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Earliest symbiotic rugosans in cystoporate bryozoan Ceramopora intercellata Bassler, 1911 from Late Ordovician of Estonia (Baltica)
Earliest symbiotic rugosans in cystoporate bryozoan Ceramopora intercellata Bassler, 1911 from Late Ordovician of Estonia (Baltica) Olev Vinn, Andrej Ernst, Ursula Toom PII: DOI: Reference:
S0031-0182(16)30335-2 doi: 10.1016/j.palaeo.2016.08.016 PALAEO 7947
To appear in:
Palaeogeography, Palaeoclimatology, Palaeoecology
Received date: Revised date: Accepted date:
6 June 2016 28 July 2016 11 August 2016
Please cite this article as: Vinn, Olev, Ernst, Andrej, Toom, Ursula, Earliest symbiotic rugosans in cystoporate bryozoan Ceramopora intercellata Bassler, 1911 from Late Ordovician of Estonia (Baltica), Palaeogeography, Palaeoclimatology, Palaeoecology (2016), doi: 10.1016/j.palaeo.2016.08.016
This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT Earliest symbiotic rugosans in cystoporate bryozoan Ceramopora intercellata Bassler, 1911 from Late Ordovician of Estonia (Baltica)
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Olev Vinn a*, Andrej Ernst b and Ursula Toom c
Institute of Ecology and Earth Sciences, University of Tartu, Ravila 14A, 50411 Tartu,
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Estonia, [email protected]
Institut für Geologie, Universität Hamburg, Bundesstr. 55, 20146 Hamburg, Germany,
Institute of Geology, Tallinn University of Technology, Ehitajate tee 5, 19086 Tallinn,
Corresponding author
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Estonia, [email protected]
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[email protected]
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ACCEPTED MANUSCRIPT ABSTRACT The earliest known endobiotic rugose corals are recorded in the Katian of Estonia. Multiple
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rugosans were partially embedded in colonies of the cystoporate bryozoan Ceramopora
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intercellata Bassler, 1911, leaving only their apertures free on the bryozoan growth surface.
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Bodophyllum sp. and Lambelasma sp. are rugosans that formed a symbiotic association with C. intercellata which may have been mutualistic. Rugosans presumably benefitted from
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growth within the stable substrate provided by the bryozoan, while bryozoans presumably benefitted by protection against some types of predators. Symbiosis between rugosans and
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the bryozoan Ceramopora intercellata was most likely facultative.
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1. Introduction
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Key words: Symbiosis, intergrowth, bryozoans, rugosans, Baltica, Katian.
Symbiotic interactions between different organisms are rather rarely preserved in the fossil record. The endobionts embedded (i.e. bioimmured) in the living tissues of host organisms also have great importance (see Taylor, 1990 for a review). The earliest microscopic invertebrate symbionts appeared in the Cambrian (Bassett et al., 2004). Macroscopic endobiotic invertebrate symbionts appeared later and became common in the Late Ordovician (see Tapanila, 2005 for a summary). Silurian and Devonian rugose corals were often bioimmured within the skeletons of stromatoporoids and slightly more rarely into other corals; they differ from bioclaustrations (Palmer and Wilson, 1988) by having their own skeletons. Several Paleozoic bioclaustrations may have been made by parasites, but it is 2
ACCEPTED MANUSCRIPT better to consider them simply as symbionts (Zapalski, 2007, 2011; Zapalski and Hubert, 2011; Taylor, 2015). Endobiotic rugosans were hitherto unknown from the Ordovician.
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Moreover, there are no other reports of bryozoan-hosted endobiotic rugosans.
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The faunas of bryozoans and rugose corals in the Ordovician of Estonia are relatively
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well studied (Bassler, 1911a; Bassler, 1911b; Gorjunova, 1992; Gorjunova and Lavrentjeva, 1993; Kaljo, 1958; Kaljo, 1961; Lavrentjeva, 1990; Modzalevskaya, 1953; Männil, 1959;
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Neuman, 1969; Neuman, 1986; Pushkin and Gataulina, 1992; Reiman, 1958), but symbiosis
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of rugosans and bryozoans needs a further study.
The aim of this paper are to: 1) describe the earliest known endobiotic rugosan
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symbionts, here reported from the Late Ordovician of Baltica; 2) describe the only known
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rugosan-bryozoan endosymbiosis; and 3) discuss the paleoecology of this rugosan-bryozoan
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association.
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2. Geological background and locality During the Ordovician Baltica moved from the temperate climatic zone into the subtropical realm (Torsvik et al., 1992; Nestor and Einasto, 1997; Cocks and Torsvik, 2005; Torsvik and Cocks, 2013). In the Sandbian, the area of modern Estonia was covered by a shallow epicontinental sea with little bathymetric variation and an extremely low sedimentation rate (Nestor and Einasto, 1997). Along the entire extent of the ramp a series of grey argillaceous and calcareous sediments accumulated. There was a trend of increasing clay and decreasing bioclasts in the offshore direction (Nestor and Einasto, 1997). In the Katian the climatic
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ACCEPTED MANUSCRIPT change resulted in an increase in carbonate production and sedimentation rate on the carbonate shelf (Nestor and Einasto, 1997).
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The Dapingian to Hirnantian succession in Estonia is characterized by various normal
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marine carbonate rocks (Nestor and Einasto, 1997). In northern Estonia, mostly limestones
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are exposed, which accumulated in the shallow part of the basin. In addition to limestones, marls also occur in somewhat lesser amounts. The purest limestones are mostly in the
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Katian of northern Estonia. In northern Estonia, the Sandbian is characterized by a higher content of clay in carbonate rocks. In addition to limestones, kerogenous carbonates (oil
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shales) accumulated in the Sandbian of northern Estonia (Nestor and Einasto, 1997). The carbonate rocks of the Haljala Regional Stage are especially rich in clay. Carbonate buildups
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became common in in the early Katian of the northern Estonia starting with the Keila
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Regional Stage (Nestor and Einasto, 1997). The Kõrgessaare outcrop is an old abandoned quarry in Kõrgessaare village, Hiiumaa Island, NW Estonia. Thinly bedded (2-8 cm), bluish-grey to yellowish grey clayey nodular
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limestones with thin (<2cm) marl intercalations were exposed. Kõrgessaare quarry was rich in various normal marine shelly fossils, including the rugosans Streptelasma hiumica (Reiman), Kenophyllum siluricum (Dybowski), K. subcylindricum Dybowski, Rectigrewingkia anthelion (Dybowski), Grewingkia europaeum (Roemer), Bodophyllum sp. and Lambelasma sp. The locality was also rich in bryozoans: Anaphragma mirabile Ulrich et Bassler, Ceramopora intercellata Bassler, Corynotrypa barberi Bassler, Diplotrypa densitabulata Modzalevskaya, Orbignyella expansa baltica Bassler, Eichwaldictya flabellata (Eichwald), Constellaria constellata (Dybowski) and Cuffeyella arachnoidea (Hall) (Rõõmusoks, 1962; D. Kaljo personal comm. 2016).
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3. Material and methods
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The collections of the Institute of Geology, Tallinn University of Technology (GIT) contains
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113 bryozoans and 320 rugosans from the Kõrgessaare Formation (Katian) of the Kõrgessaare outcrop, Hiiumaa Island, NW Estonia. The bryozoans in the collection were searched for the presence of symbionts. Two specimens of Ceramopora intercellata Bassler,
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1911 contained rugosans. The bryozoans with rugosans were photographed using a Nikon
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D7000 digital camera. The dimensions of both rugosan and bryozoan were obtained from
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calibrated photographs.
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4. Results
Two of 113 bryozoans from the Kõrgessaare outcrop contain partially embedded rugosans. Rugosans occur only in the cystoporate bryozoan Ceramopora intercellata Bassler, 1911.
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There are multiple rugosans embedded in both bryozoan colonies. The rugosans are oriented perpendicular to the surface of bryozoan colonies. Bryozoan zooids around the partially embedded rugosans are the same size as those in other regions of the colonies. One C. intercellata colony (GIT 666-22) contains the rugosan Bodophyllum sp., but some juvenile specimens probably belong to the other species. The other bryozoan colony (GIT 666-23) contains the rugosan Lambelasma sp., but some juvenile specimens may also belong to other species. Bryozoan colony GIT 666-22 is 5.8 cm in diameter and 1.5 cm thick, forming slightly hemispherical disk with a somewhat irregular shape. Bryozoan colony GIT 666-23 has a diameter of 5.6 cm and a slightly hemispherical shape.
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ACCEPTED MANUSCRIPT There are thirteen rugosans in C. intercellata colony GIT 666-22. The growth stages of the rugosans vary. Individuals of Bodophyllum sp. rugosans in this colony have their
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apertures elevated above the growth surface of the bryozoan colony. The edges of elevated
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rugosan is almost completely overgrown by the bryozoan.
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apertures of the rugosans are usually not overgrown by the host bryozoan, although one
There are six rugosans in C. intercellata colony GIT 666-23. The growth stages of
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these rugosans vary. Individuals of Lambelasma sp. in this colony have their apertures flush with the growth surface of the bryozoan. Two rugosans are partially overgrown by the host
5. Discussion
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5.1. Symbiotic association
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bryozoan.
The syn vivo nature of this rugosan-bryozoan association is demonstrated by the
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perpendicular orientation of the rugosans relative to the bryozoan growth surface and their partial embedment by the bryozoan. The elevated aperture of Bodophyllum sp. in colony GIT 666-22 may indicate that the coral was growing faster than its bryozoan host. Faster growth of the rugosan symbiont as compared to bryozoan host may have been an antifouling strategy. An alternative explanation for the elevated aperture is that this particular coral continued to grow after the host bryozoan died. Feeding competition between Bodophyllum sp. and its host bryozoan seems unlikely as bryozoans and corals feed on different sources. Corals usually feed on zooplankton, whereas bryozoans take phytoplankton, which is much smaller. The feeding 6
ACCEPTED MANUSCRIPT methods are also different; corals kill their food with nematocysts, and bryozoans are filter feeders. The varying growth stages of rugosans in the bryozoan colony GIT 666-22
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presumably indicate that the bryozoan host was colonized by rugosans several times. The
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partially overgrown rugosans (Lambelasma sp.) in the bryozoan colony GIT 666-23 could
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have been dead before the overgrowth began. Alternatively, the bryozoan host dominated over the rugosan symbionts and killed them by sealing them off. However, the latter is less
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likely as the corals are larger and would have been well defended by nematocysts and possibly mucus secretions.
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The host bryozoans did not provide the symbiotic rugosans with a higher tier for feeding. Both bryozoan colonies are not highly domical in shape, so even in the central
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region of the colonies, rugosans did not achieve a significantly greater elevation. However,
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the rugosans presumably benefitted from growth within a positionally stable substrate. It is
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unclear whether the host bryozoans benefitted from the rugosans, but vertical stiff skeletons of rugosans may have reinforced the bryozoan colonies. However, it is doubtful
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whether the mechanical strength of the bryozoan colonies required reinforcement – breakage of dome-shaped bryozoan colonies is rare (even those riddled with borings), in contrast to ramose branched colonies which are prone to breakage. It is more likely that the bryozoans benefitted by protection against some types of predators; cf. the very similar Neogene association between the scleractinian Culicia and the cheilostome bryozoan Celleporaria (Taylor 2015). The lack of malformations and decrease in the size of bryozoan zooids near the rugosans indicates a lack of strong negative effect of the rugosans on the bryozoans. The numerous rugosans occupied some part of the bryozoan colony feeding surface and may have slightly decreased the feeding efficiency of the whole colony. 7
ACCEPTED MANUSCRIPT The walls of symbiotic rugosans are not thinner or peculiar in any way as compared to non-symbiotic specimens, indicating that the rugosan symbionts were not anatomically
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adapted to a life within bryozoans. This could mean a relatively short evolutionary history
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behind this rugosan-bryozoan symbiosis.
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Lambelasma and Bodophyllum commonly occur independently of bryozoans in the Katian of Estonia. Similarly Ceramopora intercellata occurs without rugosans in the
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Kõrgessaare outcrop. Thus, probably described symbiosis between rugosans and bryozoan
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Ceramopora intercellata was not obligate, but facultative.
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5.2. Other cases of Paleozoic bryozoan: coral symbiosis Symbiotic associations between rugosans and bryozoans similar to the described rugosan-
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bryozoan association were previously unknown. However, encrusting species of the tabulate Aulopora and bryozoan Leioclema formed a symbiotic association in the Early Devonian of
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western Tennessee (McKinney et al., 1990). In this association colonies of the two species intergrew so that Aulopora corallites except for their calices were entirely covered by a thin encrustation of Leioclema sp. (McKinney et al., 1990). This association was presumably mutualistic with benefits including escape from limited space on the substratum into a higher tier of suspension feeders. It has been supposed that such mutualism between benthic modular competitors may have developed more readily than associations between solitary competitors (McKinney et al., 1990). The development of symbiotic relationship between the taxa is presumably similar in the rugosan-bryozoan association and Auloporabryozoan association. Some bryozoans in the Silurian of Estonia probably encrusted
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ACCEPTED MANUSCRIPT rugosans syn vivo (Vinn and Toom, 2016; Zatoń et al., 2016), but these taxa probably lacked
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close symbiotic relationships.
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5.3. Endobiotic rugosan symbionts
Rugosans form an important part of Silurian and Devonian endosymbiotic faunas (Vinn,
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2016). Endobiotic rugosan symbionts are particularly common in Silurian and Devonian stromatoporoids (Vinn, 2016), but they are also known from the Silurian tabulates
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includingheliolitids. It is interesting that the favoured rugosan hosts - stromatoporoids were common already in the Late Ordovician (Nestor, 1964), but the stromatoporoid-based
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symbiotic associations appeared much later in the Rhuddanian. In contrast to the Silurian
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and Devonian, rugosan endosymbionts are rare in the Ordovician. Most Ordovician
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endosymbiotic associations were bryozoan based (Vinn and Wilson, 2015). Thus, it is not surprising that endosymbiotic rugosans first colonized bryozoans. Ordovician bryozoan
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faunas seem to be especially rich in this symbiosis (Vinn and Wilson, 2015).
5.4. Other bryozoan-hosted symbiotic association in the Paleozoic Ordovician bryozoans hosted a variety of symbiotic endobionts. The earliest bryozoan endobionts are worm-like Anoigmaichnus bioclaustrations in the Middle Ordovician Mesotrypa bystrowi from Estonia (Vinn et al., 2014). Endobiotic conulariids inhabited several bryozoan species in the Sandbian and Katian of Estonia (Vinn and Wilson, 2015). In the latter association, conulariids (Conularia sp.) are embedded in bryozoan hosts, leaving only their apertures free on the growth surface. There can be up to four conulariids per bryozoan host 9
ACCEPTED MANUSCRIPT (Männil, 1959). Conulariids possibly gained additional protection against predators by their embedment within the bryozoan skeleton and a relatively stable growth substrate (Vinn and
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Wilson, 2015). Bioclaustrations made by colonial hydroids or ascidian tunicates occur in
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bryozoans from the Late Ordovician of North America (Palmer and Wilson, 1988). Worm-like
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bioclaustrations have recently been described from the bryozoans in the Middle Devonian of
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Germany (Ernst et al., 2014).
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6. Conclusions
Symbiotic endobionts are common in the Ordovician bryozoans in Baltica. Endobiotic
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rugosan symbionts are particularly common in Silurian and Devonian stromatoporoids, but
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they were hitherto unknown in the bryozoans. Earliest known endosymbiotic rugosans were
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discovered from the cystoporate bryozoan Ceramopora intercellata Bassler, 1911 in the Late Ordovician (Katian) of Estonia. Rugosans had presumably mutualistic relationship with their
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bryozoan hosts. Symbiosis between rugosans and the bryozoans was most likely facultative.
Acknowledgements Financial support to O.V. was provided by a Palaeontological Association Research Grant and Estonian Research Council projects ETF9064 and IUT20-34. We are grateful to Dimitri Kaljo, Institute of Geology, Tallinn University of Technology for identifications of the rugosans. We are also grateful to Gennadi Baranov, Institute of Geology, Tallinn University of Technology for digital photography of the specimens, Carlton E. Brett, University of Cincinnati, and an
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ACCEPTED MANUSCRIPT anonymous reviewer for the constructive reviews. This paper is a contribution to IGCP 653 “The onset of the Great Ordovician Biodiversity Event”.
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ACCEPTED MANUSCRIPT FIGURE CAPTIONS
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Fig. 1. The location of Kõrgessaare quarry on Hiiumaa Island in NW Estonia.
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Fig. 2. The stratigraphy of the Katian of Estonia. Location of rugosan symbionts in bryozoans marked with an asterisk.
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Fig. 3. A-D, Ceramopora intercellata Bassler, 1911b colony (GIT 666-22) with multiple partially embedded rugosans Bodophyllum sp. (GIT 666-22) from Kõrgessaare
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Formation (Katian) of Hiiumaa Island, NW Estonia. C-D, detailed view of bryozoan growth surface near rugosans (rg). E-F, Ceramopora intercellata Bassler, 1911b colony
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(GIT 666-23) with multiple partially embedded rugosans Lambelasma sp. (GIT 666-22) from Kõrgessaare Formation (Katian) of Hiiumaa Island, NW Estonia. Arrows point to
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partially sealed off rugosans.
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ACCEPTED MANUSCRIPT Highlights
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Earliest symbiotic rugosans in bryozoans recorded in the Katian. Endobiotic rugosans benefitted from stable substrate. This symbiotic association was probably mutualistic. Symbiosis was common in Ordovician bryozoans in Baltica.
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S0031-0182(16)30335-2 doi: 10.1016/j.palaeo.2016.08.016 PALAEO 7947
To appear in:
Palaeogeography, Palaeoclimatology, Palaeoecology
Received date: Revised date: Accepted date:
6 June 2016 28 July 2016 11 August 2016
Please cite this article as: Vinn, Olev, Ernst, Andrej, Toom, Ursula, Earliest symbiotic rugosans in cystoporate bryozoan Ceramopora intercellata Bassler, 1911 from Late Ordovician of Estonia (Baltica), Palaeogeography, Palaeoclimatology, Palaeoecology (2016), doi: 10.1016/j.palaeo.2016.08.016
This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT Earliest symbiotic rugosans in cystoporate bryozoan Ceramopora intercellata Bassler, 1911 from Late Ordovician of Estonia (Baltica)
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Olev Vinn a*, Andrej Ernst b and Ursula Toom c
Institute of Ecology and Earth Sciences, University of Tartu, Ravila 14A, 50411 Tartu,
b
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Estonia, [email protected]
Institut für Geologie, Universität Hamburg, Bundesstr. 55, 20146 Hamburg, Germany,
Institute of Geology, Tallinn University of Technology, Ehitajate tee 5, 19086 Tallinn,
Corresponding author
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Estonia, [email protected]
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[email protected]
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ACCEPTED MANUSCRIPT ABSTRACT The earliest known endobiotic rugose corals are recorded in the Katian of Estonia. Multiple
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rugosans were partially embedded in colonies of the cystoporate bryozoan Ceramopora
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intercellata Bassler, 1911, leaving only their apertures free on the bryozoan growth surface.
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Bodophyllum sp. and Lambelasma sp. are rugosans that formed a symbiotic association with C. intercellata which may have been mutualistic. Rugosans presumably benefitted from
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growth within the stable substrate provided by the bryozoan, while bryozoans presumably benefitted by protection against some types of predators. Symbiosis between rugosans and
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the bryozoan Ceramopora intercellata was most likely facultative.
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1. Introduction
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Key words: Symbiosis, intergrowth, bryozoans, rugosans, Baltica, Katian.
Symbiotic interactions between different organisms are rather rarely preserved in the fossil record. The endobionts embedded (i.e. bioimmured) in the living tissues of host organisms also have great importance (see Taylor, 1990 for a review). The earliest microscopic invertebrate symbionts appeared in the Cambrian (Bassett et al., 2004). Macroscopic endobiotic invertebrate symbionts appeared later and became common in the Late Ordovician (see Tapanila, 2005 for a summary). Silurian and Devonian rugose corals were often bioimmured within the skeletons of stromatoporoids and slightly more rarely into other corals; they differ from bioclaustrations (Palmer and Wilson, 1988) by having their own skeletons. Several Paleozoic bioclaustrations may have been made by parasites, but it is 2
ACCEPTED MANUSCRIPT better to consider them simply as symbionts (Zapalski, 2007, 2011; Zapalski and Hubert, 2011; Taylor, 2015). Endobiotic rugosans were hitherto unknown from the Ordovician.
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Moreover, there are no other reports of bryozoan-hosted endobiotic rugosans.
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The faunas of bryozoans and rugose corals in the Ordovician of Estonia are relatively
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well studied (Bassler, 1911a; Bassler, 1911b; Gorjunova, 1992; Gorjunova and Lavrentjeva, 1993; Kaljo, 1958; Kaljo, 1961; Lavrentjeva, 1990; Modzalevskaya, 1953; Männil, 1959;
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Neuman, 1969; Neuman, 1986; Pushkin and Gataulina, 1992; Reiman, 1958), but symbiosis
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of rugosans and bryozoans needs a further study.
The aim of this paper are to: 1) describe the earliest known endobiotic rugosan
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symbionts, here reported from the Late Ordovician of Baltica; 2) describe the only known
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rugosan-bryozoan endosymbiosis; and 3) discuss the paleoecology of this rugosan-bryozoan
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association.
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2. Geological background and locality During the Ordovician Baltica moved from the temperate climatic zone into the subtropical realm (Torsvik et al., 1992; Nestor and Einasto, 1997; Cocks and Torsvik, 2005; Torsvik and Cocks, 2013). In the Sandbian, the area of modern Estonia was covered by a shallow epicontinental sea with little bathymetric variation and an extremely low sedimentation rate (Nestor and Einasto, 1997). Along the entire extent of the ramp a series of grey argillaceous and calcareous sediments accumulated. There was a trend of increasing clay and decreasing bioclasts in the offshore direction (Nestor and Einasto, 1997). In the Katian the climatic
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ACCEPTED MANUSCRIPT change resulted in an increase in carbonate production and sedimentation rate on the carbonate shelf (Nestor and Einasto, 1997).
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The Dapingian to Hirnantian succession in Estonia is characterized by various normal
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marine carbonate rocks (Nestor and Einasto, 1997). In northern Estonia, mostly limestones
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are exposed, which accumulated in the shallow part of the basin. In addition to limestones, marls also occur in somewhat lesser amounts. The purest limestones are mostly in the
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Katian of northern Estonia. In northern Estonia, the Sandbian is characterized by a higher content of clay in carbonate rocks. In addition to limestones, kerogenous carbonates (oil
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shales) accumulated in the Sandbian of northern Estonia (Nestor and Einasto, 1997). The carbonate rocks of the Haljala Regional Stage are especially rich in clay. Carbonate buildups
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became common in in the early Katian of the northern Estonia starting with the Keila
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Regional Stage (Nestor and Einasto, 1997). The Kõrgessaare outcrop is an old abandoned quarry in Kõrgessaare village, Hiiumaa Island, NW Estonia. Thinly bedded (2-8 cm), bluish-grey to yellowish grey clayey nodular
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limestones with thin (<2cm) marl intercalations were exposed. Kõrgessaare quarry was rich in various normal marine shelly fossils, including the rugosans Streptelasma hiumica (Reiman), Kenophyllum siluricum (Dybowski), K. subcylindricum Dybowski, Rectigrewingkia anthelion (Dybowski), Grewingkia europaeum (Roemer), Bodophyllum sp. and Lambelasma sp. The locality was also rich in bryozoans: Anaphragma mirabile Ulrich et Bassler, Ceramopora intercellata Bassler, Corynotrypa barberi Bassler, Diplotrypa densitabulata Modzalevskaya, Orbignyella expansa baltica Bassler, Eichwaldictya flabellata (Eichwald), Constellaria constellata (Dybowski) and Cuffeyella arachnoidea (Hall) (Rõõmusoks, 1962; D. Kaljo personal comm. 2016).
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3. Material and methods
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The collections of the Institute of Geology, Tallinn University of Technology (GIT) contains
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113 bryozoans and 320 rugosans from the Kõrgessaare Formation (Katian) of the Kõrgessaare outcrop, Hiiumaa Island, NW Estonia. The bryozoans in the collection were searched for the presence of symbionts. Two specimens of Ceramopora intercellata Bassler,
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1911 contained rugosans. The bryozoans with rugosans were photographed using a Nikon
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D7000 digital camera. The dimensions of both rugosan and bryozoan were obtained from
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calibrated photographs.
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4. Results
Two of 113 bryozoans from the Kõrgessaare outcrop contain partially embedded rugosans. Rugosans occur only in the cystoporate bryozoan Ceramopora intercellata Bassler, 1911.
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There are multiple rugosans embedded in both bryozoan colonies. The rugosans are oriented perpendicular to the surface of bryozoan colonies. Bryozoan zooids around the partially embedded rugosans are the same size as those in other regions of the colonies. One C. intercellata colony (GIT 666-22) contains the rugosan Bodophyllum sp., but some juvenile specimens probably belong to the other species. The other bryozoan colony (GIT 666-23) contains the rugosan Lambelasma sp., but some juvenile specimens may also belong to other species. Bryozoan colony GIT 666-22 is 5.8 cm in diameter and 1.5 cm thick, forming slightly hemispherical disk with a somewhat irregular shape. Bryozoan colony GIT 666-23 has a diameter of 5.6 cm and a slightly hemispherical shape.
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ACCEPTED MANUSCRIPT There are thirteen rugosans in C. intercellata colony GIT 666-22. The growth stages of the rugosans vary. Individuals of Bodophyllum sp. rugosans in this colony have their
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apertures elevated above the growth surface of the bryozoan colony. The edges of elevated
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rugosan is almost completely overgrown by the bryozoan.
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apertures of the rugosans are usually not overgrown by the host bryozoan, although one
There are six rugosans in C. intercellata colony GIT 666-23. The growth stages of
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these rugosans vary. Individuals of Lambelasma sp. in this colony have their apertures flush with the growth surface of the bryozoan. Two rugosans are partially overgrown by the host
5. Discussion
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5.1. Symbiotic association
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bryozoan.
The syn vivo nature of this rugosan-bryozoan association is demonstrated by the
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perpendicular orientation of the rugosans relative to the bryozoan growth surface and their partial embedment by the bryozoan. The elevated aperture of Bodophyllum sp. in colony GIT 666-22 may indicate that the coral was growing faster than its bryozoan host. Faster growth of the rugosan symbiont as compared to bryozoan host may have been an antifouling strategy. An alternative explanation for the elevated aperture is that this particular coral continued to grow after the host bryozoan died. Feeding competition between Bodophyllum sp. and its host bryozoan seems unlikely as bryozoans and corals feed on different sources. Corals usually feed on zooplankton, whereas bryozoans take phytoplankton, which is much smaller. The feeding 6
ACCEPTED MANUSCRIPT methods are also different; corals kill their food with nematocysts, and bryozoans are filter feeders. The varying growth stages of rugosans in the bryozoan colony GIT 666-22
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presumably indicate that the bryozoan host was colonized by rugosans several times. The
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partially overgrown rugosans (Lambelasma sp.) in the bryozoan colony GIT 666-23 could
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have been dead before the overgrowth began. Alternatively, the bryozoan host dominated over the rugosan symbionts and killed them by sealing them off. However, the latter is less
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likely as the corals are larger and would have been well defended by nematocysts and possibly mucus secretions.
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The host bryozoans did not provide the symbiotic rugosans with a higher tier for feeding. Both bryozoan colonies are not highly domical in shape, so even in the central
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region of the colonies, rugosans did not achieve a significantly greater elevation. However,
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the rugosans presumably benefitted from growth within a positionally stable substrate. It is
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unclear whether the host bryozoans benefitted from the rugosans, but vertical stiff skeletons of rugosans may have reinforced the bryozoan colonies. However, it is doubtful
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whether the mechanical strength of the bryozoan colonies required reinforcement – breakage of dome-shaped bryozoan colonies is rare (even those riddled with borings), in contrast to ramose branched colonies which are prone to breakage. It is more likely that the bryozoans benefitted by protection against some types of predators; cf. the very similar Neogene association between the scleractinian Culicia and the cheilostome bryozoan Celleporaria (Taylor 2015). The lack of malformations and decrease in the size of bryozoan zooids near the rugosans indicates a lack of strong negative effect of the rugosans on the bryozoans. The numerous rugosans occupied some part of the bryozoan colony feeding surface and may have slightly decreased the feeding efficiency of the whole colony. 7
ACCEPTED MANUSCRIPT The walls of symbiotic rugosans are not thinner or peculiar in any way as compared to non-symbiotic specimens, indicating that the rugosan symbionts were not anatomically
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adapted to a life within bryozoans. This could mean a relatively short evolutionary history
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behind this rugosan-bryozoan symbiosis.
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Lambelasma and Bodophyllum commonly occur independently of bryozoans in the Katian of Estonia. Similarly Ceramopora intercellata occurs without rugosans in the
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Kõrgessaare outcrop. Thus, probably described symbiosis between rugosans and bryozoan
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Ceramopora intercellata was not obligate, but facultative.
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5.2. Other cases of Paleozoic bryozoan: coral symbiosis Symbiotic associations between rugosans and bryozoans similar to the described rugosan-
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bryozoan association were previously unknown. However, encrusting species of the tabulate Aulopora and bryozoan Leioclema formed a symbiotic association in the Early Devonian of
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western Tennessee (McKinney et al., 1990). In this association colonies of the two species intergrew so that Aulopora corallites except for their calices were entirely covered by a thin encrustation of Leioclema sp. (McKinney et al., 1990). This association was presumably mutualistic with benefits including escape from limited space on the substratum into a higher tier of suspension feeders. It has been supposed that such mutualism between benthic modular competitors may have developed more readily than associations between solitary competitors (McKinney et al., 1990). The development of symbiotic relationship between the taxa is presumably similar in the rugosan-bryozoan association and Auloporabryozoan association. Some bryozoans in the Silurian of Estonia probably encrusted
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ACCEPTED MANUSCRIPT rugosans syn vivo (Vinn and Toom, 2016; Zatoń et al., 2016), but these taxa probably lacked
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close symbiotic relationships.
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5.3. Endobiotic rugosan symbionts
Rugosans form an important part of Silurian and Devonian endosymbiotic faunas (Vinn,
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2016). Endobiotic rugosan symbionts are particularly common in Silurian and Devonian stromatoporoids (Vinn, 2016), but they are also known from the Silurian tabulates
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includingheliolitids. It is interesting that the favoured rugosan hosts - stromatoporoids were common already in the Late Ordovician (Nestor, 1964), but the stromatoporoid-based
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symbiotic associations appeared much later in the Rhuddanian. In contrast to the Silurian
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and Devonian, rugosan endosymbionts are rare in the Ordovician. Most Ordovician
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endosymbiotic associations were bryozoan based (Vinn and Wilson, 2015). Thus, it is not surprising that endosymbiotic rugosans first colonized bryozoans. Ordovician bryozoan
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faunas seem to be especially rich in this symbiosis (Vinn and Wilson, 2015).
5.4. Other bryozoan-hosted symbiotic association in the Paleozoic Ordovician bryozoans hosted a variety of symbiotic endobionts. The earliest bryozoan endobionts are worm-like Anoigmaichnus bioclaustrations in the Middle Ordovician Mesotrypa bystrowi from Estonia (Vinn et al., 2014). Endobiotic conulariids inhabited several bryozoan species in the Sandbian and Katian of Estonia (Vinn and Wilson, 2015). In the latter association, conulariids (Conularia sp.) are embedded in bryozoan hosts, leaving only their apertures free on the growth surface. There can be up to four conulariids per bryozoan host 9
ACCEPTED MANUSCRIPT (Männil, 1959). Conulariids possibly gained additional protection against predators by their embedment within the bryozoan skeleton and a relatively stable growth substrate (Vinn and
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Wilson, 2015). Bioclaustrations made by colonial hydroids or ascidian tunicates occur in
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bryozoans from the Late Ordovician of North America (Palmer and Wilson, 1988). Worm-like
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bioclaustrations have recently been described from the bryozoans in the Middle Devonian of
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Germany (Ernst et al., 2014).
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6. Conclusions
Symbiotic endobionts are common in the Ordovician bryozoans in Baltica. Endobiotic
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rugosan symbionts are particularly common in Silurian and Devonian stromatoporoids, but
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they were hitherto unknown in the bryozoans. Earliest known endosymbiotic rugosans were
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discovered from the cystoporate bryozoan Ceramopora intercellata Bassler, 1911 in the Late Ordovician (Katian) of Estonia. Rugosans had presumably mutualistic relationship with their
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bryozoan hosts. Symbiosis between rugosans and the bryozoans was most likely facultative.
Acknowledgements Financial support to O.V. was provided by a Palaeontological Association Research Grant and Estonian Research Council projects ETF9064 and IUT20-34. We are grateful to Dimitri Kaljo, Institute of Geology, Tallinn University of Technology for identifications of the rugosans. We are also grateful to Gennadi Baranov, Institute of Geology, Tallinn University of Technology for digital photography of the specimens, Carlton E. Brett, University of Cincinnati, and an
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ACCEPTED MANUSCRIPT anonymous reviewer for the constructive reviews. This paper is a contribution to IGCP 653 “The onset of the Great Ordovician Biodiversity Event”.
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ACCEPTED MANUSCRIPT FIGURE CAPTIONS
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Fig. 1. The location of Kõrgessaare quarry on Hiiumaa Island in NW Estonia.
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Fig. 2. The stratigraphy of the Katian of Estonia. Location of rugosan symbionts in bryozoans marked with an asterisk.
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Fig. 3. A-D, Ceramopora intercellata Bassler, 1911b colony (GIT 666-22) with multiple partially embedded rugosans Bodophyllum sp. (GIT 666-22) from Kõrgessaare
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Formation (Katian) of Hiiumaa Island, NW Estonia. C-D, detailed view of bryozoan growth surface near rugosans (rg). E-F, Ceramopora intercellata Bassler, 1911b colony
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(GIT 666-23) with multiple partially embedded rugosans Lambelasma sp. (GIT 666-22) from Kõrgessaare Formation (Katian) of Hiiumaa Island, NW Estonia. Arrows point to
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partially sealed off rugosans.
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Earliest symbiotic rugosans in bryozoans recorded in the Katian. Endobiotic rugosans benefitted from stable substrate. This symbiotic association was probably mutualistic. Symbiosis was common in Ordovician bryozoans in Baltica.
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