Calcareous tubeworms of the Phanerozoic

Morphological similarities indicate that Palaeozoic problematic tubeworms, e.g. tentaculitids, cornulitids, microconchids, trypanoporids, Anticalyptraea, and Tymbochoos, form a monophyletic group. This group may also include hederelloids. Members of this group share affinities with lophophorates and their evolution could have partly been driven by predation. The extinction of Palaeozoic tubeworms in the Middle Jurassic was possibly at least partly caused by the ecological pressure by serpulid and sabellid polychaetes. The input of Palaeozoic tubeworms to the general ocean biocalcification system may have been smaller in the Ordovician to Jurassic than that of calcareous polychaetes in the Late Triassic to Recent. There seems to have been some correlation between the aragonitecalcite seas and the skeletal mineralogy of TriassicRecent polychaete tubeworms.

The aims of the paper are to discuss (1) the zoological affinities and phylogeny of Palaeozoic problematic tubeworm faunas, (2) the biomineralization of calcareous polychaete tubeworms throughout the time, (3) the morphological convergence and similarities in the ecology of Palaeozoic problematic tubeworms and calcareous polychaete tubeworms, (4) the evolutionary replacement of Palaeozoic problematic tubeworms by calcareous polychaete tubeworms, and (5) the comparative input of problematic tubeworms and calcareous polychaete tubeworms to global biocalcification.

Phylogenetic relationships of substrate-cemented Palaeozoic problematic tubeworms
There are strong morphological similarities between the Palaeozoic problematic tubeworms, including microconchids, trypanoporids, cornulitids, and Anticalyptraea.These features include calcitic, substrate-cemented tubes, microlamellar tube structure, pseudopunctae (but not in all species), bulb-like embryonic shells part and septae, all of which suggest a monophyletic origin.Unfortunately, the embryonic shell of Tymbochoos is not known, but we tentatively assign it to this group because of the microlamellar shell structure and pseudopunctae.

Phylogenetic relationships of cornulitids and tentaculitids
The morphology of cornulitids (Vinn 2005a;Vinn & Mutvei 2005) and thick-walled tentaculitids (Larsson 1979;Farsan 2005) exhibits several similarities, such as the calcitic shell of a similar shape, similar microlamellar shell structure, and the presence of similarly oriented pseudopunctae, both internal and external annulation, septae, and a bulb-like embryonic shell separated by constriction from the adult part of the shell.These features suggest a close phylogenetic relationship, and most likely an ancestor-descendant relationship (Bouček 1964;Dzik 1991;Vinn 2005a;Vinn & Mutvei 2005).However, these fossils had different life styles (substrate-cemented in cornulitids versus free-living in tentaculitids) and their shell formation began at different ontogenetic stages.Cornulitids have a post-larval shell (Vinn & Mutvei 2005) which begins with the initial bulbous embryonic shell.In tentaculitids the shell first appeared in the larval stage as a long conical process, which was then followed by a bulb-like embryonic shell in the post-larval stage (Farsan 2005).This could mean that tentaculitids may have had a longer larval stage than cornulitids.If that was the case, the thick-walled tentaculitids may have had a planktotrophic larva and cornulitids a lecithotrophic larva.On the basis of the geological age, Dzik (1991) suggested that younger tentaculitids could have been derived from older cornulitids.Indeed, it seems more likely that tentaculitids originated from cornulitids than vice versa, because the substrate-cemented lifestyle does not require loss of the larval shell.In substrate-cemented mollusks, such as vermetid gastropods, the larval shell is preserved.The same could be expected of cornulitids if they had evolved from a tentaculitid ancestor with a larval shell.

Phylogenetic relationships of Palaeozoic problematic tubeworms
Considering on the morphological similarities, we hypothesize here that tentaculitids, cornulitids, microconchids, trypanoporids, Anticalyptraea, and Tymbochoos form a monophyletic group and that their skeletons are homologous (Fig. 2).It is possible that hederelloids also belong to this group.We also hypothesize that the substrate-cemented forms (lacking larval shell) form a sister group to free-living tentaculitids (larval shell present) (Fig. 2).Within the substrate-cemented group, it is possible that spirorbiform microconchids (Upper Ordovician) have been derived from the geologically older, nonspiral cornulitids (first known from the Middle Ordovician) (Fig. 2).Similarly, spirally coiled trypanoporids (Devonian) have most likely been derived from the geologically older microconchids (Upper Ordovician) (Fig. 2).The reef-forming Tymbochoos most probably originates from a cornulitid ancestor (Fig. 2), because it has similar, inwardly pointed pseudopunctae and constrictions resembling the annulation in the tube interior of Cornulites.The position of the spirally coiled Anticalyptraea remains controversial in the phylogeny of the problematic tubeworms and needs further study (Fig. 2).Anticalyptraea has either evolved directly from cornulitids, because of similar inwardly pointed pseudopunctae and vesicular tube wall, or from spiral microconchids.In the latter case it must have changed the direction of the pseudopunctation and evolved a vesicular tube wall.On the basis of the occurrence of the microlamellar shell structure, cross-bladed lamellar structure, regularly foliated structure, pseudopunctae (both outwardly and inwardly pointed), pores, and possible periostracum-like external organic layer (Vinn & Taylor 2007;Filipiak & Jarzynka 2009) we suggest that the problematic tubeworms with tentaculitid affinities were phylogenetically closely linked to lophophorates (e.g.bryozoans and brachiopods), but probably most closely to phoronids.

Diversity and evolution of Palaeozoic problematic tubeworms
Lophophorate (e.g.brachiopods and bryozoans) diversity during the Phanerozoic was highest in the Palaeozoic.However, if we add Palaeozoic tubeworms of lophophorate affinities to this record, the shelly faunas of the Palaeozoic era may have been even more dominated by lophophorates than previously thought.The diversity of Palaeozoic problematic tubeworms was highest in the Silurian and Devonian (Bouček 1964;Richards 1974;Larsson 1979;Vinn 2004Vinn , 2005aVinn , 2006a;;Taylor & Wilson 2008;Vinn & Mõtus 2008) and decreased markedly in the Carboniferous.Hitherto reported shell repair indicates attempted predation on the problematic tubeworms in the Late Ordovician (Vinn 2009a), Silurian (Larsson 1979;Vinn & Mutvei 2005;Vinn & Isakar 2007;Vinn 2009a), and Devonian (Wilson & Taylor 2006).Thus, predation pressure may have had some role in shaping the evolution of Palaeozoic problematic tubeworms.Taxa with large soft-body volumes, such as some Late Ordovician to Silurian Cornulites and tentaculitids, are lacking in the Late Palaeozoic, supporting, at least partially, predation-driven evolution.The occurrence of numerous endosymbiotic tubeworms in the Silurian (Vinn & Mõtus 2008;Vinn & Wilson 2009) and Devonian (Weedon 1991;Tapanila 2005) also reflects the pressure by predators.

MESOZOIC TURNOVER FROM PALAEOZOIC PROBLEMATIC TUBEWORMS TO CALCAREOUS POLYCHAETE TUBEWORM FAUNAS
Microconchids are the only problematic tubeworms in the Permian.Microconchids survived the P/T mass extinction (Taylor & Vinn 2006), and opportunistic microconchids are present in extinction recovery faunas from the Early Triassic of North America (Taylor et al. 2006).Microconchids are relatively common encrusters on biogenic substrates of the Early Triassic in Europe (O. Vinn pers. obs. 2007).The extinction of microconchids was probably gradual and lasted from the Early Jurassic until their final extinction at the end of the Middle Jurassic (Taylor & Vinn 2006;Vinn & Taylor 2007).The earliest calcareous polychaete tubeworms were serpulids, which appeared in the Triassic (Vinn et al. 2008a(Vinn et al. , 2008c)), whereas their oldest unequivocal representatives are known from the Middle Triassic of China (Stiller 2000).The diversification of serpulids in the Late Triassic (Ziegler & Michalík 1980;Stiller 2000;Senowbari-Daryan & Link 2005;Senowbari-Daryan et al. 2007) and Early Jurassic (Parsch 1956;Jäger & Schubert 2008) coincides with the decrease in the abundance of microconchids.The extinction of microconchids in the Jurassic was possibly driven by the ecological pressure by serpulids if serpulids were more rapidly growing and more efficient suspension feeders than microconchids.The abundance and diversity of Mesozoic hard substrate encrusters increased in the Jurassic (Taylor & Wilson 2003), which could have added additional competition pressure into the hard substrate communities.In the latter case, the extinction of microconchids may have also been driven by the increase in the abundance and diversity of the other Mesozoic efficient suspension feeders such as Bivalvia.
The biomineralization systems of Palaeozoic problematic tubeworms and calcareous polychaete tubeworms are comparable in respect of their ability to produce advanced skeletal ultrastructures.The foliated structures (e.g.Cornulites, Vinn & Mutvei 2005) and cross-bladed lamellar structures (e.g.Tentaculites, Towe 1978) of problematic tubeworms are as advanced and complex as the lamello-fibrillar structures of some serpulids (Vinn et al. 2008a(Vinn et al. , 2008b(Vinn et al. , 2008d)).However, the spherulitic prismatic structures of the Cirratulidae and Sabellidae (Vinn et al. 2008a(Vinn et al. , 2008b) ) are less advanced and probably inferior with respect to material properties than the structures of problematic tubeworms.The advanced, complex oriented structures, such as lamello-fibrillar structures, may have appeared late in the evolution of serpulids (Late Cretaceous to Early Cenozoic).Primitive Triassic and Jurassic serpulids may have possessed only simple, unoriented structures (Vinn & Furrer 2008).Thus, the complexity of skeletal ultrastructures was presumably not related to the evolutionary replacement of problematic tubeworms by calcareous polychaete tubeworms in the Middle Mesozoic.

Reefs formed by Palaeozoic problematic tubeworms
Only a few studies have been published on reefs formed by problematic tubeworms in the Palaeozoic.The oldest are reefs formed by Tymbochoos in the Upper Ordovician of North America (Steele-Petrovich & Bolton 1998;Vinn 2006b).The earliest microconchid bioherms occur in the Upper Devonian of Arizona (Beus 1980) and Upper Devonian of Belgium (Dreesen & Jux 1995).Microconchid patch reefs, bioherms, and biostromes are known from the Lower Carboniferous (Tournaisian) of Cumberland and Roxburghshire (Leeder 1973).Although upper Ordovician and Silurian cornulitids (e.g.Cornulites) may occur in aggregations (Hall 1888;Richards 1974), they have never been found to form structures larger than a few centimetres in diameter (Hall 1888;Fisher 1962;Richards 1974;Vinn 2005a).

Rocks formed by Palaeozoic problematic tubeworms
Palaeozoic sedimentary rocks contain problematic tubeworms, especially tentaculitids, often in large numbers, but only microconchids (such as 'Serpula spp.') are reported to form rocks (banks) in the Upper of Austria (Suttner & Lukeneder 2004).Notable tentaculitid concentrations may occur on bedding planes in Silurian and Devonian limestones (Bouček 1964;Lindemann & Melycher 1997), but they do not form thick biogenic layers.

Reefs formed by calcareous polychaetes
Among Recent calcareous polychaete tubeworms, serpulids and cirratulids may form reefs (ten Hove & van den Hurk 1993;Fischer et al. 2000).The earliest serpulid build-ups are known from the Late Triassic (Norian) of Europe (ten Hove & van den Hurk 1993;Berra & Jadoul 1996;Cirilli et al. 1999), and cirratulid reefs from the Oligocene of Mexico (Fischer et al. 2000).Serpulid build-ups occur also at the Triassic-Liassic boundary in Spain (Braga & López-López 1989), in the Middle Jurassic of SE Spain (Navarro et al. 2008), in the Miocene and Pliocene of Spain (ten Hove & van den Hurk 1993), and in the Mid-Holocene of Argentina (Ferreroa et al. 2005).Serpulid build-ups are relatively common in modern oceans and are found in all climatic zones in shallow-water environments (ten Hove & van den Hurk 1993;Ramos & San Martín 1999;Smith et al. 2005).The earliest cirratulid reefs occur in the Oligocene of Mexico (Fischer et al. 2000), with later examples from the Plio-Pleistocene of Oregon and California (ten Hove & van den Hurk 1993).Recent cirratulid patch-reefs occur in the Caribbean of Yucatan, Mexico (ten Hove & van den Hurk 1993).

Rocks formed by calcareous polychaetes
Serpulids are the only rock-forming calcareous polychaetes in the Middle Jurassic to Recent (ten Hove & van den Hurk 1993).From the Middle Jurassic to Danian, Glomerula (Sabellidae) is the most common calcareous tubeworm, at least among European tubeworm associations (M.Jäger, pers. comm. 2009).Serpulid limestones became more common from the Late Jurassic-Early Cretaceous onwards on various continents (Palma & Angeleri 1992;ten Hove & van den Hurk 1993;Kiessling et al. 2006).In modern oceans serpulids, especially Ditrupa, form banks or shell concentrations that have been reported from continental shelves in temperate to tropical seas all over the world (ten Hove & van den Hurk 1993).

Comparison of Phanerozoic calcium carbonate accumulation by polychaete tubeworms and by Palaeozoic problematic tubeworms
Among Mesozoic encrusters, mollusks and serpulids grew to a much larger size than their Palaeozoic counterparts, and thick biogenic layers of shelly material were often built on tops of original hardground surfaces (Palmer & Fürsich 1974;Taylor & Wilson 2003).Such biogenic layers are rare on Palaeozoic hardgrounds (Palmer 1982;Wilson & Palmer 1992).A possible explanation is that the main Palaeozoic encrusters (trepostomes, cryptostomes, echinoderms, corals) had scour-susceptible soft tissue covering their skeletons, whereas the dominant Mesozoic encrusters (serpulids, bivalves, most cyclostomes) had true exoskeletons into which soft parts of the living animals could withdraw completely (Palmer 1982).However, Palaeozoic problematic tubeworms also had true exoskeletons offering similar protection as calcareous polychaete tubes.Thus, the inability of problematic tubeworms to form thick biogenic layers on Palaeozoic to Jurassic hard substrates can be explained by their general slower calcification rate in ocean ecosystems as compared to Mesozoic to Recent calcareous polychaetes.
In the Late Palaeozoic microconchids become more common as secondary frame builders in microconchidalgal build-ups, but they never contributed to reef formation like calcareous polychaetes from the Mesozoic to Recent.There is no analogue to the Jurassic and Cretaceous serpulite (formed by serpulids) in the Palaeozoic and Triassic.It seems that calcareous polychaetes contributed to sedimentary rock formation of their time (Triassic to Recent) notably more than problematic tubeworms did in the Palaeozoic and Triassic.Thus, it is possible that Palaeozoic to Early Mesozoic problematic tubeworms never reached the level (quantity) of calcification carried out by polychaete annelids in the Late Mesozoic to Recent oceans.
Much of the Middle Mesozoic polychaete calcification was performed by sabellids, which play a minor role among calcifying annelids of the Recent oceans.Their primitive biomineralization system, as compared to that of serpulids, could be among the reasons why their abundance has decreased in the long term.However, changing seawater chemistry could also have affected calcification by sabellids.Sandberg (1983Sandberg ( , 1985) ) found that the composition of nonskeletal carbonate precipitates (early marine cements and ooliths) has undergone oscillations during Phanerozoic time: there have been three intervals of aragonite seas (Early Cambrian, Late Carboniferous-Early Jurassic, Oligocene-Recent), and two intervals of calcite seas (Middle Cambrian-Early Carboniferous, Middle Jurassic-Eocene) (Stanley 2006).Although some organisms exercise considerable control over their biomineralization, seawater chemistry has affected skeletal secretion by many Phanerozoic animal taxa (Stanley 2006;Taylor 2008).There are no records of an aragonitic mineralogy in Palaeozoic to Middle Jurassic problematic tubeworms.They appeared in the Ordovician calcite seas and seem to have remained exclusively calcitic throughout their evolution, even in Late Carboniferous to Early Jurassic aragonitic seas.Thus, they may have exercised a considerable control over their biomineralization.The primitive mineralogy of serpulids was presumably aragonitic (Vinn et al. 2008c), and they began to calcify in the aragonitic seas of the Triassic.Recent sabellids (e.g.Glomerula) are aragonitic, and they also appeared in the aragonitic seas of the Early Jurassic (Vinn et al. 2008a).However, in the Middle Jurassic to Eocene calcite seas sabellids may have had a calcitic or predominantly calcitic mineralogy, as they are usually very well preserved compared to co-occurring aragonitic mollusks in the Mesozoic of Europe (M.Jäger, pers. comm. 2009).Sabellid abundance peaked in Mesozoic calcite seas (M.Jäger, pers. comm. 2009).If sabellids were calcitic in the Middle Jurassic to Eocene calcite seas, they may have favoured the calcite sea conditions over aragonite sea conditions.Thus, there could have been some correlation between the aragonite-calcite seas and skeletal mineralogy of polychaetes, but further studies are needed, especially on the mineralogical history of sabellids (e.g.Glomerula).The mineralogy of probable aragonitic cirratulids (O.Vinn pers.obs.2007) also needs further study.

Morphological similarities indicate that Palaeozoic
problematic tubeworms -tentaculitids, cornulitids, microconchids, trypanoporids, Anticalyptraea, and Tymbochoos -form a monophyletic group and their skeletons are homologous.It is possible that hederelloids also belong to this group.The group likely shares affinities with lophophorates.2. The complexity of skeletal ultrastructures was presumably not related to the evolutionary replacement of Palaeozoic problematic tubeworms by calcareous polychaete tubeworms in the Middle Mesozoic.3. The extinction of Palaeozoic problematic tubeworms in the Middle Jurassic could have been at least partly driven by the ecological pressure from serpulids and sabellids because calcareous polychaete tubeworms probably grew more rapidly and were more efficient suspension feeders.
4. The input of Palaeozoic problematic tubeworms to the general ocean biocalcification system may have been smaller in the Ordovician to Jurassic than that of calcareous polychaetes in the Late Triassic to Recent.Palaeozoic problematic tubeworms may have been less efficient calcifiers than calcareous polychaete tubeworms.