at http://dx.doi.org/10.1098/rspb.2014.2396.© 2015 The Author(s) Published by the Royal Society. All rights reserved.References1Liu AG, Matthews JJ, Menon LR, McIlroy D& Brasier MD. 2014Haootia quadriformis n. gen., n. sp., interpreted as a muscular cnidarian impression from the Late Ediacaran Period (approx. 560 Ma). Proc. R. Soc. B 281, 20141202. (doi:10.1098/rspb.2014.1202). Link, ISI, Google Scholar2Miranda LS, Collins AG& Marques AC. 2015Is Haootia quadriformis related to extant Staurozoa (Cnidaria)? Evidence from the muscular system reconsidered. Proc. R. Soc. B. 282, 20142396. (doi:10.1098/rspb.2014.2396). Link, Google Scholar3Liu AG& McIlroy D. 2015Horizontal surface traces from the Fermeuse Formation, Ferryland (Newfoundland, Canada), and their place within the Late Ediacaran ichnological revolution. Ichnology: publications arising from ICHNIA III, Geological Association of Canada, Miscellaneous Publication, vol. 9 (ed. & McIlroy D), pp. 141–156. Google Scholar4Liu AG, McIlroy D& Brasier MD. 2010First evidence for locomotion in the Ediacara biota from the 565 Ma Mistaken Point Formation, Newfoundland. Geology 38, 123–126. (doi:10.1130/G30368.1). Crossref, ISI, Google Scholar5Liu AG, McIlroy D, Brasier MD& Matthews JJ. 2014Confirming the metazoan character of a 565 Ma trace-fossil assemblage from Mistaken Point, Newfoundland. Palaios 29, 420–430. (doi:10.2110/palo.2014.011). Crossref, ISI, Google Scholar6Menon LR, McIlroy D& Brasier MD. 2013Evidence for Cnidaria-like behavior in ca. 560 Ma Ediacaran Aspidella. Geology 41, 895–898. (doi:10.1130/G34424.1). Crossref, ISI, Google Scholar Previous ArticleNext Article VIEW FULL TEXT DOWNLOAD PDF FiguresRelatedReferencesDetailsCited by Chen Z, Tu C, Pei Y, Ogg J, Fang Y, Wu S, Feng X, Huang Y, Guo Z and Yang H (2019) Biosedimentological features of major microbe-metazoan transitions (MMTs) from Precambrian to Cenozoic, Earth-Science Reviews, 10.1016/j.earscirev.2019.01.015, 189, (21-50), Online publication date: 1-Feb-2019. Matthews J, Liu A and McIlroy D (2017) Post-fossilization processes and their implications for understanding Ediacaran macrofossil assemblages, Geological Society, London, Special Publications, 10.1144/SP448.20, 448:1, (251-269), . Liu A, Menon L, Shields G, Callow R and McIlroy D (2016) Martin Brasier's contribution to the palaeobiology of the Ediacaran–Cambrian transition, Geological Society, London, Special Publications, 10.1144/SP448.9, 448:1, (179-193), . 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