Abstract

The earliest known symbiotic rugosan endobionts occur in stromatoporoids from the early Rhuddanian of Estonia. The stromatoporoid Ecclimadictyon nikitini from the Tamsalu Formation contains the rugosan Donacophyllum middendorffii endobiont. A stromatoporoid Clathrodictyon boreale from the Varbola Formation contains Streptelasma estonica and Bodophyllum sp. endobionts. There are up to three endobiotic rugosans per stromatoporoid host. Stromatoporoid hosts were beneficial for symbiotic rugosans as elevated substrates on a seafloor that offered a higher tier for feeding; they also offered enhanced substrate stability. Stromatoporoids of the end‐Ordovician mass‐extinction recovery fauna hosted a diverse fauna of symbiotic endobionts. There were few if any negative effects of this mass extinction on the symbiotic endobionts.

Keywords

  1. Endobionts
  2. rugosans
  3. Silurian
  4. stromatoporoids
  5. symbiosis
Symbiotic interactions between different organisms are relatively rarely preserved in the fossil record. Predatory borings in fossil skeletons are among best‐studied examples of syn vivo interactions between different organisms. Among the best examples of symbiosis are endobionts embedded (i.e. bioimmured) by the living tissues of host organisms (Taylor ; Tapanila ). The earliest microscopic invertebrate symbionts are known from the Cambrian (Bassett et al. ), and there are also macroscopic endobiotic invertebrate symbionts from the Late Ordovician (see Tapanila for a summary). Many of these symbiotic endobionts may have been parasites (Zapalski, ; Zapalski & Hubert ). There are cases of Palaeozoic rugosans being bioimmured by living tissues of stromatoporoids or corals. Bioimmured rugosans differ from bioclaustrations (Palmer & Wilson ) by having their own skeleton. The early symbiotic rugosan endobionts have previously been described from the Aeronian of Baltica (Vinn et al. ) and Llandovery of Laurentia (Nestor et al. ). In addition to rugosans, the tabulate coral Syringopora and cornulitids are also common endobiotic symbionts in the Silurian stromatoporoids of Baltica (Kershaw ; Vinn & Wilson ; Vinn et al. ; Kershaw & Mõtus ). The Silurian of Baltica has a relatively rich record of stromatoporoid‐hosted symbiotic associations, but such associations are also common in the Llandovery of Laurentia (Nestor et al. ). The fauna of rugose corals and stromatoporoids of the Silurian of Estonia is well studied (Kaljo ; Nestor, ). Stromatoporoids and rugosans of the early Rhuddanian and Hirnantian are rather closely related (Kaljo & Nestor ). To better understand the evolution of symbiosis between rugosans and stromatoporoids, it is important know the times these interactions occurred.
The aims of this article are as follows: (1) to describe the earliest known symbiotic rugosan endobionts in stromatoporoids of the Silurian of Baltica; (2) to discuss rugosan–stromatoporoid symbiosis in the Silurian of Baltica; and (3) to discuss the palaeoecology of this early rugosan–stromatoporoid association.

Geological background

During the Silurian, Baltica was located in equatorial latitudes and continued its northwards drift (Cocks & Torsvik ; Torsvik & Cocks ). A shallow epicontinental basin covered middle and western Estonia (Fig. ). This basin had a wide range of tropical environments and diverse biotas (Nestor & Einasto ). Five main environments (i.e. facies belts) have been recognized in the Estonian part of the Baltic basin: tidal flat/lagoonal, shoal, open shelf, basin slope and a basin depression (Nestor & Einasto ). The lagoonal, shoal and open shelf facies belts formed a carbonate platform (Nestor & Einasto ). The dry land was located in the east. These facies belts have in general an E‐W orientation.
Fig. 1. Locality map showing the location of Estonia and exposure of Silurian rocks.
The Juuru Regional Stage (Fig. ) is represented by the Varbola Formation in its lowermost part and the Tamsalu Formation in its upper part. The Juuru Regional Stage represents deposits of one sedimentary cycle in regressive succession. In the study area, nodular biodetrital limestones of the Varbola Formation are followed by Pentamerus limestones and biohermal limestones of the Tamsalu Formation. The Varbola Formation is characterized by a Stricklandia lens and Clorinda undata communities. A community of Pentamerus borealis occurs in the Tamsalu Formation (Nestor ).
Fig. 2. Stratigraphical distribution of stromatoporoids with rugosan endobionts in the Ruddanian of Estonia.

Material and methods

The collection of Estonian stromatoporoids housed at the Institute of Geology, Tallinn University of Technology, contains 794 specimens from the Juuru Regional Stage (Rhuddanian). Six stromatoporoid specimens contain rugosan endobionts. One specimen from the collection of Natural History Museum, University of Tartu, also contains rugosan endobionts.
One large stromatoporoid with rugosans from the Võhmuta Quarry (TUG 1653‐2), Tamsalu Formation, late Rhuddanian. The main section of the Võhmuta quarry (59.088050 N, 25.986940 E) exposes a massive coquinoid rudstone of Borealis borealis of the Tammiku Member. There is a stromatoporoid biostrome in the top part of the section belonging to the Karinu Member (Ainsaar ).
Two large stromatoporoids (GIT 666‐6 and GIT 666‐8) with rugosans from the Eivere Quarry, Varbola Formation, lower Rhuddanian. The Eivere quarry (58.977553 N, 25.576850 E) exposes a fossil‐rich limestone of the Varbola Formation in the lower part and the coquina limestone of the Tamsalu Formation in the upper part of the section (Ainsaar et al. ).
One stromatoporoid (GIT 666‐7) with rugosans from the Sarve peninsula, Hiiumaa Island, Varbola Formation, lower Rhuddanian. The eastern coast of the Sarve Peninsula (58.854167 N, 23.051111 E) is a beach outcrop having up to a 1 m thick section of grainstone rocks of the Juuru Stage (Varbola Formation). In the upper part of the section is a conglomerate with faunal concentrations and ripple marks (Lembit Põlma, unpublished field notes). Most abundant are fossils of brachiopods, rugosans, tabulates and stromatoporoids.
Three studied stromatoporoids (TUG 1653‐2, GIT 666‐6 and GIT 666‐8) were sectioned using a stone saw. Thin sections were made from three stromatoporoids. All together, five longitudinal thin sections were made. The thin sections were scanned with an Epson 4490 scanner. All studied stromatoporoids and rugosans were photographed using a Nikon D7000 digital camera.
All of the studied specimens are deposited in the collections of the Institute of Geology, Tallinn University of Technology (GIT) and the Natural History Museum (Museum of Geology), University of Tartu (TUG).

Results

A single stromatoporoid Ecclimadictyon nikitini (Riabinin, 1951) from the Tamsalu Formation contains a single Donacophyllum middendorffii Dybowski, 1874 endobiont (Figs , 5C). The rugosan is completely embedded in the host stromatoporoid skeleton, leaving only its calyx free on the stromatoporoid growth surface. The rugosan endobiont is oriented perpendicular to the growth layers of the stromatoporoid. A longitudinal section through Enikitini with Dmiddendorffii reveals that the growth rate of the stromatoporoid around the rugosan was the same as in places that are not infested.
Fig. 3. Ecclimadictyon nikitini (Riabinin, 1951) with Donacophyllum middendorffii Dybowski, 1874 from Tamsalu Formation, Võhmuta quarry (TUG 1653‐2).
Two stromatoporoids, Clathrodictyon boreale Riabinin, 1951, from the Varbola Formation contain both three rugosan endobionts (Figs , A, B). In one specimen of C. boreale, there are two Streptelasma estonica Dybowski, 1873 and one Bodophyllum sp. rugosans. All rugosans in Cboreale are completely embedded by the host skeleton, leaving only their calices free on the stromatoporoid growth surface. The edge of the single B. estonicum is partially overgrown by the host stromatoporoid (Fig. B). The stromatoporoid's growth surface is not elevated around B. estonicum. There is a shallow depression around Bodophyllum sp. showing concentric morphology of the stromatoporoid's growth lamellae (Fig. A). The calyx of Bodophyllum sp. reaches slightly above the stromatoporoid's growth surface. The stromatoporoid's growth surface is elevated around the calices of two unidentified rugosan endobionts (Fig. C, D). The calices of unidentified juvenile rugosans are flush with the stromatoporoid's growth surface. All rugosan endobionts are oriented more or less perpendicular to the growth layers of the host stromatoporoid.
Fig. 4. A, Bodophyllum sp. in Clathrodictyon boreale Riabinin, 1951 from the Varbola Formation, Eivere quarry (GIT 666‐6). B, Streptelasma estonica Dybowski, 1873 in Clathrodictyon boreale from the Varbola Formation, Eivere quarry (GIT 666‐6). C, Rugosan in Clathrodictyon boreale from the Varbola Formation, Eivere quarry (GIT 666‐8). D, rugosan in Clathrodictyon boreale from the Varbola Formation, Eivere quarry (GIT 666‐8). E, Streptelasma estonica in a stromatoporoid from the Varbola Formation, Sarve peninsula, Hiiumaa (GIT 666‐7). F, Streptelasma estonica in a stromatoporoid from the Varbola Formation, Sarve peninsula, Hiiumaa (GIT 666‐7).
Fig. 5. A, B, Clathrodictyon boreale Riabinin, 1951 from the Varbola Formation, Eivere quarry (GIT 666‐6 and GIT 666‐8). C, Ecclimadictyon nikitini (Riabinin, 1951) from Tamsalu Formation, Võhmuta quarry (TUG 1653‐2).
A single unidentified stromatoporoid from Varbola Formation contains a single Streptelasma estonica Dybowski, 1873 endobiont (Fig. E, F). The rugosan is completely embedded in the stromatoporoid, having only its calyx free on the stromatoporoid growth surface. The stromatoporoid's growth surface is strongly elevated around the endobiont, forming a small bump flush with the edge of rugosan calyx. The endobiont is oriented perpendicular to the growth layers of the stromatoporoid.

Discussion

Palaeoecology of the rugosan–stromatoporoid association

The syn vivo nature of the Ecclimadictyon nikitiniDonacophyllum middendorffii, Clathrodictyon boreale – rugosans and a stromatoporoid – Streptelasma estonica associations is indicated by the perpendicular to stromatoporoid growth surface orientation of embedded rugosans.
It is difficult to determine the exact nature of these symbiotic associations. It is possible that the stromatoporoid hosts were beneficial for rugosans as elevated substrates on a seafloor that offered a higher tier for feeding. Enhanced substrate stability in the hydrodynamically active shallow waters may also have been beneficial for the rugosans.
The influence of rugosans on the growth of the host stromatoporoid was variable. Bodophyllum sp. seems to have inhibited growth of Clathrodictyon boreale as indicated by the small depression surrounding the endobiont's calyx. There are sweeper tentacles in the modern coral Platygyra (Scleractinia). Platygyra corals often inhibit growth of neighbouring organisms, and this might be interpreted as a case similar to that of Bodophyllum. In contrast, the small unidentified rugosans in Clathrodictyon boreale and Streptelasma estonica in the unidentified stromatoporoid had an opposite effect. Their calices are surrounded by elevation on stromatoporoid's growth surface. The elevation of symbiont calices above the host stromatoporoid surface could have been an antifouling strategy for the symbionts as indicated by the partially overgrown edge of the single Streptelasma estonica. The elevation of symbiont calices to achieve a feeding advantage seems unlikely. In modern sponges, bacteria‐sized particles, below 0.5 micrometres, pass through the ostia and are caught and consumed by choanocytes (Ruppert et al. ). The smallest bacteria‐sized particles are by far the most common; choanocytes typically capture 80% of a sponge's food supply (Ruppert et al. ). Such a diet is unlikely for corals. It is possible that stromatoporoids might benefit from the inclusion of rigid vertical structures, such as corals. Such vertical structures could make the stromatoporoid skeleton stronger and more resistant to physical damage. However, the small number of infesting rugosans per each stromatoporoid does not support that hypothesis.
Stromatoporoids that can be infested by rugosans often occur without rugosans in the same paleoenvironment (Nestor ; Kaljo & Nestor ). Similarly, rugosans found in stromatoporoids could grow without stromatoporoid hosts in the same paleoenvironment (Kaljo & Nestor ). Thus, this association was not obligate for stromatoporoids and rugosans. Most likely the described association is an example of facultative symbiosis.

Rugosan–stromatoporoid symbiosis in the Silurian of Baltica

Symbiosis between rugosans and stromatoporoids is common throughout the Silurian of Baltica. Numerous symbiotic rugosans occur in the stromatoporoids of the Silurian of Gotland (Mori, ; Kershaw ). Similar rugosan–stromatoporoid associations have been described from the Aeronian (two specimens infested of 35) and late Sheinwoodian (three specimens infested of 60) of Estonia (Vinn & Mõtus ; Vinn et al. ). Rugosans are especially common in the stromatoporoids from the Ludlow of Estonia; usually there are numerous rugosan specimens per single stromatoporoid host (Nestor ; Vinn et al. ; Kershaw & Mõtus ). A solitary symbiotic rugosan has been recently described from a stromatoporoid of the Pridoli of Saaremaa (a single specimen infested of 18 stromatoporoids), Estonia (Vinn & Wilson ), but in this association, only two rugosans occur in a relatively large stromatoporoid. This described early Rhuddanian association differs from Aeronian, Sheinwoodian and Ludlow associations by the smaller number of rugosan symbionts per stromatoporoid host. Thus, it is possible that the early cases of stromatoporoid–rugosan symbiosis always involved small number of rugosan symbionts in a single host. The later (i.e. Aeronian) appearance of stromatoporoids with a large number of rugosans may indicate increasing host tolerance for rugosan symbionts. The stromatoporoids with symbiotic rugosans seem to be relatively rare in the Llandovery of Baltica (Vinn et al. ), but they became common in the Ludlow (Nestor, O. Vinn, personal observation). The number of rugosan symbionts per host and number of stromatoporoids with symbionts seem to have increased during the evolution of rugosan–stromatoporoid symbiosis in the Silurian of Baltica.

Symbiotic rugosans in stromaporoids

There are only a few records of symbiotic rugosans in the stromatoporoids from territories outside of Baltica. Numerous cases of stromatoporoid–rugosan symbiosis have been described from the Aeronian of Anticosti Island (Laurentia) (Nestor et al. ). The Anticosti associations in the Llandovery are similar to Baltic ones. Both stromatoporoids with few and numerous rugosan symbionts occur in the Llandovery of Baltica and Laurentia. Several rugosan species infested several stromatoporoid species both in the Llandovery of Baltica and Laurentia. In addition to North America and Baltica, rugosans occur only in the stromatoporoids of the Devonian of Spain (Soto & Méndez Bedia ).

Other symbiotic endobionts in the Silurian stromatoporoids

Ecclimadictyon nikitini (Riabinin, 1951) from the Rhuddanian of Anticosti Island (Laurentia) is known to contain cornulitid endobionts. Similar cornulitid – stromatoporoid association occurs in the Sheinwoodian of Estonia (Vinn & Wilson ). Llandovery stromatoporoids, both in Baltica and Laurentia, hosted worm endobionts leaving Chaetosalpinx bioclaustrations. Helicosalpinx bioclaustrations in stromatoporoids are known from the Ludlow of Estonia (Vinn & Mõtus ). In addition to worms and cornulitids, lingulate brachiopods also inhabited cavities in living stromatoporoids both in Baltica and Laurentia (Tapanila ; Nestor et al. ).

Symbiotic endobionts after O/S mass extinction

Symbiotic endobionts seem to be common among O/S mass‐extinction recovery faunas. Rhuddanian and Aeronian stromatoporoids hosted rugosans, cornulitids, Chaetosalpinx and lingulates (Tapanila ; Nestor et al. ; Vinn et al. ). Chaetosalpinx occurs in the Rhuddanian tabulate corals (Nestor et al. ; Vinn et al. ). Cornulitids are known from the Aeronian tabulates of Anticosti Island (Dixon ). It seems that the O/S mass extinction did not have strong negative effect on symbiotic interactions, or such an effect was lacking.

Acknowledgements

Financial support to O.V. was provided by a Palaeontological Association Research Grant and Estonian Research Council projects ETF9064 and IUT20‐34. We thank Heldur Nestor for identifying the stromatoporoids and Dimitri Kaljo for identification of the rugosans. We are grateful to P. Tonarová, M. Kubajko and A. Uffert for the collecting stromatoporoid specimens. Further we are grateful to A. Uffert and G. Baranov, Institute of Geology, Tallinn University of Technology, for preparations and making thin sections and photographing the specimens. This article is a contribution to IGCP 653 ‘The onset of the Great Ordovician Biodiversity Event’. We are grateful to M.A. Wilson, The College of Wooster for improvements to the manuscript and M. Zapalski from the University of Warsaw and an anonymous reviewer for constructive reviews.

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Go to Lethaia
Volume 50Number 21 April 2017
Pages: 237243

History

Received: 21 April 2016
Accepted: 22 June 2016
Published online: 14 October 2016
Issue date: 1 April 2017

Authors

Affiliations

Department of Geology, University of Tartu, Ravila 14 A 50411, Tartu, Estonia;
Ursula Toom [email protected]
Institute of Geology, Tallinn University of Technology, Ehitajate tee 5, 19086 Tallinn, Estonia;

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