Recently, by examination of (1) ribbing pattern and its resolution on the inner surface of the shell, (2) height of the left and right sides (i.e. symmetry) of the hooked living chamber at the point of recurvature, (3) variability in shape of the gap between the phragmocone and living chamber and (4) location of epizoan fauna on the shell, I put forward an hypothesis that the final adult stage of Cretaceous heteromorph ammonites of the suborder Ancyloceratina developed the U-shaped living chamber to be loosely hooked (Ancyloceras) or firmly clipped (scaphites) to noncalcified algal branches for brooding their eggs until hatching (Arkhipkin, 2014). Subsequently, Landman et al. (2016) have presented some new data on measurements of the shell and resolution of shell ribs in scaphites and argued that they did not find any support for the stationary adult hypothesis. They put forward objections to five points of evidence chosen by themselves from the paper (Arkhipkin, 2014), of which only the first two (ornament resolution and symmetry of the living chamber) correspond to my four main arguments outlined above.

Contrary to Landman et al. (2016), I did not report ‘worn ornament’ on the dorsal surface of the hooked living chamber. Instead, I observed the difference in rib resolution in various parts of the adult shell, with weaker (and sometimes practically indiscernible) ribs in the inner part of the hooked living chamber, as compared to those in the inner part of the shaft. I went on to suggest that the flattened ribs in the large Proustraliceras gigas might be a result of wear, which was obviously impossible to confirm as the specimens were steinkerns. Similar flattening of ribbing pattern was noticeable in Audouliceras renauxianum that had original shell walls (Arkhipkin, 2014: fig. 5). Interestingly, the ribbing pattern was less resolved in the dorsal part of the living chamber than in the inner part of the shaft in both species of ancyloceratid ammonites figured by Landman et al. (2016: fig. 2C, F). As already explained (Arkhipkin, 2014), the reason for the weaker ornament on the dorsal part of the living chamber could be the presence of an object (like a branch) in the gap formed by the shell. As a result of the application of lifting force derived from the buoyant phragmocone, the formation of the ribbing pattern on the upper part of the living chamber shell would be impeded. Even if some species of heteromorphic ammonites were loosely hooked (like Ancyloceras or Macroscaphites), relatively soft branches of brown algae would not leave any ‘kinks’ or ‘scratch marks’ on the surface of the shell as described by Landman et al. (2016).

Landman et al. (2016) also presented new data on measurements of the left and right sides of the hooked living chamber of two species of Hoploscaphites, stating that there is no asymmetry between the sides, on the basis of a regression line through all data points (although without providing formal details of statistical analysis or errors in measurements). However, their analysis has a serious flaw, because one would expect an equal opportunity for an animal to attach to a branch angled to either the right or left side of the shell. Therefore, to test asymmetry of the sides of the living chamber, it is not correct to combine data from all shells (in which either left or right side might be taller) as done by Landman et al. (2016). I have performed my own analysis by digitizing the authors' data from their graph (Landman et al., 2016: fig. 4). For each data point, I took a ratio between the heights of the left and right sides and found that the frequency distribution of the ratios is skewed with the maximum number of shells having taller right side (Fig. 1). In case of symmetry between the sides of the shell (as suggested by Landman et al., 2016) one would expect a normal distribution of ratios with the mode (and mean) being close to 1 (i.e. full symmetry). Whereas Landman et al. (2016: caption to fig. 4) stated that “the slope of the line equals approximately 1.0”, my reanalysis indicates that the skew in the distribution of ratios is sufficient that the mean ratio is in fact significantly different from 1.0 even when data from all shells are combined (mean 0.968; 95% confidence interval 0.959–0.979). A larger set of measurements is needed to test whether there is either a bimodality in distribution of ratios (i.e. equal probability of settlement on a branch angled to left or right of the shell) or skewed unimodality (preferential settlement on branch angled to one side, as the available data suggest). Back calculation of the angle between two sides to the frontal plane of the shell gave values between 83° and 87°, close to the range of 80–85° predicted by Arkhipkin (2014). Thus, using the authors' new data I confirmed my previous observations that the gap is not symmetrical, despite the cross-sections depicted by Landman et al. (2016: fig. 3).

Figure 1.

Frequency distribution of ratios between the heights of the left and right side of the living chamber in Hoploscaphites nodosus (Owen, 1852) and H. brevis (Meek, 1876) based on data from Landman et al. (2016).

Figure 1.

Frequency distribution of ratios between the heights of the left and right side of the living chamber in Hoploscaphites nodosus (Owen, 1852) and H. brevis (Meek, 1876) based on data from Landman et al. (2016).

It is known that noncalcified algae do not fossilize, so one cannot expect their presence in layers with fossilized heteromorph ammonites. However, rich Cretaceous herbivorous fauna (molluscs, echinoderms, teleost fishes) indirectly suggests the presence of algal forests and beds (Steneck, 1983), as does new genetic data on diversification of various groups of brown algae in the Upper Cretaceous (Silberfeld et al., 2010). Their branched macrophytes might provide a substrate for the attachment of hooked adult heteromorph ammonites.

The dimorphic macroconchs and microconchs observed in some ammonite groups, including heteromorphs, have been interpreted to belong to different sexes since the classic work by Callomon (1963). While the sexual dimorphism hypothesis has been widely accepted by palaeontologists, it has nevertheless yet to be proved, and therefore cannot really be an argument against the stationary hooked hypothesis. Furthermore, females of many recent cephalopods are able to store sperm in seminal receptacles and in spermatangia for an extended period after mating and therefore do not require the presence of a male during spawning and brooding of their egg masses.

Landman et al. (2016) found reasonable my hypothesis that the final, terminal countdown (T-S) ontogenetic phase of heteromorphic ammonites (Seilacher & Gunji, 1993) may represent a brooding female, especially with recent findings of ammonitellas within ammonite shells suggesting ovoviviparity (Mironenko & Rogov, 2015). However, the authors' opinion that ammonites in the T-S ontogenetic phase ‘lived swimming vertically near the bottom and fed on small planktonic organisms' contradicts the fact that all recent cephalopods brooding their eggs do not eat, but hide either in crevices (octopods) or deep water (squid) to escape predation on weakened females and eggs. Moreover, it is hard to explain why a free-living near-bottom heteromorph ammonite would severely impede its abilities to swim and catch prey by bending the hook-like living chamber to the extent that its opening almost touches the phragmocone. Modern nerito-benthic squid such as Mastigoteuthis hover over the bottom with the head pointing downwards and collect small prey with their tentacles (Roper & Vecchione, 1997)—the transitional phase of heteromorphs probably fed in the same way (as in Heteroceras spp.; Delanoy, 1997). Landman et al. (2016) also observed that many bottom-living animals have movable articulated appendages to attach themselves to seagrass and kelp branches. Adult heteromorphs, however, would not need to change their position on the branch, as the female would stay stationary until the end of her life, making her shell the ultimate shelter for the developing eggs.

In my opinion, Landman et al. (2016) have not provided strong counter-arguments against the ‘stationary adult brooding female’ hypothesis for Cretaceous heteromorph ammonites. They even presented some new data that further support my earlier conclusions about slight but significant asymmetry of scaphitid shells that is otherwise hard to explain if they were free-living in the water column. Together with other arguments raised in my earlier paper (Arkhipkin, 2014)—which somehow were left untouched by the authors, i.e. strong variability in gap shape of the shell that may reflect various thickness of branches, absence of epizoans on the inner surface of the hook and restricted post-mortem floatation of adults—the new ‘stationary adult’ hypothesis seems to be the most plausible explanation for independent development of the terminal U-shape living chamber in several lineages of Ancyloceratina ammonites. Otherwise, if not being hooked, why form one?

REFERENCES

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
.
CALLOMON
J.H.
1963
.
Sexual dimorphism in Jurassic ammonites
.
Transactions of the Leicester Literary and Philosophical Society
 ,
57
:
21
66
.
DELANOY
G.
1997
.
Biostratigraphie des faunes d'ammonites à la limite Barrémien-Aptien dans la région d'Angles-Barrême-Castellane. Étude particulière de la famille des Heteroceratidae (Ancyloceratina, Ammonoidea)
.
Annales du Muséum d'Histoire Naturelle de Nice
 ,
12
:
1
270
.
LANDMAN
N.H.
,
KRUTA
I.
,
DENTON
J.S.S.
,
COCHRAN
J.K.
2016
.
Getting unhooked: reply to the hypothesis that heteromorph ammonites were attached to kelp branches on the sea floor, as proposed by Arkhipkin (2014)
.
Journal of Molluscan Studies
 ,
82
:
351
355
.
MIRONENKO
A.A.
,
ROGOV
M.A.
2015
.
First direct evidence of ammonoid ovoviviparity
.
Lethaia
 , .
ROPER
C.F.E.
,
VECCHIONE
M.
1997
.
In situ observations test hypotheses of functional morphology in Mastigoteuthis (Cephalopoda, Oegopsida)
.
Vie et Milieu
 ,
47
:
87
93
.
SEILACHER
A.
,
GUNJI
P.Y.
1993
.
Morphogenetic countdowns in heteromorph shells
.
Neues Jahrbuch für Geologie und Paläontologie, Abhandlungen
 ,
190
:
237
265
.
SILBERFELD
T.
,
LEIGH
J.W.
,
VERBRUGGEN
H.
,
CRUAUD
C.
,
DE REVIERS
B.
,
ROUSSEAU
F.
2010
.
A multi-locus time-calibrated phylogeny of the brown algae (Heterokonta, Ochrophyta, Phaeophyceae): investigating the evolutionary nature of the “brown algal crown radiation”
.
Molecular Phylogenetics and Evolution
 ,
56
:
659
674
.
STENECK
R.S.
1983
.
Escalating herbivory and resulting adaptive trends in calcareous algal crusts
.
Paleobiology
 ,
9
:
44
61
.