Giant Parapuzosia species

In our material, we identified two species of Parapuzosia with shell diameters of >1 m. One is P. (P.) leptophylla Sharpe, 1857 [6], which was recently re-described formally [7]. 11 of the 154 specimens studied here were assigned to this species; they were originally collected from the Santonian of England, France, Germany and Mexico. The other giant species is P.(P.) seppenradensis (Landois, 1895) [1] which grew to 1.50 m shell diameter and even to ca 1.80 m as seen in the lectotype. An emended diagnosis for P.(P.) seppenradensis (Landois, 1895) is here presented in S1 File. 143 specimens from the uppermost Santonian and lower Campanian of Germany, England, Mexico and the USA are here included into P. (P.) seppenradensis.

Geographic occurrences of large and giant Parapuzosia are summarized in Fig 2. The specimens, their origin, age, morphometry and further details are summarized in S1 Table.

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Fig 2. Distribution of giant Parapuzosia in the Santonian—Early Campanian.

Area of dots approximates abundance of specimens. Abbreviations: CB: Cretaceous Basins of Europe, GM: Gulf of Mexico, WIS: Western Interior Seaway. Maps modified [from 8] under a CC BY license, with permission from deeptimemaps.org, original copyright 2016.

https://doi.org/10.1371/journal.pone.0258510.g002

Occurrence

Parapuzosia from England.

Specimens of giant Parapuzosia in the English Chalk in Kent and Sussex, UK, were first mentioned by Sharpe [6] and Spath [13], but few have been collected. We located P. (P.) leptophylla in upper Santonian chalk cliffs in east Kent, at Minnis Bay (two), Palm Bay (one), Kingsgate Bay (one), and P. (P.) seppenradensis in foreshore outcrops of lower Campanian chalk at Peacehaven in Sussex (ca. 100). The stratigraphic distribution of these specimens within the English Chalk is shown in Fig 3. The inner whorls, measured to 0.53 m, of a large Peacehaven specimen estimated to 1.50 m shell diameter, are housed in the local museum of Littlehampton, Sussex.

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Fig 3. Stratigraphic distribution of Parapuzosia and their diameters from the English Chalk of east Kent and Sussex, U.K., and from Tepeyac, northern Coahuila, Mexico.

Chalk sections are [redrawn from 14, 15]. Colors refer to growth stages in P. (P.) seppenradensis (see also Fig 5). δ¹³C distribution in the Chalk from [4]. The East Kent and Sussex sections are correlated by bio- and lithostratigraphy, correlation to Mexico by δ¹³C chemostratigraphy. Abreviations for biostratigraphy: M. corangium: Micraster corangium M. (D.) delaw.: Menabites (Delawarella) delawarense, M. (D.) tequesqu.: Menabites (Delawarella) tequesquitense, M.t. and M. testud.: Marsupites testudinarius, O. p.: Offaster pilula, U. soc.: Uintacrinus socialis.

https://doi.org/10.1371/journal.pone.0258510.g003

Ontogeny and dimorphism

Phragmocone diameters of the Tepeyac Parapuzosia range from 0.10 to 1.65 m. Based on the last suture preserved, the original size of the largest specimen can therefore be calculated to about 2 m. This specimen (TPY P19, S2K Fig) thus represents the largest ammonite of North America and the second largest in the world. The enormous size range identified in the 143 specimens revised here allows for a discussion of individual growth and the differentiation of five ontogenetic stages in P.(P.) seppenradensis, but also a concise differentiation between this species and P. (P.) leptophylla.

The smallest individuals of P.(P.) seppenradensis, with phragmocone diameters of up to 0.11 m, show about 9 sharp primary ribs per half whorl, intercalated by seven secondary ribs, with their number gradually decreasing to three with increasing diameter (D). We refer to the morphology of these small-sized specimens as juvenile stages 1 (seven secondaries, Fig 4E and 4F) and 2 (three secondaries e.g. [22]). Secondaries disappear between 0.20 m and 0.40 m diameter, and subsequent ornamentation consists solely of straight primary ribs, or shells are smooth (juvenile stage 3, S2A and S2B Fig, Fig 4C and 4D). The shell is approximately discoidal in juvenile stage 3 and has convergent flanks with initially thin, sharp and very regular ribs; this stage is followed by broader and wider-spaced ribs, here termed juvenile stage 4, providing greater whorl width with convergent flanks, but still a narrowly rounded venter (S2A, S2B and S2C–S2G Fig). This gradual transition is identified at phragmocone diameters ranging from 0.30 to 0.60 m. Larger shells show a gradual transition of convergent to parallel flanks, while the venter changes from narrowly to widely rounded (growth stage 5, Figs 1, 4F and 4G, S2J Fig). This is the last growth stage, which is here interpreted to represent the adult ontogenetic stage. The transition from growth stage 4 to growth stage 5 is gradual and completed at differing diameters ranging from 0.50 m to 1.40 m. At diameters between 1.0 and 1.5 m, ribs become even wider, more undulating and irregular, leading to an almost smooth lateral surface at largest diameters (>1.5 m, Figs 1, 4F and 4G, S2J and S2K Fig). The growth stage is also characterized by the position of greatest whorl breadth (arrows in Fig 4). It is situated near the umbilicus in growth stage 1 and 2, on the inner flank in stage 3, and approximating a mid-flank position in growth stage 4; the greatest whorl breath is situated at ca. 1/3 whorl height on the outer half in growth stage 5.

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Fig 4. Ontogenetic stages of Parapuzosia (P.) seppenradensis from the Jiménez area of Coahuila, north-eastern Mexico.

A–B: juvenile stage 1, drawn from CPC–2204 from bed TPY 77. C–D: juvenile stage 3 (inner) and 4 (outer whorl), drawn from CPC–2206, macroconch from bed TPY 57 in lateral (C) and apertural view (D). E: juvenile stages 3–4 (inner) and 5 (outer whorl), drawn from CPC–2201, microconch from bed TPY57. Note that stage 5 is reached at a rather small diameter. F-G: macroconch juvenile stage 4, subadult stage 5 in the last quarter whorl, drawn from CPC–1000, precise origin within the Jiménez area is unknown. Drawings by CI. Scale bar = 100 mm.

https://doi.org/10.1371/journal.pone.0258510.g004

The lectotype of P. (P.) seppenradensis has parallel flanks, a broadly rounded venter, and wide, shallow, regular ribs throughout the last whorl, i.e. growth stage 5. The paralectotype of P. seppenradensis, as well as specimen WMN 5159 from Dülmen and a fourth individual from Seppenrade, also agree with ontogenetic stage 5 as established based on the Tepeyac material. The Tepeyac specimens of Parapuzosia are therefore assigned to P. (P.) seppenradensis Landois, 1895.

Most specimens from the Jiménez (Tepeyac) region and adjacent Texas, originally assigned to various species of Parapuzosia, fall into growth stage 3 (see S1 File). The holotype of P. americana Scott and Moore, 1928 [16] and the visible inner whorl of the holotype of P. (P.) bradyi Miller and Youngquist, 1946 [21] correspond to growth stage 4. Growth stage 5 corresponds to the morphotype of P. bosei Scott and Moore [16], 1928. These species are thus junior synonyms of P. (P.) seppenradensis.

The Santonian species P. (P.) leptophylla is distinguished from P. (P.) seppenradensis by irregular ribbing in growth stage 3 and by slightly flexuous ribs (S2E–S2G Fig). It is interpreted as adult in the smooth growth stage (stage 4) with convergent flanks, because this is the last growth stage observed. P. (P.) leptophylla never shows a rounded venter or parallel flanks near the aperture, although it is indistinguishable by standard morphometry alone (S3 Fig). The earliest growth stages of P. (P.) leptophylla are yet unknown.

The five ontogenetic growth stages described above for Parapuzosia (P.) seppenradensis are reached at varying shell diameters, shown e.g. in Fig 3. The specimens can be divided into two coeval groups of individuals (Fig 5), which is here explained by size dimorphism. The effects of dimorphism overlap with the evolutionary increase in shell size (see 3.2). This is especially seen in latest Santonian morphotypes which cover the lower range of diameters of transition between growth stages. In Campanian specimens, however, both maximum sizes and widest shell size variations are identified in both North American and European specimens. Dimorphism was earlier suggested for Parapuzosia (P.) seppenradensis [2], but based on a single specimen which is here referred to ontogenetic stage 4 and thus considered to be a juvenile macroconch.

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Fig 5. Shell diameter and associated growth stage in Parapuzosia (P.) seppenradensis.

The specimens from Mexico, Texas, Montana, England and Germany are separated after microconchs (left) and macroconchs (right). Colours refer to ontogenetic stages.

https://doi.org/10.1371/journal.pone.0258510.g005

Size

Diameters of Parapuzosia specimens generally increase throughout the Tepeyac section reaching maxima in bed 69 (Fig 3, S4 Fig). While P. (P.) leptophylla reaches shell diameters of 0.50 to 0.70 m in the upper Santonian part of the Tepeyac section (beds TPY 1–20), specimens of P. (P.) seppenradensis collected from stratigraphically younger layers (beds TPY 21 to 40) reach adult sizes of about 1.20 m. Largest shell sizes of about 1.50 m (or 2.0 m including the body chamber) are present in the lower Campanian section (beds TPY 50–69); in these individuals, adult (stage 5) morphologies are first seen at shell diameters of ca. 0.75 to 1.30 m. The shell size of Parapuzosia, but also diameters of transition from one growth stage into the next, thus increases across the Santonian- Campanian boundary in both the Gulf of Mexico and the English Chalk, with largest diameters reached in the middle early Campanian on both sides of the Atlantic (S4 Fig). This stratigraphic level is approximately coeval to the layer in which the giant lectotype of P. (P.) seppenradensis was found in Germany, while smaller specimens seem to originate from beds above and below [2]. Specimens from the uppermost lower Campanian are scarce and invariably of diameters < 1m.

Stratigraphic and palaeogeographic distribution, and depositional environment

Palaeogeographic occurrences of giant Parapuzosia are shown in Fig 2. Early Santonian records of P. (P.) leptophylla exist from southern France [12]. In the late Santonian, the species is known from Austria, England [7] and Mexico, but it disappears prior to the Santonian-Campanian boundary, most possibly because it evolves into P. (P.) seppenradensis. The oldest records of this latter species are from the uppermost Santonian of Texas [22] and Mexico, its absence in Europe may be explained by a scarceness of outcrops. In the early Campanian, P. (P.) seppenradensis reaches its widest distribution, with records from Mexico, Texas, England, Germany, and possibly Montana. The species is thus distributed throughout the Central European Cretaceous basins and the northwestern Gulf of Mexico. It then becomes rare and smaller-sized in both Mexico (Tepeyac) and in England (Sussex).

The abundance of Parapuzosia, as expressed by the number of individuals per layer, increases towards the upper (lower Campanian) part of sections in both the English Chalk and Tepeyac (Mexico), unrelated to outcrop conditions. In both outcrop areas, coeval sediments elsewhere in the region are devoid of Parapuzosia shells. Near Ojinaga in northern Chihuahua, for instance, only about 300 km distance to the west of Tepeyac (S5 Fig), the expanded and exceedingly fossiliferous [25,26] Ojinaga Formation contains abundant Placenticeras and texanitids [27], but P. (P.) leptophylla and P. (P.) seppenradensis are absent. In southwestern Coahuila, lower Campanian sediments comprise a mostly endemic assemblage near Union y Progreso, including Menabites (Delawarella) vanuxemi and Pseudoschloenbachia (P.) mexicana, but without Parapuzosia [28]. The taxon is also characteristically absent along the Northern Gulf of Mexico and the Atlantic Coast of the US. A similarly patchy occurrence is seen in Europe. Abundant large specimens of P. (P.) seppenradensis are documented from Sussex in the southern UK and P. (P.) leptophylla has been found in the upper Santonian chalk of Kent. No reports exist from the early Campanian of France, but all German specimens of P. (P.) seppenradensis are from a small outcrop area in the Münsterland, a region of Westfalia.

This explicitly patchy geographic occurrence of P. (P.) seppenradensis appears to be unrelated to lithofacies. The taxon has been documented from coarse siliciclastic sediment in Montana [21] and the Münsterland [3], and from fine-grained carbonates in the case of the English Chalk and the Gulf of Mexico specimens. Possibly, the absence of P. (P.) seppenradensis in western Coahuila, in Chihuahua, and along the northern Gulf of Mexico coast line, may relate to the dominance of fine siliciclastic sediment in this region, but then its absence in the carbonate-dominated southern Chalk Basin of France remains to be explained.

Up to bed TPY69 of the Mexican Tepeyac section, P. (P.) seppenradensis is represented by subadults and adults. Above, in bed TPY70 and upsection, juvenile specimens dominate and larger shells are only occasionally present. The abundance of majorly adults followed by the dominance of early juveniles in the Mexican Tepeyac section suggests proximity to a mating and/or hatching area, which is shifted with sea-level changes. This would imply a monocyclic reproduction strategy for these giant ammonites [29,30].

Ammonoids have long been suspected to have employed a semelparous reproductive strategy, i.e. a spawning once strategy [e.g. 31–35]. Such a single spawning strategy is characterized by females producing thousands of eggs, typically laid in egg cases in mass spawning events. Adults die subsequently, although not necessarily immediately; in recent coleoids, mass accumulations of sexually mature adults are not usually found with their offspring. Accumulations of adult ammonoids have been interpreted as evidence of semelparous life cycles before [29]. A scenario of monocyclic reproduction with more than one spawning event comparable to recent coleoids [30] would also plausibly explain the abundance of giant Parapuzosia in a shallow shelf area and their absence in other nearby locations.

It should be noted that the Tepeyac and Peacehaven localities seem to comprise accumulation of subadults and adults. This indicates accumulation after a short reproduction phase. However, in the phase between hatching and spawning the individuals seem to have spent their life elsewhere, and most probably in deeper or even deep water. Records outside the Tepeyac and Peacehaven areas are isolated and unrelated to facies, they might represent isolated individuals of a species spending most of its lifetime offshore.

Sea-level, temperature and climate

Two medium range 25–75 m eustatic sea-level lows (KSa2 and KSa3) have been identified during the late Santonian and one in the early Campanian (KCa1) [36], which likely caused intermittent decrease in water depth and expansion of shallow depositional environments in the western Gulf of Mexico. At Tepeyac, these regressive phases are reflected by the occurrence of trigoniids, alectrioniid oysters, and Pinna preserved in life position. The mid-early Campanian rise in sea-level, on the other hand, may be expressed by a change from white to yellow-coloured carbonates in the Tepeyac section, i.e. from shallow to substantially deeper shelf conditions. At about this lithological change, coincident with bed TPY69, largest specimens of Parapuzosia were detected and their abundance is highest. Above and below bed TPY69, Parapuzosia juveniles are abundant, and no adults were detected above bed TPY70. Upsection, Parapuzosia is absent in the topmost part of the Tepeyac section (to bed 92) dated to the upper lower Campanian (Baculites taylorensis Zone). In England, largest specimens are concentrated at a stratigraphic level approximately coeval with bed TPY69, and above this layer individuals also become increasingly rare. The size shift identified here in England and Mexico may thus have been coeval on both sides of the Atlantic. In extant cephalopods, the final body size often depends on hatchling sizes and on seasonal effects, e.g. water temperature during hatching and subsequent initial growth [37]. Hatching often occurs during a period of increasing water temperatures, i.e. in spring. In consequence, each monthly cohort encounters warmer temperatures and grows faster than cohorts that hatched weeks before [38]. Hatchling size is unknown for Parapuzosia. Within the Puzosiinae, hatchling size is only known for Turonian Pacific species [39] with narrow geographic and stratigraphic distribution and thus a low dispersal potential, different to Parapuzosia as interpreted here; they are thus not comparable. Other Desmoceratidae (Order: Ammonitina), into which Parapuzosia is also included, have hatchling size between 0.6 and 1.5 mm, most vary around 0.9 mm [39].

Even though, the importance of hatchling size may have been minor in giant organisms such as Parapuzosia. Instead, water temperature during growth may additionally have influenced final body and shell size, and may also explain the size variation within micro- and macroconchs. Nevertheless, it cannot explain the overall shift in size documented above for Campanian specimens.

The Cretaceous warm climatic conditions extended throughout the Santonian and into the Campanian, when a long-lasting cooling trend initiated during the early Campanian [40,41]. The δ¹⁸O curve [4] shows a minor drop at the Snt/Cmp boundary, followed by a phase of stability. During the Neogene, gradual oceanic cooling is interpreted to have resulted in a size increase of marine organisms, e.g. in whales [42]. The latest Cretaceous long-term cooling trend, initiating during the early Campanian, may thus have played a role for the size increase detected in P. (P.) seppenradensis. Nevertheless, this process started earlier. In addition, it would not explain the disappearance of this giant ammonite during the late early Campanian. The stable carbon isotope curve [4,15] shows a moderate peak across the Santonian-Campanian boundary, which does not correlate to an increase in shell diameter of Parapuzosia Fig 3); it thus seems to be unrelated. In consequence, no global trend is identified towards higher, or lower, temperatures, or changes in sea-level, that readily correlates with the increase in size and subsequent decrease of P. (P.) seppenradensis.

Other large ammonoids and organisms in the Late Cretaceous seas

During the Late Cretaceous several genera of ammonoids developed large-sized species. These include the Cenomanian Puzosia, the Turonian Pachydesmoceras and Lewesiceras, the Santonian Parapuzosia, the early Campanian Pachydiscus (all in Central European Cretaceous basins), the late Campanian Pachydiscus (in the west Pacific) [43–45], and the early Maastrichtian Pseudobaculites (Western Interior Seaway) [46,47]. These giants thus represent different families and, in the case of Pseudobaculites, even orders. They were all recorded from regions which are relatively small in comparison with the distribution area of P (P.) seppenradensis. This latter species, though originating from one of these large forms, surpasses all others in both geographic distribution and size.

The gigantisms shown by the two species studied here may be a coevolution to the size increase in mosasaurs. These are known to have predated upon ammonoids [48] and considerably increase in size during the Santonian-early Campanian [49] parallel to Parapuzosia. However, the subsequent retrograde evolution of Parapuzosia from the late early Campanian on is clearly unrelated to the further increase in size of mosasaurs.

Comparison with extant coleoids

Extant coleoids are the group most closely related to ammonoids [50]. These recent cephalopods are characterized by monocyclic spawning, although it is differentiated between a single synchronous ovulation (semelparity), several spawning events without ovary regeneration (with or without further growth between these events) or asynchronous ovulation with extended and continuous spawningPolycyclic spawning with regeneration of the ovary is restricted to Nautilus [30] which is more distantly related to ammonoids [50]. A monocyclic or even single-event spawning strategy is thus also plausible for Parapuzosia from an actualistic view.

Architeuthis is the largest existing coleoid. Based on genetics, this giant squid has been shown to be monospecific [A. dux (Steenstrup, 1857) [51]], even though it is characterized by high morphological variability [52] and global geographic distribution crossing latitudes [53]. In this respect it seems comparable to giant Parapuzosia. However, Architeuthis dux is even more widely distributed than P. (P.) seppenradensis was during the Campanian and seems to dwell and reproduce in deeper water depths than giant Parapuzosia did, although the water depth in which Parapuzosia dwelled during growth cannot be estimated from the known occurrences.