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The Role of Ammonites in the Mesozoic Marine Food Web Revealed by Jaw Preservation

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Science  07 Jan 2011:
Vol. 331, Issue 6013, pp. 70-72
DOI: 10.1126/science.1198793

Abstract

Ammonites are prominent in macroevolutionary studies because of their abundance and diversity in the fossil record, but their paleobiology and position in the marine food web are not well understood due to the lack of preserved soft tissue. We present three-dimensional reconstructions of the buccal apparatus in the Mesozoic ammonite Baculites with the use of synchrotron x-ray microtomography. Buccal mass morphology, combined with the coexistence of food remains found in the buccal mass, suggests that these ammonites fed on plankton. This diet may have extended to all aptychophoran ammonites, which share the same buccal mass morphology. Understanding the role of these ammonites in the Mesozoic food web provides insights into their radiation in the Early Jurassic, as well as their extinction at the end of the Cretaceous/early Paleogene.

Ammonites were externally shelled cephalopods that lived from the Early Devonian [407 million years ago (Ma)] to the end of the Cretaceous (65.5 Ma) and commonly occur in the fossil record. They are widely used in biostratigraphy to subdivide geologic time. Ammonites are one of the most diverse fossil groups in marine environments; their ecology, however, is poorly understood (1, 2). The modern nautilus generally serves as a model to reconstruct their mode of life, but phylogenetic studies suggest that coleoids are better models (3). Information about their diet is based on examination of the buccal mass—consisting of the upper jaw, lower jaw, and radula—that is occasionally preserved inside the body chamber. Jaws have been documented in 43 genera of ammonites (4, 5), but radulae are observed in only 9 genera (6, 7) because their discovery depends on accidental breaks or fortuitous exposure by weathering. In addition, traditional techniques used to study radulae (polished serial sections) do not usually reveal sufficient detail for comparative analysis.

Here, we report phase-contrast synchrotron x-ray microtomographic three-dimensional (3D) reconstructions of the buccal masses of three fossil specimens of Baculites sp., one of the few ammonite genera that persisted up to and perhaps even across the Cretaceous-Paleogene boundary (8). In addition, we document a larval shell of a gastropod and three fragments of crustaceans that are preserved inside the jaw in one specimen. The specimens were discovered in the Upper Cretaceous Pierre Shale, Belle Fourche, South Dakota, USA (9).

As in other members of the aptychophoran group of ammonites (10), the lower jaw of Baculites is relatively large, with a slit along the midline and a blunt anterior margin (Fig. 1, A to C). The two halves of the lower jaw are covered with a pair of calcareous plates (known as the aptychus). The upper jaw of Baculites is evident in these reconstructions (Fig. 1C, fig. S1, and movie S1); it is less than one-half the length of the lower jaw and is relatively thin (140 μm thick at the anterior margin), indicating that the original chitin may have been poorly tanned and slightly flexible.

Fig. 1

Exceptionally preserved radula in ammonites from the Upper Cretaceous (Belle Fourche, South Dakota, USA). (A) Shell of Baculites sp. (AMNH 55901). Only a portion of the body chamber and phragmocone is preserved. (B) Aperture of the shell with one of the valves of the lower jaw (aptychus) exposed on the right side. (C) Virtual reconstruction of the buccal mass based on a composite of two specimens (AMNH 55901 and AMNH 66253). Green, shell; white, valves of the lower jaw; color gradation from yellow to brown, upper jaw; red, radula. The upper jaw has been enlarged to compensate for the size difference between the two specimens. (D and E) 3D virtual extraction of the radula of Baculites sp. as it appears inside the ammonite (in situ) [(D) AMNH 55901; (E) AMNH 66267]. (F) Sketch of the radula of Baculites sp. R, rachidian tooth; L1, first lateral tooth; L2, second lateral tooth; M, marginal tooth; MP, marginal plate.

All three specimens of Baculites contain a radula (figs. S2 to S4). In American Museum of Natural History (AMNH) specimen numbers 55901 and 66267, the teeth are preserved close to their original life position (Fig. 1, D and E, and movie S1). Although they were originally solid structures, the radular teeth are hollow or infilled with material similar in composition to that of the matrix (but of different density). In analogy with modern cephalopods, they may have been composed of chitin, with possibly some degree of mineralization (11). As in all cephalopod radula, the teeth and marginal plates in each transverse row repeat those in the preceding and succeeding rows (Fig. 2A) (11). In AMNH 55901, the radula forms a U-shaped structure, possibly reflecting its original shape in the radular canal (Fig. 2B and movie S1). If the radula were unfolded, it would be ~6 mm wide and ~7 mm long.

Fig. 2

Morphology of the radula and teeth in Baculites sp. (A) Virtual reconstruction of the radula in Baculites sp. (AMNH 55901) as if unfolded. Rows of teeth are repeated all along the length of the radula. Blue, marginal teeth; light pink, second lateral teeth; purple, first lateral teeth; dark pink, rachidian teeth; yellow, marginal plates. (B) Part of the radula of Baculites sp. (AMNH 55901). The radula is folded, as it may have appeared in the tube-shaped radular canal. (C) Adoral view of the rachidian tooth. (D) Lateral view of the second lateral tooth, center of the ribbon on the right-hand side. (E) Lateral view of the marginal tooth.

Each radular row consists of nine elements, including seven teeth and two marginal plates, thus corresponding to the definition of the Angusteradulata (ammonoids plus octopus, cuttlefish, and squid) (Fig. 2A) (12). Four elements appear on each side of the central rachidian tooth. The teeth vary in shape, and they are multicuspidate and comblike (11). The cusps of the rachidian tooth are narrow and sharp and decrease in height with increasing distance from the central cone (Fig. 2C, fig. S5, and table S1). Each lateral tooth (L1 and L2) bears a single small cusp on the inner side of a prominent cone that is ~1 mm high and multiple cusps on the outer side, decreasing in height toward the margin: four on the first lateral tooth (L1) and 17 on the second lateral tooth (L2) (Fig. 2D). The marginal tooth is unicuspate (Fig. 2E), 1.6 mm high, curved, and sabrelike. The marginal plates are small and flat. High-resolution scans with voxel (volumetric pixel) size of 1.4 μm reveal a carena running from the tip of the highest cone to its base on the second lateral tooth (fig. S2). These radulae are similar to a previously reported structure in the same species of Baculites, but most of the teeth in this previously reported specimen were not visible, precluding any detailed reconstruction of the radula (7).

The jaws in Baculites are similar to those in other aptychophoran ammonites. Comparison of the radula in Baculites with that of previously described ammonites is limited because of the low degree of resolution available in older studies. However, the radula reported in other aptychophoran ammonites also appears to consist of small, delicate teeth with a tall, sabrelike marginal tooth [e.g., Aconeceras (13)].

The morphology of the jaws and radula in ammonites, and mollusks in general, is related to diet (14); therefore, the study of these structures can help clarify the feeding habits and ecology of these animals. However, the buccal mass of aptychophoran ammonites has no equivalent among modern cephalopods, and its function has been debated for the past 150 years. Several of the features of the lower jaw—such as its blunt anterior margin, the presence of a slit rather than a thickening along the midline, and the very large size relative to the upper jaw—are incompatible with biting and tearing large prey (12). In contrast, the buccal apparatus in modern nautilus consists of a beaklike jaw with robust radular teeth (11), which is consistent with the scavenging mode of life of these animals (15). Similarly, in most modern coleoids such as squid and cuttlefish, which bite and tear large prey, the apical end of the jaw is very sharp, and the radular teeth are robust. There are only three examples of a buccal apparatus in modern cephalopod species that superficially resemble that in Baculites. In meso-bathypelagic octopods such as Bolitaenidae, the lower jaw ends in a finely toothed, blunt anterior margin, the upper jaw is weakly tanned, and the radula is multicuspidate (ctenoglossan) (16). The diet of Japetella diaphana and Bolitaena pygmea consists of copepods, krill, and other small organisms (17). In Argonauta argo, the buccal apparatus also superficially resembles that in Baculites (weakly tanned upper and lower jaws, absence of a sharp beak); it feeds on heteropods and pteropods. Outside of cephalopods, the radula in Baculites most closely resembles that in heteropod mollusks (multicuspidate, with sabrelike marginal teeth); they feed on plankton and gelatinous prey (18).

These comparisons suggest that the buccal apparatus in Baculites, as well as in other aptychophoran ammonites in general, is an adaptation for capturing and eating small organisms in the water column. This is consistent with rare finds of ammonite stomach contents, most of which consist of small organisms, such as tiny crustaceans and juvenile ammonites (12, 19). In addition, the radular teeth in Baculites do not show a progressive loss of cusps, which has been observed in modern cephalopods where the radula is used as an abrasive device (20).

Lending further support to this hypothesis are the remains of several small organisms preserved inside the buccal mass in AMNH 66253 (Fig. 3). Three fragments of crustaceans 5.0, 3.0, and 1.6 mm in length are present between the two valves of the aptychus (figs. S7 and S8). The anterior portion of the body is missing in two fragments, whereas the third fragment consists of a cephalon with two pereonites (fig. S7). The ventral part and appendages are not well preserved. The fragment of the cephalon matches the posterior part of the fragment near the radula, indicating that the two pieces belong to the same individual. The overall morphology of these specimens suggests that they are isopods, one of which is an adult and the other a juvenile. They probably belong to the family Cirolanidae and were capable of swimming. However, the fragmentary nature of the material does not permit a more precise determination. A small gastropod 975 μm long is present near the radula and upper jaw. It appears to be a planktotrophic larva of a benthic gastropod (fig. S9).

Fig. 3

Upper jaw, radula, and associated crustaceans (AMNH 66253). (A) Lateral view of the upper jaw (gray); anterior margin on the left. The radular teeth (yellow) are enclosed by the upper jaw. (B) Dorsal view of the crustacean (isopod) showing the segments. Posterior part of the crustacean on the bottom right; radular tooth, yellow; gastropod larval shell, pink; isopod, blue.

The presence of these organisms in the buccal mass could be explained as the result of predation by the ammonite, scavenging of the buccal mass by the isopods, or a hydrodynamic accumulation of postmortem debris (or any combination of the three). We favor the first interpretation. The fact that all of the fossils occur in the buccal mass and not in the rest of the body chamber provides evidence against their interpretation as a hydrodynamic accumulation. The gastropod may have been living in the plankton and was eaten by the ammonite. The fragments of crustaceans are broken in half, and the remains of their soft tissues are preserved inside, suggesting that they were bitten off by the ammonite jaw. Today, marine isopods live on the sea floor or in the water column just above the bottom [demersal zooplankton (21)] and are eaten by modern cephalopods, especially juveniles in which the jaw is not yet sufficiently well developed (stiff) to bite harder prey (22).

Thus, the morphology of the jaws and radula in Baculites and the presence of possible prey remains inside the buccal mass suggest that these ammonites fed on small organisms in the water column, rather than capturing and eating large prey on the ocean bottom, as exemplified by living nautilus. The aptychophoran ammonites represent a diverse clade in the Jurassic and Cretaceous, consisting of hundreds to thousands of species (23, 24) [e.g., aptychophoran ammonites represented a large portion of the Ammonoidea in the Cretaceous (24)]. They include species with a variety of shell shapes, ranging from closely coiled to straight, as in Baculites. These species may have exhibited different hydrodynamic properties (25) and lived in different habitats (for instance, different depths in the water column) (1). However, the similarity in their buccal apparatus suggests that all of them followed the same feeding habit.

The unique role of these ammonites in the marine food web may have influenced Earth system processes during the Jurassic and Cretaceous (for example, processing of particulate organic matter and its transport to the sea floor). The appearance of this feeding strategy may have led to the radiation of the aptychophoran ammonites in the Early Jurassic and Cretaceous, possibly in conjunction with the radiation of new groups of plankton (26, 27). However, this diet may have ultimately contributed to the extinction of the ammonites. The end of the Cretaceous was marked by an abrupt decline in several groups of plankton (28). The ammonites, which may have depended on these animals for food, eventually became extinct, whereas closely related groups such as the nautilids, which relied on other food sources, survived and even flourished in the succeeding era (29).

Supporting Online Material

www.sciencemag.org/cgi/content/full/331/6013/70/DC1

Materials and Methods

Figs. S1 to S9

Table S1

References

Movie S1

References and Notes

  1. Materials and methods are available as supporting material on Science Online.
  2. This work was supported by ESRF, UMR CNRS 7207, its 3D platform, and the Annette Kade Fellowship (AMNH). P. Janvier and C. Klug reviewed an earlier draft of the manuscript; A. Lethiers helped produce the figures and movie; N. Larson and K. Cochran helped in field work; and D. Defaye, N. Bruce, R. Feldmann, and K. Bandel helped in the identification of non-ammonite material. Data are available at the ESRF database http://paleo.esrf.eu.
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