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First report of fossil “keratose” demosponges in Phanerozoic carbonates: preservation and 3-D reconstruction

Naturwissenschaften volume 101, pages 467–477 (2014)Cite this article

Abstract

Fossil record of Phanerozoic non-spicular sponges, beside of being important with respect to the lineage evolution per se, could provide valuable references for the investigation of Precambrian ancestral animal fossils. However, although modern phylogenomic studies resolve non-spicular demosponges as the sister group of the remaining spiculate demosponges, the fossil record of the former is extremely sparse or unexplored compared to that of the latter; the Middle Cambrian Vauxiidae Walcott 1920, is the only confirmed fossil taxon of non-spicular demosponges. Here, we describe carbonate materials from Devonian (Upper Givetian to Lower Frasnian) bioherms of northern France and Triassic (Anisian) microbialites of Poland that most likely represent fossil remnants of keratose demosponges. These putative fossils of keratose demosponges are preserved as automicritic clumps. They are morphologically distinguishable from microbial fabrics but similar to other spiculate sponge fossils, except that the skeletal elements consist of fibrous networks instead of assembled spicules. Consistent with the immunological behavior of sponges, these fibrous skeletons often form a rim at the edge of the automicritic aggregate, separating the inner part of the aggregate from foreign objects. To confirm the architecture of these fibrous networks, two fossil specimens and a modern thorectid sponge for comparison were processed for three-dimensional (3-D) reconstruction using serial grinding tomography. The resulting fossil reconstructions are three-dimensionally anastomosing, like modern keratose demosponges, but their irregular and nonhierarchical meshes indicate a likely verongid affinity, although a precise taxonomic conclusion cannot be made based on the skeletal architecture alone. This study is a preliminary effort, but an important start to identify fossil non-spicular demosponges in carbonates and to re-evaluate their fossilization potential.

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References

  • Adachi N, Ezaki Y, Pickett JW (2007) Interrelations between framework-building and encrusting skeletal organisms and microbes: more refined growth history of Lower Devonian bindstones. Sedimentology 54:89–105. doi:10.1111/j.1365-3091.2006.00831.x

    Article  Google Scholar 

  • Arp G, Reimer A, Reitner J (2001) Photosynthesis-Induced biofilm calcification and calcium concentrations in Phanerozoic oceans. Science 292(5522):1701–1704. doi:10.1126/science.1057204

    Article  CAS  PubMed  Google Scholar 

  • Bavestrello G, Cattaneo-Vietti R, Cerrano C, Sarà M (1996) Spicule dissolution in living Tethya omanensis (Porifera: Demospongiae) from a tropical cave. Bull Mar Sci 58(2):598–601

    Google Scholar 

  • Bergquist PR, Cook SC (2002) Family Dictyodendrillidae Bergquist, 1980. In: Hooper JNA, Van Soest RWM (eds) Systema Porifera: a guide to the classification of sponges. Kluwer Academic/Plenum, New York, pp 1072–1076

    Chapter  Google Scholar 

  • Borchiellini C, Chombard C, Manuel M, Alivon E, Vacelet J, Boury-Esnault N (2004) Molecular phylogeny of Demospongiae: implications for classification and scenarios of character evolution. Mol Phylogenet Evol 32(3):823–837. doi:10.1016/j.ympev.2004.02.021

    Article  CAS  PubMed  Google Scholar 

  • Boury-Esnault N, Rützler K (eds) (1997) Thesaurus of sponge morphology. Smithsonian Contributions to Zoology Number 596. Smithsonian Institution, Washington, D.C

    Google Scholar 

  • Bowerbank JS (1864) A monograph of the British Spongiidae, vol. 1. Robert Hardwicke, London

    Google Scholar 

  • Brachert TC (1991) Environmental control on fossilization of siliceous sponge assemblages: a proposal. In: Keupp H, Reitner J (eds) Fossil and Recent Sponges. Springer, Berlin, pp 543–553. doi:10.1007/978-3-642-75656-6_45

    Chapter  Google Scholar 

  • Brice D (2003) Brachiopod assemblages in the Devonian of Ferques (Boulonnais, France). Relations to palaeoenvironments and global eustatic curves. Bull Geosci 78:405–417

    Google Scholar 

  • Brice D, Colbeaux JP (1976) Serie Devonienne du massif de Ferques s.s. tectonique du massif primaire du Bas-Boulonnais. Guide Géologique Reunion Spécialisée de la Service Géologique National, Orléans, pp 3–30

    Google Scholar 

  • Butterfield NJ (1990) Organic preservation of non-mineralizing organisms and the taphonomy of the Burgess Shale. Paleobiology 16(3):272–286

    Google Scholar 

  • Cárdenas P, Pérez T, Boury-Esnault N (2012) Chapter two - sponge systematics facing new challenges. In: Becerro MA, Uriz MJ, Maldonado M, Turon X (eds) Advances in marine biology, vol 61. Academic Press, London, pp 79–209. doi:10.1016/B978-0-12-387787-1.00010-6

    Google Scholar 

  • Edgcomb VP, Beaudoin D, Gast R, Biddle JF, Teske A (2011) Marine subsurface eukaryotes: the fungal majority. Environ Microbiol 13(1):172–183. doi:10.1111/j.1462-2920.2010.02318.x

    Article  CAS  PubMed  Google Scholar 

  • Ehrlich H, Maldonado M, Spindler KD, Eckert C, Hanke T, Born R, Goebel C, Simon P, Heinemann S, Worch H (2007) First evidence of chitin as a component of the skeletal fibers of marine sponges. Part I. Verongidae (Demospongia: Porifera). J Exp Zool B Mol Dev Evol 308(4):347–356

    Article  PubMed  Google Scholar 

  • Ehrlich H, Ilan M, Maldonado M, Muricy G, Bavestrello G, Kljajic Z, Carballo JL, Schiaparelli S, Ereskovsky A, Schupp P, Born R, Worch H, Bazhenov VV, Kurek D, Varlamov V, Vyalikh D, Kummer K, Sivkov VV, Molodtsov SL, Meissner H, Richter G, Steck E, Richter W, Hunoldt S, Kammer M, Paasch S, Krasokhin V, Patzke G, Brunner E (2010) Three-dimensional chitin-based scaffolds from Verongida sponges (Demospongiae: Porifera). Part I. Isolation and identification of chitin. Int J Biol Macromol 47(2):132–140. doi:10.1016/j.ijbiomac.2010.05.007

    Article  CAS  PubMed  Google Scholar 

  • Ehrlich H, Rigby JK, Botting JP, Tsurkan MV, Werner C, Schwille P, Petrášek Z, Pisera A, Simon P, Sivkov VN, Vyalikh DV, Molodtsov SL, Kurek D, Kammer M, Hunoldt S, Born R, Stawski D, Steinhof A, Bazhenov VV, Geisler T (2013) Discovery of 505-million-year old chitin in the basal demosponge Vauxia gracilenta. Sci Rep 3:3497. doi:10.1038/srep03497

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Erpenbeck D, Sutcliffe P, Cook SC, Dietzel A, Maldonado M, van Soest RWM, Hooper JNA, Wörheide G (2012) Horny sponges and their affairs: on the phylogenetic relationships of keratose sponges. Mol Phylogenet Evol 63(3):809–816. doi:10.1016/j.ympev.2012.02.024

    Article  PubMed  Google Scholar 

  • Erwin DH, Laflamme M, Tweedt SM, Sperling EA, Pisani D, Peterson KJ (2011) The Cambrian Conundrum: early divergence and later ecological success in the early history of animals. Science 334(6059):1091–1097. doi:10.1126/science.1206375

    Article  CAS  PubMed  Google Scholar 

  • Feng Q, Gong YM, Riding R (2010) Mid-Late Devonian calcified marine algae and Cyanobacteria, South China. J Paleontol 84:569–587

    Article  Google Scholar 

  • Fritz GK (1958) Schwammstotzen, Tuberoide und Schuttbreccien im Weißen Jura der Schwäbischen Alb. Arbeiten des Geologisch-Paläontologischen Instituts TH Stuttgart, NF 13: 1-118

  • Gaino E, Pronzato R (1989) Ultrastructural evidence of bacterial damage to Spongia officinalis fibers (Porifera, Demospongiae). Dis Aquat Org 6:67–74

    Article  Google Scholar 

  • Grant RE (1861) Tabular view of the primary divisions of the Animal Kingdom. Walton and Maberly, London

    Google Scholar 

  • Gross J, Sokal Z, Rougvie M (1956) Structural and chemical studies on the connective tissue of marine sponges. J Histochem Cytochem 4(3):227–246. doi:10.1177/4.3.227

    Article  CAS  PubMed  Google Scholar 

  • Hoffmann F, Rapp HT, Pape T, Peters H, Reitner J (2004) Sedimentary inclusions in the deep-water sponge Geodia barretti (Geodiidae, Demospongiae) from the Korsfjord, western Norway. Sarsia 89(4):245–252. doi:10.1080/00364820410002451

    Article  Google Scholar 

  • Hooper JNA (2003) Sponguide: Guide to sponge collection and identification. Queensland Museum, South Brisbane, pp 1-26. http://www.qmuseum.qld.gov.au/~/media/Documents/Findoutabout/AnimalsofQueensland/Sealife/sponguide-2003.pdf. Accessed 9 Dec 2013

  • Hooper JNA, van Soest RWM (eds) (2002) Systema Porifera: a guide to the classification of sponges. Kluwer Academic/Plenum, New York

    Google Scholar 

  • Hühne C (2005) Geochemie Porifera-reicher Mud Mounds und Mikrobialithe des Mittel- und Oberdevons (Westaustralien, Nordfrankreich). Unpublished dissertation, University of Göttingen

  • Junqua S, Robert L, Garrone R, Pavans de Ceccatty M, Vacelet J (1974) Biochemical and morphological studies on collagens of horny sponges. Ircinia filaments compared to spongins. Connect Tissue Res 2(3):193–203

    Article  CAS  PubMed  Google Scholar 

  • Kiel S, Götz S, Pascual-Cebrian E, Hennhöfer DK (2012) Fossilized digestive systems in 23 million-year-old wood-boring bivalves. J Molluscan Stud 78(4):349–356. doi:10.1093/mollus/eys021

    Article  Google Scholar 

  • Land LS (1976) Early dissolution of sponge spicules from reef sediments, North Jamaica. J Sediment Res 46(4):967–969. doi:10.1306/212f70a4-2b24-11d7-8648000102c1865d

    Google Scholar 

  • Lang B (1991) Baffling, binding, or debris accumulation? Ecology of Upper Jurassic sponge-bacterial buildups (Oxfordian, Franconian Alb, Southern Germany). In: Keupp H, Reitner J (eds) Fossil and recent sponges. Springer, Berlin, pp 516–521. doi:10.1007/978-3-642-75656-6_43

    Chapter  Google Scholar 

  • Laschet C (1984) On the origin of cherts. Facies 10:257–290

    Article  Google Scholar 

  • Lavrov DV, Wang X, Kelly M (2008) Reconstructing ordinal relationships in the Demospongiae using mitochondrial genomic data. Mol Phylogenet Evol 49(1):111–124. doi:10.1016/j.ympev.2008.05.014

    Article  CAS  PubMed  Google Scholar 

  • Levi C (1957) Ontogeny and systematics in sponges. Syst Biol 6(4):174–183. doi:10.2307/sysbio/6.4.174

    Article  Google Scholar 

  • Love GD, Grosjean E, Stalvies C, Fike DA, Grotzinger JP, Bradley AS, Kelly AE, Bhatia M, Meredith W, Snape CE, Bowring SA, Condon DJ, Summons RE (2009) Fossil steroids record the appearance of Demospongiae during the Cryogenian period. Nature 457(7230):718–721. doi:10.1038/nature07673

    Article  CAS  PubMed  Google Scholar 

  • Minchin EA (1900) Chapter III. Sponges. In: Lankester ER (ed) A treatise on zoology. Part II. The Porifera and Coelenterata. Adam & Charles Black, London, pp 1–178

    Google Scholar 

  • Mistiaen B, Poncet J (1983) Evolution sédimentologique des petits biohermes a Stromatolithes et Vers dans le Givétien de Ferques (Boulonnais). Ann Soc Géol Nord 102(4):205–216

    Google Scholar 

  • Müller WEG, Müller IM (2003) Origin of the Metazoan immune system: identification of the molecules and their functions in sponges. Integr Comp Biol 43(2):281–292. doi:10.1093/icb/43.2.281

    Article  PubMed  Google Scholar 

  • Myszkowska J (1992) Lithofacies and sedimentation of Diplopora Dolomite (Middle Muschelkalk) in the east part of the Cracovian-Silesian region. Ann Soc Geol Pol 62:19–62

    Google Scholar 

  • Neuweiler F, Burdige DJ (2005) The modern calcifying sponge Spheciospongia vesparium (Lamarck, 1815), Great Bahama Bank: implications for ancient sponge mud-mounds. Sediment Geol 175(1–4):89–98. doi:10.1016/j.sedgeo.2004.12.021

    Article  CAS  Google Scholar 

  • Neuweiler F, Daoust I, Bourque P-A, Burdige DJ (2007) Degradative calcification of a modern siliceous sponge from the Great Bahama Bank, the Bahamas: a guide for interpretation of ancient sponge-bearing limestones. J Sediment Res 77(7):552–563. doi:10.2110/jsr.2007.058

    Article  CAS  Google Scholar 

  • Pascual-Cebrian E, Hennhöfer DK, Götz S (2013) High resolution and true colour grinding tomography of rudist bivalves, exemplified with the taxonomic revision of Mathesia darderi (Astre). Caribb J Earth Sci 45:35–46

    Google Scholar 

  • Peterson KJ, Cotton JA, Gehling JG, Pisani D (2008) The Ediacaran emergence of bilaterians: congruence between the genetic and the geological fossil records. Philos Trans R Soc B Biol Sci 363:1435–1443

    Article  Google Scholar 

  • Pisera A (2002) Fossil ‘Lithistids’: an overview. In: Hooper JNA, van Soest RWM (eds) Systema Porifera: a guide to the classification of sponges. Kluwer Academic/Plenum, New York, pp 388–402

    Chapter  Google Scholar 

  • Poulicek M, Jeuniaux C (1991) Chitin biodegradation in marine environments: an experimental approach. Biochem Syst Ecol 19(5):385–394. doi:10.1016/0305-1978(91)90055-5

    Article  CAS  Google Scholar 

  • Reitner J (1993) Modern cryptic microbial/metazoan facies from Lizard Island (Great Barrier Reef, Australia): formation and concepts. Facies 29:3–40

    Article  Google Scholar 

  • Reitner J, Schumann-Kindel G (1997) Pyrite in mineralized sponge tissue - product of sulfate reducing sponge-related bacteria? Facies 36:272–276

    Google Scholar 

  • Reitner J, Wörheide G (2002) Non-lithistid fossil Demospongiae - origins of their palaeobiodiversity and highlights in history of preservation. In: Hooper JNA, van Soest RWM (eds) Systema Porifera: a guide to the classification of sponges. Kluwer Academic/Plenum, New York, pp 52–68

    Chapter  Google Scholar 

  • Reitner J, Gautret P, Marin F, Neuweiler F (1995) Automicrites in a modern marine microbialite: formation model via organic matrices (Lizard Island, Great Barrier Reef, Australia). Bull Inst Oéanogr Monaco 14(2):237–263

    Google Scholar 

  • Reitner J, Hühne C, Thiel V (2001) Porifera-rich mud mounds and microbialites as indicators of environmental changes within the Devonian/Lower Carboniferous critical interval. Terra Nostra 4:60–65

    Google Scholar 

  • Reitner J, Luo C, Duda JP (2012) Early sponge remains from the Neoproterozoic-Cambrian phosphate deposits of the Fontanarejo area (Central Spain). Proceedings of the 17th Field Conference of the Cambrian Stage Subdivision Working Group, International Subcommission on Cambrian Stratigraphy & Celebration of the 30th Anniversary of the Discovery of the Kaili Biota. Guizhou. J Guizhou Univ (Nat Sci) 29 (Sup. 1): 184-186

  • Rigby JK (1986) Sponges of the Burgess Shale (Middle Cambrian), British Columbia. Palaeontogr Can 2:1–105

    Google Scholar 

  • Rigby JK, Collins D (2004) Sponges of the Middle Cambrian Burgess Shale and Stephen Formations, British Columbia. ROM Contrib Sci 1:1–155

    Google Scholar 

  • Schumann G, Manz W, Reitner J, Lustrino M (2004) Ancient fungal life in North Pacific Eocene oceanic crust. Geomicrobiol J 21:241–246

    Article  Google Scholar 

  • Shu D, Isozaki Y, Zhang X, Han J, Maruyama S (2014) Birth and early evolution of metazoans. Gondwana Res 25(3):884–895. doi:10.1016/j.gr.2013.09.001

    Article  Google Scholar 

  • Sollas WJ (1904) A method for the investigation of fossils by serial sections. Philos Trans R Soc Lond Ser B 196(214–224):259–265. doi:10.1098/rstb.1904.0008

    Article  Google Scholar 

  • Sperling EA, Peterson KJ, Pisani D (2009) Phylogenetic-signal dissection of nuclear housekeeping genes supports the paraphyly of sponges and the monophyly of Eumetazoa. Mol Biol Evol 26(10):2261–2274. doi:10.1093/molbev/msp148

    Article  CAS  PubMed  Google Scholar 

  • Steiner M, Mehl D, Reitner J, Erdtmann B-D (1993) Oldest entirely preserved sponges and other fossils from the lowermost Cambrian and a new facies reconstruction of the Yangtze Platform (China). Berl Geowiss Abh E 9:293–329

    Google Scholar 

  • Sutton MD (2008) Tomographic techniques for the study of exceptionally preserved fossils. Proc R Soc B Biol Sci 275(1643):1587–1593. doi:10.1098/rspb.2008.0263

    Article  Google Scholar 

  • Szulc J (1997a) Middle Triassic (Muschelkalk) sponge-microbial stromatolites, diplopores and Girvanella-oncoids from the Silesian Cracow Upland. In: 3rd IFAA Regional Symposium and IGCP 380 International Meeting, Guidebook. Cracow, pp 10-15

  • Szulc J (1997b) Stop 3 Libiąż, active dolomite quarry, Cracow Upland. In: 3rd IFAA Regional Symposium & IGCP 380 International Meeting, Guidebook. Cracow, pp 42-43

  • Walcott CD (1920) Cambrian geology and paleontology IV, No.6 Middle Cambrian Spongiae. Smithson Misc Collect 67(6):261–364

    Google Scholar 

  • Warnke K (1995) Calcification processes of siliceous sponges in Viséan Limestones (Counties Sligo and Leitrim, Northwestern Ireland). Facies 33(1):215–227. doi:10.1007/bf02537453

    Article  Google Scholar 

  • Wood RA (2011) Paleoecology of the earliest skeletal metazoan communities: implications for early biomineralization. Earth Sci Rev 106(1–2):184–190. doi:10.1016/j.earscirev.2011.01.011

    Article  CAS  Google Scholar 

  • Wörheide G, Dohrmann M, Erpenbeck D, Larroux C, Maldonado M, Voigt O, Borchiellini C, Lavrov DV (2012) Chapter One - Deep Phylogeny and evolution of sponges (Phylum Porifera). In: Becerro MA, Uriz MJ, Maldonado M, Turon X (eds) Advances in marine biology, vol 61. Academic Press, London, pp 1–78. doi:10.1016/B978-0-12-387787-1.00010-6

  • Wu W, Yang AH, Janussen D, Steiner M, Zhu MY (2005) Hexactinellid sponges from the Early Cambrian black shale of South Anhui, China. J Paleontol 79(6):1043–1051

    Article  Google Scholar 

  • Xiao SH, Hu H, Yuan XL, Parsley RL, Cao R (2005) Articulated sponges from the Lower Cambrian Hetang Formation in southern Anhui, South China: their age and implications for the early evolution of sponges. Palaeogeogr Palaeoclimatol Palaeoecol 220(1–2):89–117. doi:10.1016/j.palaeo.2002.02.001

    Article  Google Scholar 

  • Yang B, Zhang L, Danelian T, Feng Q, Steiner M (2014) Chert-hosted small shelly fossils: expanded tool of biostratigraphy in the Early Cambrian. GFF 00 (1):1-6. doi:10.1080/11035897.2014.882977

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Acknowledgments

We thank Dr. Steffen Kiel (University of Göttingen) for his help and suggestions concerning the grinding tomography method and Axel Hackmann and Wolfgang Dröse for the laboratory support. The beneficial comments from Dr. Imran Rahman (University of Bristol) are also appreciated. This research was sponsored by the Excellence Initiative-DFG, Courant Research Centre of Geobiology, Göttingen. The China Scholarship Council (CSC) financially supported the doctoral studies of the first author at the University of Göttingen.

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  1. Department of Geobiology, Centre of Geosciences, University of Göttingen, Goldschmidtstraße 3, 37077, Göttingen, Germany

    Cui Luo & Joachim Reitner

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  1. Cui Luo
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Correspondence to Joachim Reitner.

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Communicated by: Sven Thatje

Electronic supplementary material

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Consecutively ground planes of Boul (Devonian) (MPG 5484 kb)

3-D reconstruction of sample Boul (Devonian) without manual interpretation. (MPG 21240 kb)

3-D reconstruction of a part of Boul (Devonian) with minimum interpretation. See Fig. 4c for the exact location of the reconstructed area (MPG 15792 kb)

3-D reconstruction of a part of Boul (Devonian) with moderate manual interpretation. See Fig. 4c for the exact location of the reconstructed area (MPG 16166 kb)

3-D reconstruction of a part of Boul (Devonian) with intensive manual interpretation. See Fig. 4c for the exact location of the reconstructed area (MPG 17214 kb)

Consecutively ground planes of Pol (Triassic) (MPG 2766 kb)

3-D reconstruction of sample Pol (Triassic) (MPG 15710 kb)

3-D reconstruction of a part of Pol (Triassic). See Fig. 4b for the exact location of the reconstructed area (MPG 13528 kb)

Supp. 3a

Consecutively ground planes of Au (thorectid Keratosa, Recent) (MPG 1110 kb)

3-D reconstruction of sample Au (thorectid Keratosa, Recent) (MPG 8758 kb)

Supp. 3c

3-D reconstruction of a part of Au. See Fig. 4a for the exact location of the reconstructed area (MPG 11474 kb)

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Luo, C., Reitner, J. First report of fossil “keratose” demosponges in Phanerozoic carbonates: preservation and 3-D reconstruction. Naturwissenschaften 101, 467–477 (2014). https://doi.org/10.1007/s00114-014-1176-0

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