Introduction

Direct evidence of predation activity is rarely observed in the fossil record (e.g. preservation of gut contents; Kear 2006; Kriwet et al. 2008) and is especially important in order to establish ancient predator−prey relationships. Most of previous reports of vertebrate predation on ammonoids consist of bite marks present on shells from various geological periods (e.g. Middle Jurassic of France; Martire and Torta 2000). Numerous case studies have shown that such marks were caused by Carboniferous ctenacanthiform sharks (Mapes and Hansen 1984; Hansen and Mapes 1990; Mapes et al. 1995; Mapes and Chaffin 2003), Jurassic semionotid fishes (Martill 1990), or Cretaceous mosasaurid reptiles (Kauffman and Kesling 1960; Hewitt and Westermann 1990; Kauffman 1990, 2004). However, teeth lost by the predator while catching prey and sunk into the shell represent a peculiar taphonomic condition that has never been observed so far. Such a direct evidence for a trophic relationship between the aspidoceratid ammonite Orthaspidoceras and the hybodontiform shark Planohybodus is described here on the basis of a fossil specimen coming from the Kimmeridgian of western France. A cast of the original specimen (specimen 42K7 of the Vaubourg private collection, Aytré, France) is housed in the Muséum d'Histoire naturelle of La Rochelle (MHNLR RYV 1).

Geological setting

The specimen discussed here was found in the Upper Kimmeridgian (Mutabilis Zone, Lallierianum Subzone) deposits that are exposed at the Pointe du Rocher near Yves, south of La Rochelle (Charente-Maritime, western France) (Fig. 1). This Upper Jurassic section was described in detail by Fürsich and Oschmann (1986). The benthic macrofauna is well developed, with numerous shell beds of the small oyster Nanogyra virgula. With the exception of the common ammonite Orthaspidoceras, the pelagic fauna is scarce. As revealed by surface collected fossils, sharks are only represented by the hybodont Planohybodus. In addition, some rare vertebrate remains indicate the presence of various fishes (e.g. semionotids, pycnodontids, ichthyodectiforms), turtles, thalattosuchians, and ichthyosaurs. Sedimentological and palaeontological data suggest a rather shallow shelf palaeoenvironment characterized by low energy conditions (Fürsich and Oschmann 1986).

Fig. 1
figure 1

Location (a) of the Pointe du Rocher at Yves (Charente-Maritime, western France) and stratigraphical position (b) of the studied specimen within the Kimmeridgian (Upper Jurassic) series south of La Rochelle (asterisk). EZ Eudoxus Zone, LSZ Lallierianum Subzone, MZ Mutabilis Zone, OSZ Orthocera Subzone

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Description

The ammonite is preserved as an uncrushed internal mould, showing the phragmocone and most of the body chamber (diameter, 118 mm; whorl width, 56 mm). It is characterized by a rounded whorl section and by a row of strong, spiny lateral tubercles slightly bent towards the umbilicus. The mould displays some small shallow depressions or perforations that may correspond to puncture marks (Fig. 2a). An elongated bean-shaped mark (6 mm in width) is present in the posterior part of the body chamber (Fig. 2b). Another falciform mark (3 mm in width) with tapered ends can be observed in the dorsal region of the shell, close to the shark tooth (Fig. 2c). The non-preservation of the shell does not permit observation of other damages (e.g. shell cracks and crushed portions of the shell).

Fig. 2
figure 2

Direct evidence of hybodont shark predation on ammonites and tooth morphology of ammonoid predators. Scale bars represent 50 mm (a), 10 mm (c-f), and 1 mm (b). a Internal mould of the ammonite Orthaspidoceras associated with a tooth of the hybodont shark Planohybodus (42K7; cast MHNLR RYV 1) from the Late Kimmeridgian of the Pointe du Rocher, western France. The two dotted outlines indicate the approximate position of the two other teeth that were originally preserved on this specimen. The arrow indicates the hole that is interpreted as a tooth puncture mark; other marks are more hypothetical. b Close-up of 42K7 showing the possible tooth mark indicated in a by the arrow. c Close-up of 42K7 showing the morphology of the Planohybodus tooth and a sickle-shaped mark (arrow) on the ammonite mould (tooth puncture mark?). Isolated Planohybodus teeth (MHNLR GRE 1 and MHNLR CHA 1) from the Early Kimmeridgian of Ré Island (d) and Châtelaillon (e) (La Rochelle ablerea, western France) displaying unusual damage on the main cusp probably due to predation activity on hard-shelled prey items such as ammonites. f Cladodont tooth (USNM 14107) of the ctenacanthiform shark Glikmanius, a Carboniferous predator of ammonoids, showing a general morphology similar to that of Planohybodus teeth

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The tooth of Planohybodus shows a high (9.2 mm) and robust main cusp flanked by a pair of lateral cusplets (only the distal one is preserved here) (Fig. 2c). The crown is labiolingually flattened. Numerous longitudinal folds develop from the base of the crown up to the middle of the main cusp. The tip of the main cusp is broken. The tooth is not impressed into the ammonite but is situated a few millimetres above the surface of the internal mould.

It must be noted that two more Planohybodus teeth were present adjacent to the tooth described above. Unfortunately, they were destroyed by the amateur palaeontologist who discovered and prepared the ammonite.

Discussion

The ammonite Orthaspidoceras lallierianum is very common in the early Late Kimmeridgian deposits of the Pointe du Rocher. In the northern part of the Aquitaine Basin, this endemic and monotaxic Orthaspidoceras fauna developed in distal, quiet, rather shallow water environments (Fürsich and Oschmann 1986; Hantzpergue 1989, 1995). The dense Orthaspidoceras populations may have constituted the major prey source for the predators of the pelagic realm able to attack shelled organisms. The marine reptiles found at the Pointe du Rocher correspond to long-snouted predator forms (an indeterminate species of the thalattosuchian Steneosaurus with slender teeth and an indeterminate ichthyosaur) that may have preyed upon unshelled items such as small to medium-sized fishes. The same remark can be made about the large ichthyodectiform fish present in this locality. The more robust dentition of Planohybodus suggests that this shark was a more generalist predator that could include ammonites in its prey range. This assumption is confirmed by the new specimen described here. For the first time, a body fossil belonging to the predator that attacked the ammonite is preserved in association with the shell. The hybodont tooth associated to the ammonite is very similar to those of Planohybodus grossiconus from the Bathonian of Western Europe (Rees and Underwood 2008) as well as that from the Kimmeridgian of southern England described as “Hybodus” sp. 2 (now to be referred to Planohybodus sp.) (Underwood 2002).

Taken as a whole, what hybodont sharks ate remains somewhat unclear. Some demersal forms, such as Ptychodus or Tribodus, have a highly specialized grinding-type dentition which indicates obvious durophagous feeding habits, with a prey spectrum likely dominated by benthic invertebrates (Kauffman 1972; Maisey and Carvalho 1997; Vullo and Néraudeau 2008). Recently, Whitenack and Motta (2010) noted that there are no dietary data for hybodont sharks. However, the stomach content of a unique specimen of Hybodus hauffianus from the Toarcian Posidonia Shale of Holzmaden displays over 250 belemnite guards (Levy 2009). The clutching-type teeth of H. hauffianus have a relatively low, robust, multicusped crown, especially in the posterolateral tooth rows (Duffin 1997). Such a dental morphology would rather suggest that this species preferentially fed upon shelled prey items. Results of performance testing undertaken by Whitenack and Motta (2010) also indicate that such teeth were suited for durophagy.

On the other hand, an exhaustive review of predation on cephalopods through time was provided by Mapes and Chaffin (2003). It is generally assumed that the vertebrates which have most likely preyed upon shelled cephalopods corresponded to durophagous forms with crushing or grinding dentitions, such as the Late Paleozoic petalodonts or the Jurassic hybodont Asteracanthus among selachians (Walker and Brett 2002; Mapes and Chaffin 2003). The specimen discussed here unambiguously shows that sharks with tearing-type dentition were able to catch and bite shelled cephalopods. This is in accordance with previous studies that have assigned the bite marks observed on the Carboniferous ammonoid Gonioloboceras goniolobum to the ctenacanthiform shark Glikmanius occidentalis (Mapes and Chaffin 2003). Indeed, this early shark has cladodont teeth (Fig. 2f) that are strikingly similar to those of Planohybodus (Ginter et al. 2005). The tooth crowns of these two taxa display convergent morphological features such as the strong labiolingual compression, longitudinal folds of the enamel present on both faces, and sharp lateral cusplets. Such teeth are especially efficient for puncturing prey. In the case of predation on ammonoids, Mapes and Chaffin (2003) described in detail a hypothetical scenario of such an attack: the predator strategy would have been to puncture gas chambers of the shell and thus to cause a buoyancy control problem, making prey vulnerable. With the exception of the indentation observed at the level of the body chamber (plus a few ambiguous marks), no major damage can be detected on the conch of the Orthaspidoceras specimen dealt with herein. It is difficult here to determine whether the hybodont shark (i.e. Planohybodus) attacked and bit an alive Orthaspidoceras individual (healthy or not) or scavenged on a dead animal. However, it is worth to note that the preserved tooth (plus the two removed teeth) and the assumed indentations are located in the dorsal part of the shell, suggesting that the attack may have come from above.

Unlike in most aspidoceratids with two spine rows, the shell of Orthaspidoceras displays on each side only one row of periumbilical short, spiny tubercles. Their function can be regarded as defence against predators (Checa and Martin-Ramos 1989). Added to the globular shape of the conch (i.e. sphaerocone type), these massive tubercles may have also increased the sturdiness of the shell (Ward 1981; Kröger 2002).

Two isolated Planohybodus teeth from the underlying Lower Kimmeridgian deposits (Cymodoce Zone) outcropping around La Rochelle (Ré Island and Châtelaillon) display some damage that might be linked to the feeding habits of this shark (Fig. 2d, e). Both teeth, moreover perfectly preserved, show a main cusp of which the apex is snapped clean through, suggesting that it broke whilst the shark was biting a hard-shelled prey. In one of the teeth, the intensity of the impact even caused the loss of a large fragment on the labial face of the crown. The Cymodoce Zone deposits of the La Rochelle area have yielded a rich ammonite fauna dominated by medium- to large-sized, robust forms (e.g. Lithacosphinctes, Paraspidoceras, Physodoceras, Rasenioides) that lived in open marine environments (Hantzpergue 1989, 1995). Such observations suggest that the predation behaviour of Planohybodus in these Early Kimmeridgian ecosystems was probably similar to that directly inferred from the Pointe du Rocher specimen here described.

As underlined by Whitenack and Motta (2010), the relation between tooth morphology and biological role should be used with more caution for inferring feeding habits from the dentition type. Indeed, the tooth morphology of Hybodus (robust clutching-type teeth) and Planohybodus (more slender tearing-type teeth) would have rather suggested dental adaptations for predation on ammonites (hard-shelled prey items) and belemnites (unshelled, soft prey items), respectively. Surprisingly, exceptional direct evidence from the fossil record shows that the prey range of such sharks was actually much broader and sometimes unexpected in accordance to the dentition features.