Miocene sepiids ( Cephalopoda , Coleoidea ) from Australia

Two sepiid genera, Notosepia Chapman, 1915, and Sepia Linnaeus, 1758, are described from the Neogene deposits of Australia. A new and unique record of the middle Miocene Sepia sp. is reported from southern Australia. Based on similarities to contemporaneous sepiids, the new sepiid cuttlebone described herein belongs to the genus Sepia. Notosepia cliftonensis is suggested herein to be a descendant of the archaeosepiid stem lineage. Microstructures (lamellafibrillar nacre is the nacre Type II of septa and pillar prismatic layers) of the excellently preserved cuttlebone of Sepia sp. display a modern character of the phragmocone, fully comparable to the recent taxa. The stratigraphically wellcalibrated (based on foraminifera) cuttlebone represents the first unambiguous fossil record of the genus Sepia from the Southern Hemisphere. It significantly extends the biogeographical distribution of modern sepiids in the Miocene and suggests the existence of a sepiid eastward migratory route. Moreover, the presence of both conservativeand moderntype cuttlebones suggests a dual colonisation of Australian waters: the first (archaeosepiid) during the late Eocene–late Oligocene and the second (sepiid) during the early Miocene.


Introduction
The extant genus Sepia (and the entire family Sepiidae) is found worldwide (with the exception of North and South America) and is locally abundant and diverse, containing about 120 species (Reid et al., 2005).Evolutionary development of sepiids can be reconstructed thanks to the calcareous cuttlebone (sepion in other terminologies), although the fossil record of Sepiidae is relatively scarce.Higher abun-dances and diversities have been recorded in the Miocene from the Tethys (Mediterranean region) and the Central Paratethys (Košt'ák et al., 2016).Outside this area, only a single record from western India (Saurashtra region, Gujarat state) is documented (Mohan and Chatterji, 1956); however, these specimens were neither figured nor described (see below).A new record from Australia significantly influences our knowledge about the geographical distribution of modern cuttlefishes during the Neogene.Based on the cuttlebone described herein, it becomes clear that the genus Sepia had already reached Australia in the Miocene.Australia's shelf areas are among the biotopes with the highest actual cuttlefish diversity, counting 34 species of Sepia (including two questionable records), one Metasepia species and two Sepiella species.Northern Australia actually has a higher diversity than the southern part (23 versus 15 Sepia species).Moreover, the genera Metasepia and Sepiella are restricted to northern Australia.This is in striking contrast with a single fossil record presented herein.The highest diversity of Miocene sepiids is documented from the Mediterranean and Paratethys seas, whereas only three species inhabit the recent Mediterranean Sea (S. elegans Blainville, S. officinalis Linnaeus and S. orbignyana Férussac in d'Orbigny).
Precursors of the Sepiidae, the Belosaepiidae, first appeared in the Late Cretaceous (Ceratisepia Meyer, 1993) and diversified during the Palaeocene (two to three genera) and the Eocene (five genera).Belosaepiid cuttlebones mainly differ from their modern derivates by a strongly mineralised dorsal shield (composed of both calcite and aragonite), inclined septa, the absence of a fork, and the absence of pillars in the phragmocone chambers (see below).Chapman (1915) described the genus Notosepia from the Balcombian (middle Miocene) of Australia and he correctly separated Notosepia from Sepia, owing to belosaepiid features such as a massive shield and spine as well as widely spaced chambers.Nevertheless, the cuttlebone of Notosepia appears transitional between modern Sepia (see below) and Paleogene belosaepiids.In this respect, the mosaic character of Notosepia's morphology represents an important taxon that enhances our understanding of sepiid evolution.It is the aim of the present contribution to investigate a poorly known Neogene sepiid fauna from Australia with emphasis on systematics, stratigraphy and palaeobiogeography.

Material and methods
Five specimens of Notosepia cliftonensis Chapman, 1915, deposited in the collections of Museums Victoria in Melbourne in Australia (no.P12607, P12609, P126010, P324157, P324158), were studied.The only specimen not figured herein (no.P12608) is the counterpart of the holotype (no.P12607).Here, we refigure the type material for the first time since the original publication of Chapman in 1915.The new Miocene specimen determined as Sepia sp. is stored under item no.28324, Tate Museum, University of Adelaide.Sepia sp. is represented by two three-dimensionally preserved fragments of the cuttlebone embedded in yellowish limestone.
The latter specimen was cleaned with a pneumatic air scribe and a residuum was used for micropalaeontological study.It was wetted with hydrogen peroxide for several days and wet sieved over 71 µm and 1 mm screens.Foraminifera were picked and identified for the biostratigraphical analyses using a binocular stereoscopic microscope, a biological polarising microscope and a scanning electron microscope (SEM).Determination of foraminifers followed Loeblich and Tappan (1992), Holbourn et al. (2013) and Turco et al. (2011).Palaeoecological parameters of the obtained foraminiferal assemblage were evaluated based on the presence and dominance of taxa exhibiting special environmental significance (Boltovskoy, 1976;Boltovskoy and Wright, 1976;Murray, 2006).

Geographical, geological and stratigraphical settings
The new Miocene cuttlefish specimen described herein was collected from an unnamed outcrop along a road cut (Fig. 1) south of Mount Gambier (Gambier district, South Australia).The exposed bioclastic limestone, a well-sorted mediumgrained grainstone with dispersed macrofossils, represents the uppermost part of the Gambier Limestone Formation.The Gambier Limestone is a neritic (mid-to outer shelf), extratropical limestone up to 500 m thick, deposited in the Gambier Basin.It consists of grey to creamy bryozoan calcarenites with thin intercalations of marl and clay.The stratigraphic range is from the late Eocene to the middle Miocene based on planktonic and benthic foraminiferal assemblages (Li et al., 2000).Generally it is divided into three members, the Greenways Member, the Camelback Member and the Green Point Member (White, 1996), in the stratigraphical order.Deposition of the Gambier Limestone Formation ceased due to a regional regression in the early middle Miocene (around the Langhian-Serravallian boundary; Li et al., 2000).
Biostratigraphy of the sepia-bearing outcrop is based on foraminifera (Fig. 1).The strong secondary calcification of foraminiferal tests, which cover the original ornamentation and hide the chamber organization, was a major obstacle for their determination.Calcite molds of the tests are abundant.Using an optical microscope with immersion oil allowed us to explore the inner structure of the foraminiferal tests and to identify some of the better-preserved specimens (Fig. 2).Calcification also cemented foraminiferal specimens to each other as well as to the mineral and rock clasts.In addition to foraminiferal tests, the ostracodan valves, echinoid spines, scarce fragments, and molds of gastropods and bivalves were observed.

Systematic palaeontology
The terminology of macroscopic features used herein follows previous authors (see Košt'ák et al., 2013, and the discussion therein).The microstructure terminology follows Le Pabic et al. (2016).Sepiid and belosaepiid cuttlebones and their terminology are shown in Fig. 3.    Description.For a detailed description, see Chapman (1915: p. 357-358).
Discussion.Though the available cuttlebones are fragmentary and imperfectly preserved, Chapman (1915: p. 358) correctly recognised the peculiarity of Notosepia cliftonensis.The cuttlebone appears belosaepiid-like in many aspects: the dorsal shield is thick, coarsely granulated and www.foss-rec.net/20/159/2017/Foss.Rec., 20, 159-172, 2017 strongly convex.The spine (prong in other terminologies) is massive, the shoulder is indistinct but in some specimens may be slightly indicated, and septa are oblique and widely spaced.However, in contrast to most belosaepiids, the ventral process (corona in other terminologies, Chapman's alveolar lip) is poorly developed and not flared backwards.Also, the belosaepiid ventral deck (Fig. 3) is missing.Finally and most importantly, a fork is evident, a feature that does not exist in belosaepiids and that chiefly delimits primitive (belosaepiid) and advanced (sepiid) cuttlebones.
Family Locality and age.Road cut south of Mount Gambier, Gambier district, South Australia (Fig. 1).Gambier Limestone Formation, Green Point Member.The age is restricted by the presence of Orbulina suturalis, which indicates an age younger than 15.1 Ma, and the regional regression around the Langhian-Serravallian boundary.This stratigraphic interval corresponds to the late Batesfordian-Balcombian, equivalent to the Langhian-early Serravallian on the Mediterranean scale, middle Miocene.
Description.The incomplete specimen consists of the middle part of the cuttlebone.The preserved piece (L = 55 mm, W = 43 mm) probably represents about two-fifths of the total cuttlebone length (Fig. 5a).The estimated length of 130 mm suggests a medium-sized cuttlebone.
The broken anterior and posterior ends are 37 and 35 mm wide respectively.The anterior height of the cuttlebone is 9.3 mm.Details of the cuttlebone shape remain unclear, but the posterior free rims of septa, as well as the growth lines (Fig. 5b-c), suggest a prolonged oval shape (Fig. 6).
Septal suture lines are densely spaced in early ontogenetic stages and are more elliptically prolonged in later growth stages.The height of the chambers (Fig. 5b-c) in early ontogenetic stages is approximately 2 times lower than in the latest preserved chamber.Septal suture lines are fine and parabolic, prominent in particular in the median portion of the shell forming visible ribs.The space between the ribs varies between 1.3 and 1.5 mm.The surface of the dorsal part (shield) is very faintly and irregularly granulated (Fig. 8c-d).The dorsal shield is very thin and only preserved as a relic in the mediolateral posterior part.The median field area is separated only by fine lines and carries an extremely low, barely pronounced median keel.The lateral fields are markedly splayed at anterior margins, displaying straight parallel lines.Lateral keels are not developed and false keels (sensu Košt'ák et al., 2016), formed by rows of granules, are missing.Posterior and anterior parts are not preserved.Only the anterior margin of the outer cone is apparent through a fine radial striation.Chitinous and calcareous rims are not present.Morphological features of the ventral surface of the siphuncular zone (striated zone in other terminologies), indicated only in the cross section, clearly document a very wide and shallow ventral groove (rather shallow depression) in the median part of the cuttlebone (Fig. 6).
Discussion.Notosepia cliftonensis differs from this record by having a well-developed thick dorsal shield (Fig. 4) and more widely spaced septa (see Chapman, 1915, pl. 8, figs. 20, 22).In Notosepia, the dorsal granulation is also extremely developed in the middle portion (Fig. 4), in contrast to the fine granules in Sepia sp.Other morphological characteristics such as the spine and the external ornamentation of the posterior cuttlebone part cannot be compared.Sepia sp.shows very close similarities (general shape of the cuttlebone, suture lines, ornamentation character, etc.) to the Miocene cuttlefish fauna from the Mediterranean and the Central Paratethys, clearly demonstrating affinities to the extant genus Sepia.Cuttlebone microstructures support this classification (see below).
The globally less-diversified (seven species) but locally abundant genus Sepiella Gray forms almost identical cuttlebones, with only the apical spine missing.We cannot confirm the presence or absence of the spine in the studied specimen, but rather we suggest the new record to be a representative of the genus Sepia.According to the phylogeny of Sepiidae based on molecular data (Yoshida et al., 2006), Sepiella forms a clade with Sepia taxa, suggesting that the spine was lost in different lineages (i.e.Sepiella and Metasepia Hoyle).In this respect, we consider that both mentioned genera evolved later from the genus Sepia.

Structures and microstructures
The sepiid cuttlebone basically consists of the strongly mineralised dorsal shield and the delicate chamber complex (Figs.3c, 7-8).The chamber complex is characterised by horizontal to subhorizontal septa, vertical pillars, and horizontal and vertical pillar membranes (Fig. 7).Mineralogically, the cuttlebone is composed of calcite, aragonite and organic matter (β-chitin linked with proteins; Le Pabic et al., 2016).Microstructures of extant and extinct sepiid cuttlebones were studied in detail by numerous authors (Bandel and Boletzky, 1979;Ward and Boletzky, 1984;Gutowska et al., 2010;Doguzhaeva and Mutvei, 2012;Doguzhaeva et al., 2014;Doguzhaeva and Dunca, 2015;Checa et al., 2015;Le Pabic et al., 2016).Doguzhaeva and Dunca (2015) summarised ultrastructural terms of the siphonal zone and subsequently introduced a new term for the contacting ridges based on well-preserved recent material.Our extraordinarily well-preserved cuttlebone from the Australian Miocene revealed surprising micro-and ultrastructural details without significant diagenetic alterations.The dorsal shield (Fig. 8a-d), whose marginal parts are partly preserved, displays a fine granulation (Fig. 8c-d).It is formed by well-developed prismatic crystals.The septum is formed by lamella-fibrillar nacre, typical for phragmoconebearing coleoids (nacre Type II sensu Mutvei, 1970).It is characterized by microlaminated ultrastructure (Doguzhaeva and Dunca, 2015), where each lamella consists of aragonite fibres of different orientation, in some cases with visible criss-cross patterns.The most important observation concerns vertical structures, which support the horizontal septa.These structures unambiguously represent pillars (columns, undular plates or intracameral walls in other terminologies).The pillars are formed by a prismatic layer, strictly delimited from the septum proper (Fig. 8e-f).Horizontal striae along the pillars (Fig. 7a) do represent growth stages (Checa et al., 2015).The pillars are typically meandering as can be seen on weathered septal surfaces (Figs.5d-f, 8g-h).The attachment of the pillars to the preceding and succeeding septum therefore (Fig. 8h) resembles ammonoid sutures.Seilacher and Chinzei (1993, and the discussion therein) used the term pillar sutures for this ornamentation.They figured (Seilacher and Chinzei, 1993, fig.2b-d) lineages of broken pillars (stumps), banding of pillars or pillar-elevated basis (and their drawings) but not the suture lines, which are visible in our specimen (Fig. 8g-h).Horizontally spanned organic membranes as known in a couple of extant Sepia species are not visible.

Discussion
The record of Sepia sp. from the Miocene of Australia significantly extends the geographical distribution of the genus.
The majority of fossil cuttlefish species are concentrated in the Mediterranean and the Paratethys (Košt'ák et al., 2016), while scarce records are reported from the Atlantic coast of France (Roger, 1947) and Spain (Mayoral and Muñiz, 1994).
The easternmost Miocene record (before the specimen described herein) of a cuttlefish was reported from the Indian coast of Gujarat state in western India (Mohan and Chatterji, 1956); however, this material was not figured.The specimen described herein represents the first Miocene cuttlebone of modern type in the Southern Hemisphere.Thus, our record of Sepia sp.directly suggests more extensive migratory routes and subsequently clearly documents the existence of genus Sepia in the Indo-Pacific area (Fig. 9).Chapman (1915) described the peculiar sepiid genus Notosepia from southern Australia (Victoria state).He correctly mentioned affinities to the extinct genus Belosaepia and analysed the differences in great detail (see Chapman, 1915, p. 358).Morphologically, Notosepia appears to be intermediate between belosaepiids and sepiids.Both belosaepiids and sepiids probably originated and radiated in the Mediterranean.
Belosaepiids migrated westwards (Košt'ák et al., 2013) and disappeared worldwide during the late Eocene: in North and South America (Weaver and Ciampaglio, 2003;Yancey et al., 2010) without descendent and in the Mediterranean with descendent, namely less-well-known sepiids like Archaeosepia Szörényi (late Eocene-late Oligocene), which are the root of advanced sepiids.Notosepia is also possibly a descendent of the Archaeosepia species group possessing a mosaic of primitive (e.g.massive spine, massive dorsal shield, wide chambers) and advanced (fork) features.This assumption implicates the development of the fork within Archaeosepia (which needs to be tested in the future).Notosepia accordingly colonised Australian waters after the decline of belosaepiids.Thus, at least three migration waves are recognisable within the order Sepiida: belosaepiid, archaeosepiid and sepiid (Fig. 9).Notosepia is seen here as a Miocene remnant of the Oligocene archaeosepiid migration, while Sepia sp.reached Australia with the Miocene sepiid eastward migration.This triple migratory hypothesis is largely congruent with Khromov (1998), who was the last one to discuss the palaeobiogeography of Sepiida.Khromov's first three (out of five) colonisation phases correspond to our belosaepiid, archaeosepiid and sepiid migrations.He assumed that sepiids invaded Australian waters once during the third (Miocene) phase, while we suggest a dual coloni-sation: archaeosepiid during the late Eocene-Oligocene and sepiid during the early Miocene.
It is notable that undamaged sepiid cuttlebones may float for a very long time -more than a year (Hewitt and Pedley, 1978) -and thus may be transported over long distances.During this period, they form a nekroplankton, commonly used by pseudoplanktonic organisms (i.e.algae, barnacles; Jongbloed et al., 2016).No signs of any organism interactions with the cuttlebone have been seen in our specimen.Therefore, we do not assume a longer post-mortem transport in the ocean.Furthermore, its exceptional state of preservation suggests the rather rapid burial of a fresh specimen.

Conclusions
A new and exceptionally well-preserved specimen (including cuttlebone microstructures) of Sepia sp. from the mid-Miocene of Australia documents the already wide geographical distribution of the genus in the Miocene.Before, the Miocene Sepiidae were exclusively known from the European Atlantic coast, the Mediterranean and the Central Paratethys areas.The Miocene sepiid record from western India still needs confirmation.This observation is very important for phylogeny and palaeogeography (suggesting a new sepiid eastward migratory route) as well as for the molecular analysis.The new Australian specimen from the Mount Gambier vicinity is stratigraphically calibrated based on foraminifera, indicating the late Batesfordian to Balcombian age.
Sepia sp. from southern Australia possesses all morphological features comparable to the recent genus Sepia on both macro-and microstructural levels.In these respects, we place this specimen within the genus Sepia.
The genus Notosepia described by Chapman (1915) is unique in having a mosaic of primitive and advanced features.Despite primitive belosaepiid characters, the presence of a fork led us to regard Notosepia as a descendent of the late Eocene-late Oligocene genus Archaeosepia.
Exceptionally well-preserved microstructures of the phragmocone display septal and pillar micro-and ultrastructures, including lamella-fibrillar nacre, which are typical for sepiids.Inside the microstructures observed, unusual suturelike structures (pillar sutures sensu Seilacher and Chinzei, 1993) resembling ammonite sutures occurred.Analogically, these structures may play a role in the chamber reinforcement.
Biogeographically, we can now recognize three periods of sepiid migrations: a belosaepiid during the Eocene, an archaeosepiid during the late Eocene-late Oligocene and a sepiid during the early Miocene.The presence of both a conservative (Notosepia) and a modern type (Sepia sp.) of cuttlebone suggests a dual (archaeosepiid and sepiid) colonisation of Australian waters.
Material.A single rock sample comprising two cuttlebone fragments (not clear if they belong to one individual), with the larger one possessing important morphological features.Specimen stored in the Tate Museum of the University of Adelaide under item no.28324.