Presumed postlarval pentacrinoids from the Lower DevonianHunsr€uck Slate, Germany

THOMAS W. KAMMER, CHRISTOPH BARTELS AND WILLIAM I. AUSICH

Kammer, T.W., Bartels, C., Ausich, W.I. 2015: Presumed postlarval pentacrinoidsfrom the lower Devonian Hunsr€uck Slate, Germany. Lethaia, DOI: 10.1111/let.12147.

Several tiny crinoids with crowns as small as 1 mm, or less, in width are newly recog-nized from the Hunsr€uck Slate of southwestern Germany. The presence of erect armsabove an amorphous calyx in some specimens can be inferred. Based on comparisonwith the size and gross morphology of developmental stages in living crinoids, thesetiny Hunsr€uck crinoids are judged to be at an early postlarval stage that is analogousto the pentacrinoid stage just after development from the stalked, but armless, smallercystidean larval stage found in both living comatulids and isocrinids. Some of thesetiny crinoids have a stalk up to 4 mm long attached to a now pyritized former sub-strate. Their clustered occurrence suggests gregarious settlement of larvae. Taxonomicidentification of these presumed pentacrinoids is not possible, even to the sub-classlevel, although they are preserved with larger juveniles of the cladids Propoteriocrinusand Lasiocrinus. These larger juveniles exhibit 3-D pyritized calcite plates, whereas theprobable pentacrinoids appear to be preserved as flattened, micro-crystalline pyritizeddermal tissues that enclosed lightly calcified, porous ossicles. The pentacrinoids werelikely buried within weeks or months of hatching, based on developmental stages insimilar-sized living crinoids. These tiny crinoids, presumably pentacrinoids, are a fur-ther example of the extraordinarily detailed preservation of delicate tissues in pyritefrom the Hunsr€uck Slate. They are most likely the pentacrinoid stage from one ormore of the crinoid taxa (30 genera) present in the Hunsr€uck Slate. Assuming theseare not microcrinoids, they are the first report of pentacrinoids from the fossil recordand document that a Palaeozoic sister group to modern crinoids had similar develop-mental stages. □ Crinoidea, Echinodermata, juveniles, postlarval, pyritization.

Thomas W. Kammer [tkammer@wvu.edu], Department of Geology and Geography, WestVirginia University, Morgantown 26506-6300 WV, USA; Christoph Bartels[Christoph.Bartels@bergbaumuseum.de], German Mining Museum, Am Bergbaumu-seum 28 D-44791 Bochum, Germany; William I. Ausich [ausich.1@osu.edu], School ofEarth Sciences, The Ohio State University, 155 South Oval Mall, Columbus 43210 OH,USA; manuscript received on 3/12/2014; manuscript accepted on 3/03/2015.

The Lower Devonian Hunsr€uck Slate, near theRhine Valley in western Germany, is well knownfor its high diversity of marine fossils exhibitingextraordinary preservation of both hard and softtissues by selective pyritization, including those ofechinoderms (Bartels et al. 1998; K€uhl et al. 2012).Recently, we reported the first known occurrenceof crinoid tube feet in the fossil record (Ausichet al. 2013) from the Hunsr€uck cladid Codiacrinus.We now report the discovery of tiny crinoids inthe Hunsr€uck Slate, judged to be early-stagepostlarval pentacrinoids (or equivalent to that stagein living articulate crinoids), preserved by pyritiza-tion of the dermal tissues that encased the ossiclesand early juveniles with pyritized plates. Thesemay be the earliest developmental stages of macro-crinoids known in the fossil record, assuming thatmicrocrinoids are in fact paedomorphic adults(Sevastopulo 2008). These Hunsr€uck specimens arecertainly the smallest fossil crinoids known withcrowns attached to their stems.

Methods, materials and geologicalsetting

These tiny crinoids were prepared using preparationtechniques developed during the early 1990s (Bartelset al. 1998). This involves using an air abrasive unitmodified to limit static electricity as powders passthrough the pressure hose. With this modified device,pure iron filings are used at low pressures (see discus-sions in Bartels et al. 1998; Glass & Blake 2004). Thismethod allows for very precise removal of the softerrock matrix with minimal or no damage to the pyri-tized fossil. The specimens reported here were pre-pared by C.B. using this technique. The single slabcontaining them is deposited in the German MiningMuseum (Bochum), Bartels Collection (GMMBC HS99). The slab is 17 cm high by 13 cm wide, with thecrinoids concentrated in an area 5 9 6 cm (Fig. 1A).

The Hunsr€uck Slate is an informal stratigraphicalterm that includes the Lower Devonian roofing slatesfrom the Rhenish Massif of Germany (Schindler et al.

DOI 10.1111/let.12147 © 2015 Lethaia Foundation. Published by John Wiley & Sons Ltd

2002; Sutcliffe et al. 2002). The slab with the tiny cri-noids (GMMBC HS 99) was collected from theEschenbach-Bocksberg Quarry at Bundenbach. It isfrom the Eschenbach Member of the middle KaubFormation (lower Emsian), which is in the centralpart of the roofing slate outcrops at Bundenbach. Thecrinoids were presumably buried by turbidites andshow current alignment (Sutcliffe et al. 2002),although they were probably not transported far (Far-rell 2014) as many organisms in the Hunsr€uck Slatewere essentially buried in situ (Bartels et al. 1998).

Tiny crinoids

Slab GMMBC HS 99 contains at least 10 specimensof small crinoids (Fig. 1A). Five of the larger speci-mens, cladids with crowns several mm in dimension,

are likely juveniles of the cladids Propoteriocrinus(Fig. 1A,B) and Lasiocrinus (Fig. 1A,C), based onchecking their characters against the list of knowncrinoid genera from the Hunsr€uck Slate (Bartelset al. 1998). Juveniles do not have the fully devel-oped pattern of arm branching present in adult spec-imens that define taxa described in the literature;thus, the identifications are tenuous. Identificationto the species level is not attempted because of theirsmall size and underdeveloped arms. The five small-est specimens of crinoids cannot be identified, evento the sub-class level, but we are confident these arecrinoids based on the gross morphology of thecrowns and stems (Fig. 1B,D–F). Their co-occur-rence with known cladids suggests they are cladids aswell, although that cannot be confirmed. In each ofthese smallest crinoids, the crown is approximately

A B

C D

E

F

Fig. 1. Early postlarval and juvenile Hunsr€uck crinoids. A, slab GMMBC HS 99 with crinoids concentrated in an area 5 9 6 cm, fromthe 17 9 13 cm (H,W) slab; B, enlargement of right centre of A, the largest crinoid is a Propoteriocrinus juvenile, with smaller pen-tacrinoids on either side; C, enlargement of left lower corner of A with three juveniles of Lasiocrinus, bright areas are large pyrite crystals;D, enlargement of upper left of B with three elongate presumed pentacrinoids, including one with a complete stem apparently attachedto a small mass of pyrite crystals; E, presumed pentacrinoid with stem showing possible faint triple junction plate suture boundaries inlower left of calyx and two arms above the calyx, unidentifiable mass to upper left; F, enlargement of right centre of B showing a bulbouspresumed pentacrinoid. A, photographed dry, low-angle light; B–F, photographed wetted with ethanol, low-angle light. Scale bars: A,1 cm; B–D, 1 mm; E–F, 0.5 mm.

2 Kammer et al. LETHAIA 10.1111/let.12147

1.0 mm, or less, in width and 1.0–2.0 mm in height.The stem ossicles are evident, indicating that stemlength ranges from 3.0 to 4.0 mm for the two speci-mens that appear to have complete stems that wereattached to a substrate in life (Fig. 1B,D). Each ofthese two stems appears attached to a small mass ofpyrite crystals, which may have been an organic sub-strate of unknown affinity on which the larvaesettled. Ossicles on the crowns of these smallest spec-imens cannot readily be resolved to recognize dis-tinct calyx plates (but see Fig. 1E) and arm plates,but the gross crown morphology suggests closedarms are present (Fig. 2).

Discussion

The smallest Hunsr€uck crinoid specimens are verysimilar in size to those of the early pentacrinoid stagein living comatulids and isocrinids, with the calyxless than 1.00 mm in width (Mortensen 1920;Mladenov & Chia 1983; Kohtsuka & Nakano 2005;Haig & Rouse 2008; Shibata et al. 2008; Amemiyaet al. 2014;). In the swimming comatulids, the pen-tacrinoid stage, with a stalk and developing arms,follows the stalked, but armless, non-feeding cys-tidean stage (Breimer 1978; Balser 2002; Kohtsuka &Nakano 2005; Haig & Rouse 2008; Shibata et al.2008). In comatulids, pentacrinoids are consideredthe final larval stage before final development to theswimming stage by autotomy of the stalk. The pen-tacrinoid stage develops at 17–19 days after fertiliza-tion of the eggs and ends anywhere from 26 days tosix months later when the stalk is autotomized

(Balser 2002; Kohtsuka & Nakano 2005). In livingstalked crinoids, the isocrinids, larval developmentwas previously unknown beyond the doliolaria stage(Nakano et al. 2003) and the cystidean and pen-tacrinoid stages were unknown. However, a recentstudy on Metacrinus rotundus has identified both thelarval cystidean stage and the postlarval pentacrinoidstage during development into the stalked adult(Amemiya et al. 2014). The pentacrinoid develop-mental stage in isocrinids is the earliest juvenile stageafter development from the larval, non-feeding cys-tidean stage. The pentacrinoid has a relatively largeaboral cup with very simple arms as compared to theadult with a relatively small aboral cup in a crowndominated by long arms with multiple branchings.Breimer (1978) questioned whether the pentacrinoidstage should be defined when the stalk is not auto-tomized, but Amemiya et al. (2014) recognized thepentacrinoid stage in isocrinids as it is essentiallyidentical in form and function to that stage incomatulids. Amemiya et al. (2014) were unable tokeep pentacrinoids ofMetacrinus rotundus alive untilthey reached typical adult morphology. Thus, theydo not define the developmental limits of the pen-tacrinoid stage in isocrinids.

Based on similar size and morphology, we judgethese smallest Hunsr€uck crinoid specimens to beequivalent to the early postlarval pentacrinoid stagejust after development from the cystidean larvalstage. Traditionally, the pentacrinoid stage was onlyrecognized in comatulids, ending by autotomy ofthe stem (Mortensen 1920; Kohtsuka & Nakano2005; Haig & Rouse 2008). Amemiya et al. (2014)were the first ever to raise isocrinid larvae beyond

A BDC

Fig. 2. Comparisons between pentacrinoids of the living comatulid Isometra vivipara Mortensen and Hunsr€uck specimens. A, early-stagepentacrinoid of I. vivipara with oral plates prominent between the early developing arms, each with a single primibrachial (calyx width0.75 mm) (Mortensen 1920; pl. 22, fig. 11); B, specimen from Fig. 1F (calyx width 0.75 mm), similarity in shape and size to I. viviparain A suggests it is comparable to an early-stage pentacrinoid with orals forming a bulbous crown; C, further developed pentacrinoid of I.vivipara with branching arms extending well above the calyx (calyx width 1.0 mm) (Mortensen 1920; pl. 23, fig. 6); D, specimen fromtop of Fig. 1D (calyx width 1.0 mm), similarity in shape and size to I. vivipara in C suggests it is comparable to a later-stage pentacrinoidwith arms extending above the calyx, which though faint appear to be present around the upper perimeter of the crown.

LETHAIA 10.1111/let.12147 Devonian pentacrinoids 3

the swimming stage and induce development tothe cystidean and pentacrinoid stages. Thus, theywere the first to recognize the pentacrinoid stagein living stalked crinoids. Following their lead, wealso recognize the possibility of a pentacrinoidstage in Palaeozoic stalked crinoids. Similar toAmemiya et al. (2014), we are unable to define thedevelopmental limits of this stage when the stem isnot autotomized. The overall shape of the crown(elongated vs. bulbous), as compared to that ofliving pentacrinoids (Mortensen 1920; Kohtsuka &Nakano 2005; Haig & Rouse 2008; Amemiya et al.2014), suggests that infolded arms at death arepresent, although the preservation is not fineenough to recognize distinct arms, apart fromwhat appears to be arm ossicles on two specimens(Figs 1D,E, 2D).

The bulbous specimen (Figs 1F and 2B) is simi-lar in form to the cystidean stage, which is cappedby oral plates and lacks arms, and is generallythought to be non-feeding, although podia mayextend from the oral plates (Amemiya et al. 2014).However, cystideans are usually 500 microns, orless, in diameter (Mortensen 1920; Kohtsuka &Nakano 2005; Haig & Rouse 2008; Amemiya et al.2014), whereas this specimen is about 750 micronsacross. Rather than being a cystidean larva, thisspecimen may be at a stage immediately followingthe cystidean stage; thus, it has poorly developedarms between large oral plates, as shown by thespecimen of the comatulid Isometra vivipara Mor-tensen (Fig. 2A).

By comparison with the developmental timingof the pentacrinoid stage in living crinoids (Balser2002; Kohtsuka & Nakano 2005; Shibata et al.2008; Amemiya et al. 2014), these crinoids mayhave been only a few weeks or months old at thetime of their death and burial. Aside from Palaeo-zoic microcrinoids, which are thought to havebeen paedomorphic adults that fed by extendingpodia through open oral plates, or along very sim-ple arms (Sevastopulo 2008), these are possiblythe smallest known fossil juvenile crinoids (Broweret al. 1978; Peters & Lane 1990), and perhaps theonly known occurrence of pentacrinoids in thefossil record. Crinoid larvae are known to settlegregariously (Mladenov & Chia 1983). The clusterof presumed pentacrinoids (Fig. 1B) may havesettled together from a clutch of larvae and werelater swept along together by currents beforeburial.

The crinoids on slab GMMBC HS 99 were appar-ently rapidly buried by turbidite currents in fine-grained sediments, as were other fossils of theHunsr€uck Slate (Bartels et al. 1998; K€uhl et al. 2012).

All the crinoids, including the smallest Hunsr€uckspecimens, were pyritized rapidly following burial assulphides produced by decay combined with reducediron in the sediment pore water (Briggs et al. 1996;Raiswell et al. 2008; Farrell 2014). Pyritization occurswhere sub-oxic pore waters are rich in reduced iron,so that dissolved sulphide does not diffuse awayfrom the decaying carcass into the surroundingsediment, thus producing iron sulphide precipita-tion at the site of decay. Crinoid ossicles of theearly pentacrinoid stages in living comatulids andisocrinids consist of highly porous, reticulatedstereom filled with soft dermal tissue (Lahaye &Jangoux 1987; Shibata et al. 2008; Amemiya et al.2014). The Hunsr€uck pentacrinoids appear to bepreserved as black, micro-crystalline, pyrite replac-ing the soft dermal tissues that filled the highlyporous stereom of this early developmental stage.The delicate calcitic ossicles apparently werecrushed during burial compaction producing flatcalyxes lacking distinct plate boundaries. The pyri-tized dermal tissues were resistant to the air abra-sive stream of iron particles that removedsurrounding rock matrix (Fig. 1D–F). This is incontrast to the heavily calcified ossicles, with brassypyrite coatings, standing in 3-D relief on the largerjuveniles (Fig. 1B,C). All specimens have highercontrast from the matrix when wetted (Fig. 1B–F)than when dried (Fig. 1A).

These are the smallest juvenile crinoids reportedfrom the Palaeozoic. The specimens discussed hereare unique because very nearly complete, articulatedspecimens have now been recovered from theHunsr€uck Slate. This new material demonstrates thata Palaeozoic sister group to living crinoids haddevelopmental stages similar to those in livingcrinoids.

Conclusions

The Hunsr€uck Slate continues to reveal exquisiteexamples of pyritized delicate tissues as shown bytiny crinoids interpreted to be early-stage, postlar-val pentacrinoids from one or more of the 30 gen-era of macro-sized crinoids known from thisformation. These presumed pentacrinoids are simi-lar in size and shape to living pentacrinoids ofboth comatulids and isocrinids, and their clusteredoccurrence suggests gregarious settlement by larvae.Assuming these are not microcrinoids, they are thefirst report of pentacrinoids from the fossil record,suggesting that developmental stages in living cri-noids are conserved from a Palaeozoic sistergroup.

4 Kammer et al. LETHAIA 10.1111/let.12147

Acknowledgements. – This research was supported by theNational Science Foundation who partially supported this work(DEB 1036356 (TWK) and DEB 1036416 (WIA)). We thank K.Benison (WVU) for help with photography. The authors declarethat no conflict of interests exists.

References

Amemiya, S., Omori, A., Tsurugaya, T., Hibino, T., Yamaguchi,M., Kuraishi, R., Kiyomoto, M. & Minokawa, T. 2014: Earlystalked stages in ontogeny of the living isocrinid sea lily Me-tacrinus rotundus. Acta Zoologica (Stockholm) doi: 10.1111/azo.12109.

Ausich, W.I., Bartels, C. & Kammer, T.W. 2013: Tube footpreservation in the Devonian crinoid Codiacrinus from theLower Devonian Hunsr€uck Slate, Germany. Lethaia 46, 416–420.

Balser, E.J. 2002: Phylum Echinodermata: Crinoidea. In Young,C.M., Sewell, M.A. & Rice, M.E. (eds): Atlas of Marine Inverte-brate Larvae, 463–482. Academic Press, San Diego.

Bartels, C., Briggs, D.E.G. & Brassel, G. 1998: The Fossils of theHunsr€uck Slate: Marine Life in the Devonian, 309 pp. Cam-bridge University Press, Cambridge.

Breimer, A. 1978: General morphology, recent crinoids. InMoore, R.C., Teichert, C. (eds): Treatise on Invertebrate Pale-ontology, Part T, Echinodermata 2, 9–58. The Geological Soci-ety of America and the University of Kansas, Boulder,Colorado.

Briggs, D.E.G., Raiswell, R., Bottrell, S.H., Hatfield, D. & Bartels,C. 1996: Controls on the pyritization of exceptionallypreserved fossils: an analysis of the Lower Devonian Hunsr€uckSlate of Germany. American Journal of Science 296, 633–663.

Brower, J.C., Lane, N.G. & Wienberg Rasmussen, H. 1978: Post-larval ontogeny of fossil crinoids. In Moore, R.C.Teichert, C.(eds): Treatise on Invertebrate Paleontology, Part T, Echinoder-mata 2, 244–274. The Geological Society of America and theUniversity of Kansas, Boulder, Colorado.

Farrell, �U.C. 2014: Pyritization of soft tissues in the fossil record:an overview. The Paleontological Society Papers 20, 35–57.

Glass, A. & Blake, D.B. 2004: Preservation of tube feet in an ophi-uroid (Echinodermata) from the Lower Devonian Hunsr€uckSlate of Germany and a redescription of Bundenbachia beneckeiand Palaeophiomyxa grandis. Pal€aontologische Zeitschrift 78,73–95.

Haig, J.A. & Rouse, G.W. 2008: Larval development of the feath-erstar Aporometra wilsoni (Echinodermata: Crinoidea). Inver-tebrate Biology 127, 460–469.

Kohtsuka, H. & Nakano, H. 2005: Development and growth ofthe feather star Decametra tigrina (Crinoidea), with emphasison the morphological differences between adults and juveniles.Journal of the Marine Biological Association of the United King-dom 85, 1503–1510.

K€uhl, G., Bartels, C., Briggs, D.E.G. & Rust, J. 2012: Visions of aVanished World, 128 pp. Yale University Press, New Haven.

Lahaye, M.-C. & Jangoux, M. 1987: The skeleton of the stalkedstages of the comatulid crinoid Antedon bifida (Echinoder-mata). Zoomorphology 107, 58–65.

Mladenov, P.V. & Chia, F.S. 1983: Development, settling behav-ior, metamorphosis and pentacrinoid feeding and growth ofthe feather star Florometra serratissima. Marine Biology 73,309–323.

Mortensen, T.H. 1920: Studies in the development of crinoids.Papers from Department of Marine Biology, Carnegie Institutionof Washington 16, 1–94.

Nakano, H., Hibino, T., Oji, T., Hara, Y. & Amemiya, S. 2003:Larval stages of a living sea lily (stalked crinoid echinoderm).Nature 421, 158–160.

Peters, J. & Lane, N.G. 1990: Ontogenetic adaptations in somePennsylvanian crinoids. Journal of Paleontology 64, 427–435.

Raiswell, R., Newton, R., Bottrell, S.H., Coburn, P.M., Briggs,D.E.G., Bond, D.P. & Poulton, S.W. 2008: Turbidite deposi-tional influences on the diagenesis of Beecher’s Trilobite Bedand the Hunsr€uck Slate; sites of soft tissue preservation. Amer-ican Journal of Science 308, 105–129.

Schindler, T., Sutcliffe, O.E., Bartels, C., Poschmann, M. & Wut-tke, M. 2002: Lithostratigraphic subdivision and chronostrati-graphical position of the middle Kaub Formation (lowerEmsian, Lower Devonian) of the Bundenbach area (Hunsr€uck,SW Germany). Metalla 9, 73–88.

Sevastopulo, G.D. 2008: Paleobiology of Carboniferous micro-crinoids. In Ausich, W.I., Webster, G.D. (eds): EchinodermPaleobiology, 55–69. Indiana University Press, Bloomington,Indiana.

Shibata, T.F., Sato, A., Oji, T. & Akasaka, K. 2008: Developmentand growth of the feather star Oxycomanthus japonicus to sex-ual maturity. Zoological Science 25, 1075–1083.

Sutcliffe, O.E., Tibbs, S.L. & Briggs, D.E.G. 2002: Sedimentologyand environmental interpretation of fine-grained turbidites inthe Kaub Formation of the Hunsr€uck Slate: analysis of a sec-tion excavated for the project Nahecaris. Metalla 9, 89–104.

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