The Origin of the Mangrove and Saltmarsh Snail Ellobium (Eupulmonata, Ellobiidae)

: The pulmonate gastropod genus Ellobium has its greatest diversity in the modern Indo-West Paciﬁc Region (IWP). Its origin, however, is traced to the Early Oligocene of the Northeastern Atlantic and the Western Tethys Region. Two Ellobium species are documented from the Rupelian of France and Italy and a new species is recorded from the Chattian of Hungary: Ellobium kerwaensis nov. sp. The ﬁrst records in the IWP are known from the Early Miocene, suggesting an eastward range expansion of the genus around the Oligocene/Miocene boundary, when Ellobium became extinct in the European seas. Extant Ellobium species are bound to habitats above the high tide line in salt marshes and mangroves. Comparable environmental requirements are expected for the fossil congeners. Ellobium may derive from Eocene ancestors, such as the Bartonian Eoellobium heberti from the Northeastern Atlantic. Eoellobium is introduced in this paper as a new genus.


The Habitat of Ellobium
Ellison et al. [2] and Groh [16] discussed Ellobium as a mangrove-associated gastropod genus.Whilst a general affinity to the mangrove ecosystem can be stated for the genus, an obligate relationship with mangrove trees is not obvious for most of the species.Ellobium aurisjudae is found in estuaries on saltmarshes above high tide, under logs, and within mangrove swamps [17].It is also found on mangrove trunks [18] but not higher on mangrove trees [19].Similarly, E. aurismidae dwells in salt marshes above the high tide line and may be associated with the Nypa trunks [17].In the Avicennia mangroves of Sumatra, E. aurismidae and E. aurisjudae were found to be rare compared to typical mangrove-dwelling species, such as Cerithidea cingulata (Gmelin, 1791) [20] and Nerita balteata (Reeve, 1855) [21,22].Setyadi et al. [23], found Ellobium aurisjudae to be among the most frequent gastropods in the Rhizophora and the Bruguiera mangroves of Papua, Indonesia.Ellobium scheepmakeri is found in the saltmarshes of estuaries between long grass and under logs above the high tide line and in the dry Nypa mangrove forests at salinities of 6-7 ppt [17,24].Similarly, E. tornatelliforme (Petit de la Saussaye, 1843) [25] prefers the saltmarshes and occurs between the long grasses and among the rotting logs above the high tide line [17].Ellobium gangeticum (Pfeiffer, 1855) was recorded from the salt marshes and the estuaries among the mangrove roots [26].Ellobium chinense occurs between the stones in freshwater tidelands and on the halophytes such as Zoysia saltmarshes [27,28] and is also found on the trunks of the mangrove trees [29].The Western Atlantic 'Ellobium' dominicense also lives in embayments, mangrove creeks and estuaries at low salinities [30,31] but is mainly buried in the humic sediment and under rotting logs [14].Thus, the lowest common denominator for the IWP-species of Ellobium in terms of habitat, is an occurrence in the saltmarshes above the high tide line in close vicinity of the mangroves.We propose comparable habitat requirements for the fossil species.This is also supported by the co-occurrence of Nerita and Potamididae at the type locality of Ellobium kerwaense (author's data, NHMW collection).
Taxonomy 2023, 3,2 Ellobium aurisjudae is found in estuaries on saltmarshes above high tide, under logs, and within mangrove swamps [17].It is also found on mangrove trunks [18] but not higher on mangrove trees [19].Similarly, E. aurismidae dwells in salt marshes above the high tide line and may be associated with the Nypa trunks [17].In the Avicennia mangroves of Sumatra, E. aurismidae and E. aurisjudae were found to be rare compared to typical mangrovedwelling species, such as Cerithidea cingulata (Gmelin, 1791) [20] and Nerita balteata (Reeve, 1855) [21,22].Setyadi et al. [23], found Ellobium aurisjudae to be among the most frequent gastropods in the Rhizophora and the Bruguiera mangroves of Papua, Indonesia.Ellobium scheepmakeri is found in the saltmarshes of estuaries between long grass and under logs above the high tide line and in the dry Nypa mangrove forests at salinities of 6-7 ppt [17,24].Similarly, E. tornatelliforme (Petit de la Saussaye, 1843) [25] prefers the saltmarshes and occurs between the long grasses and among the rotting logs above the high tide line [17].Ellobium gangeticum (Pfeiffer, 1855) was recorded from the salt marshes and the estuaries among the mangrove roots [26].Ellobium chinense occurs between the stones in freshwater tidelands and on the halophytes such as Zoysia saltmarshes [27,28] and is also found on the trunks of the mangrove trees [29].The Western Atlantic 'Ellobium' dominicense also lives in embayments, mangrove creeks and estuaries at low salinities [30,31] but is mainly buried in the humic sediment and under rotting logs [14].Thus, the lowest common denominator for the IWP-species of Ellobium in terms of habitat, is an occurrence in the saltmarshes above the high tide line in close vicinity of the mangroves.We propose comparable habitat requirements for the fossil species.This is also supported by the co-occurrence of Nerita and Potamididae at the type locality of Ellobium kerwaense (author's data, NHMW collection).

The Fossil Record of Ellobium
The last complete synopsis of the fossil record of Ellobium was published by Wenz [32], who listed 13 species and subspecies from the Lutetian to the Pliocene of Europe.Glibert [33,34] provided another overview with eight fossil species from the Eocene and Miocene of Europe, and one fossil species from the Paleocene (Danian from Belgium) but did not consider the Oligocene species.Since then, several new species have been described, which are still placed in Ellobium by MolluscaBase eds.[6], e.g., 'E.' boriesi (Plaziat, 1970) [35].The census of 23 species, listed by MolluscaBase eds.[6], however, must not be read as a critical revision and comprises Jurassic ('E.' koerti Huckriede, 1967 [36]) and Danian ('E.' olivaeforme (Briart & Cornet, 1887) [37]) species sharing rather superficial

Material and Methods
All specimens are stored in the collections of the Natural History Museum Vienna (Austria), the Muséum national d'Histoire naturelle, Paris (France) and the Naturalis Biodiversity Center, Leiden (The Netherlands).For conchological terminology see [54].
Diagnosis.Large sized, ovate to elongate ovate shell with conical spire, convex spire whorls and occasional varices.Prominent subsutural collar, delimited by deep spiral groove.Sculpture of close-set, rugose axial ribs, crossed by weak spiral threads, resulting in irregularly granulose sculpture.Aperture moderately wide.Columellar callus forming sharply delimited, moderately thickened callus rim in adapical half of aperture, detached from base; callus becoming thinner adapically.Columellar fold moderately prominent, twisted; parietal fold weak.Outer lip slightly thickened without prominent palatal swelling.Differing from Ellobium in the convex spire whorls, the presence of varices and the prominent subsutural cord.
Description.As for type species.
species, E. scheepmakeri is morphologically closest to Eoellobium heberti concerning the convex spire whorls and the relatively wide aperture.Ellobium scheepmakeri, however, lacks the prominent subsutural collar and develops a prominent parietal fold.
Ecology.The mollusk assemblage from Bois-Goüet at Saffré (France) is very diverse and comprises more than 1000 species [58] derived from terrestrial, freshwater, brackish water and shallow marine paleoenvironments.Therefore, it is difficult to interpret the preferred habitat of Eoellobium.Discussion.Eoellobium nov.gen.differs from Ellobium in the convex spire whorls, the presence of varices and the prominent subsutural cord.In addition, the weak columellar and parietal fold and the less thickened outer lip distinguish it from Ellobium.Crosse (1896: 107) wrote: "A.Heberti, Vasseur, grande et belle espèce, de la taille de l'A.auris-Midae, mais ne lui ressemblant d'ailleurs en aucune façon" [=A.heberti, Vasseur, a large and beautiful species, the size of A. auris-Midae, but in no way resembling it] [57].Moreover, Ellobium does not develop such prominent axial ribs.In particular, the presence of varices suggests a different mode of ontogeny for Eoellobium.Nevertheless, Eoellobium heberti might represent an early representative of the Ellobiidae-lineage from which Ellobium developed around the Eocene/Oligocene boundary.Among the modern Ellobium species, E. scheepmakeri is morphologically closest to Eoellobium heberti concerning the convex spire whorls and the relatively wide aperture.Ellobium scheepmakeri, however, lacks the prominent subsutural collar and develops a prominent parietal fold.
Ecology.The mollusk assemblage from Bois-Goüet at Saffré (France) is very diverse and comprises more than 1000 species [58] derived from terrestrial, freshwater, brackish water and shallow marine paleoenvironments.Therefore, it is difficult to interpret the preferred habitat of Eoellobium.
Revised description.Large sized, ovate to elongate ovate shells with conical spire; apical angle c. 65 • .Protoconch and early teleoconch whorls unknown.Spire of more than seven convex whorls.Suture narrowly incised.Prominent subsutural collar, delimited by deep spiral groove.Last whorl convex with high-placed, rounded shoulder, passing into weakly convex base.Occasional varices.Sculpture of close-set, rugose axial ribs, crossed by weak spiral threads, resulting in irregularly granulose surface.Axial ribs most prominent along and below subsutural collar.Aperture moderately wide, posteriorly angulated, with faintly incised basal margin.Columellar callus forming sharply delimited, moderately thickened callus rim in abapical half of aperture; callus narrowing adapically.Columellar fold very weak to subobsolete.Parietal fold weak, placed roughly mid-aperture.Outer lip slightly thickened without marked palatal swelling.Fasciole broad, convex with prominent growth lines.
Discussion.This species was placed in Ellobium by Wenz 1923 [32] and Lebrun et al. 2012 [58] but the similarity in outline, sculpture and size with this genus is superficial.Melampus britannus Vasseur, 1882 and Auricula simplex Cossmann, 1895 are both found also at Bois-Goüet together with Eoellobium heberti.Eoellobium britannus and E. simplex represent shells with strongly reduced sculpture and weak spiral groove below the subsutural collar.'Auricula' boriesi Plaziat, 1970, from the Ypresian of France, differs from Eoellobium heberti in its stronger, thicker columellar and parietal folds, by the presence of a third posterior parietal fold and by the strongly thickened outer lip, which has a prominent palatal swelling.Moreover, it lacks a subsutural collar.Similarly, 'Ellobium' viai Calzada & Urquiola, 1995 [61] from the Priabonian of Spain, lacks a subsutural collar and has a sculpture of prominent axial ribs.
Diagnosis."Shell moderately large and thin (25 mm) to large and thick (100 mm) and covered with pale brown periostracum.Spire low to moderately high, sculptured with granular spiral lines crossed by more or less conspicuous axial cords.Body whorl about 80% shell length, with same sculpture as spire, sometimes weakly depressed dorsoventrally.Aperture about 80% length of body whorl; small, very oblique, twisted columellar tooth, stronger anterior parietal tooth; posterior parietal tooth sometimes present; outer lip thin to thick, sharp to weakly reflected."Martins (1996) [14] (178).Inner shell walls partly resorbed in [17] and figs 9.2c-d in [64].For anatomical data see Martins (1996) [14].
Ellobium kerwaense nov.sp.   .Protoconch and early teleoconch whorls unknown.Spire consisting of more than six weakly convex whorls.Last whorl ovoid, moderately convex with periphery usually in adapical third (but may be below mid-whorl in some specimens).Suture narrowly canaliculate.Base slowly contracting.Sculpture of prominent, slightly irregular, faintly sigmoidal, finely granulose axial ribs separated by narrower interspaces.Weak spiral threads most distinct on base separating slightly better defined, subquadratic granules.Aperture moderately narrow, posteriorly angulated with convex basal margin.Columellar callus very prominent, broad, thickened, well demarcated from base, forming broad, thickened callus detached at base and with distinct chink with base.Fasciole broad, indistinct.Columellar fold not very prominent, slightly twisted, fading out on columellar callus.Parietal fold prominent, raised, moderately narrow, in abapical third of aperture, fading out on columellar callus.Outer lip strongly thickened, very broad with prominent palatal swelling slightly above midwhorl.
Taxonomy 2023, 3, 7  Discussion.Ellobium kerwaense nov.sp. was compared with or confused with Ellobium subjudae and E. vicentinum [66,71].Ellobium vicentinum differs in its smaller size, slenderer outline, higher spire, more adapical position of the parietal fold and distinctly less thickened outer lip.Ellobium subjudae is distinguished by its much higher spire and the wider aperture, which lacks a palatal swelling.Moreover, the outer lip and columellar callus are much more thickened in E. kerwaense nov.sp.Ellobium mizutanii Kawase & Ichihara, 2021, from the Early Miocene of Japan [50], is similar in outline but is even more inflated, has a wider aperture and a less thickened outer lip, which lacks a palatal swelling.The Early Miocene E. yatsuoense Tsuda, 1959, from Japan [52], is similar to E. kerwaense in outline but has slightly higher spire whorls and its sculpture is weaker [51] (pl.7, figs 4a,b).Among the extant Ellobium species, E. aurismidae is reminiscent of the Paratethyan species in its general shell shape.However, E. aurismidae has a much larger shell, with flat spire whorls bearing more prominent granules, and a much weaker palatal swelling than that seen in E. kerwaensis.Moreover, below the shoulder the whorls in E. aurismidae are usually smooth and not finely granular as seen in E. kerwaensis.
Concerning the prominent palatal swelling, E. kerwaense nov.sp. is morphologically closer to the extant E. aurisjudae, which is far more elongate and bears a second parietal fold.
Distribution.Central Paratethys Sea: Known so far only from Máriahalom and Esztergom in the Komárom-Esztergom district in Hungary [67,70].

Ellobium subjudae (d'Orbigny, 1852)
Figure 4(A1,A2)    Revised description.Medium-sized, elongate ovate, solid shell with conical spire, apical angle c. 60 • .Protoconch and early teleoconch whorls unknown.Spire of more than six weakly convex whorls.Last whorl elongate ovoid, with faint subsutural concavity; base convex.Suture narrowly incised; suture on last whorl slightly oblique.Sculpture of rugose, faintly sigmoidal axial ribs, separated by narrow interspaces.Granules most distinct over subsutural ramp and on base.Aperture moderately wide, posteriorly angulated, with wide, convex basal margin.Columellar callus, moderately thickened, forming broad rim, well demarcated from base.Abapically, columellar callus becoming thick, demarcating narrow chink from base.Columellar fold relatively weak, broad fading out on smooth columellar callus.Parietal fold prominent, relatively narrow (compared to some of the extant species like E. aurisjudae), slightly oblique, fading out on columellar callus.Outer lip thickened with beveled edge, the inner beveled portion concave, without palatal swelling.adapically Discussion.Ellobium subjudae is similar to the coeval E. vicentinum but differs in its much larger size and the more prominent parietal fold.Because E. vicentinum bears a palatal swelling, whereas E. subjudae lacks such feature, it is unlikely that E. vicentinum is based on a subadult specimen of E. subjudae.For a separation from E. kerwaense nov.sp.see discussion on that species.The extant Ellobium aurisjudae is reminiscent of E. subjudae in its elongate outline, but differs clearly in its higher last whorl, the narrower and high aperture, the presence of a second parietal fold, and broader folds.
Revised description.Medium sized, moderately narrowly ovate with acute spire, solid.Spire conical, moderately high, of more than 5 weakly convex whorls; apical angle 63 • .Protoconch and early teleoconch whorls unknown.Shell surface of spire abraded.Last whorl moderately convex, attaining about 80% of total height, with periphery distinctly below suture.Suture narrowly canaliculate, slightly oblique on last whorl.Base slowly contracting.Sculpture on last two whorls of coarse, finely rugose, broad, low, irregular, faintly sigmoidal axial ribs with narrow interspaces, composed of coalescent subquadratic nodes.Sculpture persisting to base.Aperture moderately narrow with acute posterior angulation and convex basal margin.Columella with broad, not very thickened callus narrowing adapically.Columellar callus relatively weak, delimitating narrow chink on base.Columellar fold moderately prominent, weakening inside aperture.Parietal fold relatively weak for genus, not very broad, weakly oblique, slightly below middle of aperture.Outer lip thickened with palatal swelling above mid-whorl.
Discussion.The description of this species by Fuchs (1870) was misleading as he did not describe and illustrate the columellar fold.The mollusk fauna from Soggio di Brin is a rich assemblage typical for shallow sublittoral environments with cassid, cypraeid and marginellid gastropods but lacks genera typical for mudflats, saltmarshes and mangroves.Therefore, the single Ellobium shell is parautochthonous and transported.
Distribution.Western Tethys: Only known so far from the two close-by Early Oligocene (Rupelian) localities Soggio di Brin at Salcedo and Casa Priva at Bassano in the Vicenza Province (Italy) [88].

Discussion
The modern distribution pattern of Ellobium, with the greatest diversity being in the Indo-West Pacific-Region (IWP Region), suggests that this region was a center of origin of the genus.However, this hypothesis conflicts with the fossil record, as the oldest records are not from the IWP Region but from the Rupelian of the Western Tethys and the Northeastern Atlantic (Figure 5).A Rupelian first appearance of Ellobium is in excellent agreement with the molecular data [89], which includes E. aurisjudae, E. chinense and E. scheepmakeri.This molecular analysis suggested an origination of the genus during the Oligocene times.However, the taxonomic revision presented herein suggests older roots for the group, extending back to the Middle Eocene, represented by Eoellobium nov.gen.from the North Eastern Atlantic.The oldest fossil Ellobium species in the IWP Region post-dates the European occurrences.Ellobium mizutanii Kawase & Ichihara, 2007 and one unnamed species from Mizunami (Gifu Prefecture, Japan), E. yatsuoensis Tsuda, 1959 from Osa-wano-machi and Kaminiikawa-gun (Toyama Prefecture, Japan) and E. cf.aurisjudae from Ninohe City (Iwate Prefecture, Japan) were described from the Early Miocene [50,[90][91][92][93].After this first radiation in the IWP Region, the fossil record of the genus becomes rather poor.An unnamed species was recorded from the Middle Miocene of Java [94] and Ellobium aurismidae was reported from the Late Miocene or Early Pliocene of the Philippines [95].Another unnamed Late Miocene Ellobium was reported from Japan [96].Ellobium aurisjudae was documented from the Late Pliocene of Java [93] and from the Holocene of Malaysia [17] from where Ellobium scheepmakeri was also documented from the Late Pleistocene or Holocene [17].The molecular data suggests Ellobium chinensis was present at least since the Pleistocene [28].Despite this fragmentary record, it can be stated that Ellobium was established in the IWP Region represented by several species since the Early Miocene.Ellobium aff.pellucens (Menke) [='E.' aff.dominicense] from the Lower Miocene of Panama [97] documents that the Western Atlantic lineage 'E.' dominicense can also be traced back to the Early Miocene but it is questionable if this lineage is directly related to Ellobium.
This pattern of stratigraphic occurrences would suggest the Northeastern Atlantic and the Western Tethys as the centers of origin from where Ellobium spread into the IWP Region.It is possible that the Western Atlantic 'E.' dominicense represents a Transatlantic offshoot of this radiation.

Conclusions
The tropical pulmonate genus Ellobium has its highest diversity in the Indo-West Pacific Region and does not occur in the modern Mediterranean Sea and the Eastern Atlantic.Its origin can be traced back to the Early Oligocene in the Northeastern Atlantic and Western Tethys, where it is documented by two species.During the Late Oligocene, Ellobium also reached the Central Paratethys Sea, from where it is documented by the newly described Ellobium kerwaense nov.sp.No species are known from the European Miocene suggesting an extinction around the Oligocene/Miocene boundary.The radiation in the IWP Region started during the Early Miocene.Since then, the genus is documented by fragmentary fossil records in the entire IWP Region.The Oligocene appearance of Ellobium is in excellent agreement with the proposed age of the genus in a molecular phylogeny of the Ellobiidae [89].The roots of Ellobium might be represented by the Middle Eocene genus Eoellobium, which is morphologically closely similar to Ellobium but differs in its prominent subsutural collar and weaker columellar and parietal folds.Ellobium is another example of an eastward range expansion of a mollusk group, as it originated in the Paleogene of the Western Tethys and subsequently spread into the Indo-West Pacific via the Tethys Gateway.Acknowledgments: Thanks to Anita Eschner (NHMW) for providing access to the collection of extant Ellobium species.We are grateful to Anton Breitenberger (Bad Vöslau) for donating two shells of Ellobium kerwaense.The other three type specimens were collected and donated by the late Reinhold Kunz (Vienna) who is forever in our memory.We thank two anonymous reviewers for their constructive comments.We thank Alice Schumacher (NHMW) for taking pictures of most of the illustrated specimens.The pictures of Ellobium subjudae were made by Laurent Charles (Muséum d'Histoire naturelle de Bordeaux) and the pictures of Eoellobium heberti were provided by Philippe Loubry (MNHN/CNRS).

Conflicts of Interest:
The authors declare no conflicts of interest.Similar range expansions were documented for some Western Tethyan strombids and for the tridacnine bivalves [98][99][100].These taxa first appeared in the Northeastern Atlantic and Western Tethys and arrived during the Oligocene via the open Tethys Gateway in the IWP Region (Tridaninae) and in part also arrived in the Western Atlantic (e.g., Persististrombus Kronenberg & Lee, 2007 [101]).We note however, that the mode of dispersal of marine taxa, such as strombids and tridacnids, is clearly different from that of pulmonate ellobiids.

The Extinction of Ellobium in European Seas
Ellobium species are rare in the fossil record and the three European Oligocene species are known from only a few specimens.Nevertheless, we consider it unlikely that the genus was overlooked thus far in the well-known Early Miocene assemblages of the Northeastern Atlantic, the Western Tethys and the Central Paratethys Sea.This is especially true for the enormously rich mangrove fauna of the Korneuburg Basin, which has been systematically screened by citizen scientists for nearly 30 years resulting in a significant amount of material [102,103].Similarly, the Aquitanian and Burdigalian faunas from the Aquitaine Basin are well documented and extensively collected.Therefore, we assume that Ellobium vanished from this region at the end of the Chattian.It would be tempting to explain this extinction by the cooling around the Oligocene/Miocene boundary, which coincided with the M1 glaciation, due to a major expansion of Antarctic ice shields [104,105].Other species of the Oligocene mangrove assemblage, however, persisted into the Early Miocene.The potamidids Mesohalina margaritacea (Brocchi, 1814), and Ptychopotamides cinctus (Bruguière, 1792) and the bivalve Polymesoda subarata (Schlotheim, 1820) [106] occur in Rupelian and Chattian assemblages of the Western Tethys and passed the Oligocene/Miocene boundary [107].Therefore, the correlation with the M1 glaciation might be too simplistic.

Conclusions
The tropical pulmonate genus Ellobium has its highest diversity in the Indo-West Pacific Region and does not occur in the modern Mediterranean Sea and the Eastern Atlantic.Its origin can be traced back to the Early Oligocene in the Northeastern Atlantic and Western Tethys, where it is documented by two species.During the Late Oligocene, Ellobium also reached the Central Paratethys Sea, from where it is documented by the newly described Ellobium kerwaense nov.sp.No Ellobium species are known from the European Miocene suggesting an extinction around the Oligocene/Miocene boundary.The radiation in the IWP Region started during the Early Miocene.Since then, the genus is documented by fragmentary fossil records in the entire IWP Region.The Oligocene appearance of Ellobium is in excellent agreement with the proposed age of the genus in a molecular phylogeny of the Ellobiidae [89].The roots of Ellobium might be represented by the Middle Eocene genus Eoellobium, which is morphologically closely similar to Ellobium but differs in its prominent subsutural collar and weaker columellar and parietal folds.Ellobium is another example of an eastward range expansion of a mollusk group, as it originated in the Paleogene of the Western Tethys and subsequently spread into the Indo-West Pacific via the Tethys Gateway.

Figure 5 .
Figure 5. Middle Eocene to Holocene geographic and stratigraphic distribution of Eoellobium and Ellobium.

Author Contributions:
Conceptualization, M.H.; writing, M.H., J.-M.P. and B.M.L.All authors have read and agreed to the published version of the manuscript.Funding: This research received no external funding.Data Availability Statement: All data are given in this publication.

Figure 5 .
Figure 5. Middle Eocene to Holocene geographic and stratigraphic distribution of Eoellobium and Ellobium.