First Direct Evidence of Ammonoid Ovoviviparity

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First direct evidence of ammonoid ovoviviparity

ALEKSANDR A. MIRONENKO AND MIKHAIL A. ROGOV

Mironenko, A.A., & Rogov, M.A. 2015: First direct evidence of ammonoid ovoviviparity. Lethaia, DOI: 10.1111/let.12143.

Ammonoids had high evolutionary rates and diversity throughout their entire history and played an important role in the high-resolution sub-division of the Mesozoic, but much of their palaeobiology remains unclear, including the brooding habitat. We present our study of the first recorded ammonite embryonic shell clusters preserved with calcified embryonic aptychi in situ within the body chambers of mature macroconch shells of the Early Aptian (Early Cretaceous) ammonite Sinzovia sazonovae. The following support the idea that the clusters are egg masses, which developed inside ammonite body chambers: the absence of post-embryonic shells and any other fossils in these clusters, the presence of the aptychi in all embryonic shell apertures and peculiarities of adult shells preservation. These facts confirm earlier speculations that at least some ammonoids could have been ovoviviparous and that, like many modern cephalopods, they could have reproduced in mass spawning events. The aptychi of ammonite embryonic shells are observed here for the first time, indicating that they were already formed and calcified before hatching. Our results are fully congruent with the peculiar modes of ammonoid evolution: quick recovery after extinctions, distinct evolutionary rates, pronounced sexual dimorphism and the nearly constant size of embryonic shells through ammonoid history. We assume that adaptation to ovoviviparity may be the reason for the presence of these features in all post-Middle Devo- nian ammonoids. □ Ammonites, Aptian, aptychi, brooding habitat, Early Cretaceous, evolution, ovoviviparity.

Aleksandr A. Mironenko [[email protected]], Kirovogradskakya st. 28, 117519 Moscow, Russia; Mikhail A. Rogov [[email protected]], Geological Institute of RAS, Pyzhevski lane 7, 119017 Moscow, Russia; manuscript received on 7/12/2014; manuscript accepted on 03/03/2015.

Ammonoids, which flourished during ca. 340 Ma et al. 1993, 2008, 2010; Kulicki & Doguzhaeva from the Early Devonian to the end of the Creta- 1994), but these shells are at different stages of devel- ceous, are one of the most significant groups of opment (including post-embryonic juveniles) and/ invertebrate fossils. They are very popular among or are mixed with other fossils, such as small amateur palaeontologists and extremely important bivalves, gastropods and fish scales and sometimes for high-resolution biostratigraphy, especially in the even plants remains (Landman 1985; Tanabe et al. Late Palaeozoic and Mesozoic. For more than two 1993, 2008, 2010). Therefore, these clusters are con- centuries of their research, ammonoids have been sidered to be post-mortem accumulations, not origi- very well studied. However, some aspects of their nal egg masses. biology remain elusive. One of these unresolved Assumptions about ammonoid egg-laying beha- issues is the question about ammonoid egg-laying viour are very speculative (De Baets et al. 2015). behaviour and reproductive strategy. To date, no Some researchers have assumed that ammonoids one has found undoubted ammonoid egg masses, could have laid their eggs on the sea bottom (Tanabe yet spherical egg-like objects with sizes correspond- et al. 1993), or could have formed gelatinous egg ing to ammonoid embryonic shells, and clusters of masses that could have been attached to the floating such objects, have been found repeatedly both material (e.g. Westermann 1996) or suspended it in within ammonoid body chambers and beside them the water column (Etches et al. 2009; Mapes & (Lehmann 1966; Wetzel 1969; Baranov 1985; Urlichs Nutzel€ 2009). Many researchers, however, have spec- 2006; Etches et al. 2009; Landman et al. 2010; Klug ulated that at least some ammonoids might have had et al. 2012). These are interpreted as either ammo- external brood care (Walton et al. 2010) or even noid eggs or eggs of unknown invertebrates; how- internal brooding (i.e. ovoviviparity; Ward & Bandel ever, no ammonoid embryonic shells have been 1987; Jacobs & Chamberlain 1996; Landman et al. observed within these objects. Clusters of ammonoid 1996, 2010; Lewy 1996, 2002; Westermann 1996; embryonic shells (widely known as ammonitellae) in Tsujita & Westermann 1998; De Baets et al. 2012, Palaeozoic and Mesozoic deposits have been found 2015). This assumption was based on an analogy several times (Wetzel 1959; Landman 1985; Tanabe with modern pelagic coleoids, finds of aforementioned

DOI 10.1111/let.12143 © 2015 Lethaia Foundation. Published by John Wiley & Sons Ltd 2 A. A. Mironenko & M. A. Rogov LETHAIA 10.1111/let.12143 egg-like structures in ammonoid body chambers and them are separated from the shells; therefore, it is on peculiarities of ammonoid adult morphology and difficult to determine whether or not they belong to dimorphism. However, all speculations about embryonic or post-embryonic ammonoids. ammonoid egg-laying behaviour have been based on In this study, we report, for the first time, three indirect evidence. Data from the brooding habits of embryonic shell clusters found inside the body modern cephalopods without additional facts have chambers of Lower Aptian ammonite Sinzovia not helped resolve this problem because among sazonovae Wright and discuss their palaeobiological these animals many different kinds of egg laying and implications in relation to ovoviviparity. Sinzovia egg sizes are known (e.g. von Boletzky 2003). sazonovae is also well known in palaeobiological lit- Bivalved calcitic aptychi (which are currently con- erature as ‘Aconeceras trautscholdi (Sinzov)’ (e.g. sidered as ammonite lower jaw elements) have not Kulicki et al. 1988; Kulicki & Doguzhaeva 1994; been reported to date in ammonoid embryonic Doguzhaeva 2002; Tanabe et al. 2008, 2010). shells. All previously found embryonic shell clusters do not contain aptychi (Tanabe et al. 1993; Kulicki & Doguzhaeva 1994). Aptychi have been found Material and Methods in situ in body chambers of small, but undoubtedly post-embryonic, ammonites (Kulicki & Wierzbowski The three embryonic shell clusters here described 1983; Kulicki et al. 1988). Only once have aptychi of were found by Anatoly Evzhenko (amateur palaeon- embryonic shells with diameters of 1 mm from the tologist) at the Volga river’s right bank, close to Shi- Lower Aptian of the Volga river shore been briefly rokiy Buerak settlement (Saratov region, Russia, 0 0 mentioned together with aptychi of larger ammo- 52°07 20″ N, 47°47 30″ E, Fig. 1), from Lower Creta- nites (Doguzhaeva 2002), but these were neither ceous (Lower Aptian, ca. 120 Ma) black shales. The illustrated or described. Clusters of small aptychi settlement of Shirokiy Buerak is located 120 km which are mixed with other fossil fragments were from Saratov and 240 km from Ulyanovsk (Simbirsk found in body chambers of adult ammonite shells until 1924). All previously studied Sinzovia embry- (Michael 1894; J€ager & Fraaye 1997; Keupp 2000; onic shells were found in the vicinity of Ulyanovsk, Ritterbush et al. 2014); however, these clusters are within the same palaeobasin (Kulicki et al. 1988; currently interpreted as food remains due to their Kulicki & Doguzhaeva 1994; Doguzhaeva 2002; Tan- position in the shells and other characteristics. Most abe et al. 2008, 2010). The Lower Aptian black shales of the aptychi in such clusters are crushed, and all of in the Saratov and Ulyanovsk areas deposited under

Fig. 1. Map showing Early Aptian palaeogeography of the Russian Sea (after Baraboshkin et al. 2003; Zakharov et al. 2013) and position of the locality where the studied clusters were found (marked by red star). LETHAIA 10.1111/let.12143 Ammonoid ovoviviparity 3 dysoxic to anoxic conditions in the central part of a boshkin. The ammonites greatly vary in size (from relatively shallow (~50 m deep or slightly more, 5–50 mm in diameter) and most likely represent dif- below the level of storm waves, see Baraboshkin ferent ontogenetic stages. In addition to the ammo- et al. 2003; Zakharov et al. 2013 for details) epicon- nites, the studied slab also contains fish scales and tinental sea. The clusters are located inside the body several small gastropod and bivalve shells. The shell chambers of adult Sinzovia sazonovae ammonite fragments have not moved relative to each other, shells, on a thin 16 9 10 cm bituminous shale slab that is there is no evidence these shells had any (Fig. 2). This slab is deposited in the Moscow State change of position. University Museum (MSU), collection No 117. The All three studied embryonic shell clusters found total thickness of ammonite-bearing shales is nearly are situated inside Sinzovia sazonovae (Aconecerati- 4.5–4.6 m. These shales are characterized by a very dae) body chambers. The diameter of these shells is thin horizontal lamination without traces of biotur- approximately 40–50 mm and is comparable with bation and overlying by remarkable lens-like platy the typical size of Sinzovia macroconchs (Glazunova limestones, so-called ‘Aptian plate’ (Gavrilov et al. 1973; Riccardi et al. 1987). All clusters consist of 2002). These shales contain numerous ammonites, ammonite embryonic shells with their aptychi providing its attribution to the Deshayesites volgensis (Fig. 3). The embryonic shells are formed of arago- ammonite zone, which corresponds to global anoxic nite, their aptychi of calcite. The size of individual event OAE-1a (‘Selly level’) (Gavrilov et al. 2002). embryonic shells varies slightly: most of them have a The studied slab contains several layers of flattened diameter of 0.9–1 mm, and this is comparable to ammonite shells, belonging to the species Sinzovia previously described diameters of Sinzovia embry- sazonovae Wright, Deshayesites volgensis Sasonova onic shells (Kulicki & Doguzhaeva 1994; Tanabe and Volgoceratoides schilovkensis Mikhailova & Bara- et al. 2008, 2010). Some of the embryonic shells have a slightly greater diameter up to 1.5 mm. All embryonic aptychi have lengths close to 0.5 mm. The outer A surface of all aptychi is covered by frequent longitu- dinal ribs, and the inner surface is smooth, without growth lines (Fig. 4). Organic parts of embryonic jaw apparatuses, that is chitinous elements of upper and lower jaws, are not preserved. None of the shells containing clusters is entirely visible: they are partially hidden in the clay beneath other shells and other embryonic clusters. So it is impossible to estab- lish the exact number of embryonic shells initially contained in any of the clusters. However, based on the space which is filled with clay and free of embryonic shells in all clusters (see Fig. 2), we can assume with great certainty that these shells did not occupy B most of the volume of any of the body chambers. Studied ammonitella clusters were examined with an optical microscope and under the scanning electronic microscope (SEM) TESCAN//VEGA with BSE detector in Paleontological institute of Russian Academy of Science (PIN RAS). The slab with clusters was inspected in an uncoated state, while the fragment of the shell containing cluster 3, with several embryonic shells, was coated by gold.

Description of the embryonic shell Fig. 2. A, general view of the three ammonite embryonic shell clusters clusters. A, general view of the embryonic shell clusters. B, cluster location. The black dots mark the complete embryonic shells, brown dots, incomplete shells and grey dots, phosphatized rings. The dotted lines show the missing part of the shell containing Cluster 1 cluster 1. The apertures of the shells containing clusters 2 and 3 and last septum of ammonite with cluster 1 are shown. Scale bar The specimen containing cluster 1 is a shell partially 1 cm. hidden under the clay and other shells, the central 4 A. A. Mironenko & M. A. Rogov LETHAIA 10.1111/let.12143

A B

C D

Fig. 3. Ammonite embryonic shells and their aptychi. A, general view of the cluster 1a. The arrow marks the distance between the venter of the host shell and a thin red-brown line, bordering the cluster. Scale bar 2.5 mm. B, C and D, ammonite embryonic shells in cluster 1a. Scale bars 0.5 mm. E and F, embryonic shells with an incomplete shell wall together with complete shells in cluster 2. Scale bars 0.5 mm. part of the body chamber of this ammonite is lack- Hence, either all embryonic shells originally were ing. So the cluster 1 is actually split into two parts: inside some kind of organic membrane or the red- 1a, in the fragment of the body chamber near the brown line marks a boundary between the cluster crushed last septum, and 1b, behind the aperture of and ammonite soft tissue. the host’s shell (Fig. 2). All embryonic shells in cluster 1 seem to be at the same type of preservation, all Cluster 2 of them have aptychi (Fig. 3). They are very tightly grouped in sub-cluster 1a, at the apical end of body The specimen containing cluster 2 is partially pre- chamber and sparse in sub-cluster 1b. Establishing served and located under the clay layers on top of the original position of the ammonitellae inside the the aperture of the shell with the cluster 1. Only the adult body chamber is not possible. However, in anterior third part of the body chamber of this sub-cluster 1a, embryonic shells are situated within a ammonite is available for research (Fig. 2). The clus- short distance (about 2–3 mm) from the venter ter 2 contains fully formed ammonitellae similar to (Fig. 3A), they are bordered by a ﬁne red-brown the samples from cluster 1 together with partially line. It is very likely that this line represents the rem- incomplete embryonic shells (Fig. 3E, F). These nants of some phosphatized organic structure. incomplete ammonitellae also had aptychi and LETHAIA 10.1111/let.12143 Ammonoid ovoviviparity 5

A B

C D

Fig. 4. Aptychi of embryonic shells. A, embryonic shells with aptychi. Scale bar 500 lm. B, aptychus of the embryonic shell. Scale bar 250 lm. C, outer side of the aptychus and aperture of the embryonic shell. Scale bar 100 lm. D, smooth inner side of the aptychus with a groove on the edge. Scale bar 100 lm. All specimens are from cluster 2. clearly visible apertures, however, away from the theclayandontheinnersurfaceofhostshells.The aperture, their shell walls gradually disappear with- clay within many of the rings is different in colour out a noticeable clear edge. They are mixed in this from the clay outside, likely because it is covered by a cluster with complete embryonic shells. thin mineral film. The size of these objects is somewhat In clusters 1 and 3, all embryonic shells are located less than the embryonic shell diameter: 0.7–0.8 mm. inside the body chambers of adult ammonites. In Several of these structures are not fully enclosed rings, cluster 2, however, several embryonic shells are they are cup shaped (Fig. 5C). The boundaries of these located on the host’s shell surface near the large objects are very similar to the fine line bounding the break. Nevertheless, there are no embryonic shells sub-cluster 1a, presumably both these structures are near the shell of adult ammonite in the clay matrix. remnant of fossilized organic tissue. There are no such brown ring-like structures outside cluster 3. Embry- Cluster 3 onic shells in the cluster 3, which mixed in the clay together with ring-like structures, have aptychi and are The Sinzovia shell containing cluster 3 partially lies not fully flattened, they are filled with sediment. under the ammonite with a cluster 1. Approximately only half of its body chamber (anterior part) with the aperture is visible (Fig. 2). Cluster 3 has fewer embry- Discussion onic shells than the others but is the most complex. There are unusual thin brown ring-like structures Taphonomy and preservation of host (Fig. 5), probably phosphatized, in this cluster, apart ammonites and embryonic shells from a small number of fully formed and incomplete embryonic shells. Unlike three-dimensional embryonic Large numbers of ammonite embryonic shells are shells, the ring-like objects are flat, imprinted both on well known from Lower Aptian bituminous shales 6 A. A. Mironenko & M. A. Rogov LETHAIA 10.1111/let.12143

A B

CDE

Fig. 5. Ring structures, presumably organic stage of embryonic shell. A, two brown ring structures together with an embryonic shell on the inner side of the shell wall of the host ammonite. B, two ring structures on the inner side of the shell wall of the host ammonite. C, unclosed ring structure (below) and a poorly preserved embryonic shell (above). D, E, ring structures on the clay surface in cluster 3. All specimens from cluster 3, scale bars 0.5 mm.

(Gavrilov et al. 2002) and calcareous concretions are et al. 2002) and the presence of shells of probably embedded in these shales (Kulicki & Doguzhaeva immature ammonites (with 5–15 mm in diameter) 1994; Tanabe et al. 2008, 2010). Sometimes, the in this shell cluster. Such periodical events of oxygen shale layers are literally covered with ammonite deficiency and high concentrations of hydrogen sul- embryonic shells (Gavrilov et al. 2002). However, in phide in the water column were previously discussed such agglomerations, embryonic shells are located (Doguzhaeva 2002; Gavrilov et al. 2002), these outside of large ammonites, mixed with other fossils events are confirmed by geological data (Gavrilov (fish scales, gastropods etc.) and have no aptychi. All et al. 2002) and by findings of numerous clusters of three clusters described herein are located inside the embryonic, post-embryonic and juvenile ammonite body chambers of adult Sinzovia sazonovae shells shells (Kulicki & Doguzhaeva 1994; Doguzhaeva (each cluster in its own body chamber). The embry- 2002; Tanabe et al. 2008, 2010) in the Deshayesites onic shells do not occur separately or in the shells of volgensis Zone of the Saratov and Ulyanovsk regions. the other ammonite species in this slab (Deshayesites Moreover, many shells of Sinzovia found in these and Volgoceratoides found close to Sinzovia speci- layers show developmental abnormalities of the shell mens, contain no embryonic shells). All visible walls and septa, probably caused by oxygen defi- embryonic shells have aptychi (fully preserved or ciency (Doguzhaeva 2002). crushed) on top of their apertures. We have not Preservation of ammonites in the Lower Aptian found separate aptychi or embryonic shells without bituminous shales is worse than the preservation in them. Larger ammonites or other fossils, such as gas- concretions embedded in these shales: the ammonite tropods or fish scales, are absent from these clusters, shells in the clay are flattened and broken with numer- but present in the surrounding clay. The embryonic ous cracks. Judging by their bright pearlescent colour shell-bearing ammonite cluster is preserved in black (Fig. 2A), their external prismatic layer was dissolved, shale layers, formed in an anoxic environment and but the nacreous layer is preserved. Embryonic shells lack any traces of bioturbation (Gavrilov et al. are also partly flattened and partially submerged in the 2002). Very likely, all ammonites that are preserved sediment. Their shell wall consists of an outer homoge- on the studied slab, including Sinzovia macroconchs, neous layer and in several specimens of an inner reticu- could have died due to one catastrophic event, prob- lar layer (Fig. 6). The reticular ‘grid’ structures in ably caused by oxygen deficiency in the water col- Sinzovia embryonic shells were depicted by Kulicki & umn, as evidenced by the lack of traces of Doguzhaeva (1994, figs 11D, 12A, B). In some embry- bioturbation, anoxic bottom condition (Gavrilov onic shells studied herein, the inner reticular layer is LETHAIA 10.1111/let.12143 Ammonoid ovoviviparity 7 visible on the surface, usually closer to the apical part niles; passive accumulation of embryonic shells in of the shell (Fig. 6). The outer prismatic layer is lacking the empty body chambers of large ammonites due to in all embryonic shells, as well as tubercles, which usu- ocean currents; oviposition of ammonoid eggs into ally are located on the surface of this layer (Kulicki & empty shells located on the sea bottom; egg laying Doguzhaeva 1994; Tanabe et al. 2008, 2010). It is diffi- into floating, empty ammonite shells suspended in cult to determine with certainty whether the absence of the water column and eggs developed inside the the outer prismatic layer is due to the fact that the body chamber of the female ammonite. shells are at an early stage of development when this layer has not yet appeared (see Tanabe et al. 2010: fig. Hypothesis 1. – Embryonic shells inside adult body 10), or if this layer was dissolved during diagenesis. chambers are stomach content – they were eaten by adult ammonites nearly after their hatching. Canni- Origin of embryonic shell clusters balism is a common feeding strategy for many modern coleoids (Nesis 1985). It is very likely that We considered several hypotheses of the origin of ammonites could have preyed on their hatchlings: studied embryonic shell clusters: stomach content – fragments of small ammonite shells and aptychi the result of predation of adult ammonoids on juve- repeatedly had been described in body chambers of

Fig. 6. Reticulate structure of the inner layer of the shell wall of embryonic shells. A, inner side of two embryonic shells located on the fragment of the host shell. Cluster 2, scale bar 300 lm. B and C, reticulate layer in the same specimens, scale bar 50 lm. D, embryonic shell with aptychus and reticulate layer, visible on the surface of the shell wall. Cluster 2, Scale bar 500 lm. E, reticulate layer in the same specimen, scale bar 100 lm. 8 A. A. Mironenko & M. A. Rogov LETHAIA 10.1111/let.12143 adult ammonites and are currently interpreted as on the slab (Deshayesites, Volgoceratoides and small food remains (Michael 1894; Barthel & Janicke 1970; presumably immature Sinzovia) are empty. All these Lehmann & Weitschat 1973; J€ager & Fraaye 1997; facts allow us to reject the hypothesis of transporta- Keupp 2000; Ritterbush et al. 2014). However, all tion of embryonic shells into Sinzovia body cham- known examples of stomach content are markedly bers by water currents. different from clusters which are described herein. Remains of the ammonite food include fragments of Hypothesis 3. – Ammonites laid their eggs into shells and aptychi (Lehmann & Weitschat 1973; empty Sinzovia shells on the sea bottom. Many mod- J€ager & Fraaye 1997; Keupp 2000; Ritterbush et al. ern cephalopods lay their eggs on the bottom. It was 2014), even if the shell or aptychi remain intact, they assumed that ammonoids could have had a similar are separated from each other (Michael 1894; J€ager oviposition strategy (Tanabe et al. 1993). However, & Fraaye 1997). Most of the embryonic shells in our most ammonoids likely were meso- or epipelagic clusters are intact, their fragments are not displaced (Westermann 1996; Tsujita & Westermann 1998) even if they are crushed, aptychi are always located and could have had no contacts with the sea bottom. at the embryonic shell apertures. Cephalopods are Bituminous shales, in which embryonic shell clusters unable to swallow large pieces of food, because their were found, were formed in an anoxic environment oesophagus passes through of the brain (Nesis 1985, (Gavrilov et al. 2002), and there are no traces of bio- 1995). So they break down their food using the turbation in these layers. Although, in some cases, radula, ammonites could have used the same strat- the bottom anoxic conditions can be inconstant and egy (Kruta et al. 2011). It seems highly unlikely that interrupted by periods of increased concentration of ammonites could have swallowed juvenile shells oxygen (Klompmaker & Fraaije 2012), in this case, entirely without the radula and jaws crushing or such a situation is unlikely. On the slab studied damaging them. Furthermore, the amount of herein as well as on other specimens from the same embryonic shells in clusters 1 and 2 is considerably beds examined by the authors, there are no traces of larger than the size of all known examples of stom- bioturbation, benthic fauna such as large or med- ach content. Therefore, the large size of clusters and ium-sized bivalves and gastropods, crustaceans or preservation of undamaged embryonic shells with epicoles (Davis et al. 1999) on the ammonite shells. their aptychi allow us to reject this hypothesis. Several gastropod shells found on the slab with ammonites are very small (<2 mm) and could have Hypothesis 2. – Embryonic shells with their aptychi been pelagic or lived on floating objects in the water were carried into the empty body chambers of dead column. Empty Deshayesites and Volgoceratoides ammonites by water currents. Maeda (1991) shells found close to Sinzovia specimens, contain no described so-called ‘sheltered preservation’, in which embryonic shell. If ammonites had laid eggs into the ocean currents carry ammonite and other mollusc empty shells, they would not have needed to choose shells of different ages and sizes into the empty body some single type of shell to hide their eggs. The posi- chambers of large ammonites, where they are stored. tion of the ammonite containing cluster 1 is also However, it is important to note that in the case of important: its aperture is blocked by other shells, ‘sheltered preservation’ in one body chamber accu- including the shell with cluster 2 (Fig. 2), oviposi- mulated fossils differ by size and taxonomy: shells tion into this shell seems to be difficult if not impos- and shell fragments of ammonites, bivalves and gas- sible. Therefore, due to all these facts, especially to tropods, pieces of wood and fish scales are mixed in an anoxic bottom environment, the bottom spawn- such body chambers. The clusters described herein ing was impossible thus making this hypothesis consist only of embryonic shells. Larger ammonites invalid. or other fossils are absent in these clusters, but present in the surrounding clay. Furthermore, all visible Hypothesis 4. – Oviposition into floating, empty embryonic shells have aptychi on top of their aper- shells suspended in the water column. After the tures. Undoubtedly, if these shells were on the sea death of ammonites, their shells could have bottom for some time before being carried by water remained for some time in the water column due to currents into the body chambers of large ammonites, phragmocone buoyancy. One can imagine that other part of the aptychi must have been lost due to ammonites could have laid their eggs in these empty decomposition of the soft body. Initially, organic shells. This hypothesis, regarding the studied embry- ring-shaped structures from cluster 3 also confirm onic shell clusters, is indirectly confirmed by the in situ preservation of content of these clusters. absence of findings of aptychi of adult host ammo- Moreover, apertures of all host ammonites oriented nites. However, it is difficult to imagine at what in different directions and shells of other ammonites point ammonites could have laid their eggs into LETHAIA 10.1111/let.12143 Ammonoid ovoviviparity 9 empty shells in the water column. During the The lack of finds of host ammonite aptychi while decomposition process in the ammonite body cham- embryonic aptychi are preserved may contradict this bers, there were undoubtedly low levels of oxygena- hypothesis, but does not disprove it. First of all the tion, a large number of bacteria and high levels of aptychi of adult ammonites may be preserved, but metabolic products secreted by these bacteria. Mod- hidden in the clay in the body chambers or in front ern coleoids always provide sufficient aeration of egg of them. It is also possible that if the dead ammo- mass and clean bacteria from them to promote nites had not immediately sunk, their aptychi, which hatching of their eggs (Nesis 1985; Seibel et al. were located at the front end of the body, could have 2005). So female octopods wash their egg clusters separated during body decomposition and sunk ear- with a jet of water from the hyponome (Nesis 1985) lier than the whole shell, whereas embryonic shells and squids Gonatus onyx flush water through the egg which were in the oviducts or special organ in the mass with periodical arm movement (Seibel et al. rear part of the body chamber could have remained. 2005). This variant seems possible due to the short length It is unlikely that ammonoid eggs could have been of Sinzovia body chambers (~180°) – in brevidomic so strongly different from other cephalopods eggs in shells, the aptychi must have been located not far that they could have developed not just in oxygen from the apertural edge. Another important point is deficiency, but also in the presence of bacterial tox- the structure of the Sinzovia aptychi. Doguzhaeva & ins in the decomposing soft tissues of other ammo- Mutvei (1990, 1993) described Sinzovia aptychi nites. After the decomposition of the soft body, the mainly consisting of organic material with thick cal- ammonite shells, especially the relatively small ones, cified front ends (‘calcitic beaks’). Later, it leads to sank very quickly (Wani et al. 2005). The sinking of erroneous classification of Sinzovia jaws as rhyn- shells certainly must have led to the death of eggs chaptychi (e.g. Engeser & Keupp 2002). Our obser- attached inside them, especially in the regions with vation does not confirm these data: the aptychi of anoxic bottom conditions. Therefore, such floating Sinzovia are attributed to lamellaptychi (Rogov & shells could not have been a reliable shelter for Mironenko 2014), however, we agree that their outer ammonoid eggs. Moreover, the three shells with calcitic layer is very thin. Likely, this layer of the embryonic clusters studied herein have no signs of aptychus is mostly thinner than its anterior (embry- long-time floating, such as epicoles or bioerosion. onic) part. It cannot be completely excluded that Thus, this hypothesis also seems to be highly unli- this thin calcitic layer has been dissolved before or kely. after burial, as it probably happened with the previously studied specimens of Sinzovia aptychi. In such Hypothesis 5. – Egg development inside the body case, the aptychi of embryonic shells in the clusters chamber of the female ammonite – that is ovo- could have remained preserved not only due to their viviparity. As oviposition of the eggs into the empty thickness, but also due to protection by a host shell ammonite shells is considered to be unlikely, as well or by remnants of the ammonite soft tissue. as other earlier mentioned hypotheses, only one ver- A small difference in size of embryonic shells does sion remains: embryonic shells were located inside not contradict ovoviviparity as it can be result of the body chambers of Sinzovia macroconchs when post-mortem deformations or various shell positions these ammonites died and sank to the bottom. in the clay: some shells can be more highly deformed Although Lewy (1996, 2002) speculated that than the others, immersed slightly deeper in clay or ammonite shells could have been used by female rotated at various angles. Moreover, asynchronous ammonites as egg cases like the shell of the modern development rates and variation in the size of hatch- octopus Argonauta, this comparison seems incorrect lings were documented in bottom attached egg (see Hewitt & Westermann 2003). Female Argonauta strands of Sepioteuthis (Robin et al. 2014). live in their shells, but they are not attached to the shell walls, whereas the ammonite soft body was Possibility of the ammonoid ovoviviparity attached to the shell by retractor muscles and siphuncle tissues in the rear part of the body cham- Although ammonoid habitat remains a subject of ber and by a mantle edge in the apertural region debate, most published data on the oxygen isotope (Doguzhaeva & Mutvei 1996). Therefore, if embry- composition of ammonoid shells show significantly onic shells had been located inside body chambers of higher palaeotemperatures compared to associated living ammonites, these ammonites must have been benthonic fossils or of belemnites (Anderson et al. ovoviviparous, like modern pelagic octopuses 1994; Wierzbowski et al. 2013; Zakharov et al. Vitreledonella and Ocythoe (Nesis 1985, 1995; Bello 2013). High palaeotemperatures indicate that 2012). ammonoids could have lived in a pelagic zone, 10 A. A. Mironenko & M. A. Rogov LETHAIA 10.1111/let.12143 mostly epipelagic. It should be noted that very high to be most similar to ammonoids in regard to habi- palaeotemperatures have been obtained from Aptian tat and dimorphism. It should be noted, however, ammonites from the Ulianovsk region (Central Rus- that ammonoids were mainly neritic, while modern sia), including Sinzovia sazonovae (Zakharov et al. coleoids characterized by strong sexual dimorphism 2013). Even if oxygen isotopic compositions suggest belong to oceanic species. mesopelagic (Lukeneder et al. 2010) or demersal From the three brooding types of modern pelagic habitats of several ammonoids (Moriya et al. 2003), octopuses (egg case shell, external brooding and hatchlings of such taxa are still epipelagic. Many ovoviviparity), the last seems to be the most possible ammonoids, including Sinzovia, lived in the water for ammonoids. The ammonoid soft body was column above the permanently or periodically attached to the body chamber walls by muscle anoxic bottom water layers. Embryonic and post- retractors and siphuncle tissues; therefore, the hatchling shells have been found in anoxic deposits ammonoid shell could not have been used as an egg (Westermann 1996; Mapes & Nutzel€ 2009), but they case, like the shell of Argonauta (Hewitt & Wester- could not have been carried a long distance by cur- mann 2003). The external brooding, similar to the rents nor could they have grown under reduced oxy- strategy of Tremoctopus or Gonatus, proposed by gen conditions. several researchers for ammonoids (Walton et al. If ammonoids had mainly been epi- or mesopela- 2010), seems to be unlikely due to large numbers of gic and had had no relation with the bottom, it can eggs, attached to the arms which could have inter- be assumed that they could have realized spawning fered with withdrawing the anterior part of the soft strategies which might have been similar to the strat- body into the shell. It could have reduced the protec- egy of modern pelagic cephalopods also living in a tive function of the shell completely and also could similar environment, in upper water layers without have made eggs and females vulnerable to predators. any contact with the bottom. Some Jurassic and Cre- From existing strategies among modern pelagic taceous ammonoids (especially Ammonitida) show cephalopods, only ovoviviparity seems to be avail- extreme dimorphism. In several taxa, macroconchs able for ammonoids and it could have allowed them (putative female) can be 10–15 times greater in to protect their eggs without reducing protection of diameter than micro-conchs (putative males) the female. (Makowski 1962), whereas in other taxa, this ratio Among the members of the family Aconeceratidae can be smaller and attains only 1.5–2 times. Among to which Sinzovia belongs, the difference in size of modern cephalopods, the same type of dimorphism sexual dimorphs is not great – females are usually has been observed in three epipelagic octopod gen- only twice as large as males. However, this ‘reduced’ era which belong to superfamily Argonautoidea (Ne- dimorphism most likely did not indicate any differ- sis 1985, 1995; Laptikhovsky & Salman 2003; Bello ence in their reproduction from other dimorphic 2012). Very likely, it is not a coincidence, but evi- ammonoid taxa. Among modern epipelagic Arg- dence of ecological similarity, and possibly of similar onauta, different species demonstrate a different size breeding strategies (Ritterbush et al. 2014). Epipela- ratio between sexual dimorphs. For example, the gic members of Argonautoidea do not form free- females of Argonauta argo are almost 10 times larger floating egg masses – they brood their eggs in several than the males (Nesis 1995), while the size of Arg- ways. Argonauta females use a special egg case shell onauta hians dimorphs is differ in 2–3 times only (not homologous to other cephalopod shells), and (Sukhsangchan & Nabhitabhat 2007). However, Tremoctopus females attach eggs to their arms (Nesis their spawning strategies are identical. All members 1995; Bello 2012). A similar brood care strategy is of family Aconeceratidae are relatively small ammo- carried out by females from mesopelagic species of nites and 50 mm is a normal size for adult macro- Bolitanidae and Amphitretidae octopod families – conchs of this family (Glazunova 1973; Riccardi they bear eggs in the arms (Arkhipkin 1992), and by et al. 1987). Most likely the small size of aconecer- pelagic squids Gonatus which carry the large spheri- atids (and hence the small size of their macroconchs) cal egg sac in their arms (Seibel et al. 2000, 2005), could have depended on environmental factors (e.g. passively drifting with it in the water column. Two warm climate, the pressure of predators) rather than genera of pelagic octopuses – epipelagic Ocythoe and the type of their reproduction. mesopelagic Vitreledonella – are ovoviviparous (Ne- The discovery of embryonic shells at early sis 1985, 1995; Arkhipkin 1992; Bello 2012), that is stages of development outside the macroconch their eggs develop inside the body of adult females. shells (Kulicki & Doguzhaeva 1994; Tanabe et al. Therefore, the brooding eggs strategies and ovo- 2008, 2010) does not contradict the ovoviviparity viviparity not only exists among modern cephalo- hypothesis. Such isolated embryonic shells could pods, but also present in those lineages, which seems have resulted from the decomposition of dead LETHAIA 10.1111/let.12143 Ammonoid ovoviviparity 11 female ammonite bodies in the water column. The eggs and hatchlings of modern cephalopods The female ammonites may also have aborted vary greatly in size (von Boletzky 2003). A noticeable undeveloped embryos in dangerous maleficent difference in egg size is observed not only among environments. closely related species (Nesis 1985) of coleoids, but We can assume that depletion of oxygen in the also among different populations of the same species water could have caused the brooding Sinzovia (Laptikhovsky et al. 2009). In contrast to other females and their offspring to die, potentially during cephalopod groups, ammonoids had a nearly con- a Sinzovia mass brooding season. Possible mass stant egg size throughout the most part of their his- ammonoid spawning events were discussed recently tory (Landman et al. 1996; Laptikhovsky et al. (Stephen & Stanton 2002; Walton et al. 2010). Our 2013). The sub-spherical shape of the embryonic discovery of embryonic clusters inside three Sinzovia shell consisting of the one whorl is invariable, shells which are nearly identical in size may serve as regardless of adult shell shape (Drushchits et al. confirmation of the occurrence of mass brooding 1977). Only the earliest Early and Middle Devonian seasons among these ammonites. ammonoids had markedly large (ca. 1.5–2.6 mm in Based on studied clusters, it is difficult to say diameter) embryonic shells (House 1996; De Baets where exactly the eggs were located in the female et al. 2012, 2013, 2015) ornamented with transverse ammonite soft body. In ovoviviparous octopus lirae (Landman et al. 1996; Klofak et al. 2007). At Ocythoe, the developing eggs are located in the ovi- the same time, clear trends of a decrease in size in duct (Laptikhovsky & Salman 2003) perhaps the embryonic shells and eggs were quantitatively eggs had been in the same location in female ammo- demonstrated from the Early Devonian towards the nites. However, other variants are possible (in the Late Devonian (De Baets et al. 2012). Small, tightly mantle cavity, in a special soft-tissue egg case, etc.) coiled and smooth embryonic shells arose in the Late and the available data are insufficient to resolve this Devonian and remained until the ammonoid extinc- issue. tion in the Late Cretaceous. This constancy of the size of ammonoid hatchlings (consequently and When did ammonoid ovoviviparity appear? their eggs) in comparison with other cephalopods can be explained by the ovoviviparity: inside the Ovoviviparity is a very specific brooding habitat, body, the eggs have developed in nearly constant which appeared to exist independently within at conditions. least 160 animal clades (Blackburn 1999). Among Many ammonoids are also characterized by a molluscs, ovoviviparity occurred in some bivalves remarkable dimorphism in size of adult shells, which and gastropods (especially in freshwater and terres- is usually considered as sexual (Makowski 1962; Cal- trial taxa), but it is uncommon (known only in lomon 1963). The earliest cases of noticeable dimor- two genera) in cephalopods (Nesis 1995). As living phism arose at the same time as small-sized ovoviviparous cephalopod genera, Ocythoe and embryonic shells in the Late Devonian (Makowski Vitreledonella, belong to different families and their 1962; Davis et al. 1996; De Baets et al. 2012; Korn & closest relatives are not ovoviviparous, it is very Klug 2012). likely that this type of reproduction originated As extant cephalopods (e.g. Argonautoidea) are independently in these taxa. If Sinzovia was ovo- known for their brood care show a pronounced viviparous, does this mean that other ammonoids dimorphism and a small egg size, the Late Devonian shared this reproductive strategy? Was ovovivipar- ‘hot spot’ in ammonoid evolution when the same ity common among ammonoids? When did it features appeared in ammonoids might have indi- arise? cated the appearance of brood care (and probably of Sinzovia, like other members of Aconeceratidae, ovoviviparity) in the Late Devonian. Upon consider- have no fundamental differences and peculiarities in ing the presumable pelagic mode of life of most adult or embryonic shells to distinguish them from ammonoids (Westermann 1996; Ritterbush et al. other Mesozoic ammonites. This is dimorphic 2014), ovoviviparity could have been a key adapta- genus, and its embryonic shells, like in all post- tion providing protection for eggs from pelagic Devonian ammonoids, are small sized (near 1 mm predators and could have started the evolutionary in diameter) and have a sub-spherical shape (Kulicki success of ammonoids. If the small arc-shaped struc- & Doguzhaeva 1994; Tanabe et al. 2008). It seems tures in the body chamber of a Lower Carboniferous unlikely that Sinzovia was the only ovoviviparous ammonoid (Landman et al. 2010), which are similar ammonite genus because the appearance of ovo- to circular objects in cluster 3 in the Sinzovia shell, viviparity could have likely reflected on the adult or are really embryonic shells at the earliest stage of embryonic ammonite shells. development, this finding could be a confirmation 12 A. A. Mironenko & M. A. Rogov LETHAIA 10.1111/let.12143 of the occurrence of ovoviviparity in the Late Devo- Ammonitida have an ammonitella diameter of nian. approximately 1 mm (Landman et al. 1996). This However, other speculations about the first aptychi cluster recently was re-interpreted as stom- appearance of ovoviviparity among ammonoids are ach content from cannibalism (Keupp 2000), and possible. A significant reduction of the size of the the interpretation seems to be correct when the size embryonic shell during the Devonian is probably of these aptychi is taken into account. not linked directly to ovoviviparity, but with other At the base of the aptychi of adult Sinzovia, a types of brood care (e.g. external brooding, similar small calcified area with a similar smooth inner and to those of Tremoctopus or Gonatus). Ovoviviparity ribbed outer surface was previously described based on such ‘pre-adaptations’ could have appeared (Kulicki et al. 1988; Doguzhaeva & Mutvei 1993). later, when predator pressure increased, for example, This area was named as ‘calcitic conchorhynch’ near the Permian–Triassic transition, when the (Kulicki et al. 1988). However, Sinzovia, as well as tuberculate micro-ornament had appeared on the all Aconeceratidae, belongs to aptychophoran ammonitella surface (Landman et al. 1996), or in ammonites (Thomson 1972: fig. 3; Riccardi et al. the Early Jurassic, in the earliest Aptychophora 1987: pl.11, fig. 13), whereas the true conchorhynchs (Engeser & Keupp 2002) characterized by appear- occur on rhynchaptychus-type lower jaws of phyllo- ance of bivalve aptychi, one of which functions ceratids and lytoceratids (Tanabe et al. 2011). Our could have been to protect the soft body from preda- observations also suggest that Sinzovia aptychi tors (Lehmann & Kulicki 1990; Parent et al. 2014), belong to Lamellaptychi (Rogov & Mironenko and strong dimorphism (Makowski 1962). The cur- 2014). It could be assumed that this «con- rently available data do not allow for a choice chorhynch» is only an embryonic aptychus, which is between these speculated variants. Although the probably denser and better preserved in fossil state authors believe that ovoviviparity is likely to have than the remaining part of the outer aptychus layer. appeared in the Late Devonian, future findings are Interpretations of aptychi functions are very needed to verify this assumption. diverse (Parent et al. 2014). However, two functions are widely considered: aptychi were a part of the Aptychi of embryonic shells lower jaws and they could have been used as opercula for protecting the ammonoid body chamber The aptychi of ammonite embryonic shells were (Lehmann & Kulicki 1990; Parent et al. 2014). The observed here for the first time, all previously stud- study of our findings confirms these and some other ied embryonic shell clusters contain no aptychi functions of aptychi. (Landman 1985; Tanabe et al. 1993, 2008; Kulicki & In all investigated clusters, all aptychi are located Doguzhaeva 1994). Aptychi of Sinzovia embryonic at the apertures of embryonic shells, outside of the shells are formed of calcite (in contrast with arago- embryonic shell body chambers (Figs 3, 4). This fact nite embryonic shell walls) and have a ribbed outer indicates that these aptychi, at least in the early and smooth inner surface (Fig. 4). Many aptychi stages of ammonite ontogeny, could have been used remained intact, many broke into small pieces due as opercula. Moreover, most aptychi have the same to pressure of the overlying clay layers (for example orientation: their wide edge closely fits the base of Fig. 3B–D), but their fragments are not displaced the primary constriction (see Landman et al. 1996 and are preserved in the apertures. They have a for terminology). There is a thin groove on the edge slightly elongated shape but their length is not much of the aptychus (Fig. 4C), which corresponds to a larger than the width. ledge on the bend of the apertural constriction of the Previously, the clusters of small aptychi were embryonic shell (Fig. 4D). If the edges of the aptychi observed from body chambers of adult ammonoids had been at the base of the constriction, embryonic (Michael 1894; J€ager & Fraaye 1997; Keupp 2000; shells with aptychi would have had a spherical shape. Ritterbush et al. 2014). However, in most of these This gives a basis for the assumption that the pri- clusters aptychi are crushed and mixed with other mary constriction is not only associated with the fossil fragments (Michael 1894; J€ager & Fraaye 1997; mechanism of shell growth, but also provided sup- Keupp 2000; Ritterbush et al. 2014). Therefore, these port for the aptychi that cover the delicate apertural clusters are currently interpreted as food remains edge (probably, it was important during the hatch- (Keupp 2000; Ritterbush et al. 2014). One of such ing of young ammonites). clusters was initially described as remnants of As was previously shown, the ratio of aptychi ammonoid embryos (Michael 1894); however, these length to embryonic shell diameter and length of its aptychi have a length of about 2–2.5 mm which body chamber corresponds to the ratios described excludes their relationship to embryonic shells as all for jaws of late embryos and hatchlings of recent LETHAIA 10.1111/let.12143 Ammonoid ovoviviparity 13

Coleoidea (Morton & Nixon 1987). The average embryonic shells may have two possible explanations: diameter of the studied embryonic shells in all three either it is an incomplete preservation or these clusters is 0.9–1 mm. The body chamber length of embryonic shells are at an early stage of develop- Sinzovia embryonic shells varies from 275 to 360°, ment. The exterior of adult shells evidence in 320° on average (Drushchits & Doguzhaeva 1981). favour of the first version (incomplete preserva- The length of the embryonic aptychi in all three clus- tion): the shells look bright pearlescent (Fig. 2A), ters is 0.5 mm or about 50% of the shell diameter. apparently, their outer prismatic layer was dis- The angular length of aptychi is about 90 degrees, solved during diagenesis. However, aptychi of which corresponds to approximately 30% of the embryonic shells do not bear any traces of dissolu- angular length of the young ammonite body cham- tion, and the shells with incomplete walls are ber. Similar ratios of jaws and body length exist in located near to complete ones (Fig. 3E, F) – it modern squid Alloteuthis subulata hatchlings (Mor- seems unlikely that the shells could have dissolved ton & Nixon 1987). This is one more confirmation so selectively. Moreover, all embryonic shells in to the widely accepted hypothesis that aptychi could studied clusters have no primary varix. The lack of have functioned not only as the opercula, but also as the primary varix in all specimens is difficult to a part of the ammonite jaw apparatus (Lehmann & explain by dissolution because the primary varix is Kulicki 1990; Parent et al. 2014). the thickest part of the embryonic shell; most Apart from their functions as jaws and opercu- likely, it had not yet been formed. If the shell wall lum, some aptychi may have provided additional of embryonic shells initially had no prismatic outer functions (Parent et al. 2014). The thick and heavy layer, we can assume that they all belong to stage aptychi could have influenced the animal’s orienta- 1, according to the aforementioned classification tion in the water (Gasiorowski 1960; Schweigert (specimens with an incomplete shell wall are at the 2009; Parent et al. 2014). Our findings could sup- beginning of stage 1). If the embryonic shell wall port this hypothesis, at least for the early ontogenetic had partially dissolved during diagenesis, it is pos- stages when the aptychi were relatively large. The sible that these embryos had been at a later stage aptychi of Sinzovia embryos are 0.5 mm in length of development, however, likely at the stage 2 (embryonic shell diameter is about 1 mm), and they rather than 3, due to the lacking of the primary are formed from the dense calcite. Although addi- varix. tional calculations are required, undoubtedly, the The brown-bordered presumably phosphatized weight of such relatively large calcitic plates influ- rings (Fig. 5) could be remnants of soft organic enced the orientation of ammonite hatchlings dur- structures. It is likely that their thin border arose ing the early stages of their life. during bacterial phosphatization of flattened (initially three dimensional) organic objects. Probably, – Stages of embryonic shell development it was embryonic shells of stage 0 previously considered as hypothetical. Several of these structures The stages of ammonite embryonic shell growth have a cup-shaped form (Fig. 5C), and similar small have been studied in many ammonite taxa, includ- arc-shaped structures have been described from the ing Sinzovia from concretions of the Volga river- body chamber of a Lower Carboniferous ammonoid banks near the Ulyanovsk (Kulicki & Doguzhaeva (Landman et al. 2010). It also possibly that rings are 1994; Tanabe et al. 2008, 2010). Four stages of imprints of egg membranes because the chorion of embryonic shell development have been described cephalopods is relatively dense, and the size of the (Kulicki & Doguzhaeva 1994; Tanabe et al. 2008, eggs may be less than the size of hatchlings due to 2010). Stage 0 would be the organic shell which, the expansion of the chorion during embryo devel- however, has never been observed; stage 1 was opment (Robin et al. 2014). defined by the deposition of amorphous calcium The presence within a single egg mass of embryos carbonate, followed by the adoral deposition of an at different developmental stages is common in inner prismatic layer; stage 2 was characterized by cephalopods: it was described in modern epipelagic the secretion of an outer prismatic layer associated octopuses Argonauta (Laptikhovsky & Salman 2003) with tubercles; and stage 3 was defined by the and ovoviviparous Ocythoe (Salman & Akalin 2012). completion of a fully mineralized embryonic shell. Even in bottom attached egg strands of Sepioteuthis Embryonic shells in the clusters in Sinzovia body asynchronous development rates were documented chambers have no signs of the outer prismatic (Robin et al. 2014). layer or tubercles. Moreover, several embryonic In all three clusters, the aptychi of all embryonic shells in clusters 2 and 3 have incomplete shell shells are fully developed. Only the brown ring struc- walls (Fig. 3E, F). These peculiarities of the studied tures have no aptychi. This indicates that the aptychi 14 A. A. Mironenko & M. A. Rogov LETHAIA 10.1111/let.12143 had formed and calcified before hatching, which through help by Roman Rakitov (PIN RAS, Moscow, Russia). This study was partly supported by Program by Presidium of coincides with the data regarding the formation of RAS no. 28 and grant of the RFBR № 15-05-06183. the jaws in modern cephalopods (von Boletzky 2003). Due to the type of shell preservation, it is difficult to say at what stage of embryonic shell formation the aptychi appeared. If studied embryonic References shells are actually at stage 1, the aptychi could have Anderson, T.F., Popp, B.N., Williams, A.G., Ho, L.-Z. & Hudson, J.D. 1994: The stable isotopic records of fossils from the Peter- been the first mineralized part of the embryos. How- borough Member, Oxford Clay Formation (Jurassic), UK: ever, for verification of this assumption, better pre- palaeoenvironmental implications. Journal of the Geological served embryonic shells with aptychi are needed, Society 151, 125–138. Arkhipkin, A.I. 1992: Reproductive system structure develop- which in turn will allow for unequivocal identifica- ment and function in cephalopods with a new general scale for tion of stage of formation. maturity stages. Journal Of Northwest Atlantic Fishery Science 12,63–74. Baraboshkin, E., Alekseev, A.S. & Kopaevich, L.F. 2003: Cretaceous paleogeography of the North-Eastern Peri-Tethys. Palaeogeogra- Conclusions phy, Palaeoclimatology, Palaeoecology 196,177–208. 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Taking into account the size 2013: Emsian Ammonoidea and the age of the Hunsruck€ Slate and position of embryonic aptychi, they must (Rhenish Mountains, Western Germany). Palaeontographica A have been used as operculum in the early stages 299,1–113. De Baets, K., Landman, N.H. & Tanabe, K. 2015: Ammonoid of the ammonite ontogeny. embryonic development. In Klug, C., Korn, D., De Baets, K., Kruta, I., Mapes, R.H. (eds): Ammonoid Paleobiology: From Acknowledgements. – We are sincerely grateful to Anatoly Evz- Anatomy to Ecology, 113–213. Springer, Dordrecht. henko (Balakovo, Saratov region) for donation the unique speci- Doguzhaeva, L.A. 2002: Pre-mortem septal crowding and patho- men, containing ammonitellae clusters. J. K.Wright (University logical shell wall ultrastructure of ammonite younglings from of London, UK) is acknowledged for reading first draft of this the lower Aptian of Central Volga (Russia). In Wagreich, M. manuscript. 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