Dark bands on pyritic internal moulds of the Early Jurassic ammonites Oxynoticeras and Cheltonia from Gloucestershire, England: interpretation and significance to ammonite growth analysis

Authors


Abstract

Abstract:  Thin, radiating, darker bands occur on pyritic internal moulds of the Early Jurassic ammonites Oxynoticeras and Cheltonia from Bishop’s Cleeve, Gloucestershire. They closely resemble true colour patterns preserved in Early Jurassic Calliphylloceras from Kutch, India, and false colour patterns reported in Carboniferous and Triassic ammonoids. Up to five dark bands occur within the body chamber, suggesting that they do not represent serially repeated anatomical structures, but the same feature repeatedly formed during growth. Dark bands are interpreted as traces of black bands deposited on the inside of the shell at the aperture during pauses in growth. The angles between dark bands and between septa correlate strongly in Cheltonia, suggesting that pauses in growth coincided with septal secretion during the chamber formation cycle. There are, however, no other indications that growth was episodic in either genus.

C  olour patterns are rarely preserved in ammonites. In their review, Mapes and Davis (1996, table 1) listed 27 occurrences, eight Cretaceous, 13 Jurassic and six Triassic. These were reported in 18 papers and involved just 14 genera. Comfort (1950, 1951a, b) reviewed the biochemistry and pigmentation of molluscan shells in general, and Hollingworth and Barker (1991) the preservation of molluscan colour patterns in the fossil record. The latter authors, in particular, pointed out that in molluscs, colour pigments are typically deposited in the outer organic cover of the shell (the periostracum) and/or in the outermost shell layer. Bardhan et al. (1993) described radial colour bands in the outer shell layer of the Jurassic ammonite Calliphylloceras, while Mapes and Sneck (1996) illustrated similar, though more frequent, radial colour patterns in the Early Triassic ammonoid, Owenites. Ammonites appear to have produced colour patterns in the same way as other molluscs. It was, therefore, surprising to find five examples of the Early Jurassic ammonite Oxynoticeras oxynotum (Quenstedt, 1845) and more than two dozen of Cheltonia acciptris (J. Buckman, inMurchison, 1844) preserved as pyritic internal moulds, yet bearing narrow, radial, darker bands that strongly resemble the colour pattern seen in Calliphylloceras. Manley (1977) described an internal mould of the body chamber of Asteroceras stellare (J. Sowerby, 1815) with putative colour markings, so the occurrences described herein are not the first examples of possible colour patterns preserved on internal moulds of ammonites.

However, Mapes and Davis (1996, p. 117) also discussed ‘false (= nonbiological) colour patterns’ preserved on ammonites. More recently, Klug et al. (2007) have reviewed the occurrence and preservation of primarily organic structures associated with ammonite shells, and their terminology for these apparent colour patterns is followed herein. Two of the terms used by Klug et al. (2007) are particularly relevant. The ‘black band’ is a dark band composed of conchiolin and secreted on the inside of the aperture in Nautilus only when fully mature (Collins and Ward 1987). The ‘black aperture’ is a black line formed round the aperture owing to injury or adverse conditions and not confined to the terminal aperture. The present paper describes the darker radial bands on pyritic internal moulds of the ammonites Oxynoticeras and Cheltonia and discusses their interpretation and significance in ammonite growth.

Occurrence

All the examples described herein were collected in situ from the Charmouth Mudstone Formation in a temporary exposure west of Bishop’s Cleeve, Gloucestershire (Text-fig. 1). Simms (2003) described the stratigraphy of the Lower Lias of the area in detail. The pit exposed the whole of the Oxynotum Subzone, and all the specimens came from a narrow interval within this subzone (Text-fig. 2). Pyritized ammonites are abundant at this locality, but no other examples with clearly preserved darker bands are known. All specimens have been deposited in the Lyme Regis Philpot Museum, registration numbers LYMPH 2011/3–29.

Figure TEXT‐FIG. 1..

 Location map. B centre of Bishop’s Cleeve, E site of the temporary exposure (Text-fig. 2). The shaded area to the east of the pit represents outcrop of the Oxynotum Subzone previously identified by Simms (2003, fig. 4), from which this figure is simplified. Grid lines from the British National Grid at 1-km intervals.

Figure TEXT‐FIG. 2..

 Exposures at the ‘Oxynoticeras Zone pit’ on 13 July 2010 to show the level from which the specimens came. Line, upper left.

Methods

All ammonites collected were dried and then soaked in water to remove excess clay. In those with darker bands, chamber angle was measured by making camera lucida drawings. The total angle between the first and last sutures in the last whorl was measured, and the mean chamber angle was calculated. Where the last two sutures were approximated, the final chamber was omitted from the calculation. Mean band angle was calculated in the same way, although more commonly darker bands could be traced over less than a whorl (Table 1). Correlation between chamber angle and band angle was calculated using a Microsoft Excel spreadsheet.

Table 1.   Mean angle between dark bands and between sutures in Cheltonia acciptris (J. Buckman, 1844)
Cheltonia acciptris  Bands Sutures
SpecimenWH (mm)Total angleNumberMean angleTotal angleNumberMean angle
LYMPH 2011/85.7236739.33361037.3
LYMPH 2011/94.1165727.53391721.2
172.5824.63391721.2
LYMPH 2011/104.4251741.8331.51036.8
LYMPH 2011/115.72641518.93491721.8
LYMPH 2011/124.596524.03601427.7
194924.33601427.7
LYMPH 2011/134.5146724.33571623.8
LYMPH 2011/142.7109436.34101141.0
109436.33421038.0
LYMPH 2011/152.5149537.33801042.2
149537.3340942.5
LYMPH 2011/163.3155538.8198733.0
LYMPH 2011/174.83211522.93601722.5
LYMPH 2011/185.0312662.4352.5850.4
LYMPH 2011/195.8192638.4121530.3
192638.4106435.3
LYMPH 2011/204.6264.51029.42581629.8
LYMPH 2011/215.02861226.03601525.7
LYMPH 2011/223.13881043.13551039.4
LYMPH 2011/235.03231424.83601722.5
LYMPH 2011/243.4198639.63541039.3
LYMPH 2011/254.13301036.7378.51234.4
3301036.73441134.4
LYMPH 2011/264.4298937.3354.51135.5
LYMPH 2011/273.5117439.03601040.0
LYMPH 2011/284.1260932.5227928.4
LYMPH 2011/292.8115357.5379.5854.2
115357.5335755.8
Maximum   62.4  55.8
Minimum   18.9  21.2

Descriptions

Oxynoticeras

LYMPH 2011/3–5 are wholly septate, 18.5, 18.0 and 8.5 mm in diameter, respectively, as preserved, and with 14, 12 and 10 chambers in the last whorl (Text-fig. 3A–E). On the right side of the last whorl in LYMPH 2011/3 (Fig. 3A), eleven thin (<1 mm wide) darker bands radiate out from the umbilical seam and curve forwards (adaperturally) as they approach the venter. On the left-side matching, symmetrical darker bands can be traced back to the other umbilical seam. Within the umbilicus, six or seven additional dark bands occur in the last half whorl. The darker bands are angled slightly more prorsiradially than the ribbing near the umbilicus, and some bands cross over the ribs. Towards the periphery of the ammonite, weak hints of additional, secondary, narrower dark bands, which do not extend onto the flanks, can be seen. On the venter in LYMPH 2011/3–4, traces of the ventral muscle scars occur in front of the sutures (especially on later growth stages), which are usually indicated by incised lines parallel to the venter. No trace of the paired dorsal muscle scars can be seen on any specimen. The sutures make an angle of 40–50 degrees with a radial line (see Paul 2011).

Figure TEXT‐FIG. 3..

 A–E, Oxynoticeras oxynotum with radiating dark bands. A, Right side of LYMPH 2011/3 showing 11 narrow, dark bands in the last preserved whorl (1-11). Note that bands 3, 4 and 6 cross the ribbing. B, Left side of LYMPH 2011/4 showing narrower and more sinuous dark bands than in A. The two uppermost bands in this orientation cross ribbing close to the umbilicus. C–E, Left, right and ventral views of LYMPH 2011/5 showing about nine dark bands one of which can be seen to be symmetrical across the venter (E). Scale bars represent 5 mm (A, B) and 2 mm (C–E). Charmouth Mudstone Formation, upper Oxynotum Subzone (upper Sinemurian), near Bishop’s Cleeve, Gloucestershire.

In LYMPH 2011/4 (Text-fig. 3B), the dark bands are slightly more sinuous near the umbilical seam and slightly narrower than those in LYMPH 2011/3. In LYMPH 2011/5 (Text-fig. 3C, E), dark bands can be seen on both sides (Text-fig. 3C, D) and are symmetrical across the venter (Text-fig. 3E). They are proportionately thicker than in the larger examples but are otherwise very similar. LYMPH 2011/6 differs in that it has just over half a whorl of the body chamber preserved. Traces of a few, narrow, radiating dark bands can be detected, especially on the right side, but the total number per whorl cannot be determined. The specimen is now 14.5 mm in diameter with a whorl height of 4.5 mm at the last suture, which suggests it was about 18 mm in diameter when complete. LYMPH 2011/7 is wholly septate, 10 mm in diameter, and has three radiating darker bands on the last growth stages, but they thicken considerably towards the venter and are very thin near the umbilical seam. It is possible that other soft tissue traces, such as the lateral sinuses, may be overprinting the dark bands ventrally. The bands are so weak and indistinct, and so few occur that both the last two specimens would have been overlooked if the first three examples had not occurred in the same collection.

Cheltonia

The specimens of Cheltonia show similar, though usually narrower, radiating darker bands (Text-fig. 4A–D). In many examples, the darker bands can only be detected near the umbilical seam, but in a few, they can be traced over the venter and are symmetrical on either side. The relevant information is summarized in Table 1. In particular, there are enough examples to detect a significant correlation between the spacing of the sutures and of the darker bands (Text-fig. 5).

Figure TEXT‐FIG. 4..

 A–D, Cheltonia acciptris with radiating dark bands. A, Right side of LYMPH 2011/25 showing very narrow, strongly curved, dark bands, at least three of which occur in the body chamber (compare Text-fig. 6B). B, Right side of LYMPH 2011/22 with nine narrow dark bands in the last whorl (1–9), four of which occur in the body chamber. C, Left side of LYMPH 2011/14 an example with five bands (1–5) in the body chamber. Last suture arrowed. D, Right side of LYMPH 2011/21, a wholly septate example with 16 sutures in the last whorl, the last two very closely approximated, and eight dark bands (arrowed) in the last half whorl. Scale bars represent 2 mm. Charmouth Mudstone Formation, upper Oxynotum Subzone (upper Sinemurian), near Bishop’s Cleeve, Gloucestershire.

Figure TEXT‐FIG. 5..

 Band angle, chamber angle and size in Cheltonia acciptris from Bishop’s Cleeve, Gloucestershire. A, Correlation between mean band angle and mean chamber angle. B, Correlation between mean band angle and size. C, Correlation between mean chamber angle and size. Note the highly significant correlation between chamber angle and band angle, but the much weaker inverse correlation between both and size. Best correlation is linear in A, exponential in B and C.

Interpretation

The most similar structures reported in Jurassic ammonites are the colour bands in Calliphylloceras illustrated by Bardhan et al. (1993), who described narrow, darker bands radiating out from the umbilicus and curving towards the aperture as they approached the venter (e.g. Text-fig. 6A), and which were symmetrical on either side. The darker bands were also slightly discordant to the growth lines, although broadly parallel. No specimen was complete, but by extrapolation, nine or ten bands occurred in the last whorl. The darker bands in Calliphylloceras occur in the outer layer of the shell, and they represent true colour bands. The bands reported in Oxynoticeras and Cheltonia are very similar, with a pattern of narrow, radiating, darker bands curving forwards as they approach the venter, slightly discordant to ribbing and symmetrical on either side of the ammonite (Text-figs 3, 4, 6B). The principal difficulty in interpreting them as colour bands lies in the fact that they are present on internal moulds, whereas colour patterns in molluscs are normally deposited in the periostracum or outer shell layer (Hollingworth and Barker 1991).

Figure TEXT‐FIG. 6..

 A, Tracing of three colour bands on the left side of Calliphylloceras (redrawn from the study of Bardhan et al. 1993, fig. 2.2). B, Camera lucida drawing of the darker bands on the right side of Cheltonia acciptris, LYMPH 2011/25 (compare Text-fig. 4A). Note that two dark bands (heavy lines) occur in the body chamber.

However, Klug et al. (2007, figs 2–4) illustrated false colour patterns preserved in the shells of Carboniferous and Triassic ammonoids, which also strongly resemble the patterns in Oxynoticeras and Cheltonia. These were interpreted as preservation of repeated black bands deposited during pauses in the ammonoid shell growth. Modern Nautilus secretes a black band on the inside of the shell at the aperture only when fully mature (Saunders and Spinosa 1978; Collins and Ward 1987; Ward 1987), but it seems some ammonoids produced black bands repeatedly in an analogous manner to repeated apertural modifications in gastropods (see, for example, the review by Bucher 1997). Because the black bands were deposited on the internal surface of the shell at the aperture, this removes the difficulty of explaining how colour patterns formed in the external layers of the shell could be preserved on an internal mould.

Megastriae (Bucher and Guex 1990, figs 6G, 9) are distinctive thick lines on ammonite shells, which arose during pauses in shell growth. They have been reported in various ammonite groups, e.g. by Matsumoto (1991), Tozer (1991) and Bucher et al. (1996), among others, whereas Urdy et al. (2010) have developed theoretical models to account for the production of megastriae. The dark bands in Oxynoticeras and Cheltonia bear a very similar relationship to the ribbing that the megastriae of the Triassic ammonoid Parafrechites do to its ribs (Bucher et al. 1996, fig. 12). As far as I am aware, however, megastriae have not been reported in Oxynoticeras or Cheltonia, and the rare specimens from Bishop’s Cleeve with parts of the shell and growth lines preserved show no trace of megastriae (Paul 2011).

The colour bands in Calliphylloceras were present at the same positions on the shell as structures that Bardhan et al. (1993) referred to as pseudoconstrictions. The pseudoconstrictions arise because the ammonite stopped growing periodically and thickened its aperture with an internal rib. This produced a groove in the internal mould of the shell parallel to the aperture but slightly crosscutting growth lines in Calliphylloceras. The grooves resemble true constrictions on other ammonites but leave no trace on the external surface of the shell.

Many snails with episodic shell growth produce similar thickenings of the internal lining of the aperture (Paul 1991). Oleacinid land snails often produce a narrow, dark brown, colour band in the shell just behind the aperture at each such resting place. Pleistocene examples of Euvaricella nemorensis (C. B. Adams, 1849) from Red Hills Road Cave, Jamaica (Paul and Donovan 2005), show the colour is distributed through the shell, not confined to the outer shell or periostracum. Similarly, many European snails secrete colour internally (e.g. Kerney et al. 1999, pl. 23, fig. 1a–f; pl. 28, figs 3, 8). Thus, at least in gastropods, true colour patterns are deposited on the internal surface of the shell and especially at the aperture, a fact reported by Comfort (1951a) in discussing shell pigments in terrestrial pulmonates. The oleacinids are particularly relevant because Bardhan et al. (1993, p. 142) reported that, ‘where preservation is better, the shell material of the internal ridges is of a different color from the remainder of the shell.’ Thus, it would seem that growth of the shell of Calliphylloceras was episodic, with the aperture thickened periodically at each resting stage and narrow, radiating colour bands produced just behind the aperture. Oxynoticeras and Cheltonia show no signs of internal thickenings of the shell nor of megastriae, but the darker bands on the internal moulds could represent original black bands parallel to the aperture that were produced periodically during growth. Portlandian ammonites of the genus Titanites quite commonly have a black band lining the aperture on internal moulds when fully grown (see, for example, the specimen in Shrewsbury Museum at http://www.darwincountry.org/explore/005765.html). Klug et al. (2007, figs 3–9) illustrated other examples of preserved black bands in Triassic and Jurassic ammonites. Furthermore, Collins and Ward (1987) listed the presence of a thin black band on the internal surface of the aperture of Recent Nautilus as one of eleven morphological characteristics of fully mature Nautilus shells. Thus, Recent Nautilus secretes a black band within its aperture when fully grown (Arnold 1985; Collins and Ward 1987; Landman and Cochran 1987; Ward 1987), and other examples of fully mature ammonites with black bands preserved on internal moulds are known.

Discussion

A possible alternative explanation of the darker bands in Oxynoticeras and Cheltonia is that they represent internal organs of the original ammonites, traces of which are quite commonly preserved on internal moulds (e.g. Andrew et al. 2010, fig. 13; Doguzhaeva and Mutvei, 1996), including those of Oxynoticeras and Cheltonia (Paul 2011). This seems unlikely because examples of Cheltonia have up to five colour bands within the body chamber when it is preserved. Five and four are preserved, respectively, in the body chambers of LYMPH 2011/14 and 2011/22 (Text-fig. 4B, C). Although Mutvei et al. (1993, p. 1) suggested that ‘Nautilus may retain some evidence of metamerism’, four or five serially repeated anatomical structures within body chambers have not been reported in ammonites before and all Recent cephalopods lack this many. On balance, it seems more likely that the darker bands represent black bands secreted on the internal surface of the ammonite shell at the current aperture during pauses in growth, analogous to the black band of Nautilus when fully mature.

It is also possible that the dark bands in Oxynoticeras and Cheltonia represent black apertures (sensuKlug et al. 2007). However, there is no sign of injury that accompanies such black apertures, and it is difficult to explain the correlation between spacing of dark bands and of septa in Cheltonia under such an interpretation.

Manley (1977, fig. 1) described a series of oval dark spots arranged in regular spiral rows and also parallel to growth lines on an internal mould of the body chamber of a single specimen of Asteroceras stellare. The outer surface of the shell of A. stellare bears a similar pattern of oval tubercles (Manley 1977, fig. 2). A possible explanation as to how a colour pattern normally present on the outer surface of a shell could become preserved on an internal mould is that in Asteroceras, the colour pattern was apparently associated with thicker portions of the shell. As the shell dissolved, insoluble organic matter may have been concentrated at the thicker portions and preserved on the internal moulds, thus reproducing the colour patterns of the original shell. Hagdorn (1995) described a similar phenomenon involving colour bands in the Triassic bivalve Pleuronectes. The colour bands resisted pressure dissolution and frequently produced a false sculpture of radiating ridges. These ridges are retained on internal moulds even after the entire shell has been dissolved. Incidentally, Comfort (1951a) confirmed by experiment that protein-bound colour pigments in Recent gastropods are insoluble in acids.

The pattern of dark bands in Oxynoticeras and Cheltonia resembles megastriae, which are resting traces that occur in episodic growth (Bucher and Guex 1990). Equally, the true colour pattern in Calliphylloceras is associated with pseudoconstrictions, which also represent resting points during episodic growth. It is possible that Oxynoticeras and Cheltonia grew episodically, although there is no other evidence of this. A resting trace recorded by a dark band would relate to a septum secreted at the rear of the body chamber, i.e. about 240–270 degrees behind the aperture. So, it is not easy to relate the dark bands to the corresponding septa. However, in Cheltonia, mean chamber size correlates very well with mean band spacing (Text-fig. 5A). Specimens with few sutures in the last whorl have few dark bands; those with many sutures have many dark bands. The supposed resting traces may have coincided with a phase of the chamber formation cycle. It is tempting to suggest that the shells of these ammonites grew forwards at the aperture while the ammonites were emptying fluid from their chambers, but they ceased growing at the aperture while the new septum was being secreted. Doguzhaeva (1982) previously suggested a link between growth increments of the shell and septal formation.

Ward et al. (1981) described the chamber formation cycle in Nautilus macromphalus G. B. Sowerby, 1849. They reported that N. macromphalus continues to grow its shell at the aperture while also secreting a new septum. They argued that the combination of both additions to the shell produced the most rapid increase in the weight of the shell and that this increase was compensated for by removal of fluid from earlier chambers. In Nautilus, no fluid is removed from the newly formed chamber until the new septum reaches about 60 per cent of its final thickness. However, Kröger (2002) and Klug et al. (2008) have argued from independent evidence that ammonites may have been able to replace chamber fluids more rapidly than nautiloids. If the present interpretation of episodic growth in Oxynoticeras and Cheltonia is correct, then this is an important difference between the chamber formation cycle in these ammonites and that of modern Nautilus (see, for example, Doguzhaeva 1990). Furthermore, there is no other evidence of episodic growth in these genera, such as the presence of pseudoconstrictions or megastriae, suggesting that other ammonites lacking periodic structures may nevertheless have grown episodically.

Acknowledgements.  I thank Grundon Waste Management Ltd for access to the site at Bishop’s Cleeve. Mike Simms (Ulster Museum), Paul Ensom and Murray Edmonds provided useful information and discussion. John Marriage (Lyme Regis) assisted with the photography. The initial draft was greatly improved by comments of Larisa Doguzhaeva and Christian Klug.

Editor. John W. M. Jagt

Ancillary