bs_bs_bannerJournal of Zoology Journal of Zoology. Print ISSN 0952-8369 Pelagic palaeoecology: the importance of recent constraints on ammonoid palaeobiology and life history K. A. Ritterbush1, R. Hoffmann2, A. Lukeneder3 & K. De Baets4 1 Department of Earth Sciences, University of Southern California, Los Angeles, CA, USA 2 Institute for Geology, Mineralogy und Geophysics, Ruhr University Bochum, Bochum, Germany 3 Department for Geology and Palaeontology, Museum of Natural History Vienna, Vienna, Austria 4 Geozentrum Nordbayern, Friedrich-Alexander University Erlangen-Nuremberg, Erlangen, Germany Keywords Abstract palaeoecology; isotope analysis; reproductive strategy; predator–prey A review of fossil evidence supports a pelagic mode of life (in the water column) relationships; habitat; anatomy. of ammonoids, but they may have spent their life close to the seabottom (demersal), planktonically, or nektonically depending upon the ontogenetic stage Correspondence and taxon. There are good indications for a planktonic mode of life of ammonoid Kenneth De Baets, Geozentrum hatchlings, but a broad range of reproductive strategies might have existed (egg- Nordbayern, Section Palaeoenvironmental laying, fecundity). Isotope and biogeographical studies indicate that some forms Research, Friedrich Alexander University migrated or swam for considerable distances, whereas others may have been Erlangen Nuremberg, Loewenichstr. 28, primarily transported by oceanic currents during early and/or late ontogeny. 91054 Erlangen, Germany. Diverse ammonoid habitats are also supported by evidence from predator–prey Email: [email protected] relationships derived from characteristic injuries and exceptional fossil finds, which indicate chiefly predatory or scavenging lifestyles. Sublethal injuries pre- Editor: David Hone served in some ammonoid shells, as well as rare stomach and coprolite contents, provide evidence of predation by other cephalopods, arthropods and various Received 7 July 2013; revised 3 November jawed vertebrates. Various lines of evidence suggest that different groups of 2013; accepted 19 November 2013 ammonoids had quite different ecologies, but shell shape alone can only give upper constraints on ammonoid capabilities, a matter that needs to be considered doi:10.1111/jzo.12118 when interpreting their diversity and evolutionary history. Introduction coleoids (Engeser, 1996) than to Nautilida; the former thus presents an adequate model for some aspects of ammonoid Ammonoids, a now extinct group of externally shelled ecology and appearance (Jacobs & Landman, 1993; Warnke cephalopods, had a successful ecological and evolutionary & Keupp, 2005). Nevertheless, coleoids have internalized, and history for over 300 million years, surviving at least three largely reduced shells, leaving Nautilus as the only living ana- major mass extinction events (House, 1989). These molluscs logue to constrain the accretionary growth and function of the are palaeontology’s model organisms for the study of ammonoid shell. Here, we review how recent investigations biostratigraphy, diversity, biogeography and macroevolution and syntheses, aided by advanced technology and exception- due to their wide geographical distribution, high diversity and ally well-preserved specimens, can advance earlier models (e.g. disparity, and high evolutionary rates (Kennedy & Cobban, Wiedmann, 1973; Batt, 1993; Westermann, 1996) of ammo- 1976; Landman, Tanabe & Davis, 1996; Monnet, De Baets & noid life mode and ecology. Klug, 2011). Although preservation of the accretionary shells of ammonoids is nearly ubiquitous, preservation of soft-part anatomy is very rare and often cryptic when present (Klug, The ammonoid animal in Riegraf & Lehmann, 2012). As a result, reconstructions of phylogenetic context their appearance are often conjectural and work upon their ecology has been based primarily upon study of the morphol- Morphological details of ammonoid shells and soft parts ogies and facies distribution of their shells (e.g. Ebel, 1992; reveal their anatomy and confirm the ammonoid’s phylo- Westermann, 1996). Classically, ammonoids have been com- genetic position within the cephalopods. All ammonoid shells pared with extant nautilids, which is also reflected in historical have a chambered part (phragmocone) and a final open reconstructions (e.g. Fraas, 1910). However, it is now widely chamber (body chamber), which houses the soft body of the accepted that ammonoids are more closely related to extant animal (Fig. 1). Most post-embryonic ammonoid shells Journal of Zoology 292 (2014) 229–241 © 2014 The Zoological Society of London 229 Pelagic palaeoecology of ammonoids K. A. Ritterbush et al. the shell. Similar to most extant cephalopods, the mouthparts of ammonoids consist of jaws and a radula, a minutely toothed, chitinous ribbon used for feeding in molluscs (Nixon, 1996). The ammonoid radula is similar to that of coleoids (in size, shape and the amount of elements per row), but differs from the radula of more basal externally shelled cephalopods and Nautilus (Nixon, 1996; Gabbott, 1999). The close phylogenetic relationship between ammonoids and coleoids (Engeser, 1996; Kröger, Vinther & Fuchs, 2011) is further supported by a transitional series from straight orthoceratid nautiloids, over straight to slightly curved bactritoids (which also gave rise to coleoids) to coiled ammonoids (Erben, 1966; see Fig. 2), which was recently stratigraphically cor- roborated (Kröger & Mapes, 2007; De Baets et al., 2013). All these closely related extinct groups share similar small, initial chambers of their embryonic shells with the extant coleoid Spirula (Warnke & Keupp, 2005). Developmental, neontological, fossil and genetic studies (Shigeno et al., 2008; Sasaki, Shigeno & Tanabe, 2010; Wani, Kurihara & Ayyasami, 2011; Ogura et al., 2013) indicate that the unique Nautilus features (90 arms, pinhole eyes, large yolk-rich eggs) developed in their lineage separately from the other extant cephalopods (probably after they split from the Orthocerida; Kröger et al., 2011). The timing of evolutionary divergence of extant nautiloids and the ancestors of coleoids has often been traced back to at least 480 Ma (origin of the Oncocerida; Kröger, Zhang & Isakar, 2009) using the fossil record, but the deep ancestry of extant nautiloids is still debated (Dzik & Korn, 1992; Turek, 2008) and their divergence from extant coleoids has been esti- mated by the most recent molecular clock analyses to be near to the Silurian/Devonian boundary (∼416 ± 60 Ma; Kröger et al., 2011 and references therein). Figure 1 Ammonoid life cycle (a) and general conch morphology (b) as Constraints on ammonoid anatomy come from exception- exemplified by the Late Devonian ammonoid Manticoceras. (a) Growth ally preserved specimens and from phylogenetic inference. stages and important events in the life history (modified from Korn & The rare preservation of soft tissues is often interpreted as a Klug, 2007, with permission from the authors). (b) From left to right: consequence of delays in the pelagic animals’ sinking (De cross section, ventral and lateral views. Note the suture lines (intersec- Baets et al., 2013) and burial (Wani et al., 2005; Wani, 2007). tions of the septa with the shell) on the internal mould, where the shell is not preserved (modified from Korn & Klug, 2002, with permission Still, extraordinarily preserved specimens reveal digestive from the authors). tracts, gills, questionable eye capsules and details of the buccal apparatus (e.g. Klug et al., 2012). Computer tomography has revealed new morphological details about the ammonoid mouth parts (e.g. Kruta et al., 2011, 2013; Klug & Jerjen, are coiled planispirally, but some ‘heteromorph’ taxa have 2012). Ammonoids might have had a lens eye (if the develop- trochospiral, uncoiled or even straight shells. Ammonoid ment of the pinhole eye was specific for the nautiloids; Ogura buoyancy was probably controlled not only by shell and soft- et al., 2013) and the arguable presence of a hood in tissue growth but also by manipulation of gas and fluid trans- ammonoids has been deemed unlikely by Keupp (2000) based port through the siphuncle, a tube of ‘connecting rings’ upon the findings of dorsally tongue-shaped black layers. It is between the phragmocone chambers (Tanabe et al., 2000). most parsimonious to assume the presence of 10 arms in Ammonoids had a functional phragmocone similar to the ammonoids due to the presence of 10 arm buds in the embry- Nautilida, where the mantle secreted the calcium carbonate onic development of all extant cephalopods (Shigeno et al., (aragonite) shell with the septa subdividing the phragmo- 2008). However, both the amount and the appearance of the cone into chambers as well as its proteinaceous coating adult arms might have varied from taxon to taxon, as found in (periostracum; cf. Mutvei, 1964). Additionally, the mantle extant coleoids (Westermann, 1996). Based upon the lack of performed shell repairs evident on ammonoid body chambers preserved arms in the fossil record and constraints imposed by (Kröger, 2002). The other living cephalopods, the coleoids narrow aperture and mouth parts, Landman, Cobban & (octopods, cuttlefish and squids), are very different from Nau- Larson (2012) suggested very short arms, whereas Keupp & tilus, most obviously in the internalization and reduction of Riedel (2010) have speculated on very short or delicate arms 230 Journal of Zoology 292 (2014) 229–241 © 2014 The Zoological Society of London K. A. Ritterbush et