Pelagic Palaeoecology: the Importance of Recent Constraints on Ammonoid Palaeobiology and Life History K

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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

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 estimated 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

Figure 2 Evolutionary transformations of shell morphology from bactritoids (with a dark grey background) to ammonoids (with a light grey background). Note the change in body chamber length (BCL) and orientation of the aperture (OA). There appears to be a strong tendency towards horizontal apertures, which applies also to the majority of Mesozoic ammonoids. These changes in shell morphology potentially correlate with changes in increasing swimming velocity, manoeuvrability and fecundity as well as decreasing embryo size (modiﬁed from Klug & Korn, 2004, with permission from the authors).

spanning a mucous net in order to feed on plankton in some 2006), and the orientation of the shell in the water column derived Jurassic and Cretaceous ammonoids. (Saunders & Shapiro, 1986; Klug & Korn, 2004; see Fig. 2). Muscle attachment scars are more commonly preserved in Such models and calculations can only provide maximum fossil ammonoid shells, which reveal how muscles were constraints on ammonoid capabilities and are based upon attached to the shell. A pair of lateral retractor muscles is the several simplifications and assumptions. Flawed estimates of most conspicuous structure (e.g. Doguzhaeva & Mutvei, 1996; negative buoyancy and erroneous assumptions about ammo- Richter, 2002), which probably served for jet propulsion and noid growth and soft tissues have led to some extreme inter- the retraction of the head, the arm crown and the hyponome; pretations that ammonoids were epibenthic crawlers (e.g. sometimes, the portions of the muscle insertion responsible for Ebel, 1992). However, it is widely accepted that calculations the hyponome and for the cephalic part can be distinguished. are in the range of neutral buoyancy (within the limit of esti- At least some of these muscles were already present at the mate) when making reasonable assumptions (Westermann, ammonitella stage; the dorsal muscle scars are commonly long 1996; Kröger, 2001). Furthermore, novel computer tomo- in Triassic and more rounded in Jurassic ammonoids (Keupp, graphic methods allow for more precise volume determina- 2000). An additional pair of muscle scars at the umbilical edge tions of cephalopod shells, which can be used to further refine is present in Mesozoic ammonoids. A pair of ventrolateral buoyancy calculations of extinct cephalopods (e.g., Hoffmann muscles was reported for Aconeceras, which significantly et al. 2013). There is also support from modelling results that change in shape and position during ontogeny and between even heteromorphs with the most aberrant shell morphologies species (Doguzhaeva & Mutvei, 1996). Two tongue-shaped were living in the water column (Okamoto, 1996). Facies ventral muscles were probably connected with the funnel and distribution and hydrodynamic considerations have led therefore responsible for the adjustment of the swimming to seemingly detailed hypotheses on ammonoid ecology direction (Keupp, 2000). (Westermann, 1996), with coiled ammonoids being considered The great disparity in ammonoid shell shape has prompted as nektonic, demersal and planktonic depending upon their studies for environmental associations to test interpretations shell shape, orientation and streamlining, whereas most correlating differing shell morphologies with different life heteromorphic ammonoids have been interpreted as plank- modes (e.g. Batt, 1993; Westermann, 1996). Ammonoid conch tonic drifters or vertical migrants. Such models must be more geometry has been used to calculate flow resistance and swim- widely tested in time and space with different types of data. ming velocities (Jacobs & Chamberlain, 1996), septal strength The next section will review some recent investigations of and maximal diving depths (Hewitt, 1996), the positions of the associations between ammonoid shell shape and habitat centres of gravity and buoyancy (e.g. Hammer & Bucher, (facies), biogeography and diversification events.

Spatiotemporal associations of (2011) attributed this pattern to selection pressure by preda- ammonoid shell shape and tion in addition to hydrodynamics. Oxygenation is another factor classically attributed to influence ammonoid morph environmental phenomena distribution (Batt, 1993; Tsujita & Westermann, 1998). However, the model of Batt (1993) does not always uphold as Investigations of spatiotemporal and evolutionary trends in evidenced by more high-resolution stratigraphic studies, ammonoid shell shape generally focus upon bivariate plots of which could not find a link between anoxia and the extinction geometric parameters (e.g. Klug & Korn, 2004; Yacobucci, of various morphotypes (e.g. Monnet & Bucher, 2007). Some 2004) or the combination of many parameters in ordinated immigrants that diversified within isolated seaways or basins spaces (e.g. Dommergues, Laurin & Meister, 2001; Klug et al., showed gradual morphologic change, possibly reflecting eco- 2005; Saunders et al., 2008; Dera et al., 2010; Korn & Klug, logical selection on hydrodynamic properties (Yacobucci, 2012; Brosse et al., 2013). Ordinations detect subtle or 2004; Klug et al., 2005; see Fig. 2), whereas other groups complex shape changes within a specific collection of shells failed to establish endemic lineages (Fernández-López & (Yacobucci, 2004) or assess the extent of variation within a Meléndez, 1996). collection (Brosse et al., 2013), but the results from these Detailed studies of ammonoid diversification events also studies cannot be directly compared visually or statistically show that selection on shell shape may be more complex than (see McGowan, 2004 for discussion). Particularly relevant to Wiedmann’s (1973) model of control by sea level. Early evo- the present discussion are recent approaches that allow direct lutionary lineages of ammonoids show rapid, progressive comparison between studies and focus upon parameters that coiling of the shell, which might have resulted in changes in could influence shell hydrodynamics. Monnet et al. (2012) aperture orientation, locomotion and reproductive strategy tested for increasing hydrodynamic streamlining within the (Klug & Korn, 2004; De Baets et al., 2012; see Fig. 2). In long ranging ammonoid family Acrochordiceratidae by com- addition to the common trend in lineages to produce increas- paring involution, whorl compression and ornamentation ingly tightly coiled shells (Monnet, De Baets & Klug, 2011), (ribbing density) in a ternary diagram. Ritterbush & Bottjer heteromorphic post-embryonic shells evolved repeatedly in (2012) introduced the ‘Westermann’s morphospace method’ – the Mesozoic, which may be linked to changes in trophic juxtaposing umbilical exposure, whorl expansion and overall conditions, environmental stress and/or sea-level changes inflation to compare coiled ammonoid shells from different (Cecca, 1997; Keupp, 2000; Guex, 2006). Analyses of taxo- studies (Fig. 3) to common and hydrodynamically distinc- nomic extinction and rediversification after the end-Permian tive end-member shapes according to the hypotheses of and end-Triassic mass extinctions (Brayard et al., 2009; Guex Westermann (1996). The possible influence of ornamentation et al., 2012) are matched with analyses of selection on mor- and body chamber length (associated with shell orientation; phological disparity (Dera et al., 2010; Brosse et al., 2013) and Saunders & Shapiro, 1986; Klug & Korn, 2004) is not directly biogeographic trends (Dommergues et al., 2001; Brayard, considered in this approach. Escarguel & Bucher, 2007; Dera et al., 2011; Brayard & Useful case studies apply these methods to test associations Escarguel, 2013). Brayard et al. (2007) discovered that assem- between ammonoid shell shape and environmental character- blages of ammonoid genera were more similar on opposing istics (Tsujita & Westermann, 1998) or evolutionary patterns. coasts of Pangaea than at neighboring sites along the coasts at Jacobs, Landman & Chamberlain (1994) showed that more higher latitude (cf. Brayard & Escarguel, 2013; Brosse et al., streamlined morphs of the Cretaceous genus Scaphites could 2013). Analysis in ‘Westermann Morphospace’ shows that be more hydrodynamically efficient at high speeds than ammonoid shell forms traditionally interpreted to be more inflated morphs, and that these streamlined morphs are asso- streamlined might have traversed the tropical global ocean ciated with coarser grained, higher energy inshore habitats of (Brosse et al., 2013; see Fig. 3). In contrast, following the end- the Western Interior Seaway (cf. Courville & Thierry 1993 for Triassic mass extinction, earliest Jurassic ammonoid faunas a similar case in a different Cretaceous taxon). Strong intra- featured chiefly serpenticonic shells (Ritterbush & Bottjer, species variation in shell morphology without apparent facies 2012), which have classically been interpreted as planktonic association questions a close correlation between shell shape drifters (Westermann, 1996). However, evidence from shell and ecology in several Palaeozoic (e.g. Korn & Klug, 2007; De shape alone is insufficient to corroborate such hypotheses. Baets, Klug & Monnet, 2013) and Mesozoic ammonoids (e.g. Kennedy & Cobban, 1976; Dagys & Weitschat, 1993; Morard Ammonoid habitats through & Guex, 2003). However, the situation might be more ontogeny complex as demonstrated in a study of facies distribution by Wilmsen & Mosavinia (2011), who demonstrated different Like in other molluscs, accretionary shells of extant and fossil modes of intra-specific variation within the same Cretaceous cephalopods record stable isotopic signatures of δ13C and δ18O ammonoid species (Schloenbachia varians) depending upon throughout the animal’s lifespan. Only pristine aragonite pres- the type of environment. More compressed forms are more ervation allows measurement of these isotopic signals along common in open water and more heavily ornamented, the shell spiral, from embryonic to adult stages. Recent studies depressed variants in shallow water facies, which is opposite to (cf. Lukeneder et al., 2008, 2010; see Fig. 4) include shells of the facies distribution reported by Jacobs, Landman & modern Nautilus, the common Atlantic cuttlefish (Sepia), the Chamberlain (1994) for Scaphites. Wilmsen & Mosavinia internally shelled deep sea squid Spirula as well as several

Figure 3 Results from three studies of ammonoid shell shape change through time and space are compared in ‘Westermann Morphospace’ (Ritterbush & Bottjer, 2012). (a) Yacobucci (2004) examined intra-species variation of Neogastroplites through the biozones Hassi, Cornutus, Muelleri, Americanus and Mclearni (time series left to right; small dot = one specimen). She hypothesized that intra-species variation would decrease after the immigration event (IE) of Metengonoceras (large dots, centre frame), but instead Neogastroplites populations included a morphological shift to cadicones, away from the oxycone shape of Metengonoceras, without decreasing overall variation. (b) Klug et al. (2005) investigated Ceratites, Paraceratites and Discoceratites (275 specimens) from 16 stratigraphic intervals. Contours indicate the shapes present within each interval, and the largest specimens are plotted individually with corresponding interval numbers. At first, the shells found within the basin drift from discocone to planorbicone shapes, but after two IE, shells present increasingly hydrodynamic shapes (but the potential influence of ornament and other factors is ignored here) when using the interpretative diagram shown in (d). Contour peaks of intervals 5, 6 (black lines) and 7 overlap. (c) Brosse et al. (2013) quantified shell shape disparity in different regions during the Early Triassic. Here, Smithian stage shells from Tropical Panthalassa (palaeo-Pacific) are contrasted to those from the more restricted high latitude Tethys seaway with density contours (all data) and circles (largest specimen of each genus). The Tropical Panthalassa ammonoids had significantly more oxycones (potential swimmers) and significantly fewer serpenticones (probable drifters) when the largest specimens are categorized with the interpretive diagram shown in (d). Shape distributions in adjacent geographic regions vary gradually from these without significant difference. This may be an ecological consequence of coincident increased latitudinal stratification in ammonoid taxonomic presence (Brayard et al., 2007) and persistent tropical oxygen minimum zones (Winguth & Winguth, 2012). (d) Hypothetical diagram showing traditional interpretations of ammonoid shell shapes (cf. Westermann, 1996). Note that some extreme values fall outside the diagrams because the triangular diagrams contain only common ammonoid shapes. Dashed lines on the interpretive diagram designate the overlapping fields of oxycones, serpenticones and spherocones, which Westermann (1996) interpreted as nekton, plankton and vertical migrants, respectively. The shaded region of intermediate shapes between planorbicones and platycones was interpreted as serving a demersal life mode by Westermann (1996).

Jurassic to Cretaceous ammonoids (Baculites; Fatherree, stages allows interpretation of transitions in habitat tempera- Harries & Quinn, 1998; Cadoceras, Hypacanthoplites, ture and indirectly depth (see Fig. 4; Lukeneder et al., 2010). Nowakites, Perisphinctes; Lécuyer & Bucher, 2006) and fossil Various strategies are documented in the stable isotope record nautiloids (Cenozoic Aturia; Schlögl et al., 2011). Dynamic of the shells of derived Jurassic and Cretaceous ammonoids, transitions in an isotope record through ontogeny may have some of which can be compared with modern cephalopods. been inﬂuenced by transitions in the animal’s environment Cadoceras demonstrates an isotopic record similar to modern (sea water temperature, salinity or habitat depth) and meta- Nautilus and the cuttleﬁsh Sepia, suggesting that it would have bolic processes (diet, reproduction). been a planktonic migrant travelling from warm shallow to Division of δ18O isotopic records of modern and fossil cool deep waters, then returning to the shallows to spawn. In cephalopod shells into embryo, juvenile, mid-age and adult contrast, the ammonoid Hypacanthoplites rose from cold,

Figure 4 Ontogeny in recent shelled cephalopods Spirula, Sepia and Nautilus (left), ancient nautiloids with Aturia (left) and ammonoids Cadoceras, Hypacanthoplites and Nowakites (right), and ammonoids Baculites and Perisphinctes (right). δ18O curves in growth direction indicating calculated water temperatures and depth distribution of the cephalopods investigated compared with additional recent Sepia, Spirula, Nautilus, and fossil Perisphinctes and Baculites (all available literature data). Clear separation of the juvenile, mid-age and adult phase is evident, adapted from Lukeneder et al. (2010) and Schlögl et al. (2011). Stable isotope records in Cadoceras and Hypacanthoplites suggest three main phases, which probably correspond to ontogenetically controlled, vertical, long-time migrations within the water column. The δ18O values of Hypacanthoplites reﬂect an ontogenetic migration of Hypacanthoplites from shallow, warm marine environments to even warmer environments (∼27–28°C). The δ18O values of juvenile Cadoceras shells steadily decrease from juvenile (+0.93‰) to adult (+0.39‰), with a juvenile minimum of +1.35‰ and a mid-aged minimum of +0.75‰. These values point to a shallow, c. 21°C, warm marine habitat of juvenile Cadoceras. Later, the mid-aged animal preferred slightly cooler and deeper environments (∼12–16°C). Finally, the adult Cadoceras migrated back to slightly warmer and shallower environments (c. 17°C).

deep habitats to warmer, shallower habitats in adulthood, further test these apparent trends and their association with which resulted in a record partially similar to the modern deep shell shape and environmental variables. sea squid Spirula. Habitat temperature changes of 6–10°C (Fig. 4) would imply a depth change of 50–700 m today, and Reproductive strategy potentially more in unstratiﬁed Mesozoic seas (Lukeneder et al., 2010), although these values may be overestimates The accretionary shells of ammonoids record the life history because the chambers of ammonoid shells have been estimated from embryo to adult, which makes them important subjects to only withstand hydrostatic pressure of depths up to 400– of ontogenetic studies (Davis et al., 1996; Klug, 2001; Gerber, 500 m in most ammonoids (Hewitt, 1996). Alternatively, Eble & Neige, 2008; Lukeneder et al., 2010; De Baets et al., changes in temperature might also be related to horizontal 2012). The end of the embryonic and adult stages is marked by migrations or seasonal changes in water temperature (Lécuyer constrictions and changes in shape, shell thickness and orna- & Bucher, 2006). As in modern cephalopods, it seems reason- mentation (see Davis et al., 1996 and Landman et al., 1996 for able to assume that ammonoids initiated migrations due to a review). They were probably fecund producers of planktonic changes in diet or later in the mating/spawning phase young. (Lukeneder et al., 2008, 2010). Such migrations through Ammonoids produced a large number of offspring (com- ontogeny would explain the separation of juvenile and adult pared with extant Nautilus), which is supported by their evo- ontogenetic stages of several taxa in the fossil record. Com- lutionary history as well as size class distributions and high parison of oxygen isotope data of ammonoids with exception- abundance of early ontogenetic stages in fossil assemblages ally well-preserved co-occurring plankton and benthos (Landman et al., 1996). During their early evolutionary demonstrates that at least some Cretaceous ammonoids might history, ammonoids show a fast, progressive coiling, a size have lived and fed close to the seaﬂoor (Moriya et al., 2003). reduction of their embryonic shell and a synchronous trend Recent improvements in the precision and affordability of towards larger adult size in some lineages (Klug & Korn, 2004; isotopic studies should allow the generation of more data to see Fig. 2), which probably resulted in the increase of fecun-

Figure 5 Pathologies, stomach content and radula of ammonoids, adapted from Keupp (2000, 2012). (a) Neochetoceras sp. with aptychus at the bottom, parts of the siphuncle (grey arrow) preserved and within the body chamber crop content (black arrow) consisting mainly of Saccocoma (comatulid, crinoids), Upper Jurassic, Daiting, southern Germany, specimen about 13 cm in diameter (Coll. H. Keupp MAa73). (b) Crop content of Neochetoceras sp. mainly consisting of small Laevaptychi (black arrow) indicating that this specimen fed on small (?juvenile) ammonoids, Upper Jurassic, Eichstätt, southern Germany (Coll. H. Keupp MAa74). (c) Arnioceras sp. with radula teeth (black arrows) within the body chamber, Lower Jurassic (Sinemurian) from Yorkshire, image section about 3 mm (photo by H.J. Lierl). (d) Cleoniceras besairiei, Lower Cretaceous (Lower Albian), Madagascar (Ambatolaﬁa) showing characteristic stomatopod injuries (forma aegra fenestra), specimen about 77 mm in diameter (Coll. H. Keupp PA19138). (e) Serpenticone Dactylioceras athleticum Simpson with a ‘Bandschnitt’ injury caused by a benthic crustacean, Lower Jurassic (Toarcian), Schlaiffhausen, South-eastern Germany (Coll. H. Keupp PA-10338). ◀

the abundance of embryonic shells in a coprolite of a yet unidentified predator (Tanabe, Kulicki & Landman, 2008). A planktonic mode of life for hatchlings is supported by studies on their shells: buoyancy calculations within the error range of neutral buoyancy (Shigeta, 1993; Tanabe, Shigeta & Mapes, 1995), their common occurrence in dysoxic sediments, where they are associated with planktonic gastropods and little to no benthos (Mapes & Nützel, 2009), and their small size compared to the adults, similar to modern cephalopods that disperse as plankton (De Baets et al., 2012). The wide distribution of various loosely coiled or not-planispirally coiled heteromorphic ammonoids, which are interpreted to be poor swimmers, also supports the hypothesis of a wide transporta- tion by oceanic currents during the planktonic stage (Ward & Bandel, 1987; De Baets et al., 2012). The different geographical ranges of ammonoids with different shell morphologies and similar embryonic shell sizes, however, have been interpreted to indicate that at least some ammonoids could also have dispersed considerable distances later in their ontogeny (Brayard & Escarguel, 2013), similar to some modern coleoids. Whether or not ammonoids had a vast variety of reproductive strategies just like modern coleoids is poorly known, but various strategies also known from their extant relatives have been suggested for different ammonoids including egg-laying on the seafloor or on algae (Westermann, 1996), floating egg masses (Mapes & Nützel, 2009), broadcast spawning (Walton, Korn & Klug, 2010) or brood care up to hatching (Ward & Bandel, 1987). Etches, Clarke & Callomon (2009) have sug- dity (De Baets et al., 2012). Higher fecundity and mortality of gested benthic egg deposition of some Jurassic ammonoids derived ammonoids is supported by small hatchling size and like in modern Sepia; direct evidence for their ammonoid local occurrences of large numbers of preserved embryonic origin (like ammonoid remains inside the eggs) is, however, shells in the Late Devonian to Mesozoic (Landman et al., still missing. The smallest embryonic shells and the most 1996; Tomašových & Schlögl, 2008; De Baets et al., 2012). extreme cases of dimorphism (e.g. largest differences in Ammonoid hatchlings might have been an abundant food size – up to 15:1 – and morphology) occur in some source as indicated by the remains of smaller ammonoids in Jurassic ammonoids (such as Phlycticeras and Oecoptychius; the stomachs of larger ones (Keupp, 2000; see Fig. 5b) and by Schweigert & Dietze, 1998). Such examples are not rare and

Journal of Zoology 292 (2014) 229–241 © 2014 The Zoological Society of London 235 Pelagic palaeoecology of ammonoids K. A. Ritterbush et al. suggest that some derived ammonoids not only had a very composition of amino acids in their shells, as has recently been high fecundity, but possibly also performed brood care until performed for Spirula (Ohkouchi et al., 2012). hatching, analogous with some extant octopods (e.g. Synchrotron technology has increased the level of details Argonauta). It is important to note, however, that ammonoid known about the ammonoid mouth parts, which can help shells could not have been used as egg cases like in the modern constrain their capacity to process prey (Kruta et al., 2011). pelagic octopus Argonauta, which produces a brood chamber Many pre-Jurassic ammonoids had non-mineralized jaws that superficially resembles an ammonoid shell (Hewitt & similar to modern coleoid beaks, and a set of homodont or Westermann, 2003). Differential investment into reproduction heterodont radular teeth (Klug & Jerjen, 2012). In the Jurassic between males and females is interpreted in species with sexual and Cretaceous, many ammonoids had a mineralized lower dimorphism, which has been reviewed by Davis et al. (1996). jaw (aptychus) and an array of more complex radular teeth The smaller forms (microconchs) have been interpreted to be (Engeser & Keupp, 2002; Kruta et al., 2011; Tanabe et al., the males, whereas the larger forms (macroconchs) might be 2013; see Fig. 5c). In some, the buccal architecture is more the females because of the larger space for gonads (and thus similar to rare pelagic coleoids than to most other modern eggs) as well as occasional umbilical bulges (Landman et al., cephalopods (Kruta et al., 2011). The size and shape of both 2012). Not all ammonoids show a pronounced dimorphism teeth and jaws vary substantially, and this may prove to (Davis et al., 1996), and in some, the males might even have covary with phylogeny, shell shape or both (Kruta et al., 2011, been slightly larger than females (as in extant Nautilus: 2013; Klug et al., 2012; Tanabe et al., 2013). At least some Saunders & Landman, 1987). The large variability in ammo- lower jaws within two major ammonite lineages, the noid adult size and shape as well as differences in the extent of phylloceratids and lytoceratids, bore similarities to modern sexual dimorphism suggests that large differences in reproduc- and fossil nautilids. Tanabe et al. (2013) proposed that these tive strategies between different groups of ammonoids existed ammonoids convergently evolved a scavenging predatory (De Baets et al., 2012). feeding mode similar to modern Nautilus, but this awaits further corroboration from crop or stomach remains. Modern Constraints on predator–prey Nautilus feeds on small fish, crustaceans, nematodes, relationships echinoids and tentacles of other nautilids (as summarized in Tanabe et al., 2013). The diets of ammonoids can be reconstructed from crop and Evidence of predation on ammonoids is more difficult to stomach contents, coprolites, regurgitates (‘Speiballen’) and match to specific predator taxa. Apart from ammonoid bite marks. Ammonoids are usually interpreted as predatory remains within other ammonoids, ammonoid jaws have been [including scavenging (Tanabe et al., 2013) and cannibalism found in plesiosaur stomachs (Sato & Tanabe, 1998), but (Keupp, 2012)] like most extant and fossil cephalopods more frequently jaws and shell fragments are found in (Nixon, 1996). One of the only exceptions known so far is the coprolites of jawed fishes and as yet unidentified predators deep sea vampire squid (Vampyroteuthis), which, despite its (Mehl, 1978; Keupp, 2012). Successful or attempted predation daunting name, is a detritivore (Hoving & Robison, 2012). can also be interpreted from fatal and repaired damage marks The diet of Palaeozoic and Triassic ammonoids is poorly on ammonoid shells. It is usually difficult to assign such shell understood, whereas the assumed loss of the catch/bite func- injuries to a particular predator (Kröger, 2000; Klug, 2007; tion of jaws of post-Triassic aptychi-bearing ammonites Klompmaker, Waljaard & Fraaije, 2009), except in rare cases (‘Aptychophora’) and the morphology of the radula of some where predator and prey are found in association (Vullo, of these (Engeser & Keupp, 2002; Kruta et al., 2011) has been 2011), or the predator can be precisely deduced from shape used to suggest that they mostly fed on zooplankton. This is and position of the injuries (Martill, 1990; Mapes & Chaffin, largely supported by the rare ammonoid crop/stomach con- 2003; Keupp, 2006; Richter, 2009). Injuries attributed to tents as recently summarized in Kruta et al. (2011) and Keupp pelagic faunas include damage by sharks (in Carboniferous (2012), although small benthic prey items are also present. ammonoids; Mapes & Chaffin, 2003), jawed fishes (Martill, Prey items reported so far include Foraminifera, benthic 1990; Keupp, 2012), controversial mosasaur bite marks (on Malacostraca (eryonids), Ostracoda, Isopoda, stalkless Cretaceous ammonoids; e.g. Tsujita & Westermann, 2001) crinoids (see Fig. 5a), pseudoplanktic Bivalvia, planktonic and triangular bite marks typical for coleoids or nautilids Gastropoda and small ammonites (see Fig. 5b). Great caution (Keupp, 2012). In addition to establishing trophic specializa- has to be applied when interpreting such rare findings because tion, associations with benthic or pelagic predators and prey post-mortem transported remains, scavengers or gregarious can support or reject interpretations of ammonoid habitat. inhabitants (Kruta et al., 2011; Klompmaker & Fraaije, 2012) Small aperture pits attributed to stomatopod damage on shells might be confused with actual prey items. An exploitation of of platycones (Cleoniceras; see Fig. 5d) and planorbicones lower levels of the food chain (Kennedy & Cobban, 1976) (Desmoceras) would be consistent with their interpretation as would also be in line with the rather sluggish swimming capa- fitting a demersal life mode, but long slits attributed to scissor- bilities inferred for externally shelled cephalopods when com- bearing eryonid crustaceans on cadicones (Ptychites) and pared with coleoids and fishes (Jacobs & Chamberlain, 1996) serpenticones (Dactylioceras, Subolenekites, Pleuroceras, and the fast recovery of ammonoid diversity following extinc- Douvilleiceras; cf. Fig. 5e) would not match a planktonic inter- tion events (e.g. Brayard et al., 2009). Their position in the pretation for these shapes (cf. Fig. 3). Other biotic interactions food chain could potentially be tested by nitrogen isotope can also constrain information on ammonoid ecology

(Keupp, 2012). Epizoa living on the shell during the lifetime of needs to be considered in studies on extinctions, biostra- the ammonoid can give information about their orientation tigraphy and macroevolution of ammonoids. and position in the water column (e.g. Keupp et al. 1999). For example, Hauschke, Schöllmann & Keupp (2011) used the Acknowledgements distribution of a barnacle encrusted in vivo on a straight- shelled ammonoid to suggest a more horizontal orientation We would like to thank Helmut Keupp (FU Berlin) for sup- during swimming, which has also been independently inferred plying pictures and Christian Klug (University of Zürich) for from shell modelling (Westermann, 2013). It is clear from the proofreading a previous draft and supplying figures. We studies presented herein that interpretations of ammonoid greatly appreciate the thoughtful and constructive reviews by ecology for certain taxa and time frames cannot necessarily be two anonymous reviewers. David Button (University of generalized to other time frames or forms with similar shell Bristol) and Laura Wilson (The University of New South shapes. More data are necessary before such models can be Wales, Sydney) proofread a previous version of the paper. used to investigate local or global changes in diversity. References Ammonoid ecology and their extinction Alegret, L., Thomas, E. & Lohmann, K.C. (2012). End- Ammonoids (as well as belemnites with equally small embry- Cretaceous marine mass extinction not caused by produc- onic shells) went extinct after the Cretaceous Mass Extinction, tivity collapse. Proc. Natl. Acad. Sci. USA 109, 728–732. whereas nautilids with larger embryonic shells survived (Wani Arkhipkin, A.I. & Laptikhovsky, V.V. (2012). Impact of et al., 2011). The ammonoid extinction at the end of the Cre- ocean acidification on plankton larvae as a cause of mass taceous has often been attributed to their mode of life and extinctions in ammonites and belemnites. 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