Selected specimens from the Jurassic ammonoid family Arietitidae were
investigated using morphometric methods of transverse and longitudinal conch
section analysis. The family Arietitidae is characterized by similarities in
the conch geometry, but variation can be demonstrated by means of
differences in conch morphology. Our study focuses on a specimen of the
arietitid
In the 19th century, research on the Jurassic period had already revealed the stunning diversity and disparity of its ammonite faunas (e.g. Orbigny, 1842; Quenstedt, 1858, 1885–1888; Hyatt, 1889; Wähner, 1895). Unsurprisingly, it was the same people who also discovered remains of other organisms attached to the ammonite conchs, either syn vivo or post mortem. Among Jurassic ammonites, representatives of the Arietitidae are remarkable because of the combination of their often large size (up to almost one metre; Stevens, 1988), great abundance (and correspondingly their ecological importance), and also their role in the Early Jurassic re-diversification (e.g. Donovan et al., 1981; Neige et al., 2013).
The fossil record has been yielding countless ammonoid specimens, whose conchs show signs of anomalies. Similarly, remains of other organisms settling on ammonoid conchs are quite common (e.g. Seilacher, 1960, 1982; Stilkerich et al., 2017). Evidence for an organism settling on an ammonoid conch syn vivo can mainly be found in the reaction to this epizoan by the ammonoid animal and the specific orientation of the epizoan (Seilacher, 1960; Meischner, 1968; Keupp et al., 2011). Since many organisms inhabited ammonoid conchs post mortem, Davis et al. (1999) differentiated between post-mortem epicoles and syn vivo epizoans (Linck, 1956; Klug and Korn, 2001). Hölder (1956) classified such anomalies caused by epizoans in terms of a forma aegra nomenclature, the use of which Keupp (2012) continued in an extensively illustrated work with numerous illustrated examples of a wide range of anomalies in ammonoids (see also Hengsbach, 1991, 1996; Hoffmann and Keupp, 2015). Cases in which deformation of the shell and/or deviation from the normal planispiral coiling were caused by encrusters provide incontrovertible evidence that the encrusters colonized the shell while the host lived (Checa et al., 2002; Luci and Cichowolski, 2014). A parasitic nature, but not only this, can be assumed to be the cause of some abnormal malformations of ammonoid conchs (a review over parasitoses can be found in De Baets et al., 2015). These parasitoses were defined by Keupp (2012) as “organismic interrelationships in which a parasite in or on an organism is temporarily or permanently determined and permanently damages its host”.
If parasitoses occur with Recent representatives of cephalopods as described
in the form of the negative interaction of
A thorough review of ammonites with syn vivo growth of epizoans was given by
Andrew et al. (2011), who figured a number of specimens of the Early
Jurassic
We investigated a sectioned specimen of
Our investigation of conch ontogeny in the family Arietitidae is mainly based on cross sections. This method allows the collection of large morphometric data sets (e.g. Korn, 2010; Klug et al., 2015), which optimally represent the entire ontogeny of the ammonites under investigation. The morphometric parameters and ratios taken from the cross sections for the study of the conch ontogeny are, following Korn (2010), conch diameter (dm), whorl width (ww) and whorl height (wh). The following parameters and ratios can be calculated on the basis of these measured values: umbilical width (uw), aperture height (ah); and the ratios and indexes (Fig. 3) conch width index (CWI), whorl width index (WWI), umbilical width index (UWI) and whorl expansion rate (WER).
Conch dimensions, ratios and rates obtained from ammonoid conch cross sections.
Conch cross sections and ontogenetic trajectories of whorl width
index (ww/dm), umbilical width index (uw/dm) and whorl expansion rate (WER)
in arietid specimens.
Conch cross sections and ontogenetic trajectories of whorl width
index (ww/dm), umbilical width index (uw/dm) and whorl expansion rate (WER)
in arietid specimens.
Septal distances (in degrees) and whorl expansion rate (WER)
obtained from longitudinal sections of arietid specimens.
The specimens are stored in the cephalopod collection of the Museum für Naturkunde, Berlin (catalogue numbers MB.C.) and the Paläontologisches Institut und Museum, Zürich (catalogue number PIMUZ).
The following specimens were sectioned (with the range of preserved
volutions):
MB.C.15812 (Krüger Coll.),
We obtained conch diameters from longitudinal (sagittal, in the plane of
symmetry) sections in two ways, using distances of 10 and 90 degree angles (Fig. 6). The whorl expansion rate was then calculated for
these growth increments for documentation of the coiling principles of the
species under study. In a second approach, we measured the distance of the
phragmocone septa (angle
All representatives of the family Arietitidae share a number of conch
characteristics, which are variable within genera and species with rather
narrow limits:
The adult conch is thinly discoidal (ww/dm The whorl profile is often nearly circular or quadrate (ww/wh The venter is characterized by a median keel that is accompanied on both
sides by more or less pronounced longitudinal grooves.
Analyses of the morphometric conch data revealed recurring patterns in the
ontogenetic development of cardinal conch parameters. The conch ontogeny
of arietitid ammonites is very similar between species, as outlined by the
two rather different species The conch width index (ww/dm) decreases during ontogeny; It appears that this trend is not linear as it is decelerated in relatively
large specimens, as seen in The umbilical width index (uw/dm) increases during ontogeny; This trend is monophasic in both specimens and can also be observed in the
large specimens of The whorl expansion rate (WER) decreases during ontogeny; The ontogenetic trend in coiling is not linear and shows a phase of
stagnation in both specimens. The large specimens of These patterns of allometric conch growth differ markedly from most of the
Palaeozoic and Triassic ammonoids, which usually show negative allometry of
the umbilical width index and a positive allometry of the whorl expansion
rate (e.g. Korn, 2012). Even in Palaeozoic and Triassic ammonoids which
possess evolute conchs, there is usually an adult decrease of the uw/dm
ratio and an increase or stagnation of the whorl expansion rate (Klug, 2001;
Walton and Korn, 2017). Representatives of the Late Devonian families
Platyclymeniidae, Clymeniidae and Kosmoclymeniidae, for instance show an
adult change towards a compressed whorl profile and weak reduction of the
umbilical width index (e.g. Korn and Price, 1987; Korn, 2002; Nikolaeva and
Bogoslovsky, 2005). The whorl expansion rate oscillates within limits in
these forms without a clear trend. A similar situation can be seen in
evolute Middle Devonian genus The angular length of the phragmocone chambers decreases during growth.
This ontogenetic trend, however, is occasionally interrupted by intervals
where greater and smaller septum distances occur (Fig. 6). The variation of
septum distances can be interpreted by changes in the growth rate during the
ontogenetic development of the ammonite conchs, which can occur, for
example, when the adult stage is reached (Westermann, 1971). Also adverse
environmental factors such as temperature or food availability may cause
septal crowding (Bucher et al., 1996; Kraft et al., 2008). Parasitic
infestations might locally also effect septal spacing (e.g. De Baets et al.,
2013).
Specimen MB.C.27997 was sectioned through the initial chamber in order to uncover how the worm infestation changed the morphological development of some of the conch parameters and to what degree such changes occurred. It can be seen from the cross-sectional drawing (Fig. 5a) that the worm grew on the venter of the ammonite conch over a distance of between one and a half and two whorls. The position of the worm tube changes slightly, during the growth of the ammonite the aperture of the worm tube migrated from a nearly central position on the venter to the left side of the venter, occupying a position in the ventrolateral groove.
The conch ontogeny of the worm tube bearing specimen shows a number of
characteristics deviating from other conspecific specimens in some, but not
all traits (Fig. 5a–c):
The conch width index (ww/dm) is negatively allometric and biphasic; it
is stable at 0.60 between 1 and 3 mm diameter and thereafter decreases to 0.30 at
a 100 mm diameter. In this respect the specimen closely resembles specimen
MB.C.15950.1 ( The umbilical width index (uw/dm) is positively allometric and
triphasic; after a juvenile decrease, it increases, in the growth interval
between 4 and 11 mm diameter, from 0.23 to about 0.40 and later remains at
this value. In this respect, there are also similarities with specimen
MB.C.15950.1. The whorl expansion rate oscillates between 1.90 and 2.10 in the growth
interval between 1 and 12 mm diameter without a clear trend. Thereafter, a
steep increase to 2.40 at 26 and 42 mm diameter follows with a subsequent
sudden decline to a value of 2.05 at 58 mm diameter. The data suggest that
this increase in the coiling rate was caused by the overgrowth of the worm tube on the venter of the ammonoid conch and the modified geometry. However,
a
reconstruction of the conch without the worm tube leads to an
interesting result; the coiling rate is increased even when the worm tube is
removed and the whorls would weakly embrace the preceding whorl as typical
of the species (Fig. 5b, c). This can be interpreted as a reaction of the
whorl height to the worm infestation. During the interval of infestation by the worm on the ammonite's venter,
the animal was not able to attach its new whorls to the preceding whorl. The
ammonite therefore used the worm tube as the contact surface. This happened
in such a way that the centre of the dorsal side was aligned to the tube (Figs. 2, 5a). To stabilize the upright position of the specimen in the water column,
rotation of the whorl profile was necessary (compare Stilkerich et al.,
2017) (Fig. 5a). This rotation is visible in the inclination of the whorls
beginning with the infestation on the venter. The whorl profile half a
volution prior to the first visible tube on the venter is unaffected, which
can be seen as evidence for an infestation between the eighth and the tenth
half whorl.
Examination of the conch parameters in the specimen leads to the conclusion
that the whorl height mainly responded by increasing in the presence of the
worm tube. Consequently, the coiling rate of the conch
also increased. As an increase in the coiling rate causes shortening of the body
chamber (measured in angle degrees), this might have been facilitated by the
specimen to maintain neutral buoyancy.
The morphological changes of the conch geometry, which occur in the specimen as a result of worm infestation from the tenth half-volution, need to be considered in more detail. The focus of the investigation is on the deviation of the affected whorls from the vertical symmetry axis (and thus from planispiral coiling) of the specimen. As usual for ammonoids, the growth of the conch was bilaterally symmetrical but with a variety of deviations from isometric growth (Korn, 2012) and in the absence of disturbing factors such as a worm tube on the external side of the conch or severe injuries of the shell (e.g. Keupp, 2012; Hoffmann and Keupp, 2015). Individuals with undisturbed growth may orient themselves, in the course of coiling, on the keel of the preceding volution. This is described as the road-holding model in gastropods (Hutchinson, 1989) and hypothesized as the piggyback whorl model in ammonoids (Ubukata et al., 2008). The existence of the worm tube misled the ammonoid examined here to align the subsequent whorls with the worm tube. The displacement caused by the worm tube therefore results in a lateral displacement of the whorls oriented thereon. The first half-whorl affected by the worm tube shows a strong deviation (about 5 degrees) relative to the axis of symmetry of the ammonite (Fig. 5a). Along the following volutions, the specimen appears to compensate for this deviation: the angles of deviation of the individual half-whorls oscillate around the axis of symmetry; the amplitude (i.e., the amount of deviation) decreases in the course of ontogeny.
It is evident that the worm tube was entirely overgrown by the ammonite in the course of building ontogenetically later volutions. These volutions orient themselves during their growth on the serpulid tube and show conspicuous deviations from the normal conch symmetry.
The ammonite specimen was facing three major problems when infested by the
serpulid:
Morphometric investigations of the conch geometry of specimen MB.C. 27997 of
According to Checa et al. (2002), the anomaly compensating growth of the specimen serves not only to maintain the equilibrium position in the water column, but also to ensure the correct aperture orientation, which is a prerequisite for the ammonite's buoyancy pursuing a nektonic lifestyle (Klug et al., 2004, 2010; Stilkerich et al., 2017).
The cross-sectional drawing of the specimen shows that the worm tube was attached to the ammonite conch over three half-volutions. The fact that the volutions impaired by the worm tube in the course of ontogeny are connected with further whorls shows that the animal has survived the worm infestation. Furthermore, the specimen has maintained a way of life which enabled it to continue conch growth by at least two further whorls. The survival of the host was also important for the worm itself, since it could only take advantage of the interrelationship over a longer period (Meischner, 1968; Andrew et al., 2011; Hautmann et al., 2017).
Based on our study, the extent to which the specimen was able to maintain the hydrodynamic equilibrium in the water column, especially in the ontogenetic stages immediately following worm infestation, must remain investigated. The question of the floatability of the specimen under the influence of the epizoan parasite cannot be answered in the course of this study.
It is remarkable how tolerant ammonites were towards epizoans. Epizoans are commonly encountered in numerous ammonite species (e.g. Seilacher, 1960; Keupp et al., 1999; Klug and Korn, 2001; Klug et al., 2004; Tajika et al., 2015), while in nautilids, such cases are much rarer (e.g. Landman et al., 2010). However, epizoans evidently altered the buoyancy of the ammonoid conch and caused the cephalopod's reaction to compensate for the added mass and to ultimately maintain neutral buoyancy (Klug et al., 2004). These reactions represent an indirect proof for the importance of neutral buoyancy of ammonoids and for their habitat within the water column, be it close to the sediment surface (nektobenthic) or higher (nektonic to planktonic, depending on conch shape (Naglik et al., 2015).
The data utilized in this article can be found in the Supplement.
The supplement related to this article is available online at:
The authors declare that they have no conflict of interest.
We acknowledge Kevin Page (Plymouth) for the discussion of the arietitid taxa studied here. Many thanks to Kenneth De Baets (Erlangen) and Helmut Keupp (Berlin) for reviewing an earlier version of the manuscript. Carina Klein acknowledges the Elsa Neumann Foundation for their financial support. Edited by: Rene Hoffmann Reviewed by: Helmut Keupp and Kenneth De Baets