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Recent advances in heteromorph ammonoid palaeobiology

January 2021
Biological reviews of the Cambridge Philosophical Society 96(3922):0-000

DOI:10.1111/brv.12669

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CC BY 4.0

Authors:

René Hoffmann

Ruhr University Bochum

Joshua Slattery

University of South Florida

Isabelle Kruta

Sorbonne University

Benjamin Linzmeier

University of South Alabama

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Heteromorphs are ammonoids forming a conch with detached whorls (open coiling) or non-planispiral coiling. Such aberrant forms appeared convergently four times within this extinct group of cephalopods. Since Wiedmann's seminal paper in this journal, the palaeobiology of heteromorphs has advanced substantially. Combining direct evidence from their fossil record, indirect insights from phylogenetic bracketing, and physical as well as virtual models, we reach an improved understanding of heteromorph ammonoid palaeobiology. Their anatomy, buoyancy, locomotion, predators, diet, palaeoecology, and extinction are discussed. Based on phylogenetic bracketing with nautiloids and coleoids, hetero-morphs like other ammonoids had 10 arms, a well-developed brain, lens eyes, a buccal mass with a radula and a smaller upper as well as a larger lower jaw, and ammonia in their soft tissue. Heteromorphs likely lacked arm suckers, hooks, tentacles , a hood, and an ink sac. All Cretaceous heteromorphs share an aptychus-type lower jaw with a lamellar calcitic covering. Differences in radular tooth morphology and size in heteromorphs suggest a microphagous diet. Stomach contents of heteromorphs comprise planktic crustaceans, gastropods, and crinoids, suggesting a zooplanktic diet. Forms with a U-shaped body chamber (ancylocone) are regarded as suspension feeders, whereas orthoconic forms additionally might have consumed benthic prey. Heteromorphs could achieve near-neutral buoyancy regardless of conch shape or ontog-eny. Orthoconic heteromorphs likely had a vertical orientation, whereas ancylocone heteromorphs had a near-horizontal aperture pointing upwards. Heteromorphs with a U-shaped body chamber are more stable hydrodynamically than modern Nautilus and were unable substantially to modify their orientation by active locomotion, i.e. they had no or limited access to benthic prey at adulthood. Pathologies reported for heteromorphs were likely inflicted by crustaceans, fish, marine reptiles, and other cephalopods. Pathologies on Ptychoceras corroborates an external shell and rejects the endocochleate hypothesis. Devonian, Triassic, and Jurassic heteromorphs had a preference for deep-subtidal to offshore facies but are rare in shallow-subtidal, slope, and bathyal facies. Early Cretaceous heteromorphs preferred deep-subtidal to bathyal facies. Late Cretaceous heteromorphs are common in shallow-subtidal to offshore facies. Oxygen isotope data suggest rapid growth and a demersal habitat for adult Discoscaphites and Baculites. A benthic embryonic stage, planktic hatchlings, and a habitat change after one whorl is proposed for Hoploscaphites. Carbon isotope data indicate that some Baculites lived throughout their lives at cold seeps. Adaptation to a planktic life habit potentially drove selection towards smaller hatchlings, implying high fecundity and an ecological role of the hatchlings as micro-and mesoplankton. The Chicxulub impact at the Cretaceous/Paleogene (K/Pg) boundary 66 million years ago is the likely trigger for the extinction of ammonoids. Ammonoids likely persisted after this event for 40-500 thousand years and are exclusively represented by heteromorphs. The ammonoid extinction is linked to their small hatchling sizes, planktotrophic diets, and higher metabolic rates than in nautilids, which survived the K/Pg mass extinction event.

Soft body reconstruction of an orthocone heteromorph. (A) Empty conch with body chamber and parts of the phragmocone. (B) Overlay image of conch and soft body with eyes and arms. (C) Reconstructed soft body with the digestive tract, buccal mass, and ovary. (D) Lower jaw of Aegocrioceras (Hauterivian, NW Germany). Scale bar = 1 cm. (E) Detailed parts of the buccal mass showing radula (E2) and upper and lower jaws (E1, E3). (F) Six morphological heteromorph archaetypes. Abbreviations used in A-C: arms, 10 arms of equal length without suckers or hooks; bc, body chamber; bm, buccal mass (see E for details); ca, caecum; cr, crop (covered by digestive gland); dg, digestive gland; drm, dorsal retractor muscle; fu, funnel; gi, gill; in, intestine; mc, mantle cavity; oe, oesophagus; os, ocular sinus; ov, ovary; ph, phragmocone; si, siphuncle; st, stomach.

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Raman image showing the distribution of aragonite (A) and polyenes (B) in the shell of modern Nautilus pompilius. Shell colouration, i.e. distribution of polyenes within the shell, is limited to the outer prismatic layer.

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Neutrally buoyant physical experiments on scaphitid heteromorph ammonoids. (A) Virtual model with complex internal geometry. (B) Modified virtual model for 3D printing. Bismuth counterweight corrects for differences in mass and stability between A and B. (C) 3D printed model showing counterweight and a control valve in case of flooding. (D) Neutrally buoyant model with proper hydrostastics and tracking points for hydrodynamic analyses. From Peterman et al. (2020a).

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Virtual hydrostatic models of heteromorphs with recurved body chambers at maturity. (A) Didymoceras nebrascense (Peterman et al., 2020b). (B) Audouliceras renauxianum (Peterman et al., 2020d). (C) Hoploscaphites crassus microconch (Peterman et al., 2020a). Tip of upper yellow cone, centre of buoyancy; tip of lower yellow cone, centre of mass. Scale bars = 3 cm.

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Palaeopathologies of heteromorphs. (A) Pictetia asteriana (Early Albian, Madagascar) with a band-slit pathology potentially caused by a benthic crustacean suggesting a demersal life habit of the ammonoid. Private collection of Wolfgang Grulke (Dorset, UK). (B) Aegocrioceras raricostatum (Hauterivian, NW-Germany) with a bulbous shell breakage. (C) Ptychoceras minimum (Late Aptian, Krasnodar region, Russia). Geological institute RAS, No. GIN MPC 5/2. Arrow indicates a healed sublethal injury on the second shaft of the conch. Post-traumatic inflation indicates damage of the shell-secreting mantle edge. (D) Proaustraliceras tuberculatum (Early Aptian, Ulyanovsk region, Russia). Private collection of Dmitry Vinogradov (Moscow), specimen No. 438. Arrow indicates a healed sublethal injury on the dorsal side of the conch likely produced by durophagous fish. (E) Ptychoceras minimum (Late Aptian, Krasnodar region, Russia). Geological institute RAS, No. GIN MPC 5/5. Feather-like wrinkles on the dorsal surface of the second shaft that start at the point of truncation of the first shaft. (F) Ptychoceras renngarteni (Late Aptian, Krasnodar region, Russia). Geological institute RAS, No. GIN MPC 5/1. Arrows mark healed sublethal injuries on the second shaft of the conch. (G) Aegocrioceras sp. body chamber (Hauterivian, NW-Germany) with a band-slit.

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Recent advances in heteromorph ammonoid

palaeobiology

René Hoffmann

*, Joshua S. Slattery

, Isabelle Kruta

, Benjamin J. Linzmeier

Robert E. Lemanis

, Aleksandr Mironenko

, Stijn Goolaerts

, Kenneth De Baets

David J. Peterman

and Christian Klug

Institut für Geologie, Mineralogie und Geophysik, Ruhr-Universität Bochum, Bochum, 44801, Germany

School of Geosciences, University of South Florida, 4202 East Fowler Ave., NES 107, Tampa, FL, 33620, U.S.A.

CR2P –Centre de Recherche en Paléntologie –Paris, UMR 7207, Sorbonne Université-MNHN-CNRS, 4 place Jussieu, case 104, Paris, 75005,

France

Department of Geoscience, University of Wisconsin - Madison, Madison, WI, 53706, U.S.A.

B CUBE –Center for Molecular Bioengineering, Technische Universität Dresden, Dresden, 01307, Germany

Geological Institute of RAS, Pyzhevski Lane 7, Moscow, 119017, Russia

OD Earth & History of Life, and Scientiﬁc Service Heritage, Royal Belgian Institute of Natural Sciences, Vautierstraat 29, Brussels, B-1000,

Belgium

GeoZentrum Nordbayern, Friedrich-Alexander University Erlangen-Nürnberg, Erlangen, 91054, Germany

Department of Earth and Environmental Sciences, Wright State University, 3640 Colonel Glenn Highway, Dayton, OH, 45435, U.S.A.

Paläontologisches Institut und Museum, Universität Zürich, Karl-Schmid-Strasse 4, Zürich, 8006, Switzerland

ABSTRACT

Heteromorphs are ammonoids forming a conch with detached whorls (open coiling) or non-planispiral coiling. Such

aberrant forms appeared convergently four times within this extinct group of cephalopods. Since Wiedmann’s seminal

paper in this journal, the palaeobiology of heteromorphs has advanced substantially. Combining direct evidence from

their fossil record, indirect insights from phylogenetic bracketing, and physical as well as virtual models, we reach an

improved understanding of heteromorph ammonoid palaeobiology. Their anatomy, buoyancy, locomotion, predators,

diet, palaeoecology, and extinction are discussed. Based on phylogenetic bracketing with nautiloids and coleoids, hetero-

morphs like other ammonoids had 10 arms, a well-developed brain, lens eyes, a buccal mass with a radula and a smaller

upper as well as a larger lower jaw, and ammonia in their soft tissue. Heteromorphs likely lacked arm suckers, hooks, ten-

tacles, a hood, and an ink sac. All Cretaceous heteromorphs share an aptychus-type lower jaw with a lamellar calcitic

covering. Differences in radular tooth morphology and size in heteromorphs suggest a microphagous diet. Stomach con-

tents of heteromorphs comprise planktic crustaceans, gastropods, and crinoids, suggesting a zooplanktic diet. Forms with

a U-shaped body chamber (ancylocone) are regarded as suspension feeders, whereas orthoconic forms additionally might

have consumed benthic prey. Heteromorphs could achieve near-neutral buoyancy regardless of conch shape or ontog-

eny. Orthoconic heteromorphs likely had a vertical orientation, whereas ancylocone heteromorphs had a near-

horizontal aperture pointing upwards. Heteromorphs with a U-shaped body chamber are more stable hydrodynamically

than modern Nautilus and were unable substantially to modify their orientation by active locomotion, i.e. they had no or

limited access to benthic prey at adulthood. Pathologies reported for heteromorphs were likely inﬂicted by crustaceans,

ﬁsh, marine reptiles, and other cephalopods. Pathologies on Ptychoceras corroborates an external shell and rejects the

endocochleate hypothesis. Devonian, Triassic, and Jurassic heteromorphs had a preference for deep-subtidal to offshore

facies but are rare in shallow-subtidal, slope, and bathyal facies. Early Cretaceous heteromorphs preferred deep-subtidal

to bathyal facies. Late Cretaceous heteromorphs are common in shallow-subtidal to offshore facies. Oxygen isotope data

suggest rapid growth and a demersal habitat for adult Discoscaphites and Baculites. A benthic embryonic stage, planktic

hatchlings, and a habitat change after one whorl is proposed for Hoploscaphites. Carbon isotope data indicate that some

Baculites lived throughout their lives at cold seeps. Adaptation to a planktic life habit potentially drove selection towards

*Address for correspondence (Tel: +492343223203; E-mail: rene.hoffmann@rub.de)

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium,

provided the original work is properly cited.

Biol. Rev. (2021), pp. 000–000. 1

doi: 10.1111/brv.12669

smaller hatchlings, implying high fecundity and an ecological role of the hatchlings as micro- and mesoplankton. The

Chicxulub impact at the Cretaceous/Paleogene (K/Pg) boundary 66 million years ago is the likely trigger for the extinc-

tion of ammonoids. Ammonoids likely persisted after this event for 40–500 thousand years and are exclusively repre-

sented by heteromorphs. The ammonoid extinction is linked to their small hatchling sizes, planktotrophic diets, and

higher metabolic rates than in nautilids, which survived the K/Pg mass extinction event.

Key words: cephalopods, heteromorph ammonoids, palaeobiology, anatomy, geochemistry, facies distribution

CONTENTS

I. Introduction .........................................................................2

II. Soft body reconstruction ................................................................3

(1) Buccal mass ...................................................................... 3

(a)Jaws ......................................................................... 3

(b)Radula ........................................................................ 5

(c)Enigmatic structures found in the body chamber ............................................. 5

(2) Muscle system .................................................................... 5

(3) Inksac .......................................................................... 6

(4) Digestive tract .................................................................... 6

(5) Shell colour patterns ............................................................... 7

III. Buoyancy and locomotion ...............................................................7

(1) Physical models ................................................................... 9

(2) Virtual models .................................................................... 9

IV. Ecological interactions .................................................................11

(1) Predators ....................................................................... 11

(2) Prey ........................................................................... 13

(3) Epizoa, parasites, and commensalism ................................................. 14

V. Habitat reconstruction ................................................................15

(1) Taphonomic controls on facies distributions ............................................ 15

(2) Life habit controls on facies distributions ............................................... 16

(3) Ecological requirements based on shell geochemistry ..................................... 18

(4) Reproduction ................................................................... 20

(5) Intraspeciﬁc variability ............................................................. 20

VI. Heteromorphs through time ............................................................21

(1) Devonian heteromorphs ........................................................... 21

(2) Triassic heteromorphs ............................................................. 23

(3) Jurassic heteromorphs ............................................................. 24

(4) Cretaceous heteromorphs and ammonoid extinction ..................................... 25

VII. Conclusions .........................................................................26

VIII. Acknowledgements ...................................................................27

IX. References ..........................................................................27

X. Supporting information ................................................................35

I. INTRODUCTION

Heteromorphs are ammonoids that are deﬁned by detached

whorls (open coiling) or non-planispiral coiling, and thus

deviate from the monomorph bauplan. The oldest mention

of the term ‘heteromorph’in relation to ammonoid shell

shape that we could identify is in Whitehouse (1926). Hetero-

morphy may occur at any growth stage and can be expressed

throughout ontogeny or be restricted to a single or a few

growth stages (cf. Wiedmann, 1969). Ammonoids with mod-

iﬁed apertures or angular coiling at the very end of their body

chambers due to morphogenetic countdown (sensu Seila-

cher & Gunji, 1993) are not classiﬁed as heteromorphs.

Heteromorphy occurred in many evolutionary lineages,

and thus by deﬁnition, the term ‘heteromorph ammonoid’

forms a polyphyletic ‘grouping’. Heteromorphy appeared

multiple times during the history of ammonoids, beginning

with the ﬁrst ammonoids in the early Devonian to their very

end at the Cretaceous/Paleogene boundary (see Section VI).

Heteromorphy was most common in the Cretaceous, which

is the reason why many textbooks identify heteromorphs

(only) as Cretaceous Ancyloceratina, and why most of the

available data on their palaeobiology comes from Cretaceous

examples. Only Cretaceous heteromorphs show an impor-

tant modiﬁcation of the suture line, namely a reduction from

ﬁve to four lobes in the primary suture line, which was used

2René Hoffmann et al.

by earlier workers to deﬁne them as a monophyletic group

(Korn et al., 2003), an outdated idea that is strictly rejected

herein. It was also the diversity of ‘aberrant’forms during

the Cretaceous that was used in the outdated hypothesis of

degeneration (‘typolysis’) to explain the cause of their extinc-

tion (Schindewolf, 1936; Wiedmann, 1969; Korn, 2003).

Some of their complex conch shapes (conch refers to the

entire skeleton, shell refers to the material) without apparent

streamlining have been used to argue for an immobile ben-

thic or pseudoplanktic life habit for ammonoids (Arkhipkin,

2014), an interpretation that was fuelled by the rapid replace-

ment of loosely coiled (heteromorph) forms by tightly coiled

(monomorph) ammonoids during their early evolution in

the Devonian (e.g. Klug & Korn, 2004; De Baets et al.,

2012; Klug et al., 2015a). It is now widely accepted that het-

eromorphs independently and convergently evolved from

different phylogenetic lineages during the Triassic, Jurassic,

and multiple times during the Cretaceous (Cecca, 1997).

Evolutionary relationships within the heteromorphs, particu-

larly during the Cretaceous, require reﬁnement (Wright,

Callomon & Howarth, 1996; Kaplan, 2002). To what degree

heteromorphs had comparable life habits is still debated, but

is crucial for understanding their radiations, evolutionary

successes, and extinctions during each period.

Here, we review the currently known constraints of hetero-

morph palaeobiology and ecology using a wide range of

approaches to disentangle the factors driving the organisa-

tion and evolution of heteromorph conch shapes within

Ammonoidea.

II. SOFT BODY RECONSTRUCTION

Remains of soft parts are rarely preserved in ammonoids

(e.g. Closs, 1967a,b). However, two reported cases come from

heteromorphs, namely trochospiral Allocrioceras (Wippich &

Lehmann, 2004; Keupp, Saad & Schweigert, 2016b) and

orthoconic Sciponoceras (Klug, Riegraf & Lehmann, 2012;

Klug & Lehmann, 2015). In these genera, remains of the

digestive tract including the oesophagus (well preserved due

to its original chitinous cover), crop, and stomach are pre-

served as thin organic sheets (Fig. 1).

Klug et al. (2012) and Klug & Lehmann (2015) proposed

that structures surrounding the oesophagus of Sciponoceras

might represent phosphatised parts of the cephalic cartilage

with the eye capsules. Both phylogenetic bracketing with

nautiloids and coleoids (Witmer, 1995; Klug et al., 2015a,

2019; Shigeno et al., 2018) and the limited fossil evidence sug-

gest the presence of a well-developed brain in these hetero-

morphs. We speculate that the evolution of the nervous

system in cephalopods was linked with the need to control

their position in space and to handle information from sen-

sory systems like eyes and statocysts (sensory receptors for

balance and orientation).

Phylogenetically, ammonoids are positioned between nau-

tilids with their pinhole camera eye and coleoids with a lens

eye. The shared ancestry of ammonoids and coleoids

(derived from bactritids; Kröger, Vinther & Fuchs, 2011),

and their potential for a more active lifestyle similar to

coleoids, suggests that ammonoids had lens eyes. Putative

eye capsules are relatively large in Sciponoceras, suggesting

the presence of large eyes in baculitids (Klug et al., 2012;

Klug & Lehmann, 2015), which is supported by deep lateral

sinuses on their apertures providing structural space for large

eyes useful for an active lifestyle.

The number, shape, and proportions of the arms ammo-

noids possessed are subject to ongoing debate. Structures

anterior to the jaws in Sciponoceras (Klug et al., 2012; Klug &

Lehmann, 2015) might represent arm bases. Various authors

have suggested that the arms of heteromorphs were short

(Landman, Cobban & Larson, 2012a). Klug et al. (2015a)

applied phylogenetic bracketing (Witmer, 1995), and argued

that it is most parsimonious to assume that all ammonoids

including heteromorphs had 10 arms (Klug & Lehmann,

2015). The same line of reasoning suggests that ammonoid

arms lacked suckers and hooks (but see Section II.1c), and

that they had no tentacles (extendable extremities longer

than the arms), which is weakly supported by the absence of

fossil evidence of these structures. Clements et al. (2017)

found that members of the clade comprising modern

10-armed cephalopods (sepiids and squids) decompose faster

as a function of their higher ammonia content, therefore con-

necting coleoid cephalopod taphonomy with physiology.

Thus, the scarcity of soft-part preservation in ammonoids

could be linked to both the ammonia content of their soft

parts and that potentially preserved soft parts are often cov-

ered by shell remains.

Closs (1967a,b) interpreted ammonoids as possessing a

hood, but re-examination of his Carboniferous material sug-

gests a misidentiﬁcation of a shell fragment situated near the

aperture as a hood (Lehmann, Klug & Wild, 2015). Using

phylogenetic bracketing and information from the embry-

onic development of modern nautilids Shigeno et al. (2008)

and Shigeno, Sasaki & Boletzky (2010) suggest that the hood

is derived from Anlagen (developmental foundation) of the

arm crown which is absent in ammonoids.

(1) Buccal mass

(a) Jaws

The buccal apparatus is known for several Ancyloceratina,

and in the Ammonitina for Spiroceras (Tanabe, Kruta &

Landman, 2015a) (see online Supporting Information,

Table S1). It follows the general pattern of ammonoid jaws:

a smaller upper jaw nested within a larger lower jaw (Fig.

1E). The upper jaw is conservative in ammonoids and has a

blunt rostrum with inner lamellae for the support of the mus-

cular tissue split into two rounded wings (Tanabe et al.,

2015a). Lower jaws are morphologically variable with differ-

ent shapes, ornamentation, and microstructure of the calcitic

covering. Most heteromorphs have an aptychus-type jaw

with a central commissure (symphysis) dividing the lower

Heteromorph ammonoid palaeobiology 3

Fig. 1. Soft body reconstruction of an orthocone heteromorph. (A) Empty conch with body chamber and parts of the phragmocone.

(B) Overlay image of conch and soft body with eyes and arms. (C) Reconstructed soft body with the digestive tract, buccal mass, and

ovary. (D) Lower jaw of Aegocrioceras (Hauterivian, NW Germany). Scale bar =1 cm. (E) Detailed parts of the buccal mass showing

radula (E2) and upper and lower jaws (E1, E3). (F) Six morphological heteromorph archaetypes. Abbreviations used in A–C: arms,

10 arms of equal length without suckers or hooks; bc, body chamber; bm, buccal mass (see E for details); ca, caecum; cr, crop

(covered by digestive gland); dg, digestive gland; drm, dorsal retractor muscle; fu, funnel; gi, gill; in, intestine; mc, mantle cavity;

oe, oesophagus; os, ocular sinus; ov, ovary; ph, phragmocone; si, siphuncle; st, stomach.

4René Hoffmann et al.

jaw into two valves lacking a sharp rostral tip. In Criocerati-

dae, the symphysis is poorly expressed and due to this fact,

their jaws are interpreted by some authors as an

anaptychus-type jaw (Engeser & Keupp, 2002). In contrast

to an anaptychus interpretation, Tanabe et al. (2015a) consid-

ered the crioceratid lower jaws as the inner chitinous lamella

of the aptychus. Later, Rogov & Mironenko (2016) reported

Hauterivian praestriaptychi associated with early criocera-

tids (Criosarasinella and Crioceratites) suggesting that one of

these taxa had an aptychus-type jaw (praestriaptychus, see

Table S1).

In the aptychus-type lower jaw, the surface is covered by a

calcitic layer either with a striated surface (praestriaptychus

and striaptychus) or with rugae (rugaptychus). The outline

of the lower jaw spread open matches the shape of the whorl

cross section (Baculites,Scaphites), which led to the suggestion

that this structure had an opercular function. By contrast,

Larson & Landman (2017) and Landman & Waage (1993b)

argued that the jaws of Baculites, even when fully splayed

out, did not touch the inner surface of the conch tube.

Accordingly, they rejected an operculum function of the

lower jaw in Baculites. Parent, Westermann & Chamberlain

jr. (2014) suggested that lower jaw types like praestriaptychus

and striaptychus could fulﬁll multiple functions: lower man-

dible, operculum, ﬁltering device, ﬂushing benthic prey,

pumping for jet propulsion and stabilizing against pitching

[for praestriaptychus see Parent et al. (2014) and Tanabe

et al. (2015a)].

The microstructure of the calcitic covering of aptychi varies

in ammonoids between tubular and lamellar [Farinacci et al.

(1976); see Kruta et al. (2009) for heteromorphs]. The calcitic

covering in all Cretaceous heteromorph jaws is lamellar. In

Baculites, the calcitic covering can reach 1 mm in thickness

and two main layers have been described (R1 and R2) consist-

ing of overlapping thin (3 μm thickness) calcitic increments

(Kruta et al., 2009). The aptychus is 0.5 mm thick in Hoplosca-

phites and 0.03 mm in Polyptychoceras without ornamentation.

(b) Radula

The use of tomographic techniques on three in situ Baculites

radulae allowed description of their jaw apparatus (Kruta

et al., 2011). The radular ribbon lies between the upper and

lower jaws. Each tooth row of the radula is composed of nine

elements (one central tooth, two pairs of lateral teeth, one

pair of marginal teeth, and one pair of marginal plates)

(Fig. 1E). The central rachidian tooth and the two pairs of lat-

eral teeth are delicately multicuspidate, while the marginal

tooth is long and sabre-like. The same radula composition

and morphology was revealed for a baculitid (?Sciponoceras)

from the Late Cretaceous of Germany (Klug et al., 2012).

Multicuspidate radular teeth found in situ in Rhaeboceras have

been described by Kruta et al. (2013) and Kruta, Landman &

Tanabe (2015). The only other report (see Table S1) of a rad-

ula from heteromorphs is from a Spiroceras (Tanabe et al.,

2015a) but the number of radular teeth per row and their

morphology remains unknown.

Cuspidate structures associated with jaws have been found in

the body chamber of several species of well-preserved hetero-

morphs and re-coiled scaphitids. Landman & Waage (1993b)

described bicuspidate structures in two Maastrichtian species

from South Dakota: Hoploscaphites spedeni and H. nicolletii.

Kennedy et al. (2002b) documented similar cuspidate struc-

tures in Rhaeboceras halli, a re-coiled scaphitid from the Cam-

panian of Montana, and interpreted them as radular teeth.

Kruta et al. (2013) rejected this interpretation after ﬁnding

actual radular teeth in three specimens of R. halli. These in situ

teeth match the size and morphology of radular teeth known

from other aptychophoran ammonoids (Kruta et al., 2015;

Keupp et al., 2016a). Landman et al. (2013) documented addi-

tional structures associated with H. gilberti from the Campa-

nian of South Dakota. Ongoing studies are characterising

the diverse morphology of these enigmatic structures in

R. halli (Kruta et al., 2019) and their function in scaphitids,

e.g. hooks on the hectocotylised arm.

(2) Muscle system

Although there is no unequivocal report of fossilised muscles

from ammonoids we can make inferences about their muscle

system (Doguzhaeva & Mapes, 2015). Based on dimensions

of attachment scars, the cephalic retractor muscles inserted

at the largest postero-lateral attachment sites. However, Mir-

onenko (2015b) argued that these muscles were attached dor-

sally with the nuchal retractors in Jurassic ammonoids like

Kachpurites. In his opinion, the hyponome muscles inserted

laterally in the annular elevation or the lateral sinus. Miro-

nenko (2015b) proposed that the collar was attached laterally.

Mironenko’s (2015b) interpretation of their function and

homology with muscles in nautilids and coleoids raises sev-

eral questions, which cannot yet be fully answered given the

paucity of available anatomical information.

(1) Does the arrangement of the main muscles in ammo-

noids correspond to that of modern Nautilus? Jacobs &

Landman (1993, p. 101) stated that Nautilus is in some

respects “a poor model for the function and behaviour

of ammonoids”, but is the only living ectocochleate

cephalopod for comparison. Nevertheless, in the

absence of coleoids with chambered conchs and a long

body chamber, Nautilus represents one of the most

important living relatives used to reconstruct ammo-

noid palaeobiology. Jacobs & Landman (1993) support

Mironenko’s (2015b) interpretation of a dorsal inser-

tion of retractor muscles. The muscle attachment pat-

terns of Audouliceras renauxianum from the Russian

Cretaceous ﬁgured in Doguzhaeva & Mapes (2015,

Figs. 14.1–14.4) may support this hypothesis, because

there are large dorsoventral (umbilical) ‘tongue-like

marks’. In this ancylocone, the adult body chamber

forms a characteristic hook. To enhance efﬁciency of

the retractor muscles, the distance to the head must

be minimised. Due to the curve in the adult body

Heteromorph ammonoid palaeobiology 5

chamber, a posterior insertion of straight cephalic

retractors is impossible. By contrast, an anterior inser-

tion of retractor muscles would have reduced the

length of these muscles, thereby increasing their efﬁ-

ciency. Nevertheless, this homologisation requires fur-

ther evidence. Ultimately, we will have to await

specimens preserving remains of the musculature.

(2) Are coleoid muscles homologous with ammonoid mus-

cles? Homology of the mantle in coleoids (cf. Jacobs &

Landman, 1993; Fuchs et al., 2016) with that of ammo-

noids is likely. However, it is also probable that the

ammonoid mantle could not serve the same purposes

as in coleoids because of the external conch. The man-

tle secretes the mineralised hardparts (ectocochleate or

endocochleate) in most cephalopods, except for Argo-

nauta. Klug et al. (2008) proposed that the mantle mus-

culature in ammonoids enabled the animal to move its

soft parts within the body chamber. Jacobs & Landman

(1993) suggested that the mantle played an active role

in swimming. This assumption would support a mod-

erately thick mantle with the potential to be fossilised,

which has yet to be reported. The homologisation of

other muscles would require soft tissue preservation.

(3) Did ammonoids have a collar like coleoids? Miro-

nenko (2015b) found a lateral soft tissue attachment

site close to the aperture and suggested that the collar

and funnel-locking apparatus attached at this site.

The soft tissues were presumably attached to the body

chamber wall anteriorly and posteriorly. The presence

of a nuchal and funnel cartilage in Nautilus and Sepia

implies that these were also present in ammonoids. If

we accept the intermediate position of ammonoids

between nautilids and coleoids with respect to locomo-

tory abilities, we can assume that the funnel was some-

what stiff and could be locked ﬁrmly near the aperture

to maximise the thrust of the hyponomic water jet.

Although fossil remains of the nuchal cartilage have

been reported from coleoids (Klug et al., 2016), they

have not been found in ammonoids.

We conclude that ammonoids likely had paired cephalic

and hyponome retractor muscles, a ventral muscle, and man-

tle musculature. Since ammonoid muscles are not preserved

well enough (only a few doubtful remains), homologisation

of ammonoid muscles and their attachment sites with those

of coleoids and nautilids remains uncertain. Conch morphol-

ogy of heteromorphs and the likely arrangements of muscles

in their body chambers suggest that their locomotory abilities

were limited compared to most modern coleoids because of

the indirect action of the main muscles. Efﬁciency of the mus-

cle system and the locomotory apparatus probably improved

towards the end of their lives, which is achieved through the

commonly widened body chamber and the more horizontal

orientation of the adult aperture. This ontogenetic change

in orientation allowed the approximate horizontal alignment

of the jet with the centre of mass (e.g. Klug, 2001; Klug &

Korn, 2004).

(3) Ink sac

There are four categories of colour or light display in ani-

mals: (i) pigments, (ii) bioluminescence, (iii) structural colours,

and (iv) liquid crystals. While the ink of modern coleoids is

made of the pigment melanin, coleoids also evolved biolumi-

nescence such as in the photophore of Spirula spirula. Some

cephalopod light organs are also situated within the ink sac,

for example in Sepiola atlantica (Herring et al., 1981). Struc-

tural colour is present as mirrors in photophores composed

of collagen ﬁbres forming a multilayer reﬂector e.g. in Seleno-

teuthis,Abralia,orEnoploteuthis (Parker, 2000). Reports on fos-

silised colour mostly refer to the presence of pigments in

shells or the ink sac (e.g. Roy et al., 2020).

Melanin macromolecules are classiﬁed into eumelanins

(black) that contain nitrogen and pheomelanins (broad col-

our range: yellow-red-brownish) containing sulfur (Schäfer,

2013). Melanins are stored in melanosomes, speciﬁc cell

organelles of pigment cells that share the size and shape of

bacteria (Lindgren et al., 2012). Identiﬁcation of melanin

based on structural information can be misleading. In addi-

tion, the presence of melanin in soft tissues such as visual sys-

tems (Schäfer, 2013), liver (Scalia et al., 1990), or others

(Wakamatsu & Ito, 2002) complicates the recognition of ink

in fossil cephalopods.

Reports of ink sacs in ammonoids by Lehmann (1967) for

Eleganticeras, Mathur (1996) for Eopsiloceras, and Wetzel (1969)

for Bochianites have been discarded by subsequent researchers

(Wippich & Lehmann, 2004; Klug & Lehmann, 2015). Doguz-

haeva et al. (2004) interpreted bituminous matter in ﬂattened

ammonoid body chambers of Austrachyceras as ink sacs. This

interpretation is rejected here because modern ectocochleate

cephalopods lack an ink sac and melanin occurs in other

ammonoid structures such as the black layer (Klug et al.,

2004). Unequivocal evidence for fossil ink and ink sacs are com-

moninfossilcoleoidsfromtheCarnianAustrianRheingraben

Shale, the German Posidonia Shale (Toarcian), German plat-

tenkalks (Kimmeridgian–Tithonian), and Lebanese platten-

kalks (Cenomanian) as summarised by Schäfer (2013), but are

absent in co-occurring ammonoids. Raman spectroscopy

revealed the presence of the typical melanin spectra, revealing

the effect of the carbonate matrix or the presence of iron on

these spectra (Schäfer, 2013). This method is recommended

to test for the presence of ink and related structures in hetero-

morphs (see Section II.5).

(4) Digestive tract

Fossil remains of the digestive tract (except the buccal mass;

Section II.1; Fig. 1B, C) have been documented from the het-

eromorphs Allocrioceras (Wippich & Lehmann, 2004) and Sci-

ponoceras (Klug et al., 2012; Klug & Lehmann, 2015). In both

cases, ﬂattened specimens with dissolved conchs preserve

organic remains of crop and stomach. In Allocrioceras

(Wippich & Lehmann, 2004) from the Cenomanian of Leba-

non, the remains of the digestive tract lie far behind the buc-

cal mass, suggesting that it is the stomach and not the crop. In

6René Hoffmann et al.

the case of Sciponoceras from the Cenomanian–Turonian

boundary in Germany, carbonised impressions show details

of the digestive tract (Klug et al., 2012; Klug & Lehmann,

2015). It begins with the oesophagus, which was identiﬁed

based on its elongate shape and its spatial association with

the buccal mass. Posteriorly, the digestive tract displays a

swelling, which probably represents the elongate crop, which

is known to be large in cephalopods. The elongate crop in Sci-

ponoceras is likely linked with the long body chamber in bacu-

litids. A third, further posteriorly situated elongate structure

found in Sciponoceras was interpreted as the stomach by Klug

et al. (2012).

(5) Shell colour patterns

Shell colour patterns in molluscs can be the result of pigments

or of structural colour (see Section II.3). Identiﬁcation of true

colour patterns including bands and spots is complicated by

the existence of false colour patterns, which often run parallel

to growth lines and shell thickening. Klug et al. (2012)

reported on false colour patterns, which are related to growth

halts (megastriae) accompanied by faint ribs and the secre-

tion of melanin along transverse stripes (parallel to former

apertures). Muscle attachment structures can also result in

dark patches mimicking colour patterns regarded herein as

pseudo colour patterns.

The oldest true colour patterns in ammonoids were

described from a monomorph from the Early Triassic Crit-

tenden Springs Lagerstätte (Mapes & Sneck, 1987), although

there are reports of colour patterns for Palaeozoic nautiloids

(Manda & Turek, 2009a,b, 2015) and one Devonian ammo-

noid (Ebbighausen et al., 2007). In mollusc shells, polyenes

like carotenoids represent most shell pigments as outlined

by Hedegaard, Bardeau & Chateigner (2006) and Barnard &

de Waal (2006) using in situ Raman spectroscopy. Mapes &

Larson (2015) reported true colour patterns from Hoplosca-

phites nicolletii and H. reesidei. In both species, longitudinal iri-

descent bands are preserved in nacre. This colour pattern is

a structural colour with multilayer reﬂectors, where the

nanometer thick nacre tablets fulﬁll the Bragg condition for

diffraction. Bragg diffraction by a crystal lattice occurs when

radiation (e.g. X-rays or light) with a wavelength comparable

to atomic spacing is scattered from the lattice plane undergo-

ing constructive interference (Bragg & Bragg, 1913). These

structural colours are comparable to the colours of butterﬂy

wings, gold bugs, polychaetes, and ﬁsh (Parker, 2000; Par-

ker & Martini, 2006). Based on transmission electron micros-

copy analyses, Snow et al. (2004) described a new type of

structural colour of nacre, the edge-band structure, which

produces interference colours. These are characteristic for

different widths of the edge-band structure ranging from sil-

ver tones (74 nm) to creams (80 nm) to yellow and gold (90

nm) in bivalve pearls. The same phenomenon could be

responsible for structural colours in ammonoids (Keupp,

2005; Mapes & Larson, 2015). Keupp (2005) suggested that

spiral bands resulted from original pigment-based colour

patterns in the outer prismatic layer. It is noteworthy that

the polyene pigments in modern Nautilus are restricted to

the outer prismatic layer (Fig. 2). These colour patterns can

be traced in the uppermost part of the underlying nacreous

layer due to minute differences in ultrastructure. This is

important because most ammonoids lack a preserved outer

prismatic layer. For example, spot patterns in Jurassic amalt-

heid ammonoids (Schindewolf, 1928, 1931) are visible after

the dark (pyrite) spots are lost. Mironenko (2015a) reported

on remnants of radial pigment-based colour patterns coin-

ciding with temporary apertures, representing an example

of false colour patterns.

Externally shelled (ectocochleate) cephalopods with longi-

tudinal bands fall into the planktic–vertical migrant life habit.

By contrast, spiral structural colour patterns, like in Quensted-

toceras, have been suggested to indicate a potential demersal

life habit (Keupp, 2005). Relationships between conch form,

biofacies, and colour patterns have been discussed for broad

longitudinal colour patterns on orthocone Palaeozoic nauti-

loids (Manda & Turek, 2009b). Turek & Manda (2011)

described zig-zag or wave-like transverse colour patterns of

the cyrtoconic barrandeocerids Peismoceras and Phragmoceras

as well as the oncocerids Octameroceras and Pentameroceras.

Manda & Turek (2009a)ﬁgured a similar zig-zag or wave-

like transverse colour pattern for the cyrtoconic Silurian

oncocerid Euryrizocerina, which was likely demersal. A marked

polymorphism in colour patterns has been described for

modern Nautilus (Ward et al., 1977), Quenstedtoceras (Keupp,

2005), and the Silurian nautiloid Phragmoceras (Turek &

Manda, 2011) suggesting a camouﬂage function. In this

regard, the suggestion by Balinski (2010) that marine inverte-

brates that exhibit colour patterns usually live no deeper than

200 m (photic zone) is convincing.

III. BUOYANCY AND LOCOMOTION

The bizarre morphology of many heteromorphs invites specu-

lation on the function of these convoluted conchs, which are

often considered to be poor swimmers that evolved from more

streamlined monomorphs (Jacobs, Landman & Chamberlain,

1994; Monks & Young, 1998; Mikhailova & Baraboschkin,

2009). Functional morphological work has focused on buoy-

ancy and hydrostatics to determine what life habits, typically

adult, heteromorph conch shapes might have permitted. It is

widely accepted that most ectocochleate cephalopods were

nearly neutrally buoyant during life regardless of conch shape

or ontogeny. This was controlled by adding ﬂuid to a positively

buoyant conch or counteracting slightly negative buoyancy

through swimming (Denton & Gilpin-Brown, 1966; Klinger,

1981; Lukeneder, 2012; Hoffmann et al., 2015; Lemanis

et al., 2015; Tajika et al., 2015; Peterman, Barton &

Yacobucci, 2019a; Peterman et al., 2020a,b). Thus, neutral

buoyancy is usually assumed for hydrostatic analyses, although

some authors have proposed a mobile benthic to nektobenthic

life habit for some heteromorphs (e.g. Wiedmann, 1973b;

Heteromorph ammonoid palaeobiology 7

Fig. 2. Raman image showing the distribution of aragonite (A) and polyenes (B) in the shell of modern Nautilus pompilius. Shell

colouration, i.e. distribution of polyenes within the shell, is limited to the outer prismatic layer.

8René Hoffmann et al.

Kakabadze & Sharikadze, 1993). These analyses can utilise

both physical and virtual models.

(1) Physical models

Physical models include the construction of a physical replica

of the conch that is immersed in ﬂuid. Reyment (1973) was

among the ﬁrst to use physical models to examine static

conch orientation, although these experiments were designed

to understand post-mortem drift rather than life orientation,

hence soft tissue was not considered. To determine life orien-

tation, differentiation between phragmocone and body

chamber densities must be replicated to reconstruct the posi-

tions of the centres of volume (buoyancy) and mass (gravity).

Ward (1976) used microcrystalline sculpting wax to create

models of the heteromorphs Glyptoxoceras subcompressum,Didy-

moceras elongatum,Ryugasella ryugasensis,Pseudoxybeloceras nanai-

moense,Baculites inornatus, and B. anceps paciﬁcus. Density

differences were achieved by adding carborundum (silicon

carbide), metal powder, and lead or solder strips to the

wax. G. subcompressum likely had the most signiﬁcant changes

in aperture orientation in early ontogeny during a switch

from orthoconic to torticonic to gyroconic coiling with less

variation in aperture orientation in the gyroconic stage.

D. elongatum showed a stable aperture orientation during the

growth of the torticonic conch with the ﬁnal growth stage

showing a slight upwards turn of the aperture. The orthoco-

nic B. inornatus,B. anceps paciﬁcus, and ancylocone R. ryugasensis

had a vertical conch orientation with the aperture directed

downwards. P. nanaimoense with its ancylocone conch showed

the greatest variation of orientation through ontogeny with

the aperture changing by up to 180, similar to the hamiti-

cone Dissimilites that was investigated virtually (Lukeneder,

2012). A vertical orientation of orthoconic heteromorphs is

a common result in both physical and virtual models

(e.g. Trueman, 1941; Westermann, 1977; Peterman et al.,

2019a,b). A ﬂooded apex of the phragmocone, however,

might have allowed the animals to achieve a more horizontal

orientation temporarily. This hypothesis was tested by Wes-

termann (2013) using models of Baculites composed of plexi-

glass and styrofoam with iron weights used to simulate

different weight distributions. Westermann (2013) conﬁrmed

the possibility of such conchs achieving a roughly horizontal

orientation and proposed a potential ontogenetic shift from a

vertical to a subvertical conch orientation following the

growth of conch curvature and re-ﬂooding of parts of the

phragmocone. Peterman et al. (2019b) simulated an apically

ﬂooded Baculites that was not able to deviate from a vertical

orientation while remaining neutrally buoyant. Experiments

on physical models with the same hydrostatic properties as

their virtual counterparts support a stable vertical posture.

The models represent density-corrected, neutrally buoyant

three-dimensional prints of reconstructed cephalopod

conchs (Peterman et al., 2019a,b, 2020a). These weighted

models (Fig. 3) allow the approximate analysis of the restor-

ing moment and hydrodynamic drag during rotational and

translational movement. Changes in conch orientation

during evolution from orthocones to early ammonoids were

investigated by balancing sculpted models of the whole conch

and the isolated body chamber to determine the relative posi-

tions of the centres of mass and buoyancy (Klug & Korn,

2004). They found an evolutionary shift from the aperture

horizontally pointing downwards (Bactritida) via oblique

apertures (early heteromorphs) to a near horizontal aperture

facing upwards (derived monomorphs), which implies an

increase in swimming velocity and manoeuvrability.

(2) Virtual models

Virtual models include mathematical models and simulated

conchs, either generated ex nihilo or from tomographic data

(Hoffmann et al., 2014; Naglik et al., 2015; Lemanis,

Zachow & Hoffmann, 2016; Naglik, Rikhtegar & Klug,

2016; Hebdon, Ritterbush & Choi, 2020). Trueman (1941)

ﬁrst attempted to calculate the buoyancy and hydrostatic ori-

entation of several heteromorph conchs, taking the body

chamber length versus total conch length into account. Plani-

spiral to gyrocone Crioceras ﬁssicostatum,C. duvali,andC. mulsanti

were calculated with a sub-vertical aperture orientation,

whereas the planispiral Macroscaphites yvani,Scaphites aequalis,

and Oecoptychius sp. were calculated with a near-horizontal

aperture that pointed upwards. Trueman (1941) and later

authors (e.g. Klinger, 1981; Westermann, 1996; Peterman

et al., 2020a) noted that the uncoiling of the conch has the

tendency to increase the distance between the centre of

buoyancy and the centre of mass, thereby increasing the

conch’s hydrodynamic stability (its tendency to resist changes

in orientation). Tanabe (1975) calculated the buoyancy for

Otoscaphites by volume approximations based on coiled coni-

cal geometries and the equations of Raup (1973). Otoscaphites

had a negative buoyancy that was interpreted as a shift

through the group’s evolutionary history from a benthic to

a nektoplanktic habitat. Ward & Westermann (1977) calcu-

lated the buoyancy of the vermicone Nipponites occidentalis

based on conch length, radius, cross-sectional area, and sev-

eral corrective factors to account for ornamentation, septa,

and the siphuncle. They interpreted N. occidentalis as being

planktic due to its near-neutral buoyancy, lack of hydrody-

namic streamlining or perceived adaptations to a benthic life

habit (shell thickening, reduction in sutural complexity). The

assumption of neutral buoyancy has a strong impact on

reconstructed orientations. This impact was shown for differ-

ent heteromorphs with both neutral and negative buoyancy

(Okamoto, 1988b; Okamoto & Shibata, 1997; Higashiura &

Okamoto, 2012). On the basis of simulated conchs, Oka-

moto argued for a nektobenthic life habit, in some cases with

the conch occasionally resting on the sea ﬂoor like the torti-

cone Eubostrychoceras muramotoi, the ancylocone Polyptychoceras

pseudogaultinum, and torticone nostoceratids (Okamoto,

1988b; Okamoto & Shibata, 1997; Higashiura & Okamoto,

2012). But he agreed with Ward & Westermann (1977) that

Nipponites had a near-neutral buoyancy and a planktic life

habit (Okamoto, 1988a).

Heteromorph ammonoid palaeobiology 9

Olivero & Zinsmeister (1989) calculated a positive buoy-

ancy and near-horizontal upwards aperture orientation for

the heteromorph Diplomoceras maximum.Diplomoceras is a hami-

ticone (paperclip-like ancylocone subtype) heteromorph sim-

ilar in morphology to the proposedly negatively buoyant

Polyptychoceras (Okamoto & Shibata, 1997). The role of the

U-shaped body chamber of some heteromorphs was tested

by Kaplan (2002) who abstracted the complex conch shapes

into simpler geometric forms (e.g. cones, cylinders, tori) to

calculate volumes, surface areas, and centres of mass and vol-

ume. Kaplan (2002) also took into account the effect of par-

tial phragmocone reﬁlling and alterations of the centre of

mass of the soft body due to movement within the body

chamber (Monks & Young, 1998). Kaplan (2002) found that

only heteroconic (combination of torticone and ancylocone)

conchs could consistently attain an orientation that would

allow them to feed on benthos; scaphiticones and praviti-

cones (a combination of planispiral and ancylocone) showed

limited access to benthos through manipulation of the ﬁll

fraction of the phragmocone, while ancylocones and hamiti-

cones showed no easy access to benthic prey regardless of

orientation modiﬁcation. This analysis challenged the idea

that the evolution of the U-shaped body chamber was an

adaptation for a benthic life habit. Landman et al. (2012a)

agreed with this interpretation by arguing for a more passive,

ﬁlter-feeding strategy for Scaphites.

Heteromorphs with a U-shaped body chamber (nosto-

cones, scaphiticones, ancylocones; Fig. 4) are more stable

than modern Nautilus and are unlikely to be able to substan-

tially modify their orientation by active swimming locomo-

tion by jet propulsion (Peterman et al., 2020a,b). The U-

shaped body chamber distributes organismal mass away

from the centre of buoyancy, while maintaining an upward-

facing posture (as suggested by Trueman, 1941; Klinger,

1981; Westermann, 1996). Horizontal alignment of the

hyponome with the centres of rotation, such as in ancylo-

cones, suggests that more energy would be transmitted to

translational movement with minimal rocking, i.e. these mor-

photypes are well suited for backwards horizontal swimming

at maturity. Hydrodynamic efﬁciency was investigated for

various scaphiticones (Peterman et al., 2020a) and an ancylo-

cone (Peterman et al., 2020d). The uncoiled shape increases

Fig. 3. Neutrally buoyant physical experiments on scaphitid heteromorph ammonoids. (A) Virtual model with complex internal

geometry. (B) Modiﬁed virtual model for 3D printing. Bismuth counterweight corrects for differences in mass and stability between

A and B. (C) 3D printed model showing counterweight and a control valve in case of ﬂooding. (D) Neutrally buoyant model with

proper hydrostastics and tracking points for hydrodynamic analyses. From Peterman et al. (2020a).

10 René Hoffmann et al.

drag, but with Nautilus-like thrust values they were able to

move horizontally backwards at velocities similar to Nautilus

(when normalised by mass). Coleoid-like thrusts would have

allowed them to surpass the velocities of similarly sized Nauti-

lus. These calculations depend on the largely unknown

ammonoid soft body morphology (see Section II). Thus, it

remains unclear whether they are realistic. Aside from these

open questions, the results of these studies contrast with the

interpretation of such heteromorphs as being conﬁned to

benthic habitats and the interpretation of limited horizontal

mobility (Westermann, 1996).

The adult change in coiling (U-shaped body chamber)

brought the hyponome closer to the level of the centre of

mass. This implies improved swimming capabilities. Klug

(2001) and Klug & Korn (2004) found this phenomenon in

several ammonoid clades and suggested that improved swim-

ming capabilities represent selective advantages during

reproduction particularly for the choice of mating partners

and spawning grounds. Sexual selection is a strong evolution-

ary agent and might be the main driver behind the conver-

gent evolution of more horizontally oriented apertures in

adult conch forms in many ammonoid clades, including

numerous heteromorphs.

IV. ECOLOGICAL INTERACTIONS

(1) Predators

Abnormal shell growth in modern and fossil molluscs, includ-

ing ammonoids, is often the result of sublethal injuries, which

may inform on predator–prey relationships (Keupp, 2012;

Hoffmann & Keupp, 2015). Like modern cephalopods,

ammonoids were an important part of marine food webs

and served as prey for vertebrates and invertebrates. For

food-web reconstructions, digestichnia (Vallon, 2012),

including stomach contents, cololites, coprolites, regurgita-

lites, and palaeopathologies (Keupp, 2012) have been used.

Since digestichnia including heteromorph remains were

reviewed by Hoffmann et al. (2020) we herein focus on

palaeopathologies. Various heteromorphs bear large (often

hollow) spines which might have had a protective function

against predators or encrusters (Klinger, 1981; Cecca,

1997) but other authors have speculated that these spines

were too fragile and might have had other functions such as

stabilizing the shell in the water column (Klinger, 1981; Ifrim,

Bengtson & Schweigert, 2018).

Speciﬁc reactions of the prey often result in a characteristic

abnormal growth of the repaired shell (symptoms). Assump-

tions about the ammonoid life habit including habitat depth

and proximity to the seaﬂoor are possible (Hoffmann &

Keupp, 2015). However, sublethal injuries in cephalopods

can be inﬂicted not only by predators, but also by the same

species such as in Nautilus during mating (Ward, 1987) or by

dangerous prey such as crustaceans [e.g. see Ward (1981)

for Nautilus and Landman & Waage (1986) for scaphitids].

Pathologies have been primarily reported for Jurassic and

Cretaceous heteromorphs (Table S2) but were also known

from Devonian heteromorphs, which suggest damage caused

by other cephalopods (Klug, 2007). The oldest known

injured Mesozoic heteromorph is the Late Bajocian Spiroceras

(Bayer, 1970: plate 8, Fig. 9; Dietl, 1978: Fig. 6f ). Here, we

document palaeopathologies for the Hauterivian Aegocrioceras

raricostatum (Fig. 5B, G), Aptian Proaustraliceras tuberculatum

(Fig. 5D), Albian Pictetia astieriana (Fig. 5A), Aptian Ptychoceras

minimum (Fig. 5C, E), and Ptychoceras renngarteni (Fig. 5F).

Among Cretaceous heteromorphs, palaeopathologies are

common and have been mostly reported for scaphitids

(Landman & Waage, 1986; Hengsbach, 1996; Larson,

2002; Landman et al., 2010b, 2012a, 2019; Keupp, 2012;

Fig. 4. Virtual hydrostatic models of heteromorphs with recurved body chambers at maturity. (A) Didymoceras nebrascense (Peterman

et al., 2020b). (B) Audouliceras renauxianum (Peterman et al., 2020d). (C) Hoploscaphites crassus microconch (Peterman et al., 2020a). Tip

of upper yellow cone, centre of buoyancy; tip of lower yellow cone, centre of mass. Scale bars =3 cm.

Heteromorph ammonoid palaeobiology 11

Fig. 5. Palaeopathologies of heteromorphs. (A) Pictetia asteriana (Early Albian, Madagascar) with a band-slit pathology potentially

caused by a benthic crustacean suggesting a demersal life habit of the ammonoid. Private collection of Wolfgang Grulke (Dorset,

UK). (B) Aegocrioceras raricostatum (Hauterivian, NW-Germany) with a bulbous shell breakage. (C) Ptychoceras minimum (Late Aptian,

Krasnodar region, Russia). Geological institute RAS, No. GIN MPC 5/2. Arrow indicates a healed sublethal injury on the second

shaft of the conch. Post-traumatic inﬂation indicates damage of the shell-secreting mantle edge. (D) Proaustraliceras tuberculatum

(Early Aptian, Ulyanovsk region, Russia). Private collection of Dmitry Vinogradov (Moscow), specimen No. 438. Arrow indicates

a healed sublethal injury on the dorsal side of the conch likely produced by durophagous ﬁsh. (E) Ptychoceras minimum (Late Aptian,

Krasnodar region, Russia). Geological institute RAS, No. GIN MPC 5/5. Feather-like wrinkles on the dorsal surface of the second

shaft that start at the point of truncation of the ﬁrst shaft. (F) Ptychoceras renngarteni (Late Aptian, Krasnodar region, Russia).

Geological institute RAS, No. GIN MPC 5/1. Arrows mark healed sublethal injuries on the second shaft of the conch.

(G) Aegocrioceras sp. body chamber (Hauterivian, NW-Germany) with a band-slit.

12 René Hoffmann et al.

Hoffmann & Keupp, 2015). Typically, injuries affected the

margin of temporary apertures and usually occur in early

ontogenetic stages (coiled conch part). Severe injuries of the

shell-secreting mantle epithelium sometimes resulted in the

disappearance of ventral tubercles (Hoffmann & Keupp,

2015: Fig. 21.8d). Crustaceans, ﬁsh, marine reptiles, coleoids,

ammonoids, and nautiloids were discussed as potential pro-

ducers of such damage (Landman & Waage, 1986;

Hengsbach, 1996; Larson, 2002; Landman et al., 2010b;

Keupp, 2012; Hoffmann & Keupp, 2015).

Orthoconic baculitids display palaeopathologies on their

apertural edges of different growth stages (Klinger &

Kennedy, 2001; Henderson, Kennedy & Cobban, 2002;

Kennedy, Cobban & Klinger, 2002a). In some cases, the

complete aperture was fragmented, presumably by pycno-

dontid ﬁsh (Kennedy et al., 2002a: plate 8, Fig. 9) or the conch

had long and narrow V-shaped injuries on both ﬂanks

(Kennedy et al., 2002a: plate 8, Figs. 2–4, 6–8). For the latter,

Kennedy et al. (2002a) suggested a coleoid attack, but Keupp

(2012) argued for a benthic crustacean as the predator.

Palaeopathologies may help reconstructing the soft body

organisation of the Aptian Ptychoceras. Doguzhaeva & Mutvei

(1989, 1993, 2015) argued that Ptychoceras had an internal

shell. Kakabadze & Sharikadze (1991, 1993) and Keupp

(2012) rejected that interpretation based on similarities of

Ptychoceras palaeopathologies with injuries found in other

monomorph and heteromorph ammonoids. Injured and

repaired temporal apertures (forma aegra substructa)ofPtycho-

ceras caused a strong distortion of the subsequent shaft, indi-

cating severe damage of the mantle edge (Fig. 5C, F). A

healed ventral injury located behind the terminal aperture

(forma aegra fenestra sensu Keupp, 2006) was found in another

Ptychoceras. In all cases, the healed shell is attached to the

inner surface of the preserved pre-traumatic conch wall like

in other ammonoids and modern Nautilus with repaired inju-

ries. No additional layers were secreted on top of the outer

prismatic layer, as expected for an internal shell.

Truncation of shell is restricted to the ﬁrst shaft in Ptycho-

ceras (Doguzhaeva & Mutvei, 1989, 1993, 2015). Truncation

also occurs in Palaeozoic nautiloids (e.g. Turek & Manda,

2012) and coleoids (Doguzhaeva, Mapes & Mutvei, 2002).

Doguzhaeva & Mutvei (1989) suggested that the truncation

in Ptychoceras occurred due to muscular action of the ammo-

noid body, during the formation of the second shaft. Kaka-

badze & Sharikadze (1993) assumed that the truncation

could have occurred randomly during the formation of the

ﬁrst to the beginning of the second shaft. Reported fragments

preserved in the partially broken phragmocone chambers

near the point of truncation (Doguzhaeva & Mutvei, 1989,

pl. 9, 10) support the hypothesis of Doguzhaeva & Mutvei

(1989). The feather-like structure (Fig. 5E) implies the pres-

ence of the shell-secreting mantle edge and periostracum in

Ptychoceras, which disproves the endocochleate hypothesis

for this ammonoid.

Palaeopathologies of heteromorphs include various shell

abnormalities and deformed suture lines. Pseudoinversion

of suture lines refers to pointed saddles and rounded lobes.

Pseudoinversion has been reported for the Late Cretaceous

heteromorphs Glyptoxoceras (Westermann, 1975; Ward &

Westermann, 1976) and Baculites (Henderson et al., 2002).

Rogov (2018) found this in several Jurassic and Cretaceous

monomorphs. Another internal abnormality of the ammo-

noid conch is sutural asymmetry relative to the venter, while

the conch wall is unaffected [forma aegra juxtalobata

(Landman & Waage, 1986; Keupp, 2012)]. In this case, the

siphuncular tube moved out of its ventral central position.

This type of palaeopathology occurs in both heteromorphs

and monomorphs (Keupp, 2012). However, the question of

what causes these pathologies remains unanswered. Various

authors speculated that the asymmetries were caused either

by the asymmetric development of reproductive glands due

to parasites or due to ‘epithelial diseases’(Keupp, 2012; De

Baets et al., 2015a). ‘Morton’s syndrome’also affected conch

symmetry, where the asymmetry is unrelated to external inju-

ries and occurs in 3–6% of scaphitids from South Dakota

(Landman & Waage, 1986). This phenomenon is widespread

in keeled monomorphs, such as Jurassic Graphoceras and Pleur-

oceras (Morton, 1983; Keupp, 2012). As in many other cases

of abnormalities with unclear aetiology, this asymmetry has

been explained by parasitic infestation (Morton, 1983; De

Baets, Keupp & Klug, 2015b), although traces of parasites

have not been documented in asymmetric conchs.

(2) Prey

Reports of fossil cephalopod stomach contents are rare (Table

S3). Planktotrophy was suggested for ammonoids that have

aptychus-type, calciﬁed lower jaws (Kruta et al., 2011, 2015;

Tanabe, 2011; Tanabe et al., 2015a;Keuppet al., 2016a). This

is supported by ﬁnds of stomach contents associated with a rad-

ula in Baculites (Kruta et al., 2011) and Allocrioceras (Wippich &

Lehmann, 2004), a pelagic, aperture-upwards drifter that

probably fed on echinoderms (comatulid crinoids or ophiu-

roids; Fig. 6). Diet remains from Jurassic and Triassic mono-

morphs comprise foraminifera, ostracoda, decapod

crustacean, bivalves, aptychi, and crinoid hardparts (e.g. Sacco-

coma)inNeochetoceras and corroborate planktotrophy in ammo-

noids (Wippich & Lehmann, 2004; Ritterbush et al., 2014;

Klug & Lehmann, 2015). Interestingly, the modern coleoid

Japetella shares radular tooth morphology with some Jurassic

ammonoids (Kruta et al., 2011; Keupp et al., 2016a), which

have been regarded as microphagous planktotrophs.

Jurassic–Cretaceous heteromorphs are widely accepted as

microphagous zoo-planktotrophic suspension feeders (Nesis,

1986, 2005; Kruta et al., 2011; Tajika, Nützel & Klug,

2018). Many heteromorphs reached large sizes (e.g. Baculites

grandis with a conch length of 250 cm; N. Larson, personal

communication) and are considered passive drifters with

low manoeuvrability (Westermann, 1996; Mikhailova &

Baraboschkin, 2009). Without direct evidence, Nesis (1986,

2005) suggested the presence of membranes between the

arms or a special mucus web to collect planktic prey out of

the water column. Heteromorphs likely lived in the water col-

umn (Cecca, 1997; Guex, 2006), i.e. with direct access to

Heteromorph ammonoid palaeobiology 13

meso- and microplankton. Based on the reconstructed swim-

ming position for heteromorphs with U-shaped body cham-

bers in which the aperture pointed upwards (Kaplan,

2002), it is assumed that their diet was composed of micro-

scopic particles or organisms (Kruta et al., 2011; Keupp,

2012; Ritterbush et al., 2014; Klug & Lehmann, 2015; Keupp

et al., 2016b). Remarkably, the jaw morphology of modern

coleoids does not entirely relate to diet (Clarke & Maddock,

1988). Jaw morphology only reﬂects the maximum size of

prey and dictates the area for the insertion of mandibular

muscles and hence its mass and biting force (Kear, 1994).

All Cretaceous heteromorphs, except the crioceratids, share

an aptychus-type lower jaw (Section II.1.a). The aptychus is

potentially not involved in determining prey size but prey

type. Accordingly, both the Crioceratidae with an anapty-

chus and other aptychus-bearing Cretaceous heteromorphs

may differ in their food preferences.

All modern cephalopods are carnivores –ranging from

active predators to more passive forms like Vampyroteuthis

(Norman, 2000; Golikov et al., 2019). Hanlon & Messenger

(2018) documented cannibalism for every known species of

modern coleoids except Sepioteuthis sepoidea. The occurrence

of cannibalism appears to be related to poor food supply

(Ennis & Collins, 1979). Research on stomach contents in

modern cephalopods is difﬁcult because the jaws reduce the

prey to unidentiﬁable pieces. Hardparts needed for the iden-

tiﬁcation of prey organisms are often regurgitated, leading to

an underestimation of soft-bodied prey in estimations of diet

(Rodhouse & Nigmatullin, 1996). This is because the oesoph-

agus diameter is limited because it passes through the brain.

This likely also applied to most extinct neocephalopod

groups such as ammonoids (Engeser, 1996; Klug et al.,

2016, 2019). Modern cephalopod stomachs often contain

skeletal parts of ﬁsh, crustaceans, and cephalopods (even

from the same species). A shift of food resources during

ontogeny is evident. The juveniles of most modern cephalo-

pods feed on crustaceans and shift towards larger ﬁsh and

other cephalopods later in ontogeny (Rodhouse &

Nigmatullin, 1996). Only a few coleoids seem to be special-

ists; the majority appear to be non-selective in their choice

of prey [e.g. Mather (1993) for observations on octopuses].

Rodhouse & Nigmatullin (1996) observed that squid and cut-

tleﬁsh preying on pelagic crustaceans ingest the exoskeleton,

whereas octopuses paralyse their prey with cephalotoxin,

digest only the ﬂesh and reject the exoskeleton. This is rele-

vant for the reconstruction of predator–prey relationships

in heteromorphs. This difference in behaviour might be

related to the need to form a mineralised internal skeleton

or other unknown factors. Larson (2002) speculated on can-

nibalism in scaphitids. Based on their high demand for cal-

cium, Larson (2002) postulated that ammonoids fed on

crustaceans, echinoids, molluscs, and possibly ﬁsh.

(3) Epizoa, parasites, and commensalism

Syn vivo encrustations, i.e. epizoa (in contrast to post-mortem

encrustation of dead shells –epicole; see Davis, Mapes &

Fig. 6. Stomach content of Allocrioceras (specimen shown in

Wippich & Lehmann, 2004). (A) Image taken under daylight.

(B) Same specimen imaged under ultraviolet light showing

preserved soft parts such as the siphuncle and remnants of the

stomach. (C) Close up of assumed but unidentiﬁable stomach

remains. (D) Stomach remains of planktic comatolids

(crinoids). Scale bars: A and B =5 mm, C and D =0.5 mm.

14 René Hoffmann et al.

Klofak, 1999), provide a unique source for palaeoecological

reconstructions (Lukeneder, 2008). Some cases have been

attributed to parasitism, while others might indicate syn vivo

epizoism, which ranges from associations that might have

been detrimental to both or beneﬁcial for one or both

organisms.

Four criteria have been applied to identify cases of syn vivo

associations of epizoans with ammonoid conchs (see Keupp,

2012). (i) Associations found on both ﬂanks, but not at the

apertural region mostly refer to ectoparasites or epizoans

[see exceptions in Mironenko (2016) and Landman, Slat-

tery & Harries (2016b)]; in the case of disease or endoparasit-

ism, no external injuries are visible, but pathologies develop

within soft tissues. (ii) The growth of associated organisms

stops precisely at a whorl or is otherwise outpaced by the

conch growth of the cephalopod. (iii) Associated organisms

show a growth direction consistent with shape and life posi-

tion of the cephalopod and may follow changes in growth

direction of the host. (iv) The cephalopod reacts to its epizo-

ans by altering its conch form such as non-planispiral coiling,

shortening of body chamber (Klug et al., 2004), and other

pathologies.

Cases of conch deformation or deviation from normal pla-

nispiral coiling caused by encrusters, which are still pre-

served, provide incontrovertible evidence for syn vivo

encrustation in ammonoids (Ramming et al., 2018). Syn vivo

encrustations may result in monomorphs resembling hetero-

morphs (Checa, Okamoto & Keupp, 2002). Patterns related

to criteria 1 and 3 are the only indicators useful to infer syn

vivo encrustation when host growth has stopped, but could

potentially develop in post-mortem sclerobiont attachment dur-

ing necroplanktic drift (Stilkerich, Smrecak & De Baets,

2017). However, marked post-mortem drift is unlikely in the

case of heavy encrustation and smaller conchs (Yacobucci,

2018; Wani et al. 2005). Furthermore, the conch might

change orientation during post-mortem drift and due to added

weight by epicoles. The orientation and position of encrus-

ters during life could also support the idea that heteromorphs

were nektoplanktic or at least neither demersal nor benthic.

Encrustation by cirripedes (Hauschke, Schöllmann &

Keupp, 2011), brachiopods (Landman et al., 2016b), and

bivalves (Misaki et al., 2014) have been reported on Creta-

ceous heteromorphs. Misaki et al. (2014) found anomiid

bivalves on both sides of Pravitoceras conchs, suggesting these

are epizoa. These heteromorphs come from mudstones with-

out signs of strong currents or wave-induced transport. Mis-

aki et al. (2014) suggested that Pravitoceras was neutrally

buoyant and could move vertically, thus contradicting the

hypothesis of a benthic life habit (Matsumoto et al., 1981b).

Syn vivo encrustation of a Palaeozoic Ivoites specimen by

hederelloids (?phoronids) caused trochospiral instead of

gyrocone coiling (Stilkerich et al., 2017). The pathological

specimen survived into adulthood despite multiple encrusta-

tions (Stilkerich et al., 2017). If cephalopods reached adult-

hood showing such deformations, these may not have

altered ammonoid health substantially, irrespective of

whether such trochospiral coiling was a normal variant or

pathological. Regular covariation patterns might relate to

structural constraints and may provide information about

growth. Highly irregular patterns within the same specimen

might indicate a lack of morphogenetic constraints.

Associations between heteromorphs and algae have been

suggested repeatedly. Arkhipkin (2014) suggested that Spiro-

ceras was associated with macroalgae and that adult life stages

of Cretaceous heteromorphs (e.g. scaphitids) clung to macro-

algae with their umbilical opening [see also Vašícˇek & Wied-

mann (1994) for Leptoceratoidinae such as Karsteniceras].

However, direct evidence for such associations has not been

found yet, rendering this idea speculative (Landman et al.,

2016a). The fossil record of non-calciﬁed macroalgae is

sparse; potential biomarkers like sterols may help to identify

their presence.

Hatchlings of the trochospiral Mariella or orthoconic Scipo-

noceras have been interpreted as semi-sessile based on associ-

ations with algal mats (Stinnesbeck, Frey & Zell, 2016).

However, this is likely a taphonomic artefact and solid evi-

dence for this life habit is needed because such life habit is

unknown in modern cephalopods.

V. HABITAT RECONSTRUCTION

(1) Taphonomic controls on facies distributions

The relationship between heteromorphs and facies has been

debated due to post-mortem drift. This issue stems from exter-

nally shelled cephalopods having phragmocones, which can

remain gas-ﬁlled after death allowing the conch to ﬂoat and

drift varying distances away from the living animals’habitat

[Fig. 7; Reyment (1958, 1973, 2008); for alternative perspec-

tives see Wani & Gupta (2015) and Yacobucci (2018)]. How-

ever, numerous studies have argued that post-mortem drift was

rare among ammonoids, and that their fossils closely reﬂect

their life distributions (e.g. Kennedy & Cobban, 1976;

Tanabe, 1979; Chamberlain, Ward & Weaver, 1981; Wani

et al., 2005; Wani & Gupta, 2015; Yacobucci, 2018). These

interpretations are based on the low frequency of encrusters,

degree of shell breakage, frequency of preserved jaws in body

chambers, size–frequency distribution of conchs, low drift

potential of numerous conch morphotypes, and geographic

distribution patterns. Kennedy & Cobban (1976) proposed

that facies independence and broad geographic ranges as

well as distinct facies associations and limited ranges should

reﬂect high and low post-mortem drift, respectively. They state

that the large numbers of unbroken, well-preserved ammo-

noids at many localities represent autochthonous assem-

blages, which cannot be explained by post-mortem drift. This

is supported by taphonomic and experimental studies of

modern nautilid conchs, which revealed that drifted conchs

show signs of fragmentation and encrustation (Wani, 2004;

Reyment, 2008). Yacobucci (2018) argues that most ammo-

noid conchs, except for highly inﬂated monomorphs, were

unlikely to undergo long-distance post-mortem drift. This study

Heteromorph ammonoid palaeobiology 15

also shows that most Cretaceous ammonoids, even those with

conch forms conducive to post-mortem drift, rarely had sub-

stantial biogeographic ranges (i.e. basinwide, intercontinen-

tal), which would be expected if they were ﬂoating over

great distances after death.

Post-mortem drift in heteromorphs has not been considered

to the same extent as for monomorphs; the latter being mor-

phologically more like nautilids, which are assumed to be

reasonable analogs. However, the few available studies sug-

gest that the impact of post-mortem drift on heteromorph spa-

tial distributions is minimal (Tanabe, Obata & Futakami,

1978; Tanabe, 1979; Kawabe, 2003; Reboulet, Giraud,

& Proux, 2005; Landman et al., 2010b, 2019; Landman &

Klofak, 2012; Misaki et al., 2014; Slattery, Harries &

Sandness, 2018). Stable isotopic analysis of heteromorphs

and associated benthic faunas provides evidence for limited

post-mortem drift. These studies reveal that the δ

O and

C composition of scaphitids, baculitids, and nostoceratids

more closely match the isotopic composition of associated

benthic faunas than known planktic organisms. This has been

interpreted as an indication that they were living near where

they were collected (Tsujita & Westermann, 1998; He,

Kyser & Caldwell, 2005; Landman & Klofak, 2012; Land-

man et al., 2012b; Sessa et al., 2015).

Berry (2018a,b) and Landman et al. (2019) are among the

few studies to suggest that some heteromorph conchs could

undergo long-term and/or long-distance post-mortem drift.

Berry (2018a,b) utilised changes in both bryozoan zooid size

and the direction of growth in colonies encrusting the inter-

nal body chambers of Baculites and Scaphites to suggest that

these heteromorphs experienced long-term post-mortem drift.

Landman et al. (2019) argued that the occurrences of North

American Hoploscaphites in Europe are best explained by

long-distance post-mortem drift due to their rarity. However,

Machalski et al. (2007) suggested that North American

Hoploscaphites and Discoscaphites in Europe are more likely

related to immigrant populations rather than post-mortem drift

due to the greater potential for small cephalopod shells to be

buried close to their habitats.

(2) Life habit controls on facies distributions

The association of water-column-dwelling ammonoids with a

benthic bio- and lithofacies or a lack thereof is likely due to

their preferred habitats and positions in the water column

(Ziegler, 1967; Kennedy & Cobban, 1976; Batt, 1986,

1989; Westermann, 1996; Lukeneder, 2015). They would

have tracked these environmental preferences both spatially

and temporally, which in turn would be expressed in the

stratigraphic record as changes in faunal occurrences and/or

ranges. Environmental changes in the upper water column

would be expressed in the stratigraphic record as changes in

occurrences and abundances of nektic and planktic organ-

isms (e.g. ammonoids, ﬁsh, planktic foraminifera, nanno-

plankton), while potentially showing no concomitant

pattern among benthic organisms, or lithofacies [Soule &

Kleppel (1988) and references therein]. Nektic (i.e. actively

swimming in the water column), nektoplanktic (i.e. passively

ﬂoating in the water column), and vertically migrating

(i.e. moving vertically through the water column) ammonoids

Fig. 7. Potential taphonomic pathways of modern Nautilus prior to burial (modiﬁed from Maeda & Seilacher, 1996; Mapes

et al., 2010a,b). Nautilus habitat ranges from 20 to 600 m depth; however, most live within a few meters of the seabed. The ‘Depth

Limit to Surface’is the theoretical limit where an empty conch cannot ascend to the sea surface because hydrostatic pressure

forces water into the phragmacone and causes the conch to become negatively buoyant and sink.

16 René Hoffmann et al.

likely tracked their preferred ecological conditions and food

sources through the water column. This would have

decoupled them from benthic faunas, environments, and

facies, unless their prey was tied to a benthic environment

(Westermann, 1996). By contrast, nektobenthic (i.e. living

near the sea bottom) ammonoids would have been inﬂuenced

by the same conditions (e.g. oxygen, turbidity) that controlled

the distribution of benthic organisms, which explains the

association of many ammonoids with speciﬁc benthic bio-

and/or lithofacies (e.g. Tsujita & Westermann, 1998; Land-

man et al., 2012b; Slattery et al., 2018). Documenting changes

in heteromorph occurrences and abundances across benthic

bio- and lithofacies can reveal important details about their

preferred habitats, speciﬁcally when examined within a

sequence stratigraphic framework. Kennedy & Cobban

(1976) showed that occurrences of Cretaceous ammonoids,

including heteromorphs, rarely exhibit discernable lithofa-

cies patterns. However, they also noted that there are obvious

changes in abundances among taxa across lithofacies. Varia-

tion in heteromorph abundances has also been documented

across benthic biofacies, which are attributed to changes in

marine environmental conditions (e.g. oxygen) that are inde-

pendent of lithofacies (e.g. Lukeneder, 2003, 2004, 2005;

Slattery et al., 2018).

Heteromorphs are known from an array of facies spanning

tidally inﬂuenced littoral to oceanic environments (Fig. 8;

Westermann, 1996). Most heteromorphs occur in shallow-

subtidal to offshore facies deposited in neritic (i.e. open-

ocean-facing seas) and epeiric seas (i.e. seas covering

continental interiors). They are common in continental slope

facies, but rare in bathyal, foreshore, and littoral facies

(Westermann, 1996). Most heteromorphs preferred epipe-

lagic depths (0–200 m), and for certain taxa, upper mesope-

lagic depths (200–600 m) due to depth limitations imposed

by the strengths of their shells (Hewitt, 1996). Taxa found

in oceanic facies were likely living within a few meters of

the continental slope and/or in the water column well above

the slope and bathyal seaﬂoor at epi- and/or upper mesope-

lagic depths (Hewitt, 1996; Westermann, 1996). The few

examples of heteromorphs in foreshore and littoral facies

(e.g. Hoganson & Murphy, 2002) are likely due to post-mortem

transport via drift or storms.

Devonian, Triassic, and Jurassic heteromorphs show a

preference for deep-subtidal to offshore facies but are rare

in shallow-subtidal, slope, and bathyal facies (Fig. 8A;

Table S4; Dietl, 1978; Laws, 1982; Chlupácˇ& Turek,

1983; www.paleodb.org). The rarity of Pre-Cretaceous het-

eromorphs in shallow-subtidal, slope, and bathyal facies sug-

gests that these ammonoids did not inhabit these

environments but were transported into these settings via

storms or post-mortem drift from their epipelagic, deep-

subtidal to offshore habitats.

Early Cretaceous heteromorphs preferred deep-subtidal to

bathyal facies (Fig. 8B; Table S4). Barragan, Gonzalez-

Arreola & Villaseñor (2004) documented distributions of

BarremianammonitesinMexico,whichwerecontrolledby

water-column oxygenation and the preferred water depth of

each species. They suggest that ancylocone heteromorphs were

nektic or nektoplanktic based on their abundance in anoxic

facies, which indicates a preference for offshore settings

(Barragan et al., 2004). Lukeneder (2003, 2004, 2005) suggested

that the Barremian ancyloceratid Karsteniceras preferred low-

oxygen conditions based on its mass occurrences in dysoxic

facies. Marcinowski & Wiedmann (1990) noted that Albian het-

eromorphs in Poland are restricted to clay- and marlstones

rather than sandstones, which suggests that these ammonites

preferred offshore facies rather than subtidal facies. Reboulet

et al. (2005) studied Albian ammonite occurrences and abun-

dances across Oceanic Anoxic Event 1d in the Vocontian Basin

(France) and found that most heteromorphs are associated with

offshore neritic to oceanic facies. For example, the baculitid

Lechites is most abundant in continental-slope facies. The torti-

cones Turrilitoides and Mariella as well as the hamiticones Anisoceras

and Hamites are associated with offshore neritic and oceanic

facies. Tajika et al. (2017) showed that Cretaceous cephalopod

associations of Switzerland, including heteromorphs

(e.g. Emericiceras,Mariella), are dominant in deep-subtidal to off-

shore facies and rare to absent in shallower, carbonate facies.

Several studies suggest that bochianitids are deeper-water indi-

cators due to their abundances in limestones and claystones

depositedincontinentalslopefacies(>200 m) and absence in

neriticaswellasepeiricfacies (Company, 1987; Reboulet &

Atrops, 1997; Baraboschkin & Enson, 2003; Reboulet et al.,

2005; Arkadiev, 2008; Lukeneder, 2015).

Late Cretaceous heteromorphs have a preference for

shallow-subtidal to offshore facies, but are rare in slope and

bathyal facies (Fig. 8C; Table S4). Baculitids are broadly dis-

tributed with juveniles being common in well-oxygenated,

shallow- to deep-subtidal facies and adults being common

in well-oxygenated, deep-subtidal to anoxic, offshore facies

(Fig. 9; Tsujita & Westermann, 1998; Kawabe, 2003; Slat-

tery et al., 2018). The earliest juvenile Baculites have been

recorded in shallow-subtidal to offshore facies, which indi-

cates that they might have been more facies independent

and/or more subject to drift as compared to more mature

individuals (Landman & Klofak, 2012; Slattery et al., 2018;

N.H. Landman, personal communication; Rowe et al.,

2020). The giant baculitid Pseudobaculites is common in subti-

dal facies but rare in offshore facies (W.A. Cobban, personal

communication). Turrilitids, scaphitids, diplomoceratids,

and nostoceratids are typically associated with well-oxygen-

ated, subtidal to offshore facies due to their nektobenthic life

habit (Fig. 9; Scott, 1940; Kennedy & Cobban, 1976;

Tanabe et al., 1978; Tanabe, 1979; Matsumoto et al.,

1981a; Batt, 1986, 1989; Tsujita & Westermann, 1998;

Kawabe, 2003; Landman et al., 2012b; Slattery et al., 2012,

2018; Olivero & Rafﬁ, 2018; Rowe et al., 2020; J. S. Slattery,

personal observations). The scaphitid Worthoceras likely

inhabited the middle to upper water column based on their

broad distribution in well-oxygenated, subtidal to anoxic, off-

shore facies (Scott, 1940; Batt, 1986, 1989). Several nostocer-

atids in North America are common in shallow-subtidal

facies but rare to absent in deep-subtidal to offshore facies

(Table S4; Fig. 9; Kennedy & Cobban, 1976, 1994;

Heteromorph ammonoid palaeobiology 17

Cobban, 1993; Cobban et al., 1993; Kennedy, Cobban & Scott,

2000a,b). Hamitids and anisoceratids are commonly restricted

to well-oxygenated, subtidal facies, however, the hamitid Stomo-

hamites and anisoceratid Allocrioceras have broad distributions

ranging from well-oxygenated, subtidal to anoxic, offshore

facies (Kennedy & Cobban, 1976; Batt, 1986, 1989). The

increase in heteromorph diversity in shallow-subtidal settings

duringtheLateCretaceouslikelyreﬂects an evolutionary shift

among Ancyloceratina to shallower-water settings.

(3) Ecological requirements based on shell

geochemistry

Stable isotope proxy systems provide information on habitat

depth, depth change through ontogeny, and growth rates of

individual monomorphs and heteromorphs (e.g. Moriya

et al., 2003; Lukeneder et al., 2010; Fig. 10). Most analyses

to date have been focused on baculitids and scaphitids from

the Late Cretaceous (He et al., 2005; Landman et al.,

Fig. 8. Heteromorph distributions across marine environments and depth zones during the (A) Devonian, Triassic, and Jurassic,

(B) Early Cretaceous, and (C) Late Cretaceous. Based on data from Table S4.

18 René Hoffmann et al.

2012b). Variation in the oxygen isotope ratio (δ

O) reﬂects

changes in temperature or the oxygen isotope ratio of sea

water, which often covaries with salinity (Mátyás et al., 1996).

Combined temperature and salinity gradients create a vari-

able proﬁle in δ

O between surface water and bottom water,

which is recorded in shell carbonate precipitated in equilib-

rium with those waters. Seasonal variation in these parameters

can impart sinusoidal variation and therefore a chronometer

in the shells and aptychi of heteromorphs (Fatherree, Harries &

Quinn, 1998; Kruta, Landman & Cochran, 2014; Ellis &

Tobin, 2019), although swimming behaviour and growth rate

can complicate these patterns in ammonoids (Linzmeier,

2019). Cephalopods are thought to precipitate shell aragonite

in oxygen isotope equilibrium with ambient seawater stable

oxygen isotope composition (δ

)andtemperature

(Landman et al., 1994). Stable carbon isotope ratios (δ

record a mixture of carbon dominated by dissolved organic

carbon from water and minor respired carbon

(McConnaughey & Gillikin, 2008). Therefore, the habitat

depth of modern cephalopods can be directly inferred from

measured carbonate oxygen isotope ratios of their aragonitic

shell or calcitic aptychi (Auclair et al., 2004; Lukeneder et al.,

2008; Kruta et al., 2014; Lukeneder, 2015; Linzmeier et al.,

2016). To interpret habitat depth or growth rate from δ

and δ

C of fossils, additional isotopic information derived

from co-occurring benthic and planktic organisms is required.

The habitats of Late Cretaceous heteromorphs have been

studied using stable isotope analyses. Discoscaphites and Bacu-

lites from Mississippi show δ

O values that are more similar

to both benthic molluscs and foraminifera than to planktic

foraminifera (Sessa et al., 2015). Individuals have consistent

O through the gerontic whorl, supporting an interpreta-

tion of rapid growth and consistently benthic habitat

(Ferguson et al., 2019). Analysis of the earliest whorls of

Hoploscaphites from South Dakota suggest a benthic embry-

onic development, planktic hatchlings, and a habitat change

after about one whorl (Linzmeier et al., 2018). These data

may also suggest seasonally protracted spawning like some

modern cephalopods (Rocha, Guerra & González, 2001).

Other work spanning multiple Campanian ammonoid zones

from the Western Interior Seaway suggests Didymoceras was

living in warmer or more brackish water than co-ocurring

Scaphites and Baculites (He et al., 2005).

The interpretation of δ

C in heteromorphs, like other

marine molluscs, reﬂects the δ

C of dissolved inorganic car-

bon (DIC) (McConnaughey & Gillikin, 2008). In the modern

ocean, the δ

C varies with changes in the ratio of respiration

to photosynthesis and proximity to sources of unusual δ

from DIC (e.g. methane seeps). Analyses of Baculites from

the Western Interior Seaway (WIS) suggest that some hetero-

morphs lived on or close to cold seeps throughout their lives

and exploited the diverse prey available at the seeps

Fig. 9. Shoreface to offshore ammonoid facies and habitat distributions in the late Campanian Baculites compressus Biochron (Late

Cretaceous) in the Western Interior Seaway. Based on data from: Kennedy & Cobban (1976); Cobban, Kennedy, & Scott (1993);

Cobban et al. (1993); Larson et al. (1997); Landman & Klofak (2012); Landman et al. (2012a); and Meehan & Landman (2016).

Heteromorph ammonoid palaeobiology 19

(Landman et al., 2018). Hoploscaphites and Didymoceras also

appear to use methane seep habitats both as adults

(Landman et al., 2012b) and juveniles (Rowe et al., 2020).

The growth rates of Baculites have been estimated using sta-

ble isotopic methods. Their orthoconic conchs are relatively

easy to sample serially. By interpreting the pronounced sinu-

soidal pattern in δ

O, Fatherree et al. (1998) inferred a growth

rate of 33 cm/year for a subadult Baculites compressus. Sampling

of other Baculites suggest similarly high growth rates if inter-

preting sinusoidal variability in either δ

Oorδ

C, although

there are caveats about geographic differences in both isotope

proxies that could reﬂect migration (Ellis & Tobin, 2019).

Future investigation of heteromorph living depths and growth

rates using stable isotope methods will yield important infor-

mation that cannot be gathered from other methods.

(4) Reproduction

Early ammonoids (Anetoceratinae) have slightly curved

embryonic conchs, which are among the largest of all ammo-

noids (De Baets et al., 2013a; De Baets, Landman & Tanabe,

2015c). They range from about 6 mm in Metabactrites to

5mminIvoites to 3.7 mm in Erbenoceras. This, together with

their small body chamber volume, implies low fecundity

(35–500 eggs). De Baets et al. (2012) argued that increased

coiling and a reduction in embryonic conch size with an

increase in adult size affected fecundity. To date, no embry-

onic conchs of Triassic heteromorphs have been reported

(De Baets et al., 2015c; Laptikhovsky, Nikolaeva & Rogov,

2018), but adults are generally small suggesting low fecundity.

The size of Spiroceras hatchlings is 0.8 mm (Landman,

Tanabe & Shigeta, 1996) and falls within the 95% conﬁdence

interval for all Jurassic ammonoids (De Baets et al., 2015c).

Heteromorphs have the smallest embryonic conchs of all Cre-

taceous ammonoids with median measurements of 0.8 mm,

which are smaller than in Ammonitina (0.9 mm), Phyllocera-

tina (0.9 mm), and Lytoceratina (1.2 mm; De Baets et al.,

2015c). It is tempting to attribute this to constraints imposed

by adult size and mobility, which probably drove selection

towards an increasing number of smaller hatchlings that are

better adapted to a planktic life habit (e.g. Laptikhovsky

et al., 2018; Tajika et al., 2018, 2020). However, additional

data comparing adult and embryonic sizes and distributions

will be necessary to corroborate this hypothesis.

(5) Intraspeciﬁc variability

Herein, we use the six archetype morphologies (orthocone,

gyrocone, cyrtocone, ancylocone, torticone, and vermicone)

rather than the 44 subtypes distinguished by Kakabadze

Fig. 10. Habitat depth reconstruction based on oxygen isotope (δ

O) values collected from well-preserved, coeval monomorphs,

heteromorphs, benthic faunas, and planktic faunas. Modiﬁed after (A) Ferguson et al. (2019), (B) He et al. (2005), (C) Landman

et al. (2012b), (D) Linzmeier et al. (2018), (E) Moriya et al. (2003), and (F) Sessa et al. (2015), VPDB, Vienna Pee Dee belemnite.

20 René Hoffmann et al.

(2015); Figs. 1F, 11; see also Section III). Phenotypic varia-

tion in conch shape, ornamentation, size, and suture line is

common in ammonoids (De Baets et al., 2015a). Intraspeciﬁc

variation rarely has been considered in ammonoid taxon-

omy, even less so in heteromorphs (Ropolo, 1995;

Kakabadze, 2004, 2015; Witts et al., 2020), where it might

partially relate to difﬁculties in quantitatively analysing and

comparing shape variation in orthoconic, gyroconic, or torti-

conic forms. As in monomorphs, intraspeciﬁc variation can

be continuous between two or more extremes (e.g. De Baets,

Klug & Monnet, 2013b) or discontinuous between two or

more morphs (e.g. Bert, 2013). More general principles like

an association between strength of ornamentation and whorl

cross section (Buckman’s law of covariation) illustrate com-

mon ancestry and growth principles among ammonoids

and molluscs as a whole (Monnet, De Baets & Yacobucci,

2015b). Various authors have argued that intraspeciﬁc varia-

tion might be higher in heteromorphs than in their mono-

morph relatives (e.g. Dietl, 1978; Kakabadze, 2004; De

Baets et al., 2013b). This might make sense as coiling in het-

eromorphs is less constrained by the previous whorl and

might even deviate from the planispiral plane as in gastro-

pods. In the most extreme examples like Spiroceras, orthoco-

nic, crioconic, and trochospiral coiling occurs within one

species (e.g. Dietl, 1978). The large degree of variation and

differences between different sites have been used to argue

that Spiroceras was pseudoplanktic (Westermann, 1996). Var-

ious environmental factors could explain the degree of phe-

notypic plasticity, and the association of the mode and

degree of variation in relationship to environmental factors,

partially reﬂected in the litho- and biofacies, still need to be

analysed quantitatively. Differences in coiling and ornamen-

tation occur in gastropods, even within the same species, and

are related to differences in environmental factors (Urdy,

2015). Novel methods will allow us to study intraspeciﬁc var-

iation quantitatively in orthoconic, gyroconic, and vermi-

form shapes (Okamoto, 1988ab,c, 1996; Tsujino, Naruse &

Maeda, 2003; De Baets et al., 2013a; Urdy, 2015; Ward

et al., 2015; Hoffmann et al., 2019). Even taxa that seemingly

grow chaotically like Nipponites have been demonstrated to

have a regular growth pattern consistent with a free-living,

pelagic life habit (Okamoto, 1988c; Peterman, Mikami &

Inoue, 2020c). In many cases, more traditionally deﬁned spe-

cies have been synonymised, leading to more comprehensive

analyses of drivers of the mode and degree of intraspeciﬁc

variation in different taxa (Ward et al., 2015; De Baets et al.,

2015b; Hoffmann et al., 2019).

Ammonoid conch characters vary ecophenotypically with

environmental factors such as water depth and energy

(Landman, n.d.; Landman & Waage, 1993a; Jacobs et al.,

1994; Ikeda & Wani, 2012; Yahada & Wani, 2013;

Lukeneder, 2015; Klein & Landman, 2019). Among hetero-

morphs, only scaphitid conch characters have been quantita-

tively shown to vary with environment, which is likely linked

to their nektobenthic life habit (Landman et al., 2012a). Other

clades, such as baculitids, appear to show variation in conch

characters with facies but this remains to be explored in detail

(N.H. Landman, personal communication). Jacobs et al.

(1994) documented the degree of whorl compression within

Turonian Scaphites whitﬁeldi in near- and offshore facies in

the WIS. They show that whorls are more compressed in

nearshore facies, and that compressed whorls were hydrody-

namically more efﬁcient in these higher-energy environ-

ments. Landman (n.d.) showed that Hoploscaphites became

more compressed and nodose in response to a late Campa-

nian to early Maastrichtian shift from lower-energy offshore

to higher-energy nearshore environments in the WIS. Land-

man & Waage (1993a) showed how several different conch

characters vary within late Maastrichtian Hoploscaphites and

Discoscaphites in near- and offshore facies in the WIS. Hoplo-

scaphites in nearshore facies are less umbilicate, more nodose,

and have more compressed whorl sections compared to spec-

imens in offshore facies (Landman & Waage, 1993a). Discos-

caphites are also more nodose in nearshore than in offshore

facies (Landman & Waage, 1993a). These facies-linked pat-

terns indicate that intraspeciﬁc variation in conch characters

reﬂect local adaptations of populations to the differing envi-

ronments associated with the nektobenthic life habit across

a spectrum from shallower to deeper habitats. Jacobs et al.

(1994) hypothesised that iterative evolutionary changes in

ammonoid lineages might be driven by selection for conch

characters speciﬁcally adapted to environments that ﬂuctuate

through time with sea level.

VI. HETEROMORPHS THROUGH TIME

(1) Devonian heteromorphs

Ammonoids originated from orthoconic orthoceratids via

cyrtocone bactritoid ancestors during the Early Devonian

(Kröger & Mapes, 2007; Kröger et al., 2011; De Baets et al.,

2013a; Klug et al., 2015a). This is based on a stratigraphically

consistent record of evolutionary transitions in both embry-

onic and later ontogenetic stages within these lineages

(De Baets et al., 2013a; Klug et al., 2015a). Ammonoids com-

pleting at least one whorl evolved only once (Anetoceratinae

ranging from loosely coiled Metabactrites to coiled Erbenoceras

and closely related forms). However, multiple bactritoid line-

ages evolved loosely coiled representatives including a line-

age leading to Kokenia and a lineage including Cyrtobactrites

and Pseudobactrites with a mix of morphological characters.

Irrespective of these iterative coiling trends in bactritoids

around the origin of ammonoids, heteromorph ammonoids

have a short (about 6 million years) appearance during the

Palaeozoic (Klug et al., 2015a). Early Devonian ammonoids

show a rapid trend towards increased coiling in embryonic

and post-embryonic development (Klug & Korn, 2004; De

Baets et al., 2012). This rapid coiling trend has been linked

to increased swimming velocity and manoeuvrability in the

face of increased predation pressure (Klug & Korn, 2004;

Klug, 2007), although the coiling of the early whorls and

Heteromorph ammonoid palaeobiology 21

increased body chamber volume also inﬂuenced fecundity

and reproductive strategies (De Baets et al., 2012; Klug

et al., 2015a). Constructional constraints might also have

played a role (Monnet, De Baets & Klug, 2011). Both biotic

and abiotic factors impacted this trend as there are both con-

vergent coiling trends within lineages and the preferential

Fig. 11. Stratigraphic distribution of the six arche-morphotypes of heteromorphic conchs from the Devonian, Triassic, Jurassic, and

Cretaceous. Also shown are secondarily monomorphic forms derived from heteromorphs. After Wright et al. (1996).

22 René Hoffmann et al.

extinction of loosely coiled ammonoids during Devonian

extinction events (House, 1996; De Baets et al., 2012).

Mesozoic heteromorphs repeatedly underwent convergent

uncoiling trends, which is the inverse to that observed in post-

embryonic Devonian ammonoids (Fig. 11). These forms were

not an evolutionary end stage as some show secondary trends

back to planispiral forms such as scaphitids or douvilleicera-

tids (Wiedmann, 1969; Korn, 2003). Embryonic conchs of

all Mesozoic heteromorphs are planispirally coiled unlike

those of most Early Devonian ammonoids. Torticone conchs

did not exist among Palaeozoic ammonoids. The only excep-

tion is a slightly trochospirally coiled Ivoites (De Baets et al.,

2013a), which is interpreted as a pathological phenomenon

related to in vivo encrustation (Stilkerich et al., 2017).

Early Devonian gyroconic (subtype: crioconic) hetero-

morphs (Anetoceratinae) are palaeogeographically widely

distributed from about 30N in the Kolyma basin to 45S

in the Anti-Atlas, i.e. a similar range to normally coiled

ammonoids. Other ammonoids and loosely coiled bactritoids

have a more endemic distribution, which likely indicates

poorer dispersal abilities and K-strategy selective reproduc-

tion (De Baets et al., 2012). These differences could also relate

to collection or preservation artefacts. Fragments of loosely

coiled and ﬂattened ammonoids are not considered here as

they are difﬁcult to identify or to compare with better pre-

served specimens. The oldest heteromorphs occur 404 mil-

lion years ago (Ma) during the early Emsian, and these

lineages disappear 398 Ma at the beginning of the late

Emsian (Klug et al., 2015a). Advolute ammonoids with a

closed umbilical appear 396 Ma, while advolute forms with

an open umbilicus disappear 390 Ma in the early Eifelian.

Kokenia, another loosely coiled form, is known from the late

Eifelian but is usually considered to be a bactritoid due to

the age gap as well as differences in morphology. Loosely

coiled Palaeozoic ammonoids are therefore maximally dis-

tributed for about 16 million years (Myr) and do not reap-

pear for over 170 Myr until the Late Triassic [late Norian,

at the beginning of the Sevatian following Jenks et al. (2015)].

In summary, loose coiling was successful for a short period

in the Palaeozoic (Fig. 11) probably because it provided lim-

ited swimming capabilities. Early heteromorphs represent

evolutionarily transitional forms to the fully coiled mono-

morphs. Later, speciﬁc environmental or ecological condi-

tions allowed the convergence and longer evolutionary

success of heteromorphs in the Mesozoic. However, this

was only a post-embryonic phenomenon, highlighting the

evolutionary importance of, and constraints related to, a

coiled embryonic conch.

(2) Triassic heteromorphs

Triassic heteromorphs rarely attain sizes larger than 30 mm,

possess a coarse ornamentation comprised of simple straight

ribs, and have low diversity (about 30 species) and disparity

(morphologically stable: semi-evolute, orthocone, cyrtocone,

torticone, or monomorph trochospiral; Fig. 11) compared to

Jurassic and Cretaceous heteromorphs (Monnet, Brayard &

Brosse, 2015a). Wiedmann (1973a) considered the Triassic

four-lobed heteromorphs (Choristoceratidae) as a monophy-

letic family of ceratitic ammonoids (Wiedmann, 1969;

Shevyrev, 2005). Choristoceratidae contains the subfamilies

Rhabdoceratinae including Rhabdoceras and Peripleurites,

Choristoceratinae with Choristoceras and Vandaites, as well as

Cochloceratinae comprising Cochloceras and Paracochloceras

(Shevyrev, 2005). Krystyn & Wiedmann (1985) regarded

the Clydonitidae (Pseudothetidites praemarshi) from the Late

Norian Hallstattkalk facies as direct ancestors of the Choris-

toceratidae, a viewpoint rejected by Shevyrev (2005). Based

on a quadrilobate suture, coarse ribs, and with Rhabdoceras

as its oldest representative, Shevyrev (2005) suggested the

family Cycloceltitidae (Ophiorhabdoceras –a small, monomor-

phic, coarsely ribbed form) as potential ancestors of Triassic

heteromorphs. The ﬁrst Rhabdoceras occurred at the base of

the Sevatian, a time interval that is characterised by decreas-

ing ammonoid diversity (Jenks et al., 2015). Wiedmann

(1973a) highlighted the differences in morphological variabil-

ity between the highly variable Jurassic spiroceratids and the

less variable Triassic heteromorphs.

Triassic heteromorphs occur during the Late Norian and

persist into the Rhaetian (Marshi Zone) (Fig. 11). These

occurences range from 209 to 201 Ma (aged according to

Ogg, Ogg & Gradstein, 2016) and are geographically

restricted to the Tethyan realm. Most reports come from

Europe and the Paciﬁc coast of North and South America

(Yukon Territory to central Argentina; Shevyrev, 2005).

The paucity of reports of Late Triassic heteromorphs pre-

vented Brayard et al. (2015) from developing a biogeograph-

ical reconstruction for these ammonoids.

A life habit similar to spiroceratids was suggested for the

choristoceratids (Wiedmann, 1969, 1973a). This viewpoint

changed based on the co-occurrences of heteromorphs

together with monomorphs (phylloceratids, arcestids, mega-

phyllitids), making it likely that choristoceratids were capable

of active swimming. Based on the absence of gastropods,

Laws (1982) concluded that Triassic heteromorphs from

Nevada (USA) were epibenthic scavengers or micropreda-

tors that occupied the same ecological niche as gastropods.

Wiedmann (1973a) argued that reduced selective pressure

on the suture line occurred during the change from a nektic

to a vagile benthic life habit, expressed as reduced complexity

of suture lines. Such reduction in complexity is documented

in all heteromorphs from this period, inferring a benthic life

habit.

The extinction of choristoceratid heteromorphs is likely

related to the Rhaetian marine regression, which is associ-

ated with a sharp negative excursion in the stable carbon iso-

tope curve (Pálfy, Demény & Haas, 2001; Ward, Haggart &

Carter, 2001; Guex et al., 2003, 2004; Ward, Garrison &

Haggart, 2004). This agrees with their gradual disappear-

ance during the Rhaetian (Shevyrev, 2005). The last Triassic

heteromorph Choristoceras, went extinct together with other

monomorph ceratitids at the Triassic–Jurassic boundary.

Increased volcanism (i.e. ﬂood basalts) at the Central Atlantic

Magmatic Province during the break up of Pangea (Cohen &

Heteromorph ammonoid palaeobiology 23

Coe, 2002; Guex et al., 2004) likely resulted in the release of

sulfate aerosols and other pollutants. These pollutants

reduced the effect of solar radiation, causing short-term cool-

ing, while the release of greenhouse gases (carbon dioxide)

could have led to long-term warming. We assume that these

pertubations had their largest effect in the uppermost water

column causing a plankton crisis. This crisis eventually

affected marine ecosystems on a global scale. Some tropitids

and choristoceratids survived into the earliest Jurassic based

on rare occurrences from basal Hettangian strata

(Longridge & Smith, 2015). Choristoceratids have been

reported from Hettangian strata in North and South Amer-

ica (Guex, 1995; Guex et al., 2004, 2012) and ?Tibet (Yin

et al., 2007).

(3) Jurassic heteromorphs

Parapatoceras distans and other spiroceratids (Dietl, 1978,

1981) have a higher intraspeciﬁc variability compared to Tri-

assic heteromorphs (Jain, 2018). Accordingly, their coiling

mode is insufﬁcient to characterise species. Two pathways

from planispiral to orthocone conchs have been documented

for spiroceratids (Fig. 11), including radial and axial uncoil-

ing. The recognition of large intraspeciﬁc variability resulted

in a signiﬁcant reduction in the number of species from 38 to

12 (Dietl, 1978). Jurassic heteromorphs are often preserved

as fragments or small specimens. Dietl (1978) reported a frag-

ment of 40 mm whorl height indicating that they could grow

to large sizes. Similar to Triassic choristoceratids, their

sutures are simpliﬁed, and ornamentation comprises simple

straight ribs (Jain, 2018). Rows of tubercles suggest the pres-

ence of lateral and ventral spines. Mitta (2017) reported on

micro- and macroconchs with preserved apertures (lappets)

in Spiroceras (Jain, 2018).

The Spiroceratidae is composed of the two subfamilies

Spiroceratinae with Spiroceras and Parapatoceratinae, includ-

ing Parapatoceras,Paracuariceras, and Acuariceras. Due to mor-

phological resemblance, Mitta (2017) regarded Bajocia

rarinoda as potentially ancestral to Spiroceras aff. fourneti. Jain

(2018) discussed the descent of the oldest spiroceratids from

either Strenoceras or Bajocia, favouring the former. Jain (2018)

suggests that Spiroceras gave rise to Parapatoceras, and that Para-

patoceras gave rise to Epistrenoceras (a secondary monomorph)

and Paracuariceras, with the latter being the ancestor of Acuar-

iceras. This phylogeny contrasts with the hypothesis that spir-

oceratids and parapatoceratids had independent origins

(Besnossov & Kutuzova, 1990; Mitta, 2017; Galácz, 2019),

but produced morphologically similar convergent forms.

Besnossov & Kutuzova (1990) argued that the late Bajocian

heteromorph genera Apsorroceras and Spiroceras represent

macroconchs of the monomorphs Pseudogarantiana and Streno-

ceras and that all four genera evolved from the monomorph

Caumontisphinctes as members of the Spiroceratidae. Galácz

(2019) introduced the genera Kumetaceras and Sikeliceras, which

he regarded as microconchs and possible ancestors of

Parapatoceras.

The ﬁrst Jurassic heteromorphs appear during the late

Middle Bajocian (Arkelli/Bremeri Zone) with the genus Spir-

oceras and disappear with the extinction of Acuariceras during

the Early Oxfordian (Collotiformis Subzone, Athleta Zone).

According to Jain (2018) and Bert & Courville (2016), Juras-

sic heteromorphs range from 169.5 to 163 Ma (aged accord-

ing to Ogg et al., 2016). The Tithonian Protancyloceras is

hypothesised as the ancestor of Early Cretaceous hetero-

morphs (Wierzbowski, 1990; Sarti, 1999). Some species of

the genera Spiroceras and Parapatoceras are distributed world-

wide, such as S. orbignyi and S. annulatum. The latter was

recently reported from Kenya by Galácz (2017), whereas

others are more geographically restricted.

The global distribution of some species has been explained

by a planktic life habit of their hatchlings. Genera such as

Paracuariceras and Acuariceras are only known from France,

Germany, and Romania (Jain, 2018). These heteromorphs

occur frequently in clays (‘Hamitentone’) and their conchs

show substantial morphological variability. This led to the

hypothesis that spiroceratids inhabited calm water (Dietl,

1978). A vagile benthic life habit was inferred by the large

variability of conch morphology from planispiral via helicoid

to rhabdoceratid, i.e. from bilaterally symmetric to asymmet-

ric forms within a single species. Speciﬁcally, crawling loco-

motion on plants was suggested due to associated ﬁndings

of the bivalve ‘Posidonia’(Bositra), which are thought to have

lived in ‘macroalgae forest’(Dietl, 1978).

A benthic life of spiroceratids is contradicted by records

of spiroceratids within sideritic beds devoid of benthos

except for abundant Ophiopinna elegans (ophiuroids) in the

clays of La Voulte (Dietl & Mundlos, 1972). Shevyrev

(2005) revived the benthic habitat hypothesis for spirocera-

tids with their biotopes in dense algal thickets. He argued

that their hydrostatic apparatus enabled them to change

their position within these algal mats. Since spiroceratids

rarely co-occur with planispiral ammonoids, Shevyrev

(2005) speculated that they lived in cracks in the sea bottom

in calm water. Mitta (2017), however, found spiroceratids in

Bajocian siltstone nodules together with Baculatoceras,Calli-

phylloceras,Holcophylloceras,Pseudophylloceras,andMegalyto-

ceras, i.e. forms that inhabitat the pelagic realm. Herein,

spiroceratids are regarded as having a pelagic-

nektoplanktic life habit.

The higher-level systematics of Jurassic and Cretaceous

heteromorphs remains problematic. Different schemes are

available but there is no consensus. Arkell, Kummel &

Wright (1957) included all heteromorphs in the Lytoceratina.

Wiedmann (1966a,b) then included them in the Ancylocera-

tina. Subsequently, they were split into the Turrilitina and

Ancyloceratina (Doguzhaeva & Mikhailova, 1982; Besnos-

sov & Mikhailova, 1983), which was accepted by most subse-

quent workers (see Wright et al., 1996). Later, Shevyrev

(2006) assigned them to the Lytoceratoidea and Ammoni-

tida. Vermeulen (2005) added the Protancyloceratina. These

examples reﬂect the complexity of the interpretation of their

polyphyletic origin and evolutionary record (Matsukawa,

1987; Monks, 1999, 2000a).

24 René Hoffmann et al.

(4) Cretaceous heteromorphs and ammonoid

extinction

Heteromorphs have been classically linked to the extinction

of the ammonoids (Wiedmann, 1969). Their ‘aberrant’

conch shapes were often related to degeneration and phylo-

genetic extinction (e.g. Dacqué, 1935; Schindewolf, 1936,

1945; Müller, 1955). The fact that they are a dominant fau-

nal element in many Late Cretaceous ammonoid faunas

might have sustained this hypothesis. However, Mesozoic

heteromorphs were successful, particularly in the Cretaceous

(Fig. 11), as evidenced by their high abundance, generic

diversity, and morphological disparity (Seilacher, 2013). Ele-

vated generic diversity is recognised during the late Hauteri-

vian to Aptian, late Albian, and Coniacian to Campanian,

with peaks in the late Barremian, late Albian, and early Cam-

panian (Klein et al., 2007; Mikhailova & Baraboschkin,

2009). A wide variety of heteromorph conch shapes devel-

oped in the Cretaceous, but the most complex three-

dimensional shapes evolved within the Nostoceratidae with

genera like Nipponites,Pravitoceras,Eubostrychoceras,Didymoceras,

and Anaklinoceras (Wiedmann, 1969; Wright et al., 1996).

Heteromorphs are the most abundant faunal element

(mostly scaphitids and baculitids) documented at 29 out of

31 sites preserving a record from the last 0.5 Myr of the Cre-

taceous (Landman et al., 2014, 2015). New genera within the

Diplomoceratidae, Baculitidae, and Scaphitidae evolved

during the Maastrichtian (Fig. 12). The diversity of Nostocer-

atidae declined during the late Maastrichtian with only two

Nostoceras specimens known from the Maastrichtian type area

(van der Tuuk & Zijlstra, 1979).

Goolaerts (2010) concluded that the cause of the extinction

of ammonoids must have been a catastrophic event affecting

both heteromorph and monomorph diversity on a global

scale, in colder and warmer waters, in shallow and deeper

settings, and for a wide variety of taxa exhibiting different

food and life strategies. The Chicxulub impact at the Creta-

ceous/Paleogene (K/Pg) boundary (66 Ma; Schulte et al.,

2010) is currently regarded as the most probable trigger for

Fig. 12. Ranges of Maastrichtian to earliest Danian heteromorph genera. Taxonomy after Wright et al. (1996), with the omission of

Jeletzkytes and Karlwaageites following Landman et al. (2010b), Ponteixites following Grier et al. (2007), and the subgenus Tovebirkelundites

following Kennedy & Jagt (1998). In the absence of a fully integrated stratigraphic scheme for the subdivision and correlation of all

basins, the division of the Maastrichtian into the ﬁve bins (early early, late early, early late, late late, and last 0.5 million years) is

arbitrary. Phylogenetic relationships between scaphitid genera differ among authors (e.g. Cooper, 1994; Monks, 2000a), and are

therefore not included.

Heteromorph ammonoid palaeobiology 25

ammonoid extinction (Ward, 1996; Goolaerts, 2010; Land-

man et al., 2014, 2015; Petersen, Dutton & Lohmann,

2016; Witts et al., 2016; Tobin, 2017).

Ammonoids have been reported from beds above the

K/Pg boundary. Most of these records reﬂect reworked spec-

imens or resulted from an erroneously placed K/Pg boundary

level (Sadler, 1988; Landman, Johnson & Edwards, 2004a,b;

Landman et al., 2007a). However, some may belong to possi-

ble extinction event victims or even were true short-term sur-

vivors. At Tanis, North Dakota, the monomorph Sphenodiscus

is the only ammonoid recorded from beds directly correlated

to the Chicxulub impact (De Palma et al., 2019).

In Denmark, ammonoids from the Cerithium Limestone

were considered as reworked until Machalski & Heinberg

(2005) reported early Danian age inﬁlling of the conchs,

which favoured the short-term survivor hypothesis for Hoplo-

scaphites constrictus johnjagti and Baculites vertebralis (Machalski

et al., 2009). The Cerithium Limestone was deposited

between 40 and 500 kyr after the K/Pg boundary

(Rasmussen, Heinberg & Håkansson, 2005).

In the type Maastrichtian area (The Netherlands, Bel-

gium), ammonoids were found up to 2 m above the K/Pg

boundary (Goolaerts, 2010; Jagt et al., 2013; Vellekoop

et al., 2020). The fauna consists exclusively of heteromorphs:

Eubaculites latecarinatus,Baculites spp. and H. constrictus johnjagti

(Landman et al., 2014, 2015). These are regarded as true sur-

vivors (Vellekoop et al., 2020), but in contrast to Denmark,

the ammonoids range in age from hundreds to thousands of

years after the K/Pg boundary.

In New Jersey (USA), non-reworked ammonoids were

found above an iridium anomaly, which likely represents

the K/Pg boundary (Landman et al., 2007a, 2010a, 2012c,

2014, 2015). In the Pinna Layer, which contains the iridium

anomaly at its base, the fauna is dominated by the hetero-

morphs Discoscaphites and Eubaculites. In the overlying Bur-

rowed Unit, Discoscaphites and Eubaculites have also been

recorded.

Tajika et al. (2018, 2020)discussed the ecological framework

of the ammonoid extinction at the K/Pg boundary. Tajika

et al. (2018) suggested ecological replacement of the micro- to

mesoplanktic ammonoid (and belemnite) hatchlings by holo-

planktic gastropods in the Paleogene. Tajika et al. (2020)

hypothesised that a combination of higher metabolic rates, a

microphageous diet, and small hatchling size (i.e. limited

resources) likely caused the selective extinction of the ammo-

noids. By contrast, nautilids and coleoids with different metab-

olism, macrophageous to scavenging diets, and varying

reproductive strategies survived the K/Pg mass extinction.

VII. CONCLUSIONS

(1) This review of published data on the soft body, conch

organisation, habitat, and palaeoecology of hetero-

morph ammonoids has resulted in a detailed and

robust reconstruction of their palaeobiology. It

should provide a useful background for those study-

ing the life habits of extinct animals and more specif-

ically heteromorphs.

(2) The digestive tract of heteromorphs with an oesoph-

agus, crop, and stomach, follows the molluscan U-

shaped bauplan. Their brain was likely well devel-

oped as in other cephalopods, because of the need

to control their position in the water column and to

process information provided from their lens eyes

and statocysts. Based on phylogenetic bracketing,

we assume that heteromorphs had 10 arms and

lacked suckers, hooks, and tentacles (extendable

arms). Heteromorphs had no hood and ink sac but

probably had ammonia in their soft tissues, which

resulted in the rapid decay of soft parts, explaining

their absence in the fossil record.

(3) The buccal apparatus in heteromorphs shares the

general pattern of ammonoid jaws: a smaller upper

jaw inserted into a longer and larger lower jaw. All

Cretaceous heteromorphs share an aptychus-type

lower jaw with a lamellar calcitic covering. Aptychi

may have fulﬁlled multiple functions: lower jaw,

operculum, ﬁltering device, ﬂushing benthic prey,

pumping for jet propulsion, regulating conch posi-

tion, and stabilisation against rocking.

(4) Differences in the morphology and size of radular

teeth reported for heteromorphs suggest preferences

for microphagous prey (i.e. zooplankton).

(5) Based on functional morphological and phylogenetic

constraints, the presence of muscles such as the

cephalic retractors, hyponome retractors, ventral

muscle, and mantle musculature are assumed for het-

eromorphs. Homologisation of ammonoid muscles

and their attachment sites with those of coleoids and

nautilids will require soft tissue preservation.

(6) Heteromorphs could achieve nearly neutral buo-

yancy regardless of conch shape or ontogeny. This

was potentially achieved by adding ﬂuid to a posi-

tively buoyant conch or counteracting slight negative

buoyancy through swimming. Encrustation by epizo-

ans like barnacles, brachiopods, and bivalves sup-

ports the buoyant heteromorph hypothesis and

contradicts the idea of a benthic habitat.

(7) A vertical orientation for orthoconic heteromorphs has

been proposed based on physical and virtual models.

Ancylocone conchs likely had a near-horizontal aper-

ture pointing upwards. Heteromorphs with a U-

shaped body chamber (nostocones, scaphiticones,

and ancylocones) are more stable hydrodynamically

than modern Nautilus and were unable to modify sub-

stantially their orientation by active locomotion,

i.e. had no or limited access to benthic prey. These

forms have their hyponomes horizontally aligned with

their centres of rotation, allowing more energy to be

transmitted to translational movement with minimal

rocking, i.e. these morphotypes are well suited for

backwards horizontal swimming at maturity.

26 René Hoffmann et al.

(8) Pathologies reported for ancylocone scaphitids were

likely inﬂicted by crustaceans, ﬁsh, marine reptiles,

and other cephalopods. Injuries in baculitids have

been assigned to pycnodontid ﬁsh, coleoids, and ben-

thic crustaceans. Pathologies of Ptychoceras corrobo-

rate an external shell and reject the endocochleate

hypothesis for this taxon.

(9) Stomach contents of Cretaceous heteromorphs com-

prise planktic crustaceans, gastropods, and crinoids

suggesting a zooplanktic diet. Forms with a U-shaped

body chamber (ancylocone) are regarded as suspen-

sion feeders, whereas orthoconic conchs might have

had access to benthic prey. A carnivorous diet for het-

eromorphs is supported by the fact that all modern

cephalopods are carnivorous.

(10) Heteromorphs are known from a broad range of

litho- and biofacies. These facies associations

change through time among and within respective

clades. Devonian, Triassic, and Jurassic hetero-

morphs show a preference for deep-subtidal to off-

shore facies but are rare in shallow-subtidal, slope,

and bathyal facies. Early Cretaceous heteromorphs

preferred deep-subtidal to bathyal facies but are

rare in shallow-subtidal facies. Late Cretaceous het-

eromorphs are common in shallow-subtidal to off-

shore facies but rare in slope and bathyal facies.

The increase in heteromorph species in shallow-

subtidal settings during the Late Cretaceous likely

reﬂects an evolutionary shift to shallower-water

environments.

(11) Adult Discoscaphites and Baculites show oxygen iso-

tope values supporting an interpretation of rapid

growth and a demersal habitat. Analyses of the ear-

liest whorls of Hoploscaphites suggest a benthic

embryonic stage, planktic hatchlings, and a habitat

change after about one whorl. Carbon isotope

values derived from Baculites from the Western Inte-

rior Seaway indicate that some heteromorphs lived

on or close to cold seeps throughout their lives and

likely exploited the diverse prey available at the

seeps.

(12) Heteromorphs have the smallest hatchlings of all

Cretaceous ammonoids. Constraints imposed by

adult size and mobility potentially drove selection

for more and/or smaller hatchlings adapted to a

planktic life. This implies high fecundity and an eco-

logical role of the hatchlings as micro- and

mesoplankton.

(13) Various environmental factors, partially reﬂected in

the litho- and biofacies, explain the large degree of

intraspeciﬁc variation in heteromorphs. So far, only

scaphitid conch characters have been shown to vary

with environment, in accordance with their nekto-

benthic life habit, e.g. whorls being more com-

pressed, more umbilicate, and less nodose in

nearshore facies compared to specimens from off-

shore facies.

(14) The Maastrichtian is noted for the evolution of new

ammonoid genera and at many latest Cretaceous

localities, heteromorphs are the most abundant

macrofaunal element. The cause of the extinction of

ammonoids must have been a catastrophic event

affecting their diversity on a global scale and for a

wide variety of organisms exhibiting different life

habits. The Chicxulub impact at the K/Pg boundary

(66 Ma) is the likely trigger for their ﬁnal extinction.

(15) Post-K/Pg-boundary ammonoid survivors are all

heteromorphs, which likely survived up to 40–500

kyr after the mass extinction event.

(16) The heteromorph and monomorph ammonoid

extinction is linked to their small hatchling sizes,

planktotrophic diets, and high metabolic rates. The

end-Cretaceous event caused a collapse of marine

primary producers, which allowed only cephalopods

with sufﬁcient energy reserves, macrophageous diet,

and low metabolic rates to survive.

VIII. ACKNOWLEDGEMENTS

We are grateful to Alexander Lukeneder and two anony-

mous reviewers for constructive comments that signiﬁcantly

improved the quality of this review, and to John Welch and

Alison Cooper for the handling of this manuscript.

A.M. acknowledges ﬁnancial support from RFBR grant

no. 18-05-01070, the Russian amateur palaeontologists

Marina and Andrei Belousko and Dmitry Vartanian for the

donation of Ptychoceras specimens for this study, and Dmitry

Vinogradov for permission to photograph specimens from

his collection. S.G. received funding from the Belspo

BR/175/A2/CHICXULUB project ‘Chicxulub 2016

IODP-ICDP deep drilling: From cratering to mass-extinc-

tion’. J.S. acknowledges Garett M. Brown, Peter J. Harries,

Keith P. Minor, Neil H. Landman, and Ashley L. Sandness.

R.H. is grateful to Kevin Stevens for helpful comments on

an early draft, Phyllis Mono for help with formatting, Gernot

Nehrke for the Raman images shown in Fig. 2, and M. Rogov

for helping us to ﬁnd the originator of the term ‘hetero-

morph’. Images of injured specimens were provided by Sönke

Simonsen for Aegocricoeras raricostatum, Wolfgang Grulke for

Pictetia, Kurt Wiedenroth for Aegocrioceras. R.H. thanks the

DFG for ﬁnancial support of this project (DFG HO

4674/4-1). C.K. received ﬁnancial support from the Swiss

National Science foundations (project nr. 200020_169847,

200021_149119, and 200020_169627). Open access funding

enabled and organized by Projekt DEAL. Open access fund-

ing enabled and organized by Projekt DEAL.

IX. REFERENCES

Arkadiev, V. V. (2008). Representatives of the family Bochianitidae (Ammonoidea)

from the Lower Cretaceous of the Crimean Mountains. Paleontological Journal 42,

18–26.

Heteromorph ammonoid palaeobiology 27

Arkell, W. J.,Kummel, B. &Wright, W. (1957). Mesozoic Ammonoidea. In Treatise

on InvertebratePalaeontology, Part L, Mollusca4. Cephalopoda, Ammonoidea (ed.R. C. MOORE),

pp. 80–465. Geological Society of America & University of Kansas Press, Boulder.

Arkhipkin, A. I. (2014). Getting hooked: the role of a u-shaped body chamber in the

shell of adult heteromorph ammonites. Journal of Molluscan Studies 80, 354–364.

Auclair, A.-C.,Lecuyer, C.,Bucher, H. &Sheppard, S. M. F. (2004). Carbon

and oxygen isotope composition of Nautilus macromphalus: a record of thermocline

waters off New Caledonia. Chemical Geology 207,91–100. https://doi.org/10.1016/

j.chemgeo.2004.02.006.

Balinski, A. (2010). First colour-patterned strophomenide brachiopod from the

earliest Devonian of Podolia, Ukraine. Acta Palaeontologica Polonica 55, 695–700.

Baraboschkin, E. Y. &Enson, K. V. (2003). Paleobathymetry of the Valanginian-

Aptian Basin in the Crimean Mountains based on strength indices of ammonoid

shells. Vestnik Moskov University Series 4 –Geology 4,8–17.

Barnard, W. &de Waal, D. (2006). Raman investigation of pigmentary molecules in

the molluscan biogenic matrix. Journal of Raman Spectroscopy 37, 342–352.

Barragan, R.,Gonzalez-Arreola, C. &Villasen

˜or, A. B. (2004).

Palaeoecological signiﬁcance of Barremian ammonite assemblages and facies

variations from Southwest Mexico. Lethaia 37, 223–234.

Batt, R.J. (1986). A test of the effects of paleoecological factors on the distribution of

ammonite shell morphotypes. Greenhorn Cyclothem,Cretaceous Western Interior Seaway.

Cretaceous Biofacies of the Central Part of Western Interior Seaway: A Field Guidebook,16−52.

Batt, R. J. (1989). Ammonite shell morphotype distributions in the Western Interior

Greenhorn Sea and some paleoecological implications. PALAIOS 4,32–42.

Bayer, U. (1970). Anomalien bei Ammoniten des Aaleniums und Bajociums und ihre

Beziehung zur Lebensweise. Neues Jahrbuch für Geologie und Paläontologie, Abhandlungen

135,19

–41.

Berry, K. (2018a). Baculites taphonomy: a new technique for identifying potential cases

of long-distance post-mortem dispersal in Cretaceous ammonites. In Fossil Record 6:

New Mexico Museum of Natural History and Science Bulletin (Volume 79, eds S. G. LUCAS

and R. M. SULLIVAN Albuquerque, NM: New Mexico Museum of Natural History

and Science), pp. 51–54.

Berry, K. (2018b). On the palaeoecology of the index ammonites Baculites (Lamarck,

1799) and Scaphites (Parkinson, 1811) as revealed by a study of relatively rare

epizoans. Neues Jahrbuch für Geologie und Paläontologie Abhandlungen 288, 221–226.

Bert, D. (2013). Factors of intraspeciﬁc variability in ammonites, the example of

Gassendiceras alpinum (d’Orbigny, 1850) (Hemihoplitidae, upper Barremian). Annales

de Paléontologie 100, 217–236.

Bert, D. &Courville, P. (2016). First record of late Callovian to early Oxfordian

heteromorph ammonites. Annales de Paléontologie 102, 117–121.

Besnossov, N. V. &Kutuzova, V. V. (1990). Systematic of the Middle Jurassic

heteromorphic ammonites. Paleontological Zhurnal 1990,23–30.

Besnossov, N. V. &Mikhailova, I. A. (1983). Evolution of the Jurassic-Cretaceous

Ammonoids. Doklady Akademii Nauk SSSR 269, 733–737.

Birkelund, T. (1965). Ammonites from the Upper Cretaceous of West Greenland.

Meddelser om Gronland, Kommisionen for Videnskabelige Undersögelser I Grönland 179,1–192.

Bragg, W. H. &Bragg, W. L. (1913). The reﬂexion of x-rays by crystals. Proceedings of

the Royal Society of London A 88, 428–438.

Brayard, A.,Escarguel, G.,Monnet, C.,Jenks, J. F. &Bucher, H. (2015).

Biogeography of Triassic ammonoids. In Ammonoid Paleobiology: From Macroevolution

to Paleogeography. Topics in Geobiology (Volume 44, eds C. KLUG,D.KORN,K.DE

BAETS,I.KRUTA and R. H. MAPES), pp. 359–426. Springer, Dordrecht.

Breitkreutz, H.,Diedrich, R. &Metzdorf, R. (1991). Fossilfunde aus der

Schwarz-bunten Wechselfolge (Ob. Cenoman bis Unter Turon) des

Ostwestfalendammes bei Bielefeld. Bericht des Naturwissenschaftlichen Vereins für

Bielefeld und Umgegend 32,37–48.

Casey, R. (1980). A monograph of the Ammonoidea of the Lower Greensand, part 9.

Monograph of the Palaeontographical Society 133, 633–660.

Cecca, F. (1997). Late Jurassic and Early Cretaceous uncoiled ammonites; trophism-

related evolutionary processes. Comptes rendus de l’Académie des Sciences 325, 629–634.

Chamberlain, J. A.,Ward, P. D. &Weaver, J. S. (1981). Post-mortem ascent of

Nautilus shells: implications for cephalopodpaleobiogeography.Paleobiology 7,494–509.

Checa, A. G.,Okamoto, T. &Keupp, H. (2002). Abnormalities as natural

experiments: a morphogenetic model for coiling regulation in planispiral

ammonites. Paleobiology 28, 127–138.

Chlupa

´cˇ,I.&Turek, V. (1983). Devonian goniatites from the Barrandian area,

Czechoslovakia. Rozpravy, dstredniho dstavu geologickkho 46,1–159.

Clarke, M. R. &Maddock, L. (1988). Beaks of Living Coleoid Cephalopoda, pp. 123–131.

Academic Press, Cambridge.

Clements, T.,Colleary, C.,De Baets, K. &Vinther, J. (2017). Buoyancy

mechanisms limit preservation of coleoid cephalopod soft tissues in Mesozoic

Lagerstätten. Palaeontology 60,1–14.

Closs, D. (1967a). Goniatiten mit Radula und Kieferapparat in der Itararé Formation

von Uruguay. Paläontologische Zeitschrift 41,19

–37.

Closs, D. (1967b). Upper Carboniferous anaptychi from Uruguay. Ameghiniana 5,

145–148.

Cobban, W. A. (1993). Diversity and distribution of Late Cretaceous ammonites,

Western Interior,United States.Geological Association of Canada, Special Paper 39, 435–451.

Cobban, W. A.,Kennedy, W. J. &Scott, G. R. (1993). Upper Cretaceous

heteromorph ammonites from the Baculites compressus zone of the Pierre shale in

north-Central Colorado. US Geological Survey Bulletin 2024,A1–A11.

Cohen, A. S. &Coe, A. L. (2002). New geochemical evidence for the onset of

volcanism in the Central Atlantic Magmatic Province environmental changes at

the Triassic-Jurassic boundary. Geology 30, 267–270.

Company, M. (1987). Los ammonites del Valanginiense del sector oriental de las

Cordilleras Bética (SE de Espana). Tesis Doctoral (Univ. Granada, 1987).

Cooper, M. R. (1994). Towards a phylogenetic classiﬁcation of the Cretaceous

ammonites. III. Scaphitaceae. Neues Jahrbuch für Geologie und Paläontologie,

Abhandlungen 193, 165–193.

Dacque

´,E.(1935). Organische Morphologie und Paläontologie, p. 476. Borntraeger, Berlin.

Davis, R. A.,Mapes, R. H. &Klofak, S. M. (1999). Epizoa on externally shelled

cephalopods. In Fossil Cephalopods: Recent Advances in their Study (eds A. V. ROZANOV

and A. A. SHEVYREV), pp. 32–51. Russian Academy of Sciences, Palaeontological

Institute, Moscow.

De Baets, K.,Klug, C.,Korn, D. &Landman, N. H. (2012). Early evolutionary

trends in ammonoid embryonic development. Evolution 66, 1788–1806.

De Baets, K.,Klug, C.,Korn, D.,Bartels, C. &Poschmann, M. (2013a). Emsian

Ammonoidea and the age of the Hunsrück slate (Rhenish Mountains, Western

Germany). Palaeontographica, Abteilung A 299,1–113.

De Baets, K.,Klug, C. &Monnet, C. (2013b). Intraspeciﬁc variability through

ontogeny in early ammonoids. Paleobiology 39,75–94.

De Baets, K.,Bert, D.,Hoffmann, R.,Monnet, C.,Yacobucci, M. M. &

Klug, C. (2015a). Ammonoid intraspeciﬁc variability. In Ammonoid Paleobiology:

From Anatomy to Ecology. Topics in Geobiology (Volume 43, eds C. KLUG,D.KORN,

K. DEBAETS,I.KRUTA and R. H. MAPES), pp. 359–426. Springer, Dordrecht.

De Baets, K.,Keupp, H. &Klug, C. (2015b). Parasites of ammonoids. In Ammonoid

Paleobiology: From Anatomy to Ecology. Topics in Geobiology (Volume 43, eds C.

KLUG,D.KORN,K.DEBAETS,I.KRUTA and R. H. MAPES), pp. 837–875.

Springer, Dordrecht.

De Baets, K.,Landman, N. H. &Tanabe, K. (2015c). Ammonoid embryonic

development. In Ammonoid Paleobiology: From Anatomy to Ecology. Topics in

Geobiology (Volume 43, eds C. KLUG,D.KORN,K.DEBAETS,I.KRUTA and

R. H. MAPES), pp. 113–205. Springer, Dordrecht.

De Palma, R. A.,Smit, S.,Burnham, D. A.,Kuiper, K.,Manning, P. L.,

Oleinik, A.,Larson, P.,Maurrasse, F. J.,Vellekoop, J.,Richards, M. A.,

Gurche, L. &Alvarez, W. (2019). A seismically induced onshore surge deposit

at the KPg boundary, North Dakota. Proceedings of the National Academy of Sciences of

the United States of America 116, 8190–8199.

Denton, E. J. &Gilpin-Brown, J. B. (1966). On the buoyancy of the pearly nautilus.

Journal of the Marine Biological Association of the United Kingdom 46, 723–759.

Dietl, G. (1978). Die heteromorphen Ammoniten des Doggers. Stuttgarter Beiträge zur

Naturkunde Serie B (Geologie und Paläontologie) 33,1–97.

Dietl, G. (1981). Über Paracuariceras und andere heteromorphe Ammoniten aus dem

Macrocephalen-Oolith (Unter-Callovium, Dogger) des Schwabischen Juras.

Stuttgarter Beiträge zur Naturkunde Serie B (Geologie und Paläontologie) 76,1–15.

Dietl, G. &Mundlos, R. (1972). Ökologie und Biostratinomie von Ophiopinna elegans

(Ophiuroidea) aus dem Untercallovium von La Voulte (Südfrankreich).Neues

Jahrbuch für Geologie und Paläontologie Monatshefte 1972, 449–464.

Doguzhaeva, L. A. &Mapes, R. H. (2015). The body chamber length variations

and muscle and mantle attachments in ammonoids. In Ammonoid Paleobiology

Volume: From Anatomy to Ecology. Topics in Geobiology (Volume 43, eds C. KLUG,

D. KORN,K.DEBAETS,I.KRUTA and R. H. MAPES), pp. 545–584. Springer,

Dordrecht.

Doguzhaeva, L. A. &Mikhailova, I. (1982). The genus Luppovia and the phylogeny

of Cretaceous heteromorphic ammonoids. Lethaia 15,55–65.

Doguzhaeva, L. A. &Mikhailova, I. (2002). The jaw apparatus of the

heteromorphic ammonite Australiceras whitehouse, 1926 (Mollusca: Cephalopoda)

from the Aptian of the Volga region. Doklady Biological Sciences 382,38–40.

Doguzhaeva, L. A. &Mutvei, H. (1989). Ptychoceras - a heteromorphic lytoceratid

with truncated shell and modiﬁed ultrastructure (Mollusca: Ammonoidea).

Palaeontographica A 208,91–121.

Doguzhaeva, L. A. &Mutvei, H. (1993). Shell ultrastructure, muscle-scars, and

buccal apparatus in ammonoids. Geobios 26, 111–119.

Doguzhaeva, L. A. &Mutvei, H. (2015). The additional external shell layers

indicative of “endocochleate experiments”in some ammonoids. In Ammonoid

Paleobiology: From Anatomy to Ecology. Topics in Geobiology (Volume 43, eds C.

KLUG,D.KORN,K.DEBAETS,I.KRUTA and R. H. MAPES), pp. 585–609.

Springer, Dordrecht.

Doguzhaeva, L. A.,Mapes, R. H. &Mutvei, H. (2002). Shell morphology and

ultrastructure of the early Carboniferous Coleoid Hematites Flower & Gordon,

1959 (Hematitida Ord. Nov.) from midcontinent (USA). Abhandlungen der

Geologischen Bundesanstalt (Vienna) 57, 299–320.

28 René Hoffmann et al.

Doguzhaeva, L. A.,Mutvei, H.,Summesberger, H. &Dunca, E. (2004).

Bituminous soft body tissues in the body chamber of the late Triassic ceratitid

Austrotrachyceras from the Austrian Alps. Mitteilungen aus dem Geologisch-Paläontologischen

Institut der Universität Hamburg 88,37–50.

Ebbighausen, V.,Becker, R. T.,Bockwinkel, J. &Aboussalam, Z. S. (2007).

Givetian (Middle

Recent advances in heteromorph ammonoid palaeobiology

Abstract and Figures