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Coralline red algae from the Silurian of Gotland indicate that the order Corallinales (Corallinophycidae, Rhodophyta) is much older than previously thought

Article in Palaeontology · January 2019 DOI: 10.1111/pala.12418

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CORALLINE RED ALGAE FROM THE SILURIAN OF GOTLAND INDICATE THAT THE ORDER CORALLINALES (CORALLINOPHYCIDAE, RHODOPHYTA) IS MUCH OLDER THAN PREVIOUSLY THOUGHT by SEBASTIAN TEICHERT1 , WILLIAM WOELKERLING2 and AXEL MUNNECKE1 1Fachgruppe Pal€aoumwelt, GeoZentrum Nordbayern, Friedrich-Alexander-Universit€at Erlangen-Nurnberg€ (FAU), Erlangen, Germany; [email protected] 2Department of Ecology, Environment & Evolution, La Trobe University, Kingsbury Drive, Bundoora, Victoria 3086, Australia

Typescript received 30 August 2018; accepted in revised form 3 December 2018

Abstract: Aguirrea fluegelii gen. et sp. nov. (Corallinales, within the family Corallinaceae and order Corallinales. Corallinophycidae, Rhodophyta) is described from the mid- Extant evolutionary history studies of Corallinophycidae Silurian of Gotland Island, Sweden (Hogklint€ Formation, involving molecular clocks now require updating using new lower Wenlock). The holotype is of dimerous construction calibration points to take account of the much earlier and includes a uniporate conceptacle with a sporangium, unequivocal mid-Silurian record of uniporate conceptacle- thus providing evidence that taxa of the Corallinales/Coralli- bearing taxa of Corallinales/Corallinaceae as well as the naceae existed at least 300 million years earlier than previ- parallel record of Graticula, a genus attributed to the ously documented. Aguirrea fluegelii cannot be unequivocally Sporolithales. placed in any of seven currently recognized lineages/subfami- lies/groups of the Corallinaceae as not all diagnostic charac- Key words: Aguirrea fluegelii, conceptacles, Corallinaceae, ters are preserved, and thus is accorded incertae sedis status Corallinales, coralline red algae, Gotland.

R ED ALGAE (Rhodophyta) in which calcification occurs in Recent taxa of Corallinales/Corallinaceae occur world- the form of calcite are presently grouped into the subclass wide and are found in tidal pools to more than 250 m Corallinophycidae Le Gall & Saunders (2007) and water depth (Foster 2001). They include species that func- comprise four orders: the Corallinales, Hapalidiales, tion as carbonate factories (Basso 2012; Teichert & Frei- Rhodogorgonales and Sporolithales (Le Gall et al. 2010; wald 2014) and as ecosystem engineers that enhance Nelson et al. 2015; Rosler€ et al. 2016, 2017). Species of community biodiversity (Kamenos et al. 2004; Teichert the Corallinales are characterized by the occurrence of 2014). Their function in cementing and strengthening uniporate tetrasporangial conceptacles rather than multi- Cenozoic and modern coral reefs is well known (Castro & porate conceptacles or calcified sporangial compartments, Huber 2010) but compared to corals, their ecological role which respectively occur in the Hapalidiales (Nelson et al. in ecosystems is often neglected, in part due to difficulties 2015) and Sporolithales (Le Gall et al. 2010), two other in reliable taxonomic identification (Aguirre & Braga orders of Corallinophycidae that are known from the fos- 2005), and also because the time of origin of the Coralli- sil record. Within the Corallinales, we follow Basso & nales/Corallinaceae and other Corallinophycidae is not Granier (2018), Caragnano et al. (2018), Cormaci et al. certain. (2017), Kamiya et al. (2017), Nelson et al. (2015) and Prior to this study, the Corallinales/Corallinaceae were Rosler€ et al. (2016, 2017), all of whom place all taxa/lin- thought to have emerged during the late Early Cretaceous eages/groups into a single family, the Corallinaceae. This to early Late Cretaceous (Aguirre et al. 2010; Rosler€ et al. contrasts with Athanasiadis (2016, p. 292) and Townsend 2017; Yang et al. 2016), about 15–30 myr after the oldest & Huisman (2018, pp. 86–87), who recognized more than known unequivocal records of taxa of Sporolithaceae one family within the Corallinales. (Tomas et al. 2007; Woelkerling et al. 2014) from the

© The Palaeontological Association doi: 10.1111/pala.12418 1 2 PALAEONTOLOGY upper Hauterivian. Another much older group attributed and isotype of Aguirrea fluegelii were gathered at the same to the Sporolithales, the Graticulaceae (Brooke & Riding time from the same outcrop. 2000), dates from the Wenlock epoch of the Silurian. The raw material was formatized using a low speed dia- Further details on the evolutionary history of the Coralli- mond rock saw. Sample surfaces were ground using carbon nales/Corallinaceae are summarized by Rosler€ et al. (2017, silicide in 120, 220, 400 and 800 graining and mounted on â pp. 570–573). glass surfaces with Biresin (https://advanced-resins.sika. In this study, we show that species of Corallinales/ com/gbr/en/group.html). Microphotography in normal and Corallinaceae much older than the Cretaceous with char- fluorescent transmitted light was done with a Zeiss Axio acteristic spore-bearing uniporate conceptacles unequivo- Imager 2 equipped with a Zeiss Axiocam MRc5. High reso- cally existed. Our material, belonging to the newly lution images were captured on a Zeiss LSM800 confocal described fossil-genus and species, Aguirrea fluegelii, was laser scanning microscope. Both devices were operated using found in the lower Wenlock Stage (c. 430–434 Ma) of the the Zeiss ZEN software package. We examined 30 newly pre- Silurian of Gotland Island, Sweden, a region well-known pared 5 9 5 cm thin sections from the Gutev€agen material, (Munnecke & Servais 2008) for its outstanding fossil two of which contained one specimen of A. fluegelii each, quality. We provide a detailed taxonomic account and representing the holotype and the isotype. All sections are discuss the implications for the evolutionary history of now housed at GZN except for the two sections containing the Corallinales/Corallinaceae. the holotype and isotype of A. fluegelii, which are housed at SNSB-BSPG under the inventory numbers SNSB-BSPG 2017 I 53 (holotype) and SNSB-BSPG 2017 I 54 (isotype). MATERIAL AND METHOD

Sample material Geological setting, facies and palaeoenvironment

Samples were collected from the lower part (c. 1.5 m Gotland Island is composed of a series of stacked Silurian above base) of a roughly 8 m section in Visby (Gutev€agen 2; tropical carbonate platforms ranging in age from late 57°37046.8″N18°16050.9″E) on the west coast of Gotland Llandovery to late Ludlow (Calner et al. 2004). The east- Island, Sweden by AM in 2000 (Fig. 1A, B). The holotype ern part of Gotland is dominated by shallow-water

A C

B

FIG. 1. Geographical and lithological context. A, map of the island of Gotland, Sweden, indicating the outcrop area in Visby (Gutev€agen 2; 57°37046.8″N18°16050.9″E). B, sketch map of the outcrop area. C, profile of the study site, sampling horizon is c.30cm below the position of the hammer, lithology according to Riding & Watts (1981). TEICHERT ET AL.: CORALLINALES FROM THE SILURIAN OF GOTLAND 3 lagoonal and backreef deposits whereas the western part and thus the taxonomic affinities of Aguirrea fluegelii to the is mainly composed of limestones and marls of an open Corallinales could only be elucidated from evident shelf environment (Samtleben et al. 1996). morpho-anatomical features (see below). The taxonomic The samples containing A. fluegelii belong to the Hog-€ disposition of Aguirrea fluegelii within the Corallinales/ klint Formation (Fig. 1C, lower Wenlock, lowermost Corallinaceae is considered further in the Discussion. Ozarkodina sagitta rhenana Conodont Zone (Riding & Watts 1981; Jeppsson 2008). The outcrop represents a Institutional abbreviations. GZN, GeoZentrum Nordbayern, Fach- shallowing-upward sequence of reef-derived bioclastic rud- gruppe Pal€aoumwelt, Friedrich-Alexander-Universit€at Erlangen- stones (5 m thick), mostly composed of remnants of Nurnberg€ (FAU), Erlangen, Germany; SNSB-BSPG, Staatliche crinoids, bryozoans, tabulate corals, brachiopods, stromato- Naturwissenschaftliche Sammlungen Bayerns, Bayerische € € poroids and calcareous algae. These deposits are overlain Staatssammlung fur Palaontologie und Geologie, Staatliche Natur- wissenschaftliche Sammlungen Bayerns, Munchen,€ Germany. by a prograding biostromal stromatoporoid reef (3 m thick), and an encrusted reef crest on top (0.3 m thick) mainly composed of specimens of ‘Solenopora’(later SYSTEMATIC PALAEONTOLOGY described as Graticula by Brooke & Riding (1998, 2000) and further assessed by Nose et al. (2006)), Parachaetetes by William Woelkerling, Sebastian Teichert and Axel and Hedstroemia (?cyanobacteria) (Riding & Watts 1981). Munnecke

Terminology and taxonomy Phylum RHODOPHYTA Wettstein, 1901 Class FLORIDEOPHYCEAE Cronquist, 1960 Morpho-anatomical terminology follows Hrabovsky et al. Subclass CORALLINOPHYCIDAE Le Gall & Saunders 2007 (2015) and Rosler€ et al. (2016) and is ultimately based on Order CORALLINALES Silva & Johansen, 1986 that in Woelkerling (1988) for thallus features and Family CORALLINACEAE Lamouroux, 1812 Woelkerling et al. (1993) for growth forms. Nomenclatu- ral conventions follow Turland et al. (2018). Genus AGUIRREA nov. The terms ‘coralline red algae’ and ‘coralline red algal’ apply here only to taxa belonging to the Phylum Rhodo- Derivation of name. The generic name honours Julio phyta, Class Florideophyceae, Subclass Corallinophycidae. Aguirre (Universidad de Granada) for his extensive contri- The above terms (sometimes shortened to ‘coralline algae’ bution to our understanding of fossil Corallinophycidae. and ‘coralline algal’) (e.g. Dixon 1973, p. 57; Johansen 1981; Rosler€ et al. 2017) or to corallines (e.g. Harvey 1847, text to pl. 73; Harvey 1849, p. 104) do not apply to putative fossil Type and only known species (designated here). Aquirrea ‘ancestors’ of the Corallinophycidae which are non-calcified fluegelii Woelkerling, Teichert & Munnecke, sp. nov. but sometimes have been referred to as ancestral corallines, (Figs 2, 3). stem corallines, etc. (e.g. see Xiao et al. 2004; Yang et al. 2016). The term ‘ancestral corallines’ also has been applied Diagnosis. Thallus calcified, pseudoparenchymatous, com- to a group of poorly known late Palaeozoic taxa of uncertain posed of multicellular laterally coherent filaments; pos- affinity and in need for further assessment; Brooke & Riding sessing uniporate conceptacles and evidence of bi- or (1998, p. 193) provided further information. The terms ‘co- tetrasporangia; genicula absent; other features (e.g. occur- ralline red algae’, ‘coralline red algal’ etc. also do not apply rence of cell fusions, occurrence of secondary pit-connec- to Recent or fossil red algae in which calcification occurs in tions, occurrence of palisade cells, conceptacle pore canal the form of aragonite (e.g. various genera of the Nemaliales, anatomy, mode of conceptacle roof formation) consid- see Cormaci et al. 2017; the genus Rhodopeltis in the Gigarti- ered diagnostic of currently recognized non-fossil genera € nales, see Huisman 2000, p. 90). or groups thereof (Bittner et al. 2011; Rosler et al. 2016; Based on recent molecular studies (Nelson et al. 2015; Caragnano et al. 2018) inadequately preserved. Yang et al. 2016) using DNA sequence data from living species, four major lineages within the subclass Corallino- phycidae have been detected. Taxonomically, each has been Aquirrea fluegelii sp. nov. recognized as a distinct order, namely the Corallinales, Figures 2, 3 Hapalidiales, Rhodogorgonales and Sporolithales. Distin- guishing morpho-anatomical features are summarized in Derivation of name. The species epithet honours the late Table 1. Molecular data from fossil Corallinophycidae is Erik Flugel€ (1934–2004) for his extensive contribution to virtually non-existent (an exception is Hughey et al. 2008) our understanding of fossil algae. 4 PALAEONTOLOGY

TABLE 1. Comparison of taxonomically significant morpho-anatomical characters of the Orders of Corallinophycidae. Corallinales Hapalidiales Rhodogorgonales Sporolithales

Calcification Crystalline form Calcite Calcite Calcite Calcite Occurrence Impregnated in walls of Impregnated in walls of Limited to husks Impregnated in walls most vegetative cells most vegetative cells surrounding scattered of most vegetative calciferous cells cells Vegetative features Thallus appearance Calcified Calcified Gelatinous or Calcified cartilaginous Thallus growth Subapical meristematic Subapical meristematic Diffuse Subapical cells cells meristematic cells Occurrence of genicula Present in some genera; Unknown Unknown Unknown absent in other genera Secondary pit-connections Present in some Unknown Unknown Present in some groups; absent in species; unknown in others others Cell fusions Present in some Present in nearly all Unknown Present in some groups; absent in taxa but unknown in species but rare or others several genera unknown in others Reproduction Carpogonial branches Formed in uniporate Formed in uniporate Formed on cortical Formed in uniporate and carposporophytes conceptacles conceptacles fascicles, not in conceptacles conceptacles Spermatangia Formed in uniporate Formed in uniporate Formed on cortical Formed in uniporate conceptacles conceptacles fascicles, not in conceptacles conceptacles Tetrasporangia/bisporangia Formed in uniporate Formed in multiporate Formed on Formed in calcified conceptacles conceptacles carposporophyte sporangial gominoblast filaments compartments Tetrasporangial cleveage Zonate Zonate Irregularly zonate Cruciate

Sources of data: Cormaci et al. (2017); Fredericq & Norris (1995); Le Gall et al. (2010); Nelson et al. (2015); Rosler€ et al. (2016, 2017).

Holotype (designated here). SNSB-BSPG 2017 I 53, housed filaments (partially evident in Fig. 2A on lower right side) in the Bayerische Staatssammlung fur€ Pal€aontologie und and numerous calcified, upright, branched, laterally Geologie, Staatliche Naturwissenschaftliche Sammlungen coherent, multicellular filaments that form the bulk of Bayerns, Richard-Wagner-Straße 10, 80333 Munchen,€ each thallus. This kind of anatomy is termed pseudo- Germany. The holotype is depicted in Figure 2. parenchymatous and dimerous (Woelkerling 1988) and also occurs within the Corallinophycidae in a number of Isotype (designated here). SNSB-BSPG 2017 I 54, housed species of Corallinales, Hapalidiales and Sporolithales (e.g. in the Bayerische Staatssammlung fur€ Pal€aontologie und see examples in Bassi et al. 2009; Harvey et al. 2006; Geologie, Staatliche Naturwissenschaftliche Sammlungen Hrabovsky et al. 2015; Van der Merwe et al. 2015; Bayerns, Richard-Wagner-Straße 10, 80333 Munchen,€ Woelkerling 1988). Germany. The isotype is depicted in Figure 3. Unlike other red algae, walls of most cells of taxa of Corallinales, Hapalidiales and Sporolithales (Table 1) are Diagnosis. With the characteristics of the genus, encrust- impregnated with calcite (Le Gall & Saunders 2007) thus ing growth form and dimerous thallus construction appearing calcified and often stony when alive, and com- evident. monly becoming preserved in marine fossil formations. Calcification occurs intracellularly with varying amounts

Remarks. Individuals of Aguirrea fluegelii (Figs 2A, 3A) of MgCO3 and regarding recent counterparts of the are encrusting in growth-form (Woelkerling et al. 1993) Corallinaceae, this amount ranges from 9.0–25.2 wt.% and consist of a single ventral layer of calcified, coherent (Smith et al. 2012). The subsequent stabilization of this TEICHERT ET AL.: CORALLINALES FROM THE SILURIAN OF GOTLAND 5

A

B

FIG. 2. Holotype of Aguirrea fluegelii (thin section SNSB-BSPG 2017 I 53). A, longitudinal section of encrusting thallus showing dorsiventral organization and dimerous construction and a uniporate conceptacle (black arrow) with remains of a single sporangium (arrowhead) on left side; white arrows denote elongate cavities; thallus margin is on left. B, enlarged view of sporangial conceptacle depicted in (A) with remains of a sporangium (arrow). Scale bars represent 500 lm (A); 125 lm (B). Colour online. high-Mg calcite is connected with a magnesium loss and This subsequent stabilization and the filling of cell cavities interpreted as a congruent dissolution of high-Mg calcite with calcite immediately after dead tissue is buried within and precipitation of low-Mg calcite (Oti & Muller€ 1985). the thallus by outward surface growth (Bosence 1991) 6 PALAEONTOLOGY

A

B C

FIG. 3. Isotype of Aguirrea fluegelii (thin section SNSB-BSPG 2017 I 54) in fluorescent light. A, longitudinal section of an epiphytic encrusting thallus (E) anchored to a calcified host (H), probably a graticulacean alga; note conceptacle (arrow) sectioned peripheral to the pore canal. B, enlarged view of conceptacle depicted in (A) with a crystal structure near the right top of the conceptacle chamber. C, en- larged view of the crystal contained in the conceptacle chamber depicted in (B). Scale bars represent 500 lm (A); 250 lm (B); 50 lm (C). also contribute to the high preservation potential of fossil ‘tentative’ assignment (Granier & Dias-Brito 2016a, p 215; coralline red algae like A. fluegelii in sediments of Palaeo- 2016b, p. 233) of four previously described fossil-genera zoic age. (Cordilites Pocta, 1887; Elianella Pfender & Basse, 1948; Calcite formation also occurs in the Rhodogorgonales Marinella Pfender, 1939; Parachaetetes Deninger, 1906) (Table 1) but is limited to scattered husks surrounding cer- with presumed calcite impregnated cell walls rather than tain specialized vegetative cells (Fredericq & Norris 1995; scattered husks to the Rhodogorgonales requires further Le Gall et al. 2010; Townsend & Huisman 2018). The consideration. We fully agree with Granier & Dias-Brito TEICHERT ET AL.: CORALLINALES FROM THE SILURIAN OF GOTLAND 7

(2016a, b) that the assignment of the four genera to the no evidence that they are bounded by distinct self-gener- Rhodogrogonales is ‘tentative’, not only because of the ated cell walls such as those evident in non-fossil species absence of calcified husks, but also because no reproductive of Lithophyllum depicted by Basso et al. (2014) or those structures are known and no other features characteristic of evident in a fossil species of Hydrolithon by Woelkerling the Rhodogorgonales (Table 1) are evident. et al. (2012). The cavities may involve micro-borings of Only very rarely do conceptacles or compartments in some kind or simply be artefacts of thin-section prepara- fossil specimens have preserved gametangia or sporangia tion. As noted by Basso et al. (2014), trichocytes may or (Braga 2006; Woelkerling et al. 2012, 2013, 2014). Never- may not be present within a given genus of Corallinales, theless, fossil specimens with empty sporangial compart- and thus in most cases are of limited value in assigning ments or with empty multiporate conceptacles are readily specimens to genera. identifiable to order level. By contrast, fossil specimens The question of whether the structures depicted in Fig- with empty uniporate conceptacles usually are more diffi- ures 2A and 3A–B represent trace fossil (ichnotaxa) mac- cult to place taxonomically because gametangial concepta- roborings attributable to boring organisms rather than cles of Sporolithales, Hapalidiales and Corallinales as well conceptacles requires brief consideration. Like macrobor- as tetrasporangial conceptacles of Corallinales are unipo- ings (Checconi & Monaco 2008; Checconi et al. 2010) in rate (Table 1). Conceptacles are unknown in species of red algal rhodoliths, the chambers in Figures 2A and 3A– Rhodogorgonales. B are over 300 lm in diameter (Table 2). The facts, how- One specimen of Aguirrea fluegelii (Fig. 2A, B) contains ever, are that: (1) there is a distinct indication of a single a uniporate conceptacle with remains of a sporangium. pore canal (Fig. 2A); (2) a chamber containing the The sporangium is either a tetrasporangium or a bispo- remains of a non-crystalline inclusion with the character- rangium (no unequivocal divisions of sporangium con- istics of a sporangium (Fig. 2A) occurs; and (3) a dome tents are evident) that developed from the conceptacle like roof (Fig. 3B) covering the chamber and protruding chamber floor. Its position on the conceptacle chamber above the thallus surface (Fig. 3A) is present, all of which floor, the distinctive ovate-ellipsoidal appearance in longi- strongly support the conclusion that conceptacles are pre- tudinal section, and the rounded ends and smooth sent and have a single pore canal. Numerous conceptacles margins are all characteristic of tetrasporangia and bispo- with these features are depicted in Harvey et al. (2006), rangia, numerous examples of which are depicted in the Woelkerling & Campbell (1992) and other publications literature (e.g. Farr et al. 2009; Johansen 1981; Harvey cited in the References section of this account. We are et al. 2006; Woelkerling 1988; Woelkerling et al. 2012). unaware of any macroborings that mimic such concepta- There is no evidence of carposporophyte remains, and cles in appearance. thus it is extremely unlikely that the structure is a car- Whether or not A. fluegelii is a common species in the posporangium. Unfortunately, details of pore canal anat- Hogklint€ Formation of Gotland Island remains uncertain. omy (which are important in distinguishing some genera) In the 30 newly prepared thin sections, we encountered and the immediate surrounding thallus surface are not two individuals: the holotype and the isotype. No other well preserved, but there is a distinct indication of a dimerous corallines were observed, although some sterile single, central pore canal characteristic of uniporate (and thus unidentifiable to order level) fragments of conceptacles. monomerous coralline-like algae were encountered. This Another specimen (Fig. 3A, B) contains a conceptacle suggests that the species may not be common in the with a dome-like roof sectioned off-centre (to one side) Hogklint€ Formation of Gotland Island, but numerous of the pore rather than through the pore, and no sporan- additional sections need to be examined from Visby and gia are present. A small crystal structure vaguely resem- bling a spore occurs (Fig. 3B, C) but there is no suggestion of organic remains. TABLE 2. Measured characters for Aguirrea fluegelii. Data on measured characters are summarized in Cell length 38–160 µm Table 2. The taxonomic significance of measured charac- Cell diameter 19–30 µm ters is uncertain; small differences in measured characters Length/diameter ratio 2–5.3 are often considered significant when comparing fossil Conceptacle chamber diameter 420–465 µm material but are generally of little value in taxonomic Conceptacle chamber height 140–165 lm delimitation of Recent corallines. without pore canal µ One reviewer asked for our opinion about several small Length of sporangium 116 m Diameter of sporangium 90 µm elongated cavities in the holotype (Fig. 2A, white arrows) Size of crystal structure in Fig. 2C 62 µm long; 52 µm broad because of their similarities with trichocytes of the sort reported by Basso et al. (2014). These cavities are very Cell and conceptacle data derive from the holotype and the iso- unlikely to represent trichocytes because we have found type. Sporangium data derive from the holotype only. 8 PALAEONTOLOGY other nearby localities to make a more informed judge- A third problem is that not all of the morpho-anatomi- ment on relative abundance of the species in this region. cal characters necessary to fully determine the taxonomic From a taxonomic point of view, however, there is no affinity of A. fluegelii have been preserved in our material. doubt that A. fluegelii possesses morpho-anatomical Evident characters and characters not adequately pre- features of a species that belongs to the Corallinales/ served for taxonomic identification purposes are included Corallinaceae. in the generic diagnosis of A. fluegelii. As a result, while Aguirrea belongs to the Corallinales/Corallinaceae, its placement within the family remains uncertain (Table 3). DISCUSSION Rosler€ et al. (2016), using DNA sequence data involv- ing two nuclear markers (SSU, LSU), two plastidial mark- Taxonomic placement of Aguirrea within the Corallinales/ ers (psbA, 23S) and one mitochondrial marker (COI), Corallinaceae detected seven major lineages within the Corallinaceae and thus within the Order Corallinales (Table 3). Six lin- The precise taxonomic placement and phylogeny of eages were interpreted taxonomically as subfamilies and Aguirrea fluegelii within the Corallinales/Corallinaceae are one was interpreted as a taxonomically unnamed group. hampered by three problems. The first, as noted by Rosler€ Rosler€ et al. (2016) noted that the ‘southern hemisphere et al. (2016, pp. 412, 413), is that ‘the taxonomy of coral- group’ included species hitherto referred to Spongites or line algae is not resolved at any rank’ and ‘even at the Pneophyllum, that that group was difficult to delimit from subfamily rank, the taxonomy of coralline algae is still other genera or even subfamilies in their study, and that unresolved’. The outcomes of recent analyses of Bittner the group needed a ‘profound analysis of molecular and et al. (2011), Kato et al. (2011), Hind et al. (2016), Rosler€ morphological affinities of a larger number of specimens et al. (2016, 2017) and Caragnano et al. (2018) based on and a revision of the generic and specific attribution of DNA sequence data all differ. This also has resulted in the component species’. Additional data on the taxa in different classification constructs based on morpho-anato- the southern hemisphere group mentioned in Rosler€ et al. mical data. Hrabovsky et al. (2015, p. 500), for example, (2016) can be found in Farr et al. (2009), Harvey et al. followed a classification scheme based on data in Harvey (2005) and Penrose (1996a, b). Recently, however, Carag- et al. (2003) and Kato et al. (2011) that also was used in nano et al. (2018, p. 403) concluded from a 4-marker August 2013 in AlgaeBase (http://www.algaebase.org). In (SSU, LSU, psbA, COI) DNA sequence analysis that the dealing with the marine benthic flora of the Mediter- southern hemisphere group constituted a new subfamily ranean Sea, by contrast, Cormaci et al. (2017, pp. FP184– (the Chamberlainoideae) that also included taxa from the FP187) summarized morpho-anatomical subfamily differ- northern hemisphere and that ‘has no diagnostic morpho- ences within the Corallinaceae based mainly on data in anatomical features that enable one to assign a specimen Kato et al. (2011) and Rosler€ et al. (2016). Because, as to it without DNA sequence data.’ noted by Rosler€ et al. (2016, pp. 412, 413), the taxonomy When characters evident in A. fluegelii are compared at the subfamily rank remains unresolved, the elevation of (Table 3) with the taxonomically significant morpho-ana- some (but not all) subfamilies to family rank (see Athana- tomical characters in the lineages/subfamilies/groups of siadis 2016, p. 292; Townsend & Huisman 2018, pp. 86– Corallinaceae listed in Rosler€ et al. (2016) and Cormaci 87) also has not provided resolution and thus has not et al. (2017), it is not possible to unequivocally place been adopted for this study since this only would result A. fluegelii in any of the lineages elucidated by Rosler€ in uncertain family placement for Aguirrea within the et al. (2016) and recognized by Cormaci et al. (2017). If, Corallinales. As noted by Townsend & Huisman (2018, for example, a distinct basal layer of palisade cells had p. 87), there is no single morpho-anatomical character been preserved in A. fluegelii, the species would most that separates family groups, and distinguishing these likely belong to either the Lithophylloideae or the Masto- families in a key is somewhat problematic without DNA. phoroideae, but the fact that cell connections between The situation at subfamily level has become similar, as cells of adjacent filaments are not discernible precludes noted by Caragnano et al. (2018, p. 403). any definite placement. Similarly, A. fluegelii cannot be A second problem is that it is impossible to obtain placed in any particular subfamily based on thallus con- DNA sequence data from 430+ million year old material struction and/or the occurrence of genicula, and in the of A. fluegelii because DNA degrades with time and is absence of DNA data, it is impossible to assess what unlikely to survive for more than 1 million years (Hughey affinities A. fluegelii might have to the Chamberlainoideae et al. 2008, p. 375). Consequently, it is not possible to (Caragnano et al. 2018). From a palaeontological perspec- undertake molecular-based phylogenetic analyses to eluci- tive, one also could consider that the morpho-anatomical date taxonomic affinities from an evolutionary point of characters evident in A. fluegelii might be ancestral to view. characters known from recent coralline red algae. What is TABLE 3. Comparison of characters evident in Aguirrea flugelii with taxonomically significant morpho-anatomical characters used by Rosler€ et al. (2016) and Cormaci et al. (2017) to distinguish lineages/subfamilies/groups of Corallinaceae. Aguirrea fluegelii Corallinoideae Hydrolithoideae Lithophylloideae Mastophoroi- Metagoniolithoideae Neogo- Southern deae niolithoideae hemisphere group. (no subf. name)1

Type species Not applicable Corallina Hydrolithon Lithophyllum Mastophora rosea Metagoniolithon Neogoniolithon Not applicable officinalis reinboldii (= incrustans charoides (= fosliei (not in Rosler€ H. boergesenii) M. radiatum) TEICHERT et al. 2016 Fig. 1) Number of Not applicable 1 1 1 1 22 23 1 unnamed

clades clade AL ET Vegetative traits Thallus Dimerous Monomerous Dimerous Dimerous and/or Dimerous Monomerous Dimerous Dimerous :CRLIAE RMTESLRA FGOTLAND OF SILURIAN THE FROM CORALLINALES .: construction and/or monomerous and/or and/or monomerous monomerous monomerous Genicula: Absent Present or Absent Present or absent at Absent Present or absent at Absent not indicated in occurrence absent genus level genus level Rosler€ et al. at genus level (2016) Genicula: Not applicable 1 tier of cells Not applicable 1 or more tiers of Not applicable Several cells long, Not applicable not indicated in structure not cells untiered Rosler€ et al. (2016) Cell fusions Preservation Present Present Absent or rare Present Present Present not indicated in inadequate Rosler€ et al. (2016) Secondary pit preservation absent absent present absent or very absent absent not indicated in connections inadequate rare Rosler€ et al. (2016) Basal or central Uncertain; some Absent No data in Present in some Present Absent Absent Not indicated in layer of palisade cells Rosler€ et al. taxa, absent in Rosler€ et al. palisade cells may be present (2016) or others (2016) Cormaci et al. (2017)

(continued) 9 10 PALAEONTOLOGY

TABLE 3. (Continued) Aguirrea fluegelii Corallinoideae Hydrolithoideae Lithophylloideae Mastophoroi- Metagoniolithoideae Neogo- Southern deae niolithoideae hemisphere group. (no subf. name)1

Occurrence of Trichocytes No No; but see No No Yes, but only in Trichocytes Not indicated in horizontal not seen Woelkerling clade that includes occur but Rosler€ et al. fields et al. (2012) type sp. of arrangement (2016) of trichocytes Porolithon not indicated Reproductive traits Mode of Uncertain From peripheral From peripheral From peripheral From peripheral From peripheral From peripheral From peripheral tetrasporangial filaments only and and interspersed filaments only and interspersed filaments only and conceptacle interspersed filaments or from filaments interspersed roof filaments perhipheral filaments or formation filaments only from perhipheral filaments only Position of Spermatangia Floor and side Floor only Floor only Floor only Floor only Floor and roof Not indicated in spermatangia unknown walls Rosler€ et al. in (2016) conceptacle chamber

1Southern hemisphere group not dealt with by Cormaci et al. (2017). 2In the Metagoniolithoideae, one unnamed clade includes the type species of Porolithon, P. onkodes; second unnamed clade includes three subclades, one including type species of Metagoniolithon, M. radiatum, one including the type species of Harveylithon, H. rupestre; and one including type species of Paragoniolithon (P. conicum, listed as Pneophyllum). 3In the Neogoniolithoideae, one unnamed clade includes the type species of Spongites, S. fruticulosus; the second includes the type species of Neogoniolithon, N. fosliei. TEICHERT ET AL.: CORALLINALES FROM THE SILURIAN OF GOTLAND 11 unequivocal, however, is that A. fluegelii produces unipo- calcified compartments, however, are evident in the Roth- rate sporangial conceptacles and thus belongs to the pletz figures. Corallinales (Table 1) and thus to the Corallinaceae (as Since then, most authors (e.g. see references in Johnson circumscribed in this account). Aguirrea fluegelii is the 1960; Moussavian 1989; Poignant 1991) have treated third fossil species of Corallinales in which a uniporate Solenopora and the Solenoporaceae Pia, 1927 (p. 97) as conceptacle has been found with remains of a bi/tetraspo- taxa of calcified red algae. Riding (2004), however, con- rangium. Remains of fossil tetrasporangia also are known cluded from a detailed study that the type species of in Hydrolithon braganum (Woelkerling et al. 2012) and Solenopora, S. spongioides Dybowski, is a chaetetid sponge Lithophyllum kenjikonishii (Woelkerling et al. 2013). as originally thought by Dybowski (1877), not a red alga. Aguirrea fluegelii constitutes an important discovery, As a consequence, the names Solenopora and Solenopo- for it provides firm evidence that species of Corallinales raceae, when associated with sponges, are no longer gov- bearing uniporate sporangial conceptacles existed in mid- erned by the International Code of Nomenclature for algae, Silurian (Wenlock) strata 427–433 Ma, over 300 million fungi and plants (Turland et al. 2018). years earlier than had been previously recorded. Given Brooke & Riding (1998, p. 190) considered the Roth- that it cannot be referred to any known lineage of Coral- pletz species to be a coralline red alga and placed it into linales/Corallinaceae due to inadequate preservation of their new genus Craticula (a name later replaced by the certain characters, we can only accord it incertae sedis sta- name Graticula Brooke & Riding, 2000, p. 82). Based on tus (of uncertain taxonomic position; see Hawksworth Wenlock (Silurian) material from Gotland Island, Sweden 2010, p. 98) within the Corallinales/Corallinaceae. (and from the Old Radnor area, Wales, UK), Brooke & Riding (1998, p. 190) characterized Graticula as having ‘sporangia in calcified sporangial compartments arranged Aguirrea and the evolutionary history of the Corallinales in irregular sori’ and provided one illustration (Brooke & Riding 1998, p. 187, fig. 2). They also allied Graticula According to recent evolutionary history studies, the with Sporolithon (Sporolithaceae, Sporolithales) but placed Corallinaceae are thought to have first appeared during Graticula in a separate new family (the Graticulaceae) the late Early Cretaceous to early Late Cretaceous; esti- because of the apparent gap in the fossil record between mates include 105 15 Ma (Rosler€ et al. 2017, p. 571) Silurian Graticula and Cretaceous Sporolithon. If one (Aptian, Albian or Cenomanian); 114–119 Ma (Yang accepts the conclusion that Graticula produces sporangia et al. 2016, p. 3, fig. 1) (Aptian) and 99.45 Ma (Aguirre in calcified compartments arranged in irregular sori and et al. 2010, p. 526, fig. 2) (Cenomanian/Albian border). thus belongs to the Sporolithales, then it is necessary to These timelines, however, now require updating in molec- set a Silurian calibration point for the emergence of the ular clock analyses to take account of the discovery of Sporolithales as well as the Corallinales in future molecu- A. fluegelii in the lower Wenlock (mid-Silurian). lar clock analyses (also see comments of Yang et al. 2016, Our evidence suggests that the Corallinaceae appeared p. 7). The result of using new, much older calibration (diverged) at least 430 3 Ma, not 105 15 Ma ago. points is likely to show that the divergence of lineages of This much earlier divergence time is concordant with the Corallinophycidae occurred much earlier than in the hypothesis (Yang et al. 2016) that the Corallinophycidae Cretaceous. emerged as a distinct lineage c. 579 (534–617) Ma. In resetting calibration points for molecular clock anal- yses of the Corallinophycidae, another fossil taxon needs CONCLUSION to be considered: Graticula gotlandica (Rothpletz) Brooke & Riding, 2000. Graticula gotlandica, originally described This study contains an account of Aguirrea fluegelii,a as Solenopora gotlandica Rothpletz, 1908 (p. 14, pl. 4 figs new fossil-genus and species of Corallinales/Coralli- 1–5), is based on Wenlock (Silurian) material from ‘Insel naceae (Rhodophyta) of Silurian age that possesses uni- Faro€ bei Gotland’ (= Faro€ Island, off the north-east tip of porate sporangial conceptacles. Rosler€ et al. (2016) Gotland Island, Sweden). Rothpletz (1908, pp. 8–10) fol- placed all taxa of Corallinales in a single family, the lowed Brown (1894) in treating Solenopora as a coralline Corallinaceae, within which seven lineages were eluci- red alga rather than a chaetetid sponge as done by dated based on DNA sequence data from five different Dybowski (1877), who first described the genus. Roth- genes. This was followed by a new molecular clocks- pletz (1908, p. 15) conjectured that the enlarged tubular based study of the evolutionary history of the group cells (Schlauchzellen) in his figures 2, 3 and 5 of S. got- (Rosler€ et al. 2017). landica were sporangia, a view he subsequently repeated Since the pioneering study of Aguirre et al. (2000) on and illustrated (Rothpletz 1913, p. 15, pl. 1 figs 1, 2) in the origination and extinction patterns of corallinalean additional material from Gotland Island. No spores or taxa, the first appearance of Corallinales in the Early 12 PALAEONTOLOGY

Cretaceous has been generally accepted (Rosler€ et al. Editor. George Sevastopulo 2017). Our results, however, provide clear evidence that Corallinales with uniporate sporangial conceptacles already existed in the mid-Silurian, and this necessitates REFERENCES updating and revising our ideas concerning the possible AGUIRRE, J. and BRAGA, J. C. 2005. The citation of time of origin not only of the Corallinales/Corallinaceae, nogeniculate fossil coralline red algal species in the twentieth but of all groups of the Corallinophycidae. century literature: an analysis with implications. Revista What is also needed is a much more intensive effort to Espanola~ de Micropaleontologıa, 37,57–62. discover and describe fertile fossil specimens of Corallino- -RIDING, R. and BRAGA, J. C. 2000. Diversity of coral- phycidae from pre-Cretaceous strata and more particu- line red algae: origination and extinction patterns from the larly from Early Silurian and potentially even older strata. Early Cretaceous to the Pleistocene. Paleobiology, 26, 651–667. The successful discovery of such fertile specimens will also -PERFECTTI, F. and BRAGA, J. C. 2010. Integrating provide new and more resilient calibrators for future phylogeny, molecular clocks, and the fossil record in the evo- evolutionary history accounts using molecular clock lution of coralline algae (Corallinales and Sporolithales, Rho- 36 – approaches. dophyta). Paleobiology, , 519 533. Specimens of A. fluegelii are well developed vegetatively ATHANASIADIS, A. 2016. Phycologia Europaea- Rhodophyta. Vol. 1. Published by the Author, Gothenborg, Sweden. 762 pp. and have uniporate sporangial conceptacles, but we have BASSI, D., NEBELSICK, J. H., CHECCONI, A., yet to discover how and when morpho-anatomical forms HOHENEGGER, J. and IRYU, Y. 2009. Present-day and of the complexity seen in A. fluegelii might have arisen. fossil rhodolith pavements compared: their potential for analys- The complexity of the morpho-anatomical features found ing shallow-water carbonate deposits. Sedimentary Geology, 214, in our Silurian fossils suggests that unequivocal species of 74–84. Corallinales/Corallinaceae with uniporate conceptacles are BASSO, D. 2012. Carbonate production by calcareous red algae also likely to have existed before the Wenlock Epoch of and global change. Geodiversitas, 34,13–33. the Silurian. -and GRANIER, B. 2018. Johnson & Kaska 1965 fossil The discovery of A. fluegelii also raises questions as to coralline algae from Guatemala (revision of the Jesse Harlan which group of Corallinophycidae with calcite impreg- Johnson Collection, Part 4). Rivista Italiana di Paleontologia e 124 – nated cell walls (i.e. the Corallinales, Hapalidiales, Sporo- Stratigrafia, ,91 104. - CARAGNANO, A. and RODONDI, G. 2014. Tri- lithales) is the oldest and how the sequence of divergence chocytes in Lithophyllum kotschyanum and Lithophyllum spp. of the three groups occurred. Our study and that of (Corallinales, Rhodophyta) from the NW Indian Ocean. Jour- Brooke & Riding (1998, 2000) provide evidence that taxa nal of Phycology, 50, 711–717. of Corallinales and Sporolithales existed in the mid- BITTNER, L., PAYRI, C. E., MANEVELDT, G. W., Silurian. According to Aguirre et al. (2010, p. 527), by COULOUX, A., CRUAUD, C., DE REVIERS, B. and contrast, the oldest known taxon of Hapalidiales, LE GALL, L. 2011. Evolutionary history of the Corallinales Lithothamnion tenuicrustatum Ishijima, 1978, was (Corallinophycidae, Rhodophyta) inferred from nuclear, plas- described from upper Aptian (lower Cretaceous) material tidial and mitochondrial genomes. Molecular Phylogenetics & from Borneo, Indonesia. A reassessment of the designated Evolution, 61, 697–713. lectotype and other original material of L. tenuicrustatum BOSENCE, D. W. J. 1991. Coralline algae: mineralization, tax- – by Iryu et al. (2012, pp. 189–190, figs 1I–L, 7C–F) con- onomy, and palaeoecology. 98 113.InRIDING, R. (ed.) Calcareous algae and stromatolites. Springer. firmed the occurrence of multiporate conceptacles charac- BRAGA, J. C. 2006. Preserved gamete-producing structures. teristic of the Hapalidiales but resulted in the conclusion Journal of Taphonomy, 4,47–48. that the species could not be placed with certainty in the BROOKE, C. and RIDING, R. 1998. Ordovician and Silurian genus Lithothamnion. New efforts are now needed coralline red algae. Lethaia, 31, 185–195. to determine whether multiporate conceptacle-bearing -- 2000. Graticula and its derivates, replacement name for taxa of Hapalidiales also existed much earlier than the the alga Craticula Brooke & Riding non Grunow. Lethaia, 33,82. Cretaceous. BROWN, A. 1894. On the structure and affinities of thje genus Solenopora, together with descriptions of new species. Geologi- Acknowledgements. We thank Birgit Leipner-Mata (Erlangen, cal Magazine, 4, 145–151, 195–203. Germany) and Indra Gill-Kopp (Tubingen,€ Germany) for the CALNER, M., JEPPSSON, L. and MUNNECKE, A. 2004. preparation of thin sections and Felix B. Engel (Erlangen, Ger- The Silurian of Gotland - Part I: Review of the stratigraphic many) for his imaging support using the LSM800 confocal laser framework, event stratigraphy, and stable carbon and oxygen scanning microscope (German Research Foundation, DFG, INST isotope development. Erlanger Geologische Abhandlungen, Son- 410/91-1 FUGG). We also express our gratitude to the journal derband, 5, 113–131. Editors and the anonymous reviewers, who provided construc- CARAGNANO, A., FOETISCH, A., MANEVELDT, G. tive comments that improved the manuscript. W., MILLET, L., LIU, L.-C., LIN, S.-M., RODONDI, G. TEICHERT ET AL.: CORALLINALES FROM THE SILURIAN OF GOTLAND 13

and PAYRI, C. E. 2018. Revision of Corallinaceae (Coralli- Choreonematoideae, Austrolithoideae, and Melobesioideae. nales, Rhodophyta): recognizing Dawsoniolithon gen. nov., Journal of Phycology, 39, 988–998. Parvicellularium gen. nov. and Chamberlainoideae subfam. -WOELKERLING, W. J., FARR, T., NEILL, K. and nov. containing Chamberlainium gen. nov. and Pneophyllum. NELSON, W. 2005. Coralline algae of Central New Zealand: Journal of Phycology, 54, 391–409. An identification guide to common ‘crustose’ species. NIWA Infor- CASTRO, P. and HUBER, M. E. 2010. Marine biology. mation Series, 57. NIWA, Wellington, New Zealand. 145 pp. McGraw-Hill. 461 pp. -PHILLIPS, L. E., WOELKERLING, W. J. and MIL- CHECCONI, A. and MONACO, P. 2008. Trace fossil assem- LAR, A. J. K. 2006. The Corallinaceae, subfamily Mastophor- blages in rhodoliths from the Middle Miocene of Mt. Cam- oideae (Corallinales, Rhodophyta) in south-eastern Australia. posauro (Longano Formation, Southern Apennines, Italy). Australian Systematic Botany, 19, 387–429. Studi Trentini di Scienze Naturali, Acta Geologica, 83, 165–176. HAWKSWORTH, D. L. 2010. Terms used in bionomenclature. -BASSI, D., CARANNANTE, G. and MONACO, P. Global Biodiversity Information Facility, Copenhagen. 215 pp. 2010. Re-deposited rhodoliths in the Middle Miocene hemipe- HIND, K. R., GABRIELSON, P. W., JENSEN, C. P. and lagic deposits of Vitulano (Southern Apennines, Italy): coral- MARTONE, P. T. 2016. Crusticorallina gen. nov., a non- line assemblage characterization and related trace fossils. geniculate genus in the subfamily Corallinoideae (Corallinales, Sedimentary Geology, 225,50–66. Rhodophyta). Journal of Phycology, 52, 929–941. CORMACI, M., FURNARI, G. and ALONGI, G. 2017. HRABOVSKY, J., BASSO, D. and DOLAKOV A, N. 2015. Flora marina bentonica del Mediterraneo: rhodophyta Diagnostic characters in fossil coralline algae (Corallinophyci- (Rhodymeniophycidae escluse). Bollettino dell’Accademia Gioe- dae: Rhodophyta) from the Miocene of southern Moravia nia di Scienze Naturali, Catania, 50,1–391. (Carpathian Foredeep, Czech Republic). Journal of Systematic CRONQUIST, A. 1960. The divisions and classes of plants. Palaeontology, 14, 499–525. The Botanical Review, 26, 425–482. HUGHEY, J. R., BRAGA, J. C., AGUIRRE, J., WOELK- DENINGER, K. 1906. Einige neue Tabulaten und Hydrozoen ERLING, W. J. and WEBSTER, J. M. 2008. Analysis of aus mesozioschen Ablagerungen. Neues Jahrbuch fur€ Mineralo- ancient DNA from fossil corallines (Corallinales, Rhodophyta). gie. Geologie und Pal€aontologie. Abhandlungen, 1906,61–70. Journal of Phycology, 44, 374–383. DIXON, P. S. 1973. Biology of the Rhodophyta. Hafner Press, HUISMAN, J. M. 2000. Marine plants of Australia. University New York. 285 pp. of Western Australia Press, Perth. 300 pp. DYBOWSKI, W. 1877. Die Chaetetiden der Ostbaltischen IRYU, Y., BASSI, D. and WOELKERLING, W. J. 2012. Silur-Formation. Verhandlungen der Russisch-Kaiserliche Min- Typification and reassessment of seventeen species of coralline eralogische Gesellschaft zur St. Petersburg, 14,1–134. red algae (Corallinales and Sporolithales, Rhodophyta) FARR, T., BROOM, J., HART, D., NEILL, K. and NEL- described by W. Ishijima during 1954–1978. Journal of System- SON, W. 2009. Common coralline algae of northern New Zeal- atic Palaeontology, 10, 171–209. and: an identification guide. NIWA Information Series, 70. ISHIJIMA, W. 1978. Calcareous algae from the Philippines, NIWA, Wellington, New Zealand. Malaysia and Indonesia. 167–190.InKOBAYASHI, T., FOSTER, M. S. 2001. Rhodoliths: between rocks and soft TORIYAMA, R. and HASHIMOTO, W. (eds). Geology places. Journal of Phycology, 37, 659–667. and palaeontology of Southeast Asia. University of Tokyo Press. FREDERICQ, S. and NORRIS, J. N. 1995. A new order JEPPSSON, L. 2008. The lower Wenlock Hangvar Formation (Rhodogorgonales) and family (Rhodogorgonaceae) of red – a sequence previously split between the Hogklint€ and Slite algae composed of two tropical calciferous genera, Renouxia beds (Silurian, Gotland, Sweden). GFF, 130,31–40. gen. nov. and Rhodogorgon. Cryptogamic Botany, 5, 316–331. JOHANSEN, H. W. 1981. Coralline algae, a first synthesis. GRANIER, B. and DIAS-BRITO, D. 2016a. On the fossil CRC Press, Boca Raton, Florida. 239 pp. alga Elianella elegans Pfender & Basse, 1948, and its so-called JOHNSON, J. H. 1960. Paleozoic Solenoporaceae and related lookalikes, with description of Elianella brasiliana n.sp. Revision red algae. Colorado School of Mines Quarterly, 55,1–77. of the Juliette Pfender Collection. Part 1. Carnets de Geologie, KAMENOS, N. A., MOORE, P. G. and HALL-SPENCER, 16, 213–229. J. M. 2004. Maerl grounds provide both refuge and high growth -- 2016b. On the fossil alga Marinella lugeoni Pfender, potential for juvenile queen scallops (Aequipecten opercularis L.). 1939, nom. cons., and its seven unfortunate avatars. Revision Journal of Experimental Marine Biology & Ecology, 313,241–254. of the Juliette Pfender Collection. Part 2. Revision of the Jesse KAMIYA, M., LINDSTROM, S. C., NAKAYAMA, T., Harlan Johnson Collection. Part 2. Carnets de Geologie, 16, YOKOYAMA, A., LIN, S., GUIRY, M. D., GURGEL, C. 231–245. F. D., HUISMAN, J. M., KITAYAMA, T., SUZUKI, M., HARVEY, W. H. 1847. Phycologia Britannica. Fasc. 13, pls 73– CHO, T. O. and FREY, W. (eds). 2017. Syllabus of plant 78. Reeve & Benham, London. families - A. Engler’s Syllabus der Pflanzenfamilien Part 2/2: -1849. Nereis Australis. Part II.65–124, pls 26–50. Reeve Photoautotrophic eukaryotic algae - Rhodophyta. Borntraeger Brothers, London. Science Publishers, Berlin. 171 pp. HARVEY, A. S., BROADWATER, S. T., WOELKER- KATO, A., BABA, M. and SUDA, S. 2011. Revision of the LING, W. J. and MITROVSKI, P. J. 2003. Choreonema Mastophoroideae (Corallinales, Rhodophyta) and polyphyly in (Corallinales, Rhodophyta): 18S rDNA phylogeny and resur- nongeniculate species widely distributed on Pacific coral reefs. rection of the Hapalidiaceae for the subfamilies Journal of Phycology, 47, 662–672. 14 PALAEONTOLOGY

LAMOUROUX, J. V. F. 1812. Sur la classification des Polyp- RIDING, R. 2004. Solenopora is a chaetetid sponge, not an iers coralligenes non entierement pierreux. Nouveau Bulletin des alga. Palaeontology, 47, 117–122. Sciences par la Societe Philomathique de Paris, 3,181–188. -and WATTS, N. 1981. Silurian algal reef crest in Gotland. LE GALL, L. and SAUNDERS, G. W. 2007. A nuclear phylogeny Naturwissenschaften, 68,91–92. of the Florideophyceae (Rhodophyta) inferred from combined ROSLER,€ A., PERFECTTI, F., PENA,~ V. and BRAGA, EF2, small subunit and large subunit ribosomal DNA: establish- J. C. 2016. Phylogenetic relationships of Corallinaceae (Coral- ing the new red algal subclass Corallinophycidae. Molecular Phy- linales, Rhodophyta): taxonomic implications for reef-building logenetics & Evolution, 43, 1118–1130. corallines. Journal of Phycology, 52, 412–431. LE GALL, L., PAYRI, C. E., BITTNER, L. and SAUN- --- AGUIRRE, J. and BRAGA, J. C. 2017. Tim- DERS, G. W. 2010. Multigene phylogenetic analyses support ing of the evolutionary history of Corallinaceae (Corallinales, recognition of the Sporolithales ord. nov. Molecular Phylo- Rhodophyta). Journal of Phycology, 53, 567–576. genetics & Evolution, 54, 302–305. ROTHPLETZ, A. 1908. Uber€ Algen und Hydrozoen im Silur MOUSSAVIAN, E. 1989. Uber€ die systematische Stellung und von Gotland und Oesel. Kungliga Svenska Vetenskap- die Bestimmungskriterien der Solenoporaceen (Rhodophy- sakademiens Handligar, 43,1–25. € ceae). Courier Forschungsinstitut Senckenberg, 109,51–91. - 1913. Uber die Kalkalgen, Spongiostromen und einige MUNNECKE, A. and SERVAIS, T. 2008. Palaeozoic calcare- andere fossilien aus dem Obersilur Gottlands. Afhandlinger ous plankton: evidence from the Silurian of Gotland. Lethaia, Sveriges Geologiska Unders€okning, 10,1–57. 41, 185–194. SAMTLEBEN, C., MUNNECKE, A., BICKERT, T. and NELSON, W. A., SUTHERLAND, J. E., FARR, T. J., PATZOLD,€ J. 1996. The Silurian of Gotland (Sweden): facies HART, D. R., NEILL, K. F., KIM, H. J. and YOON, H. interpretation based on stable isotopes in brachiopod shells. S. 2015. Multi-gene phylogenetic analyses of New Zealand cor- Geologische Rundschau, 85, 278–292. alline algae: Corallinapetra Novaezelandiae gen. et sp. nov. and SILVA, P. C. and JOHANSEN, H. W. 1986. A reappraisal of recognition of the Hapalidiales ord. nov. Journal of Phycology, the order Corallinales (Rhodophyceae). British Phycological 51, 454–468. Journal, 21, 245–254. NOSE, M., SCHMID, D. U. and LEINFELDER, R. R. SMITH, A. M., SUTHERLAND, J. E., KREGTING, L., 2006. Significance of microbialites, calcimicrobes, and calcare- FARR, T. J. and WINTER, D. J. 2012. Phylomineralogy of ous algae in reefal framework formation from the Silurian of the coralline red algae: correlation of skeletal mineralogy with Gotland, Sweden. Sedimentary Geology, 192, 243–265. molecular phylogeny. Phytochemistry, 81,97–108. OTI, M. and MULLER,€ G. 1985. Textural and mineralogical TEICHERT, S. 2014. Hollow rhodoliths increase Svalbard’s changes in coralline algae during meteoric diagenesis: an shelf biodiversity. Scientific Reports, 4, 6972. € experimental approach. Neues Jahrbuch fur Mineralogie, -and FREIWALD, A. 2014. Polar coralline algal CaCO3- Abhandlungen, 151, 163–195. production rates correspond to intensity and duration of the PENROSE, D. 1996a. Genus Pneophyllum. 266–272.In solar radiation. Biogeosciences, 11, 833–842. WOMERSLEY, H. B. S. (ed.) The marine benthic flora of TOMAS, S., AGUIRRE, J., BRAGA, J. and MARTIN- Southern Australia. Part 3B. Gracilariales, Rhodymeniales, CLOSAS, C. 2007. Late Hauterivian coralline algae (Rhodo- Corallinales and Bonnemaisoniales. Australian Biological phyta, Corallinales) from the Iberian Chain (E Spain). Taxonomy Resources Study, Canberra. and the evolution of multisporangial reproductive structures. - 1996b. Genus Spongites. 273–280.InWOMERSLEY, Facies, 53,79–95. H. B. S. (ed.) The marine benthic flora of Southern Australia. TOWNSEND, R. A. and HUISMAN, J. M. 2018. Coralline Part 3B. Gracilariales, Rhodymeniales, Corallinales and Bon- algae. 86–138, 143–146.InHUISMAN, J. M. (ed.) Algae of nemaisoniales. Australian Biological Resources Study, Canberra. Australia: marine benthic algae of North-western Australia. 2. PFENDER, J. 1939. Sur un calcaire phytogene du Lias Red algae. ABRS & CSIRO Publishing, Canberra, Melbourne. inferieur d’Espagne et l’extension de ce facies en quelques TURLAND, N. J., WIERSEMA, J. H., BARRIE, F. R., qutres regions. Bulletin de la Societe Vaudoise des Sciences Nat- GREUTER, W., HAWKSWORTH, D. L., HEREN- urelles, 60, 213–228. DEEN, P. S., KNAPP, S., KUSBER, W.-H., LI, D.-Z., -and BASSE, E. 1948. Elianella nov. gen. elegans nov. sp., MARHOLD, K., MAY, T. W., McNeill, J., MONRO, A. organisme constructeur de calcaires typiquement developpe M., PRADO, J., PRICE, M. J. and SMITH, G. F. 2018. dans le paleocene du SW Malgache. Bulletin de la Societe International Code of Nomenclature for algae, fungi, and plants Geologique de France, 17, 275–278. (Shenzhen Code) adopted by the Nineteenth International PIA, J. 1927. Thallophyta. 31–136.InHIRMER, M. (ed.) Botanical Congress, Shenzhen, China, July 2017. Koeltz Botani- Handbuch der Pal€aobotanik. Olendbourg, Munchen.€ cal Books, Glashutten,€ Germany. 254 pp. POCTA, P. 1887. Die Anthozoen der bohmischen€ Kreideforma- VAN DER MERWE, E., MIKLASZ, K., CHANNING, A., tion. Abhandlungen der mathematisch-naturwissenschaftlichen MANEVELDT, G. W. and GABRIELSON, P. W. 2015. Classe der K€oniglich B€ohmischen Gesellschaft der Wissenschaften, DNA sequencing resolves species of Spongites (Corallinales, 2,1–60. Rhodophyta) in the Northeast Pacific and South Africa, POIGNANT, A. F. 1991. The Solenoporaceae: a general point including S. agulhensis sp. nov. Phycologia, 54, 471–490. of view. 88–97.InRIDING, R. (ed.) Calcareous algae and WETTSTEIN, R. 1901. Handbuch der systematischen Botanik. stromatolites. Springer. Franz Deuticke, Leipzig & Wien. 201 pp. TEICHERT ET AL.: CORALLINALES FROM THE SILURIAN OF GOTLAND 15

WOELKERLING, W. J. 1988. The coralline red algae. Oxford -GRANIER, B. and DIAS-BRITO, D. 2014. Heydrichia University Press. 268 pp. (?) poignantii, sp. nov. (Sporolithaceae, Sporolithales, Rhodo- -and CAMPBELL, S. J. 1992. An account of southern phyta), a 100 million year old fossil coralline red alga from Australian species of Lithophyllum (Corallinaceae, Rhodo- north-eastern Brazil, and a new Hauterivian record of Sporoli- phyta). Bulletin of the British Museum (Natural History), thon from Switzerland. Notebooks on Geology, 14, 139–185. Botany, 22,1–107. XIAO, S., KNOLL, A. H., YUAN, X. and PUESCHEL, -IRVINE, L. M. and HARVEY, A. S. 1993. Growth- C. M. 2004. Phosphatized multicellular algae in the Neopro- forms in non-geniculate coralline red algae (Corallinales, Rho- terozoic Doushantuo Formation, China, and the early evolu- dophyta). Australian Systematic Botany, 6, 277–293. tion of florideophyte red algae. American Journal of Botany, -BASSI, D. and IRYU, Y. 2012. Hydrolithon braganum 91, 214–227. sp. nov. (Corallinaceae, Rhodophyta), the first known exclu- YANG, E. C., BOO, S. M., BHATTACHARYA, sively fossil semi-endophytic coralline red alga. Phycologica, D., SAUNDERS, G. W., KNOLL, A. H., FREDER- 51, 604–611. ICQ, S., GRAF, L. and YOON, H. S. 2016. -IRYU, Y. and BASSI, D. 2013. Fossil semi-endophytic Divergence time estimates and the evolution of major lin- species of Lithophyllum (Corallinaceae, Rhodophyta) from eages in the florideophyte red algae. Scientific Reports, 6, Tahiti, including L. kenjikonishii sp. nov., and their tapho- 21361. nomic signatures. Phycologia, 52, 387–397.

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