The fossil record and taphonomy

The fossil record of the Anomiidae dates back to the Jurassic (Fürsich and Palmer 1982). Various degrees and modes of byssus mineralisation have been suggested for these early anomiids: Eonomia is characterised by the direct, pallial secretion of the shell onto the substrate and the byssus most probably was not calcified at all. Byssal fixation lasted throughout life as indicated by the presence of a byssal foramen in the right valve but apparently attachment occurred without etching of the substrate (Fürsich and Palmer 1982). Placunopsis inaequalis had a non-mineralised byssal plug (Todd and Palmer 2002). In “Placunopsis” socialis, calcification of the byssus seems to have been variable, ranging from non-mineralised to variably calcified (aragonitic) (Todd and Palmer 2002; according to the discussion therein, Triassic members of “Placunopsis” are not included in the Anomiidae but are regarded as members of the Plicatulidae). Juranomia had a calcified byssus, which probably was calcitic because of its good preservation (Fürsich and Werner 1989). None of the Jurassic anomiids left etching traces in the fossil record.

In many of our specimens of C. eccentricus from the Upper Cretaceous chalk, fragmentary remains of the calcified byssus are still present (e.g., Figs. 5E, 6D, F, 7B, C). Because aragonite is generally not preserved in the chalk facies, we conclude that the byssus was originally composed of a mixture of calcite and aragonite, and that the aragonitic fraction was dissolved. This corresponds to the bimineralic composition of the byssus in modern anomiids (Pujol et al. 1970; Yamaguchi 1998). However, there is a conspicuous gap in the fossil record of preserved anomiid byssi across the Palaeogene and Neogene where only the byssal etchings are known, suggesting a non-mineralised or purely aragonitic byssus during this time interval. Only in rare cases, the calcitic body fossils of the trace forming anomiids were preserved in situ (Figs. 5F–H, 6C, E), but preservation was too poor to allow a confident taxonomical assessment.

Palaeobiology and palaeoecology

Growth, shape and substrate/shape relationships.—In all sampled localities, the trace-making anomiids clearly favoured belemnite rostra as substrate for settlement (Fig. 4A). In the Maastrichtian chalk of Rügen, 85.2% of the traces were found on belemnites (e.g., Figs. 5, 6A), followed by pycnodontid oysters (7.4%; Fig. 6B), terebratulid brachiopods (4.0%; Fig 6C, D), echinoids (2.7%; Fig. 6E), and inoceramids (0.7%; Fig. 6F). It should be noted, however, that our study only considers calcitic biogenic hardparts as potential substrates for anomiids. Because of the prevalent diagenetic loss of aragonite in the chalk facies it is not possible to evaluate the occurrence of anomiids and their traces on purely aragonitic shells, e.g., those of gastropods and ammonites.

The varying outline of C. eccentricus reflects the outline of the anomiid shell and is controlled by the size and shape of the substrate. Where growth of the anomiid shell was not obstructed (e.g., when it settled on the valves of large pycnodonts), the outline is almost circular. Where belemnites act as substrate for up to five traces (Fig. 4D), lateral growth is restricted by the elongate and cylindrical morphology of the rostrum. Here, the growth of the anomiid valve, as indicated by the corresponding trace, shows a clear preference for the central part of the rostrum (Fig. 4E), and follows the longitudinal axis of the belemnite (Fig. 4F). During growth, space becomes more restricted, resulting in a change from a circular (Fig. 5A) towards a more elongate and oval outline (Fig. 5B). However, the anomiid larvae did not always attach themselves in the preferred final growth direction, but were able to change direction in early life stages as indicated by a curved growth axis (Figs. 5A, 7A). The comparison of early and late stages of the traces reveals pronounced allometric growth of the trace-producing anomiids with a more dorso-ventrally elongated shell in late growth stages (Fig. 5F, I).

Competition.—From the spatial relationship between C. eccentricus and body fossils of other encrusting organisms, it can be inferred that space for settlement was at least occasionally a limiting factor and anomiids competed for space with both, fellow members of the species and other epibionts. Although most belemnite rostra from Rügen only exhibit a single attachment trace of C. eccentricus (77.3%), densely spaced multiple infestations also occurred. A maximum of five traces, each produced by an individual anomiid bivalve, were counted on a single belemnite rostrum (Fig. 4D). We observed overgrowth, displacement, and growth obstruction between C. eccentricus and cheilostome bryzoans, serpulid polychaetes, other epibiontic bivalves (Atreta nilssoni, Gyropleura ciplyana), octocorals, and scleractinian corals (Coelosmila excavata) (Fig. 6B, D, H, I). Additionally, endolithic organisms such as the producer of the trace fossil Dendrina were occasionally overgrown (Fig. 3). Superimposition of C. eccentricus on other epibionts, and vice versa, may also represent temporal successions instead of interspecific competition (Fig. 6I). These examples emphasise the importance of biological hard parts as “benthic islands” within soft-bottom communities, providing space, although limited, for recruitment and settlement of a diverse hard-substrate community. Belemnite rostra in particular littered the bottom of the chalk sea in high numbers and matched the needs of anomiid bivalves as a substrate for recruitment and life. Belemnite rostra possess a smooth surface and are composed of dense calcite, thus being suitable for etching, and are heavy enough not to sway around in modest bottom currents.

Predation.—Biting traces found on belemnite rostra associated with C. eccentricus indicate that anomiids served as diet for durophagous predators, most probably teleostean fishes. The shape and arrangement of the biting traces (Fig. 6G) indicate that a predator possessing sharp and pointed teeth has torn apart the bivalve from the substrate. Martin and Fox (2007) reported a durophagous mosasaur (Globidens) with a preserved gut content consisting mainly of anomiid shells. As a possible response to predation pressure, chalk anomiids may have evolved the deeply etched suture along the outline of the shell, providing firm attachment to the substrate as an effective defence mechanism against shell-crushing enemies such as crustaceans and small teleosts (see also below). Because of its synchrony with an intensification of predation pressure in marine environments in the Late Cretaceous (Vermeij 1987), we interpret this phenomenon to be an anti-predatory response of anomiid bivalves.

Fig. 5.

Morphology of Centrichnus eccentricus Bromley and Martinell, 1991, anomiid bivalve attachment trace on belemnite substrates from the Lower → Maastrichtian, Jasmund, Rügen, Germany (except D, F, I). A. Subcircular outline of a complete specimen (MB.W3075). B. Strongly elongate and deeply etched complete specimen (MB.W3076). C. Faintly etched complete specimen (MB.W3077). D. Series of etched pits forming anterior margin of trace (MB.W3078; Campanian, Misburg, Germany) E. Byssus attachment trace of preserved remains of calcified byssus (MB.W3079). F. Juvenile anomiid bivalve body fossil (MB.W3080; Maastrichtian, Kronsmoor, Germany). G. Right valve of anomiid bivalve partly preserved in situ on attachment trace visible through the byssus gape (MB.W3081). H. Left and partly preserved right valve of trace producing anomiid (MB.W3082). I. Immature trace illustrating allometric growth of anterior margin vs. byssus attachment (MB.W3083; Maastrichtian, Haccourt, Belgium).

Fig. 6.

Substrate types and biotic interactions between Centrichnus eccentricus Bromley and Martinell, 1991, producing anomiid bivalves and predators and competing epibionts in the Lower Maastrichtian, Jasmund, Rügen, Germany (except C, E). A. Trace on belemnite, the obliquely orientated anterior margin indicates change of growth direction in an immature state (MB.W3085). B. Two closely spaced traces on the oyster Pycnodonte vesicularis Lamarck, 1806 competing for space with a calcareous sponge (MB.W3086). C. Anomiid body fossil on the terebratulid brachiopod Carneithyris subcardinalis (Sahni, 1925) (MB.W3087; Maastrichtian, Kronsmoor, Germany). D. Trace on terebratulid brachiopod overgrown by a cheilostome bryozoan colony (MB.W3088). E. Body fossil of a juvenile anomiid attached to the test of the holasteroid echinoid Cardiaster granulosus Goldfuss, 1816 bio-immuring the echinoid's tuberculation (MB.W3089; Maastrichtian, Lixhe, Belgium). F. Faint trace and calcified byssus remains on inoceramid valve (MB. W3090). G. Two C. eccentricus traces on belemnite and predatory biting traces, probably produced by a teleostean fish (MB.W3091). H. Holdfast organ of scleractinian coral Parasmilia centralis (Mantell, 1822) abraded by anomiid tracemaker (MB.W3092). I. Trace indicates anomiid bivalve successfully suppressing growth of calcareous sponge. Note subsequent post-mortem overgrowth by a cheilostome bryozoan (MB.W3093).

Fig. 7.

SEM images illustrating details of Centrichnus eccentricus Bromley and Martinell, 1991, anomiid bivalve attachment trace on a belemnite from the Lower Maastrichtian, Jasmund, Rügen, Germany (MB.W3084). A. Complete morphology overview. B. Byssal attachment trace with preserved remains of calcified byssus. Close-up of calcified byssus (C), byssus attachment grooves (D), pits forming the anterior margin (E), posterior marginal groove (F).

Etching of the substrate and its function.—The characteristic morphological features of C. eccentricus bear implications for the behaviour of the anomiid bivalves that produced the studied traces and the effectiveness of the attachment mechanism. Primarily, attachment involves etching of the substrate surface and subsequent cementation by a calcified byssus (Bromley and Martinell 1991; Bromley 1999). In addition, the substrate is also etched along the outline of the anomiid bivalve, as indicated by the successive positions of troughs in the substrate that correspond to the growing shell margin. These chemical etchings in a carbonate substrate were possibly produced by secretions from glands along the mantle edge of the bivalve (cf. Morton et al. 2011). The etchings along the anterior margin of the trace were probably induced by the supradorsal extensions of the mantle lobes that are characteristic of anomiid bivalves (Yonge 1977). Another organ of anomiids known to be capable of carbonate dissolution is the foot. Projections of its soft tissue, which is responsible for byssus formation, produce holes in the calcified byssus through which adhesives are supplied to the bottom of the byssal apparatus (Yamaguchi 1998). However, because these holes are formed by the proximal part of the foot and the foot of adult anomiids is reduced (Yamaguchi 1998), it is much more likely that the observed etchings along the distal valve margins were generated by the mantle margins. The smooth micromorphology, apparent from SEM examination (Fig. 7), supports a chemical etching process but additional mechanical abrasion along the shell margins is conceivable.

The substrate etchings along the shell margins provide a tight fit and stability of the upper (left) valve when pulled firmly onto the substrate by the byssal retractor muscle. In combination with further muscles (see Yonge 1977), the interlocking of the shell margin with etchings in the substrate conveys increased shear resistance when the valves are closed. Thus, enhanced stability is provided to withstand torsion induced by hydrodynamic force or predators. The impression of a planar shell into a cylindrical rather than a planar substrate results in deeper cutting and thus, even more effective shear resistance, providing a potential explanation of belemnites being the preferred substrate.

Did Cretaceous anomiids possess a “pseudo-hinge”?—The anterior linear to slightly arcuate arrangement of small pits or grooves in the substrate (Fig. 5B, D, I; Fig. 7A, E) is somewhat reminiscent of the sockets of a taxodont bivalve hinge. The anomiids have lost a marginal hinge (Yonge 1977), but is it feasible that the function of a hinge is accomplished by the interlocking of the dorsal shell margin of the upper valve and the substrate, thus forming a “pseudo-hinge”. This scenario seems unlikely because it requires that shell projections at the dorsal shell margin of the left (upper) valve articulate with corresponding pits in the substrate. Evaluating the existence of such hypothetical pseudo-teeth was not possible with the few poorly preserved anomiid body fossils found in situ in the present material. Anyway, it is difficult to conceive how the calcium carbonate of the substrate is dissolved selectively and calcite is segregated as exactly corresponding projections of the dorsal shell margin. Also, the position of the rotation axis of the opening valves is defined by the position of the ligament on a stalked crurum (Fig. 2D). A shift to a new rotation axis, i.e., the pits and grooves forming the anterior part of the trace, is impractical for mechanical reasons (Fig. 2D).