Nerineoidea Zittel 1873

NERINEOIDEA AND ACTEONELLOIDEA

THE PHYLOGENY OF THE NERINEOIDEA

The earliest recorded Nerineoidea are Ceritella welschi Cossmann, 1902 and Nerinella grossouvrei Cossmann, 1902 from the Early Jurassic (Hettangian) of the Vendeé (France).From the same period, Böhm (1884) described fragments of turriculate gastropods with strongly rebounding growth lines from northern Italy as Chemnitzia canossae Böhm, 1884. Although the aperture is incomplete, Dietrich (1925) probably correctly assigned this species to Pseudonerinea. Well-preserved specimens of the Late Jurassic Pseudonerinea clytia (d’Orbigny, 1851) show a comparable external morphology (Fig. 2A).

In the Middle Jurassic, more or less broadly umbilicate taxa with siphonal aureoles evolved within the Ceritellidae (Fischer 1959, 1961). Of these, Pseudotrochalia Cox, 1954 possesses a strongly convex final whorl, an acute siphonal aureole and a palatal plait (see Fischer 1959). The other morphological features agree with those of the turriform Fibuloptyxis Cossmann, 1898.

Equally in the Middle Jurassic, the coniform Cryptoplocinae Pchelintsev, 1960, which are the earliest Ptygmatididae, appear.The Ptygmatididae are often large and possess the most sophisticated plait structure among the Nerineoidea. Their umbilicus is surrounded by a moderately acute siphonal aureole. The Ptygmatididae became extinct in the Early Cretaceous. Pictet & Campiche (1862) describe a number of internal moulds which indicate a range up the Aptian/Albian boundary.

The external morphology of Nerinella grossouvrei is almost the same as in the early Ceritellidae but differs by an obscurely angular periphery of the last whorl and three internal plaits. In stratigraphically later genera, the whorl periphery becomes distinctly angular. The Nerinellidae range stratigraphically into the Late Cretaceous (Campanian). In the Middle Jurassic they gave rise to the Eunerineidae n.fam.. Like the Ptygmatididae, the Eunerineidae n. fam. range stratigraphically into the Late Cenomanian.

The Nerineidae evolved from the Eunerineidae n. fam., of which some had become increasingly loosely coiled in late ontogenetic stages. The stratigraphically earliest Nerineidae species is the Bathonian Nerinea choffati Cossmann, 1898. It possesses three internal plaits, its whorl periphery is rounded and the base is tightly perforate. While it is morphologically still close to the Eunerineidae n. fam., the number of columellar plaits increased and the siphonal canal became larger and bent outwards, yielding a trumpet-like siphonal aureole in typical representatives of this family. The oviform Nerinea and the turriform Fibuloptygmatis Pchelintsev, 1965 extended into the Early Cretaceous (for example the Aptian Nerinea zumoffeni Delpey, 1940). From Fibuloptygmatis, the Cretaceous genera evolved. They dominate the assemblages from the Late Cenomanian upwards. Plesioptygmatis Boese, 1906 is restricted to Mexico and the Caribbean (Caribbean Province of Kauffman 1973).

Because of their totally different whorl sections, the Itieriidae cannot be an offshoot of the Nerineidae as Pchelintsev (1965) suggests. The family Itieriidae evolved in the Late Jurassic from the Ceritellidae (Cossmann 1896; Pchelintsev 1965). Late Jurassic taxa such as Ceritella polita (Sauvage & Rigaux fide Cossmann, 1895) show a comparable, broadly rounded shell outline. Pchelintsev (1965) figured a turriculate specimen with a solid columella un- der Phaneroptyxis rugifera Zittel, 1873. The Early Cretaceous Eotrochactaeon Akopjan, 1976 is similar. In other Itieriidae genera the shells are much broader while the columella is hollow and enclosed by an aureole. In the Cretaceous genera Vernedia Mazeran, 1912 and Sogdianella Djaliliov, 1972 hollow lunulae are incorporated in the columella (Kollmann & Sohl 1980) mark the limits of the siphonal beak in earlier growth stages.

PERIODS OF SHELL ENLARGEMENTS

Striking is the enormous increase in shell size in the families Eunerineidae n. fam., Nerineidae, Ptygmatididae and Itieriidae in the Oxfordian and the Kimmeridgian. Another period of enlargement is the Barremian with the diverse assemblage from Orgon, France (Cossmann 1907), and a final one took place from the Turonian onwards when the Eunerineidae n.fam. and the Ptygmatididae had died out and the Nerineidae flourished. With sizes up to 50 cm, Laevinerinea Dietrich, 1939, Simploptyxis Tiedt, 1958 and Parasimploptyxis Akopjan, 1976 are the largest Nerineoidea genera known.

In general, the enlargement periods correspond with times of warming.

This is evident from δ18 O curves presented by Weissert et al. (2004) for the Late Jurassic and Early Cretaceous and by Gale (2000) for the Cretaceous. The occurrence of large Nerineoidea fits well with a warming pulse in the Oxfordian (Weissert et al. 2004) but not with the Early Kimmeridgian (Cossmann 1898) for which the δ18 O curve indicates a cooling. This may, however, be due to inaccuracies in the correlation.

THE ORIGIN OF THE NERINEOIDEA

Besides the Nerineoidea, Haszprunar (1985a) and Bandel (1996) allocated the Streptacidoidea Knight, 1931, Mathildoidea Dall, 1889, Pyramidelloidea Gray, 1840, Architectonicoidea Gray, 1850 and Valvatoidea Gray, 1840 to the Allogastropoda Haszprunar, 1985, informally termed Lower Heterobranchia. Beyond the heterostrophy, Haszprunar quotes shell solidity, an operculum (which actually has never been recorded) and columellar plaits in the Nerineoidea as indicative for this systematic position. The limited space within the shell, leaving a “narrow labyrinth”, is reminiscent of the Pyramidelloidea. According to Schrödl etal. (2011), however, the Pyramidelloidea cluster with the Pulmonata. They have to be excluded from the Lower Heterobranchia and therefore cannot be related to the Nerineoidea.

Besides the family-specific features of the apertures, earliest Nerinelloidea agree remarkably in their external morphology. This postulates a parental group of more or less high-spired genera with adapically sinuate apertures in the Triassic. This is the case in Sinarbullina Gründel, 1997, Costacteon Gründel, 1997 and Domerionina Gründel & Nützel, 2012. Gründel& Nützel (2012) have allocated these genera to the Tubiferidae, but to me the before-mentioned morphological features seem representative for the Cylindrobullinidae Wenz, 1947, although their shells are not cylindrical like the typical representatives of the family.

THE ACTEONELLOIDEA, THE OTHER GROUP

OF LARGE MESOZOIC HETEROBRANCHIA

The Cylindrobullinidae which are the earliest Acteonelloidea possess more or less cylindrical whorls, low to moderately high spires, moderately adapically reflected growth lines and a subsutural ramp (see Gründel & Nützel 2012). The type species is C. fragilis (Dunker, 1846) from the Early Jurassic (Hettangian) of northern Germany (see Gründel 2010). Earliest Cylindrobullinidae date from the Late Triassic (Haas 1953; Gründel& Nützel 2012). Taxa from the St. Cassian Formation described by Bandel (1994a) under Acteonina (A. lancadellia Bandel, 1994, A. stuorense Bandel, 1994) have to be included in this family.

The Cylindrobullinidae were the parental group to Rugalindrites Gründel & Nützel, 2012 (pro Cylindrites Morris& Lycett, 1851). Because of its distinct subsutural notch and ramp and its columellar plaits, Rugalindrites represents the earliest Acteonellidae Gill, 1871 (see also Kollmann 1967). Occurrences in the Upper Middle Jurassic Great Oolite of Great Britain (Morris & Lycett 1854), the Bathonian of France (Fischer 1969) and the Late Jurassic of the Crimea (Pchelintsev 1963) illustrate the wide distribution and diversity of this group. In the Early Cretaceous (Barremian), Rugalindrites gave rise to Neocylindrites Sayn, 1932 (see Kollmann 1967), which is almost identical with its ancestor but differs by 2-3 strong columellar plaits (Fig. 12C). In the Aptian, a lineage leads from Neocylindrites to the convolute Acteonella d’Orbigny, 1842 (Fig. 12A, B) with “ Trochactaeon ” subrenauxi Pchelintsev, 1953 as a transitional form. In the Cenomanian, another lineage leads from Neocylindrites to the turreted Trochactaeon, which invaded littoral environments in the Late Cretaceous. As in the Nerineoidea this was connected with an increase up to 30 cm (Figs 10D; 12D). The subsutural notch indicates a semi-infaunal mode of life. In contrast to the Nerineoidea and all other Acteonelloidea genera, traces of boring sponges and epibionts are abundant on Trochactaeon shells (Schremmer 1954; Herm & Schenk 1971).Based on the boring sponges, Schremmer (1954) estimated living environments of 2 to 10 m depth. Winnowing during storm events has therefore commonly removed the surrounding sediment and accumulated the shells (Sanders etal. 1997). The shells which in contrast to the Nerineoidea were broadly convex may have been also partly uncovered from sediments the surface of the shells during lifetime. This is supported by the lack of a twisted siphonal canal or basal notch which would have elevated the inhalation opening and by the deposition of shell material in the adapical portion of the whorls (Fig. 10D) to protect these most vulnerable parts from abrasion (Kollmann 1967; Sohl & Kollmann 1985).

The apertures of the Acteonelloidea are high and narrow and broadly excavated at the base. Adjacent to the subsutural notch, the whorl interior is enlarged by a broad, bipartite parietal depression

Ebalidae

Ceritellidae

Itieriidae

Ptygmatididae Pseudonerineidae Nerinellidae

Eunerineidae n. fam. Nerineidae

Acteonellidae Pseudobullinidae

(Fig. 12E, F). I have interpreted this as an impression of a posterior adductor muscle (Kollmann 1967) but because of its position adjacent to the siphonal notch it is more likely the impression of a posterior pallial cavity.

Aperture shape and the comparatively deep and broad subsutural notch reflect a position of the mantly cavity and the anus in a right posterior position, as Morton (1972) has described for example in the Anaspidean Akera bullata Müller, 1776. In Akera Müller, 1776 the shell is partly or totally covered by the mantle. This might have been also the case in the Acteonelloidea but cannot be proved.

THE COMMON ORIGIN OF THE NERINEOIDEA AND THE ACTEONELLOIDEA

From the Cylindrobullinidae (as conceived here) the lineage of the Acteonelloidea can be followed back in time to the earliest Triassic Jiangxispira Pan, Erwin & Nützel, 2003. It possesses a fusiform shell with moderately convex, smooth whorls and the characteristic subsutural ramp. Pan etal. (2003) have pointed out the affinities to the Cylindrobullinidae and even left the possibility of an allocation to this family open. There is in fact a high coincidence of

the teleconch with Sinarbullina, which Gründel& Nützel (2012) allocated to the Tubiferidae (see above). Despite these affinities, Pan et al. (2003) allocated Jiangxispira to the Streptacididae because of the greater affinity of the protoconch. This would mean that both the Nerineoidea and the Acteonelloidea have evolved from the Streptacididae.

THE PARALLEL EVOLUTION OF THE ACTEONOIDEA Cossmann (1895a), Wenz & Zilch (1959), Bouchet & Rocroi (2005) and Gründel & Nützel (2012) have included the Acteonelloidea into the Acteonoidea. This cannot be upheld when the Acteonellidae originate from the Cylindrobullinidae. The main differences to the Acteonoidea are the subsutural notch and the smoothness of the shell, whereas the Acteonoidea are characterized by a sculpture of spiral grooves. This sculpture is a homologous morphological character persisting through geological times (see also Bandel 1994b). By considering the groove sculpture as a common feature, Mesozoic Acteonoidea would comprise the Bullinidae, the Acteonidae and the Ringiculidae in the sense of Gründel & Nützel (2012). They would further include parts of the Tubiferidae, which Gründel& Nützel conceive extremely broadly, and the “ Opisthobranchia ” by Kaim (2004).

The spiral sculpture supports the inclusion of the Early Carboniferous type species of Acteonina Meek (1863), A. carbonaria de Koninck, 1881 into the Acteonoidea and therefore into the Heterobranchia. This has been advanced by Knight (1936) and Kollmann & Yochelson (1976) but has been more or less vehemently rejected (Bandel 1994a; Schröder 1996; Nützel et al. 2000; Pan et al. 2003; Gründel & Nützel 2012). Bandel (1994a) stated that Acteonina was of “subulitid and thus of caenogastropod relation”. Later, he allocated it to the Soleniscidae (Bandel 2002). This has to be ruled out for the following reasons: The original of A. carbonaria is a cylindrical internal mould which is shouldered adapically. Knight (1941) mentions remains of a spiral sculpture and Batten (1966) figures a cylindrical specimen with narrow whorls, a distinct subsutural ramp and a well-preserved spiral sculpture. In contrast, the shell of the Soleniscidae is aciculate to subglobular, and the aperture is tightly drop-shaped with a strong columellar plait.The shells are smooth or bear a sculpture of minute collabral ribs. The morphology therefore differs totally from Acteonina carbonaria, which actually resembles the Mesozoic Acteonoidea described by Haas (1953) and Gründel& Nützel (2012). Information about the protoconch would certainly be desirable, but the preserved morphological features of the teleoconch are nonetheless highly conclusive for the Acteonoidea. The occurrence of Acteonoidea in the Palaeozoic is also supported by Acteonina permiana Hanger & Strong, 1998 from the Early Permian Coyote Butte Formation of central Oregon, USA. Again, the heterostrophy is not explicitly recognizable because of the recrystallized protoconch. Although the sculpture is not preserved, the narrow aperture and the ramps of the whorls agree well with Triassic taxa of the Tubiferidae described by Haas (1953), which undoubtedly belong to the Acteonoidea. The only disturbing fact is the large time interval between the Early Permian and the first well-preserved Acteonoidea in the Late Triassic, which has not yet been bridged.

Due to ongoing molecular studies and a reassessment of anatomical characters, the systematics of the Heterobranchia are currently in flux (see Dayrat & Tillier 2002; Vonnemann et al. 2005; Göbbeler & Klussmann-Kolb 2011; Schrödl et al. 2011). Only the following points seem certain: The Streptacididae and their descendants constitute a polyphyletic group which first appeared in the Palaeozoic and cluster outside the Euthyneura (Schrödl etal. 2011).

E XTINCTION OF THE NERINEOIDEA

AND ACTEONELLOIDEA

Fossil record

Table 1 provides a synopsis of the first appearance/ extinction of Nerineoidea and Acteonellidae families in the Cretaceous.

In many cases, the processes are obscured by facies changes or cannot be dated precisely. An exception is the Late Cenomanian extinction event: In the Bohemian and Saxonian Basin (Czech Republic and Germany), Eunerinea was recorded up to the Late Cenomanian zone of Metoicoceras geslinianum (d’Orbigny, 1842) but not in younger deposits (Kollmann et al. 1998). Comparable stratigraphic ranges were recorded by Berthou (1973) from Portugal and by Djalilov (1977) from central Asia. Eunerinea is still present in the assemblage of Cherghes Rumania, allocated by Lupu (1965) to the Early Cenomanian. Equally, Delpey (1940) recorded 2 Nerineidae species (Parasimploptyxis requieni d’Orbigny, 1842 and P. olisiponensis Sharpe, 1850) from the Turonian of the Near East, in contrast to a diverse Cenomanian fauna. Abbass (1963) reported exclusively Early Cenomanian Nerineoidea assemblages from Egypt.

The extinction of the Eunerineidae n. fam. is a good stratigraphical marker. The Nerinellidae, Nerineidae and Itieriidae survive the Late Cenomanian extinction event. Members of these families became extinct at various times during the remaining Late Cretaceous periods and do not show a single extinction pattern. In the “basins” of the Alpine Gosau Group, the large Nerineidae Simploptyxis Tiedt, 1958 and Parasimploptyxis Akopjan, 1976 persist to the Late Santonian or Early Campanian (Summesberger et al. 2002; Kollmann, own observations). Parasimploptyxis was also recorded by Czabalay (1973) from Early Campanian deposits of Ugod and other localities in Hungary and by Marincas (1965) from Sebes, Rumania. Species from Armenia and Azerbaidjan, allocated to Plesioptygmatis by Pchelintsev (1954), actually belong to Parasimploptyxis. Parasimploptyxis geissuensis Pchelintsev, 1954, according to Pchelintsev of Late Senonian age, was dated as Coniacian by Akopjan (1976). The stratigraphic range of these taxa agrees with those of European localities. Reports on stratigraphically younger Nerineoidea from Europe are based on incorrect determinations, mostly of Campanileoidea possessing internal plaits like Nerineoidea but differing by their apertures (Vaughan 1988).

A specimen from the the Xigaze Group of Tibet, allocated by Wen (1988) to Plesioptygmatis, is not well preserved. Because of its considerable thickness, the recrystallized columella must have been hollow. The high and comparatively narrow whorls possessing five internal plaits represent an undeterminable taxon of the Ptygmatididae. The extinction of this family in the Aptian confirms Yü Wen’s doubts about the Late Cretaceous age of the Xigaze Group.

A gastropod assemblage from the Zongshan Formation of the Kamba district of Tibet was first described by Douvillé (1916) and allocated to the Maastrichtian. Fragments of the large gastropod “ Nerinea ” ganesha Noetling, 1897 were removed from the Nerineoidea by Dietrich (1925) and transferred to the Campaniloidea. Douvillé described shell fragments under Acteonella crassa (Dujardin, 1835). Wen (1983), more cautiously, treated a sectioned specimen from the upper part of the Zongshan Formation with open nomenclature. The Tibetian specimens are apparently not as strongly inflated as A. crassa (see Kollmann 1965). In Trochactaeon ? tuilaensis Wen, 1983 from the highest Cretaceous Jidula Formation, the internal plaits extend to the parietal region. It represents another gastropod group but is indeterminable.

According to Saul & Squires (1998), Nerineoidea younger than Turonian do not occur along the Pacific margin of North America. From the Atlantic side of the continent, Woodring (1952) described fragments which have been found reworked in Paleogene deposits of Cuba as Nerinea epelys Woodring, 1952. This species belongs to the Nerineidae genus Parasimploptyxis, which is widely distributed in the central and southern Europe and in the Caucasian region. Knipscheer (1938) identified this taxon as Nerinea bicincta Bronn, 1934. This species was originally described from the Late Cretaceous Gosau Group of the Eastern Alps (Maiersdorf Formation in Summesberger etal. 2002). According to Tiedt (1958) it is synonymous with the Late Santonian Parasimploptyxis buchi Münster, 1829. The Maastrichtian age assumed by Woodring remains to be proved. Specifically indeterminable axial sections of Plesioptygmatis, identified by Knipscheer from the same region as P. burckhardti Boese, 1906, do not co-occur with this species. Based on the Cenomanian Nerinea bauga d’Orbigny, 1842, Dietrich (1939) described the genus Laevinerinea Dietrich, 1939 and included specimens from Cuba into this species. The exact stratigraphic position of the much smaller Cuban specimens is unknown.

The Nerineidae genus Plesioptygmatis is known exclusively from Maastrichtian deposits of the Caribbean Province determined by Kauffman (1973). The type species, P. burckhardti, was recorded from the Upper Member of the Cardenas Formation (San Luis Potosi, Mexico), which is of Early Maastrichtian age (Omana et al. 2008).An undescribed specimen from the Early Late Maastrichtian El Rayo Fomation of Puerto Rico figured by Sohl (1987) under Nerinella sp. possesses two columellar plaits and a distinctly twisted siphonal canal (Fig.5J). It represents a genuine Plesioptygmatis and is the stratigraphically youngest Nerineoidea taxon known. Plesioptygmatis became extinct in the Early Late Maastrichtian.

Stratigraphical data on Late Cretaceous Itieriidae are extremely scarce and not representative.There are only a few records of the Campanian to Maastrichtian Vernedia. These are Vernedia globoides (Stoliczka,1867) from the Arrialoor group of India and “ Itruvia ” scalaris Vogel, 1902 from Borneo. Sogdianella Djalilov, 1972 was recorded from Cuba and Peru (Kollmann & Sohl 1980) but the exact age is unknown.

As opposed to the Nerineoidea, the diversity of the Acteonelloidea increases after the Cenomanian (Sohl 1987). This is due to the evolution of the genus Trochactaeon in environments formerly inhabited by the Eunerineidae n. fam.. Trochactaeon develops extremely large shells. A typical representative is Trochactaeon ventricosus (Hojnos, 1921). The shells are almost globular and may reach sizes around 20 cm (see Figs 10D; 12E, F).

In the Eastern Hemisphere, the Acteonellidae (Trochactaeon, Neocylindrites, Acteonella) are scarce after the Campanian. Smith et al. (1995) quote Acteonella crassa (Dujardin) to extend into the Middle Maastrichtian in eastern Arabia (see also Morris & Taylor2000).The situtation is reversed in the Caribbean Province (Sohl & Kollmann 1985). Mexicotrochactaeon Akopian, 1972 and a group of Acteonella possessing two instead of three columellar plaits (for example Acteonella jicarensis Sohl & Kollmann, 1985 from Puerto Rico; Fig. 12B) are endemic to this marine palaeobiogeographic province.Studies of the Strontium isotope ratios by Steuber et al. (2002) indicate a late to latest Maastrichtian age for most Titanosarcolites limestones of Jamaica. In contrast to earlier biostratigraphic datings it is evident, that the Acteonellidae range stratigraphically up to the K/Pg boundary exclusively in this faunal province.

To conclude,the final extinction of the Nerineoidea and Acteonellidae was a long-lasting and palaeogeographically differentiated process and not a single event.

INTERPRETATION OF THE EXTINCTION EVENTS There is a remarkable congruency between the habitat and the Late Cretaceous climatic history. The Mid- Cretaceous was one of the warmest periods in phanerozoic times, with surface water temperatures up to 36°C and atmospheric CO 2 levels much higher than today (Forster et al. 2007; Pucéat 2008).From the Late Cenomanian on, temperatures increased steeply. In marine organisms, high temperatures can unbalance metabolic processes. This physiological disintegration (quoted after Levinton 1995) primarily affects stenothermic organisms that inhabit extremely shallow marine environments with restricted circulation. This clearly caused the late Cenomanian extinction of the Pseudonerineidae, Ceritellidae and Eunerineidae n. fam. Major regressions that took place earlier in the Cenomanian (Wilmsen 2012) could not have caused the extinction.

The Acteonellidae genus Trochactaeon substitutes the extinct taxa ecologically.A remarkable size increase in the comparatively short time range of this genus may reflect the high nutrient production due to favourable climatic conditions.In the Santonian, the palaeo-sea surface temperatures dropped to about 33° (Forster et al. 2007) and decreased further throughout the Campanian and Maastrichtian (Gale 2000; Burnett et al. 2000) with evidence of a seasonality (Steuber etal. 2005).The new conditions led to the extinction of the Old World Nerineidae and of Trochactaeon in the Campanian. Decreasing global temperatures caused Acteonella and Neocylindrites to retreat close to the circum-equatorial regions, where only a few species survived. Plesioptygmatis survived in the Caribbean Province until the basal Lower Maastrichtian, while Acteonella and Mexicotrochactaeon ranged up to the very Late Maastrichtian.There is, however, no indication that any of the Nerineoidea reached the K/Pg boundary.