Exceptional soft-tissue preservation in boring ctenostome bryozoans and associated “fungal” borings from the Early Devonian of Podolia, Ukraine

• Autorzy: Olempska E.
• Języki publikacji: EN

Abstrakty

EN

Colonies of boring ctenostome bryozoans and microborings of “fungi” that occur in the Early Devonian (Lochkovian, ~416 Ma) of Podolia, western Ukraine, have soft−tissue preserved by phosphatization. These comprise exceptional three−dimensional body walls of feeding zooids with probable parietal muscles inserted on the cystid wall, and setigerous collars twisted within the vestibulum. The presence of collars in this Early Devonian ctenostomes proves the existence of this feature for more than 416 Ma of ctenostome evolution. Phosphatized remains of the zooid walls are interpreted as relicts of the originally chitinous cystid walls. This is the first record of soft−tissue fossilization in a boring bryozoan. The presence of cavities (specialized heterozooids), empty or filled with laminated calcium phosphate, is also documented in bryozoans for the first time. These cavities are interpreted as “store−rooms” in which the bryozoans accumulated nutrients. The new taxon, Podoliapora doroshevi gen. et sp. nov. is described. In additional, phosphatised fungi−like endoliths co−occur with bryozoans.

Słowa kluczowe

EN

soft tissue preservation; ctenostome bryozoan; bryozoan; Early Devonian; Devonian; paleontology; Podolia; Ukraine; Bryozoa; fungi; demineralization; phosphatization

• Wydawca: -
• Czasopismo: Acta Palaeontologica Polonica
• Rocznik: 2012
• Tom: 57
• Numer: 4
• Opis fizyczny: p.925-940,fig.,ref.

Twórcy

autor

Olempska E.

• Institute of Paleobiology, Polish Academy of Sciences, Twarda 51/55, 00-818 Warsaw, Poland

Bibliografia

• Addadi, L., Joester, D., Nudelman, F., and Weiner, S. 2006. Mollusk shell formation: a source of new concepts for understanding biomineralization processes. Chemistry—A European Journal 12: 980–987.
• Alexandersson, E.T. 1975. Marks of unknown carbonate−decomposing organelles in cyanophyte borings. Nature 254: 212, 237–238.
• Allison, P.A. 1988. Konservat−Lagerstätten: cause and classification. Paleobiology 14: 331–344.
• Baliński, A. 2010. First colour−patterned strophomenide brachiopod from the earliest Devonian of Podolia, Ukraine. Acta Palaeontologica Polonica 55: 695–700.
• Baliński, A. 2012. The brachiopod succession through the Silurian–Devonian boundary beds at Dnistrove, Podolia, Ukraine. Acta Palaeontologica Polonica 57: 897–924.
• Banta, W.C., Perez, F.M., and Santagata, S. 1995. A setigerous collar in Membranipora chesapeakensis n. sp. (Bryozoa): implications for the evolution of cheilostomes from ctenostomes. Invertebrate Biology 114: 83–88.
• Bathurst, R.G.C. 1966. Boring algae, micrite envelopes and lithification of molluscan biosparites. Geological Journal 5: 15–32.
• Bentis, C.J., Kaufman, L., and Golubic, S. 2000. Endolithic fungi in reef−building corals (Order: Scleractinia) are common, cosmopolitan, and potentially pathogenic. Biological Bulletin 198: 254–260.
• Bertling, M. 1995. Ropalonaria arachne (Fischer, 1866) eine Bryozoen-Bohrspur aus dem norddeutschen Malm. Münstersche Forschungen zur Geologie und Paläontologie 77: 357–362.
• Boekschoten, G.J. 1970. On bryozoan borings from the Danian at Fakse, Denmark.In: T.P. Crimes and J.C. Harper (eds.), Trace Fossils. Geological Journal (Special Issues) 3: 43–48.
• Botquelen, A. and Mayoral, E. 2005. Early Devonian bioerosion in the Rade de Brest, Armorican Massif, France. Palaeontology 48: 1057–1064.
• Briggs, D.E.G. and Kear, A.J. 1994. Decay and mineralization of shrimps. Palaios 9: 431–456.
• Briggs, D.E.G., Kear, A.J., Martill, D.M., and Wilby, P.R. 1993. Phosphatization of soft−tissue in experiments and fossils. Journal of the Geological Society, London 150: 1035–1038.
• Briggs, D.E.G. and Wilby, P.R. 1996. The role of the calcium carbonate−calcium phosphate switch in the mineralization of soft−bodied fossils. Journal of the Geological Society, London 153: 665–668.
• Bromley, R.G. 1970. Borings as trace fossils and Entobia cretacea Portlock as an example. In: T.P. Crimes and J.C. Harper (eds.), Trace Fossils. Geological Journal (Special Issues) 3: 49–90.
• Carter, J.G. 1990. Evolutionary significance of shell microstructure in the Palaeotaxodonta, Pteriomorphia and Isofilibranchia (Bivalvia: Mollusca). In: J.G. Carter (ed.), Skeletal Biomineralization: Patterns, Processes, and Evolutionary Trends, vol. I, 135–296. Van Nostrand Reinhold, New York.
• Casadío, S., Marenssi, S.A., and Santillana, S.N. 2001. Endolithic bioerosion traces attributed to boring bryozoans in the Eocene of Antarctica. Ameghiniana 38: 321–329.
• Chacón, E., Berrendero, E., and Garcia−Pichel, F. 2006. Biological signatures of microboring cyanobacterial communities in marine carbonates from Cabo Rojo, Puerto Rico. Sedimentary Geology 185: 215–228.
• Checa, A.G., Ramírez−Rico, J., González−Segura, A., and Sánchez−Navas, A. 2009. Nacre and false nacre (foliated aragonite) in extant monoplacophorans (= Tryblidiida: Mollusca). Naturwissenschaften 96: 111–122.
• Chin, K., Eberth, D.A., Schweitzer, M.H., Rando, T.A., Sloboda, W.J., and Horne, J.R. 2003. Remarkable preservation of undigested muscle tissue within a Late Cretaceous tyrannosaurid coprolite from Alberta, Canada. Palaios 18: 286–294.
• De Paula, S.M. and Silveira, M. 2009. Studies on molluscan shells: Contributions from microscopic and analytical methods. Micron 40: 669–690.
• Dong, X.P., Donoghue, P.C.J., Cheng, H., and Liu, J.B. 2004. Fossil embryos from the Middle and Late Cambrian period of Hunan, South China. Nature 427: 237–240.
• Dornbos, S.Q. 2011. Phosphatization through the Phanerozoic. In: P.A. Allison and D.J. Bottjer (eds.), Taphonomy: Process and Bias Through Time. Topics in Geobiology 32: 435–456.
• Drygant, D.M. and Szaniawski, H. 2012. Lochkovian conodonts from Podolia, Ukraine, and their stratigraphic significance. Acta Palaeontologica Polonica 57: 833–861.
• Ehrlich, H., Koutsoukos, P.G., Demadis, K.D., and Pokrovsky, O.S. 2008. Principles of demineralization: Modern strategies for the isolation of organic frameworks. Part I. Common definitions and history. Micron 39: 1062–1091.
• Ehrlich, H., Koutsoukos, P.G., Demadis, K.D., and Pokrovsky, O.S. 2009. Principles of demineralization: Modern strategies for the isolation of organic frameworks. Part II. Decalcification. Micron 40: 169–193.
• Feng, W. and Sun, W. 2003. Phosphate replicated and replaced microstructure of molluscan shells from the earliest Cambrian of China. Acta Palaeontologica Polonica 48: 21–30.
• Filipiak, P., Zatoń, M., Szaniawski, H., Wrona, R., and Racki, G. 2012. Palynology and microfacies of Lower Devonian mixed carbonate-siliciclastic deposits in Podolia, Ukraine. Acta Palaeontologica Polonica 57: 863–877.
• Garcia−Pichel, F. 2006. Plausible mechanisms for the boring on carbonates by microbial phototrophs. Sedimentary Geology 185: 205–213.
• Garcia−Pichel, F., Ramirez−Reinat, E., and Gao, Q. 2010. Microbial excavation of solid carbonates powered by P−type ATPase−mediated transcellular Ca2+ transport. PNAS 107 (50): 21749–21754.
• Gatrall, M. and Golubic, S. 1970. Comparative study on some Jurassic and Recent endolithic fungi using scanning electron microscope. In: T.P. Crimes and J.C. Harper (eds.), Trace Fossils. Geological Journal (Special Issue) 3: 167–178.
• Glaub, I. 1994. Mikrobohrspuren in ausgewählten Ablagerungsräumen des europäischen Jura und der Unterkreide (Klassifikation und Palökologie). Courier Forschungsinstitut Senckenberg 174: 1–324.
• Golubic, S. 1969. Distribution, taxonomy, and boring patterns of marine endolithic algae. American Zoologist 9: 747–751.
• Golubic, S. and Radtke, G. 2008. The trace Rhopalia clavigera isp. n. reflects the development of its maker Eugomontia sacculata Kornmann, 1960. In: M. Wisshak and L. Tapanila (eds.), Current Developments in Bioerosion. Erlangen Conference Series 15: 95–108.
• Golubic, S., Brent, G., and Le Campion, T. 1970. Scanning electron microscopy of endolithic algae and fungi using a multipurpose casting−embedding technique. Lethaia 3: 203–209.
• Golubic, S., Friedmann, I., and Schneider, J. 1981. The lithobiontic ecological niche, with special reference to microorganisms. Journal of Sedimentary Petrology 51: 475–478.
• Golubic, S., Perkins, R.D., and Lukas, K.J. 1975. Boring microorganisms and microborings in carbonate substrates.In: R.W. Frey (ed.), The Study of Trace Fossils, 229–259. Springer−Verlag, New York.
• Golubic, S., Radtke, G., and Le Campion−Alsumard, T. 2005. Endolithic fungi in marine ecosystems. Trends in Microbiology 13: 229–235.
• Hayward, P.J. 1985. Ctenostome Bryozoans. Synopses of the British Fauna (New Series) 33: 1–169.
• Hendy, A.J.W. 2011. Taphonomic overprints on Phanerozoic trends in biodiversity: lithification and other secular megabiases. In: P.A. Allison and D.J. Bottjer (eds.), Taphonomy: Process and Bias Through Time. Second Edition. Topics in Geobiology 32: 19–77.
• Hof, C.H.J. and Briggs, D.E.G. 1997. Decay and mineralization of mantis shrimps (Stomatopoda: Crustacea)—A key to their fossil record. Palaios 12: 420–438.
• Klug, C., Hagdorn, H., and Montenari, M. 2005. Phosphatized soft−tissue in Triassic bivalves. Palaeontology 48: 833–852.
• Kobluk, D.R. and Risk, M.J. 1977. Calcification of exposed filaments of endolithic algae, micrite envelope formation and sediment production. Journal of Sedimentary Petrology 47: 517–528.
• Kouchinsky, A. 1999. Shell microstructures of the Early Cambrian Anabarella and Watsonella as new evidence on the origin of the Rostroconchia. Lethaia 32: 173–180.
• Kouchinsky, A. 2000. Shell microstructures in Early Cambrian molluscs. Acta Palaeontologica Polonica 45: 119–150.
• Kozłowski, W. 2003. Age, sedimentary environment and palaeogeographical position of the Late Silurian oolitic beds in the Holy Cross Mountains (Central Poland). Acta Geologica Polonica 53: 341–357.
• Małkowski, K., Racki, G., Drygant, D., and Szaniawski, H. 2009. Carbon isotope stratigraphy across the Silurian–Devonian transition in Podolia, Ukraine: evidence for a global biogeochemical perturbation. Geological Magazine 146: 652–674.
• Mao Che, L., Le Campion−Alsumard, T., Boury−Esnault, N., Payri, C., Golubic, S., and Bézac, C. 1996. Biodegradation of shells of the black pearl oyster, Pinctada margaritifera var. cumingii, by microborers and sponges of French Polynesia. Marine Biology 126: 509–519.
• Marcus, E. 1938. Bryozoarios perfuradores de conchas. Arquivos do Instituto Biológico 9: 273–296.
• Mass, A., Waloszek, D., and Müller, K.J. 2003. Morphology, ontogeny and phylogeny of the Phosphatocopina (Crustacea) from the Upper Cambrian ‘Orsten’ of Sweden. Fossils and Strata 49: 1–238.
• Mass, A., Braun, A., Dong, X.P., Donoghue, P.C.J., Müller, K.J., Olempska, E., Repetski, J.E., Siveter, D.J., Stein, M., and Waloszek, D. 2006. The “Orsten”—More than a Cambrian Konservat−Lagerstätte yielding exceptional preservation. Palaeoworld 15: 266–282.
• Mayoral, E. 1988. Pennatichnus nov. icnogen,; Pinaceocladichnus nov. icnogen., e Iramena. Huellas de bioerosión debidas a Bryozoa perforantes (Ctenostomata, Plioceno inferior) en la Cuenca del Bajo Guadalquvir. Revista Española de Paleontología 3: 13–22.
• Mayoral, E. 1991. Actividad bioerosiva de Briozoos Ctenostomados en el Ordovícico Superior de la zona cantábrica del Macizo Hespérico (Cabo Vidrias, Oviedo). Revista Española de Paleontología 6: 27–36.
• McKinney, F.K. 2008. Ctenostomata. AccessScience, McGraw−Hill Companies, http://www.accessscience.com.
• McKinney, M.J. and Dewel, R.A. 2002. The ctenostome collar—an enigmatic structure. In: P.N. Wyse Jackson, C.J. Buttler, and M.E. Spencer Jones (eds.), Bryozoan Studies 2001, 191–197. Swets & Zeitlinger, Lisse.
• Mukai, H., Terakado, K., and Reed, C. 1997. Bryozoa. In: F.W. Harrison (ed.), Microscopic Anatomy of Invertebrates, Vol. 13, Lophophorates, Entoprocta and Cycliophora, 45–206. Wiley−Liss, New York.
• Mutvei, H. 1983. Flexible nacre in the nautiloid Isorthoceras, with remarks on the evolution of cephalopod nacre. Lethaia 16: 233–240.
• Nikiforova, O.I., Predtechensky, N.N. [Predtečenskij, N.N.], Abushik, A.F. [Abušik, A.F.], Ignatovich, M.M. [Ignatovič, M.M.], Modzalevskaya, T.L. [Modzalevskaâ, T.L.], Berger, A.Y. [Berger, A.Â], Novoselova, L.S., and Burkov, Y.K. [Burkov, Û.K.] 1972. Opornyj razrez Silura i nižnego Devona Podolii. 258 pp. Izdatielstvo Nauka, Leningrad.
• Olempska, E., Horne, D.J., and Szaniawski, H. 2012. First record of preserved soft parts in a Palaeozoic podocopid (Metacopina) ostracod, Cytherellina submagna: phylogenetic implications. Proceedings of the Royal Society B 279: 564–570.
• Palmer, T.J., Taylor, P.D., and Todd, J.A. 1993. Epibiont shadowing: a hitherto unrecognized way of preserving soft−bodied fossils. Terra Nova 5: 568–572.
• Pohowsky, R.A. 1974. Notes on the study and nomenclature of boring Bryozoa. Journal of Paleontology 48: 556–564.
• Pohowsky, R.A. 1978. The boring ctenostomate Bryozoa: taxonomy and paleobiology based on cavities in calcareous substrata. Bulletins of American Paleontology 73 (301): 1–192.
• Porter, S.M. 2004. Closing the phosphatization window: testing for the influence of taphonomic megabias on the pattern of small shelly fossil decline. Palaios 19: 178–193.
• Prenant, M. and Bobin, G. 1956. Bryozoaires, Premiére Partie. Entoproctes, Phylactolémes, Cténostomes. Faune de France 60: 1–398.
• Priess, K., Le Campion−Alsumard, T., Golubic, S., Gadel, F., and Thomassin, B.A. 2000. Fungi in corals: black bands and density−banding of Porites lutea and P. lobata skeleton. Marine Biology 136: 19–27.
• Racki, G., Baliński, A., Wrona, R., Małkowski, K., Drygant, D., and Szaniawski, H. 2012. Faunal dynamics across the Silurian–Devonian positive isotope excursions (δ13C, δ18O) in Podolia, Ukraine: Comparative analysis of the Ireviken and Klonk events. Acta Palaeontologica Polonica 57: 795–832.
• Radtke, G. 1991. Die mikroendolithischen Spurenfossilien im Alt−Tertiär West−Europas und ihre palökologische Bedeutung. Courier Forschungsinstitut Senckenberg 138: 1–185.
• Radtke, G. and Golubic, S. 2005. Microborings in mollusk shells, Bay of Safaga, Egypt: Morphometry and ichnology. Facies 51: 125–141.
• Rogick, M.D. 1945. Studies on marine Bryozoa. I. Aeverrillia setigera (Hincks) 1887. Biological Bulletin 89: 201–214.
• Rosso, A. 2008. Leptichnus tortus isp. nov., a new cheilostome etching and comments on other bryozoan−produced trace fossils. Studi Trentini di Scienze Naturali: Acta Geologica 83: 75–85.
• Runnegar, B. 1985. Shell microstructures of Cambrian molluscs replicated by phosphate. Alcheringia 9: 245–257.
• Schmahl, W.W., Griesshaber, E., Merkel, C., Kelm, K., Deuschle, J., Neuser, R.D., Göetz, A.J., Sehrbrock, A., and Mader, W. 2008. Hierarchical fibre composite structure and micromechanical properties of phosphatic and calcitic brachiopod shell biomaterials—an overview. Mineralogical Magazine 72: 541–562.
• Schneider, J. and Le CampionAlsumard, T. 1999. Construction and destruction of carbonates by marine and freshwater cyanobacteria. European Journal of Phycology 34: 417–426.
• Schneider, J. and Torunski, H. 1983. Biokarst on limestone coasts, morphogenesis and sediment production. Marine Ecology 4: 45–63.
• Schwaha, T., Wood, T.S., and Wanninger, A. 2011. Myoanatomy and serotonergic nervous system of the ctenostome Hislopia malayensis: Evolutionary trends in bodyplan patterning of Ectoprocta. Frontiers in Zoology 8: 1–37.
• Silén, L. 1946. On two new groups of Bryozoa living in shells of molluscs. Arkiv för Zoologi 38B: 1–7.
• Silén , L. 1947. On the anatomy and biology of Penetrantiidae and Immergentiidae (Bryozoa). Arkiv för Zoologi 40A: 1–48.
• Soule, J.D. and Soule, D.F. 1969. Systematics and biogeography of burrowing bryozoans. American Zoologist 9: 791–802.
• Taylor, P.D. 1990a. Bioimmured ctenostomes from the Jurassic and the origin of the cheilostome Bryozoa. Palaeontology 33: 19–34.
• Taylor, P.D. 1990b. Preservation of soft−bodied and other organisms by bioimmuration—a review. Palaeontology 33: 1–17.
• Taylor, P.D. and Ernst, A. 2004. Bryozoans. In: B.D. Webby, F. Paris, M.L. Droser, and I.G. Percival (eds.), The Great Ordovician Biodiversification Event, 147–156. Columbia University Press, New York.
• Taylor, P.D. and Ernst, A. 2008. Bryozoans in transition: The depauperate and patchy Jurassic biota. Palaeogeography, Palaeoclimatology, Palaeoecology 263: 9–23.
• Taylor, P.D. and Todd, J.A. 2001. Bioimmuration. In: D.E.G. Briggs and P.R. Crowther (eds.), Palaeobiology II, 285–289. Blackwell Science, Oxford.
• Todd, J.A. 1993. The bivalve shell as a preservation trap, as illustrated by the Late Jurassic gryphaeid, Deltoideum delta (Smith). Scripta Geologica, Special Issue 2: 417–433.
• Todd, J.A. 1994. The role of bioimmuration in the exceptional preservation of fossil ctenostomates, including a new Jurassic species of Buskia. In: P.J. Hayward, J.S. Ryland, and P.D. Taylor (eds.), Biology and Paleobiology of Bryozoans, 187–192. Olsen and Olsen, Fredenborg.
• Todd, J.A. 1996. Buskia fowleri sp. nov.—a bioimmured ctenostome bryozoan from the Middle Eocene of southern England. Tertiary Research 16: 213–222.
• Todd, J.A. 2000. The central role of ctenostomes in bryozoans phylogeny. In: A. Herrera Cubilla and J.B.C. Jackson (eds.), Proceedings of the 11th International Association Conference, 104–135. Smithsonian Tropical Research Institute, Balboa.
• Tribollet, A. 2008. The boring microflora in modern coral reef ecosystems: a review of its roles. In: M. Wisshak and L. Tapanila (eds.), Current Developments in Bioerosion, 67–94. Springer−Verlag, Berlin.
• Tribollet, T., Decherf, G., Hutchings, P.A., and Peyrot−Clausade, M. 2002. Large−scale spatial variability in bioerosion of experimental coral substrates on the Great Barrier Reef (Australia): importance of microborers. Coral Reefs 21: 424–432.
• Trinajstic, K., Marshall, C., Long, J., and Bifield, K. 2007. Exceptional preservation of nerve and muscle tissues in Late Devonian placoderm fish and their evolutionary implications. Biology Letters 3: 197–200.
• Vendrasco, M.J., Checa, A.G., and Kouchinsky, A.V. 2011. Shell microstructure of the early bivalve Pojetaia and the independent origin of nacre within the Mollusca. Palaeontology 54: 825–850.
• Vendrasco, M.J., Porter, S.M., Kouchinsky, A., Li, G., and Fernandez, C.Z. 2010. New data on molluscs and their shell microstructures from the Middle Cambrian Gowers Formation, Australia. Palaeontology 53: 97–135.
• Viskova, L.A. and Pakhnevich, A.V. 2010. A new boring bryozoan from the Middle Jurassic of the Moskow region and its micro−CT research. Paleontological Journal 44: 157–167.
• Vogel, K., Golubic, S., and Brett, C.E. 1987. Endolith associations and their relation to facies distribution in the Middle Devonian of New York State, U.S.A. Lethaia 20: 263–290.
• Voichyshyn, V. 2011. The Early Devonian armoured agnathans of Podolia, Ukraine. Palaeontologia Polonica 66: 1–211.
• Voichyshyn, V. and Szaniawski, H. 2012. Acanthodian jaw bones from Lower Devonian marine deposits of Podolia, Ukraine. Acta Palaeontologica Polonica 57: 879–896.
• Voigt, E. and Soule, J.D. 1973. Cretaceous burrowing bryozoans. Journal of Paleontology 47: 21–33.
• Walossek, D. 1993. The Upper Cambrian Rehbachiella kinnekullensis and the phylogeny of Branchiopoda and Crustacea. Fossils and Strata 32: 1–202.
• Weitschat, W. 1995. Ostracoden (O. Myodocopida) mit Weichkörper−Erhaltung aus der Unter−Trias von Spitzbergen. Paläontologische Zeitschrift 57: 309–323.
• Williams, A., Carlson, S.J., and Brunton, C.H.C. 2000. Brachiopod classification. In: A. Williams, C.H.C. Brunton, and S.J., Carlson (eds.), Treatise on Invertebrate Paleontology, Part H, Brachiopoda (revised) vol. 2, 1–27. Geological Society of America, The University of Kansas Press, Lawrence.
• Wilson, M.A. and Palmer, T.J. 2006. Patterns and processes in the Ordovician bioerosion revolution. Ichnos 13: 109–112.
• Wisshak, M., Gektidis, M., Freiwald, A., and Lundälv, T. 2005. Bioerosion along a bathymetric gradient in a cold−temperate setting (Kosterfjord, SW Sweden): an experimental study. Facies 51: 99–123.
• Wisshak, M., Tribollet, A., Golubic, S., Jakobsen, J., and Freiwald, A. 2011. Temperate bioerosion: ichnodiversity and biodiversity from intertidal to bathyal depths (Azores). Geobiology 9: 492–520.