ISSN 0031-0301, Paleontological Journal, 2018, Vol. 52, No. 13, pp. 1517–1544. © Pleiades Publishing, Ltd., 2018.

Variability of Relative Body Chamber Length in Jurassic Ammonites of the Family Cardioceratidae Siemiradzki, 1891, and Its Taxonomic Significance D. N. Kiselev* Ushinsky State Pedagogical University, Yaroslavl, 150000 Russia *e-mail: [email protected] Received April 16, 2018

Abstract—Analysis of the variability of the angular length of the body chamber in the subfamilies Arctoceph- alitinae and Cadoceratinae (family Cardioceratidae) has shown that this feature is extremely variable both at the species level and within the genus. For most taxa the length of the body chamber (either fixed values, or mean statistical values) has no identification significance. Estimates of high variability of the body chamber length allow some classification systems of early cardioceratids to be critically evaluated and some concepts of the theoretical shell morphology and paleobiology of ammonites to be reassessed. This is primarily based on models, in which the length of the body chamber coincides with the length of the soft body, and so indi- rectly influences shell hydrodynamics and hydrostatics, as well as ammonite locomotion and life style. High variability of the body chamber length suggests that this effect was not as significant as previously thought.

Keywords: body chamber, ammonites, Cardioceratidae, taxonomy DOI: 10.1134/S0031030118130063

INTRODUCTION Later many British, American, and German authors (Hyatt, 1877; Waagen, 1875, Buckman, 1881, 1909– Body chamber length (BCL) is quite rarely used in 1930, Blake, 1905; Arkell, 1939 et al., Spath, 1927– publications containing descriptions of Jurassic 1931, Oppel, 1862, Pompeckj, 1892, Quenstedt, 1886– ammonites to solve taxonomic problems or to recon- 1887, Neumayr, 1871, etc.) indicated the length of the struct phylogenetic trees. In major reference books on body chamber in their descriptions of Mesozoic Mesozoic ammonites (Arkell et al., 1957; Osnovy pale- ammonites. ontologii…, 1958; Bogoslovsky et al., 1962; Wright et al., 1996) BCL is not mentioned in descriptions of Among Russian scientists, Nikitin (1881, 1884) was genera and higher taxa. This means that most valid apparently the first to mention the BCL in descrip- ammonoid taxa were recognized and diagnosed with- tions of Jurassic ammonites. When describing species out taking body chamber length into account. In of the genus Amaltheus Nikitin (1878) used the term more recent reference books, body chamber length is “living chamber,” but did not indicate its length either given in the diagnoses of families and some genera for the genus, or for species of the genus. In later (Howarth, 2013; 2017). papers he used the length of the body chamber to char- acterize Amaltheus lamberti (Nikitin, 1881) and the Johann Reinecke was one of the first authors to genus Cadoceras (Nikitin, 1884). Vischiakoff (1878, recognize the importance of the last chamber in 1882), Lahusen (1883), Pavlow (1886), Pavlow and ammonite shells. In his description of the species Lamplugh (1892), and Mikhalsky (1890) also used this Nautilus costatus (=Paltopleuroceras costatus (Rein.)), character in ammonite descriptions. Mikhalsky (1890, he indicated the chamber size relative to the whorl p. 286) studied the variability of the BCL and noted length (Reinecke, 1818, p. 87). that this character is inconsistent and seems unsuitable Sowerby (1812, p. 10) was the first to identify the to diagnose genera. After these seminal studies, men- body chamber as a “habitation of the animal” when tioning the size of the body chamber has become a describing cephalopods with an external conch, more common research practice. However, the num- although he did not consistently use one term and ber of genus-group and species-group taxa, for which named it a “terminal chamber,” “outer chamber,” or the BCL has been indicated, varies (Table 1). Of the “finishing chamber” (Sowerby, 1812). Sowerby (1818) above publication list, 63% of authors indicate BCL was also the first to indicate the length of the body for less than the half of the genera described in their chamber in his description of Ammonites excavatus. monographs. For species-group taxa, this is 54%.

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Table 1. Use of the body chamber length (BCL) in ammonite descriptions in selected monographs on the systematics of the Jurassic or Cretaceous ammonites Genera Species total indicating BCL indicating BCL, % total indicating BCL indicating BCL, % Mikhalsky, 1890 6 2 33 23 3 13 Krimholz and 28 6 21 90 11 12 Sokolova, 1949 Sasonov, 1957 4 1 25 40 5 13 Ammaniyazov, 1962 8 0 0 52 2 3.8 Mikhailov, 1966 5 0 0 38 29 76 Meledina, 1973 8 4 50 37 21 57 Knyazev, 1975 4 2 50 26 19 73 Meledina, 1977 18 11 61 46 29 63 Sasonova, 1977 17 2 12 39 5 13 Mitta, 1993 10 4 40 26 15 58 Mitta, 2000 6 5 83 23 6 26

Thus, indication of the body chamber length in does not change in this species from the ammonitella descriptions of Jurassic and Cretaceous ammonites is stage to the last body chamber, hence the “body cham- not a uniformly accepted practice. Sometimes owing ber length is a character reasonably consistent in indi- to poor preservation, but most commonly because of vidual development.” Meledina (1977) showed the the low taxonomic value of this character, it is not variability of the BCL for three adult specimens of given much importance. However, the idea of the pos- Eboraciceras taimyrense Meled. Landman (1987) sibility of recognition of species and phylogenetic lin- studied the variability of BCL of juvenile whorls using eages, using BCL, was first proposed in the 19th cen- statistical methods, and noted that the coefficient of tury (Suess, 1865; Haug, 1898), is now published by variation of this character (7.63) shows a large range of some contemporary authors (Mitta, 1993, 2005, variability, which could have resulted not only from 2016). the flexibility of this character, but also from an Is it really possible to use BCL similarities and dif- incomplete state of preservation of the body chambers ferences in ammonite taxonomy and phylogenetic (Landman, 1993). Discrete (polymorphic) intraspe- reconstructions? It seems evident that this question cific variability of BCL is suggested for Amaltheus mar- can only be adequately answered after studying the garitatus, in which populations contain morphs with variability of this character at the genus and species wide smoothened whorls and a shorter body chamber, levels1. In cases of high variability within a genus and and individuals with wide coarse-ribbed whorls with a low intraspecific variability, the BCL should be con- longer body chamber (Hammer and Bucher, 2006). sidered to be a good diagnostic character, and vice Despite considerable experience of studying intra- versa. Combinations of various modes of variability specific variability in ammonites (Baets et al., 2015), can differ in different families, but the so far accumu- so far there are no results permitting statistically signif- lated data suggest that the intraspecific variability icant estimates of the continuity or discreteness of the could be very significant. Hyatt (1877, p. 362) showed BCL variability. This, as much as the lack of data on that the BCL variability in the family Arietidae is so high that this character cannot be used for taxonomy. the range of variability, precludes estimating the taxo- nomic significance of this character. Bodylevsky (1925) was the first to study BCL in the ontogeny of Jurassic ammonites (ontogenetic variabil- The purpose of this paper is the study of the vari- ity as in Baets et al., 2015) using the example of Cadoc- ability of the body chamber length in the family Car- eras elatmae (Nik.). Bodylevsky showed that BCL dioceratidae (Cadoceratinae and Arctocephalinae), the taxonomy of which is debatable. This group is 1 Here and subsequently the variability is used not only for intra- characterized by high morphological diversity, hence, specific variation, i.e., in the classical sense, but also to analyze it is interesting to see how the length of the body the variability of a character within a genus. This is because the boundaries of paleontological species (in this case, ammonites) chamber correlates with the whorl shape, proportions are often conventional; hence taxa of various ranks cannot be of the whorl cross-section and other characters of the always reliably distinguished. ammonite shell.

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MATERIAL AND METHODS ° (2) Mean range of variation (Vi ) is the amplitude This paper is based on images of the last and tem- between the statistical mean maximum and minimal porary body chambers of specimens in various collec- values of L°. This parameter is expressed is a sum of tions and publications. The bulk of the samples were standard deviations calculated separately for sets of represented by last body chambers (LBC). These are ° − + positive and negative values, i.e., Vi = Sx + Sx . It is easy to recognize if the shell has a terminal septum, used for taxa of any rank as a measure of the norm of apertural constrictions and other relevant characters the maximum variation excluding rare random devia- (Pompeckj, 1894; Ruzhencev, 1962; Callomon, 1963). tions and outlying case. This parameter allows discrete If the last body chamber does not have either an aper- and continuous variability to be distinguished and the tural margin or an apertural constriction preserved, seemingly discrete variations caused by a random drift the angular length can be measured based on other of values in small samples to be identified. markers. For instance, in many cadoceratins, the LBC is characterized by a gradual decrease in the thickness (3) Relative range of variation (Vr) is the range of of the umbilical wall, 1.2–1.7 times (up to 50–80% of variance of a subdominant taxon over the range of the maximum thickness) before the aperture (Pl. 5, variation of a higher taxon in percent, e.g., Vr = figs. 1–3; Pl. 6, figs. 3, 4; Pl. 7, figs. 1, 2). At the same °° °° VVspecies family × 100 or Vr = VVgenus family × 100 (any time, the angle of the umbilical wall also changes: near possible combinations). This parameter shows the the last septum it is almost vertical to the coiling plane overlap of taxa for a character studied. and near the terminal aperture it has a small angle, sometimes up to 30°–40°. These characters allow the (4) Variation rate (Vt) is the maximum value of ° ° proximity of the apertural margin to be estimated rel- BCL (Lmax ) over the minimal value (Lmin ), from the atively precisely. °° same sample of values: Vt = LLmax min . This is a Temporary body chambers (TBC) that are formed dimensionless quantity indicating the maximum scale during morphogenesis are more difficult to recognize of the BCL increase (and hence the ammonite soft because they are less often completely preserved that body increase) in a sample of a taxon due to variability. the last body chamber. They were used for measure- ments only when they had remains of the aperture or The above parameters are useful for estimating the characters of the apertural margin. taxonomic distance between species or genera. In this paper I use several criteria and methods for The variability of the length of the body chamber in correction of the TBC length: (1) body chamber the family Cardioceratidae Siemiradzki, 1891 was length is measured correctly if the shell has an tempo- studied in nine macroconch genera with four subgen- rary apertural margin symmetrically expressed on the era of the subfamilies Arctocephalitinae Meledina, flanks and a regular outline and a falcate-shaped cur- 1968 and Cadoceratinae Hyatt, 1900. The body cham- vature (Pl. 5, fig. 4; Pl. 6, figs. 6); (2) for estimates in bers were measured for 66 species, of which only specimens, in which the apertural margin is incom- 27 species have samples that allowed determination of pletely preserved, well-preserved reference specimens the BCL variability. Of these, five species have sample considered to be normal are used. Specimens in which size of over 10 specimens, exceeding 20 specimens in BCL differs by more than 10% (mean coefficient of three species. The total number of reliably identified variation in species) to either side of the norm; specimens is 302, of which 215 are represented by last (3) specimens, in which a decrease in the shell wall body chambers (Table 2). thickness is observed near the incompletely preserved Species with arguable taxonomic status (possible apertural margin, are considered suitable for measure- synonyms) and/or with a sample insufficient for the ments; (4) BCL can be measured even if the body variability study, were artificially united according to a chamber is partially or completely absent, but the geographical or morphological criterion within the phragmocone shows an umbilical margin as a spiral indication of the group: line or a band. Accordingly, the diameter of the non- 1. Cadoceras (Cadoceras) ex gr. calyx Spath preserved body chamber was calculated from approxi- includes C. (C.) calyx Spath, C. (C.) apertum Callo- mation curves. mon, and C. (C.) simulans Spath; Thus, samples always contain body chamber mea- 2. Cadoceras (Paracadoceras) ex gr. multiforme sured with a small error. Small measurement errors Imlay includes Early Callovian cadoceratins of South- exist, but generally do not change the BCL statistical ern Alaska and Northern Canada , such as C. (P.) mul- distribution and variability. tiforme Imlay, C. (P.) glabrum Imlay, C. (P.) comma The following parameters are used in this paper to Imlay, C. (P.) harveyi Crickmay, C. (P.) wosnessenskii analyze the BCL variations (L°): (Grewingk) sensu Imlay 1953, part., and C. (P.) chisik- (1) Variability range (V°) is the total amplitude ense Imlay. between the maximum and minimal values of L°. This 3. Cadoceras (Catacadoceras) ex gr. infimum Guly- parameter is used for taxa of various ranks as a measure aev et Kiselev includes C. (Cat.) infimum Gulyaev et of maximum variation. Kiselev, C. (Cat.) keuppi (Mitta), C. (Cat.) nageli

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Table 2. Body chamber length (L°) and its variability in species, subgenera, and genera of early cardioceratids. Explanations: ° ° (BC) body chamber; (LBC) last body chamber; (V ) variation range (in degrees); (Vi ) mean variation range (in degrees); (Vr ) relative variation range (% of V° in a family); (Vri) relative variation range (% of V° in a family). Explanation in the text o o Genera, subgenera Mean value L Variability range L Nsample NTBC and species ° ° V V in all BC only in LBC V Vi r t Cardioceratidae Siemiradzki 302 215 268.8 262.7 283 78.3 100 3.06 Cadoceratinae Hyatt 254 167 272.19 271 283 77.17 100 3.06 Funiferites Kiselev et al. 22 16 276 261 223 131 78.8 2.62 F. allae (Kiselev) 9 5 328.2 326 98 87.33 34.6 1.37 F. patruus (Eichwald) 7 5 301 294 114 74.66 40.3 1.46 F. funiferus (Phillips) 6 6 167.67 167.7 63 38.66 22.3 1.46 Chamoussetia Douville 14 4 248.2 – 205 122.28 72.44 2.32 Ch. buckmani Callomon 7 4 202.43 170 135 115.6 47.7 1.87 et Wright Ch. hyperbolicum (Buckm.) 7 0 284.71 – 155 108.4 54.8 1.75 Cadochamousettia Mitta 41 31 272 265.2 196 60.8 69.26 2.03 Cad. subpatruus (Nik.) 8 8 240 240 117 67.9 41.3 1.61 Cad. surensis (Nik.) 8 6 286 274 61 46,.9 21.5 1.24 Cad. tschernyschewi (Sok.) 25 17 290 281.6 146 50.6 51.59 1.61 Cadoceras Fischer 174 119 274.7 280.12 240 69.57 84.8 2.47 C. (Rondiceras) milaschevici 38 20 277.4 303 207 75.48 73.1 2.15 (Nik.) Cadoceras s. str. 59 27 302.7 294.4 230 63.6 81.27 2.33 C. (C.) tscheffkini (Orb.) 20 7 268.7 290.2 149 62.7 52.6 1.78 C. (C.) geerzense 7 2 317.4 281 82 68.6 28.97 1.29 (Behrendsen) C. (C.) sokolovi Kiselev 20 8 315 314 145 52.4 51.2 1.53 C. (C.) sublaeve (Sow.) 10 6 314.7 300.3 69 47 24.38 1.25 C. (C.) ex gr. calyx Spath 5 3 285 277.8 82 66.9 28.97 1.37 C. (Paracadoceras) Crickmay 49 42 272.16 273.4 180 62.28 63.6 2.05 C. (P.) elatmae (Nik.) 26 24 258 258.3 180 57.59 63.6 2.05 C. (P.) frearsi (Orb.) 3 2 238.3 252.5 53 42.5 18.7 1.25 C. (P.) anabarense (Bodyl) 6 5 278.6 284.4 60 50.5 21.2 1.24 C. (P.) ex gr. multiforme Iml. 10 8 286.1 282.6 99 49.66 34.98 1.45 C. (P.) quenstedtiforme 4 3 254 245 51 33 18 1.22 (Mitta) C. (P.) suevicum Call. et Dietl 1 1 318 318 – – – – C. (Catacadoceras) 30 30 249.6 249.6 140 68.3 49.47 1.82 Bodylevsky C. (Cat.) barnstoni (Meek) 8 8 256.6 256.6 72 41.2 25.4 1.33 C. (Cat.) ex gr. infimum 6 6 185.43 185.43 52 32.5 18.37 1.31 Gul. et Kis. C. (Cat.) variabile Spath 7 7 244 244 87 48.3 30.7 1.43 C. (Cat.) catostoma Iml. 2 2 283 283 4 4 1.4 1.01 C. (Cat.) nordenskjoeldi Call. 4 4 284.7 284.7 47 34.5 16,6 1.18

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Table 2. (Contd.)

o o Genera, subgenera Mean value L Variability range L Nsample NTBC and species ° ° V V in all BC only in LBC V Vi r t Arctocephalitinae Meledina 41 41 248.24 248.24 174 60.18 61.48 1.93 Arcticoceras Spath 9 9 223.7 223.7 61 29.8 21.5 1.29 A. cranocephaloide Callomon 3 3 206.6 206.6 38 31 13.4 1.2 A. ischmae (Keys.) 6 6 231 231 32 29.16 11.3 1.15 Arctocephalites Spath 19 19 265.7 265.7 142 52.96 50.17 1.65 Cranocephalites Spath 12 12 230.5 230.5 75 33.46 26.5 1.36 Greencephalites Repin 1 1 355 355 –– –– Eckhardites Mitta 7 7 238.7 238.7 133 80.3 46.9 1.63

(Mitta), C. (Cat.) efimovi (Mitta). This group included these, which takes actual distribution into account, several closely related or synonymous species from the was used for Paleozoic ammonites (Haug, 1898) and middle reaches of the Volga River (Middle Povolzhye) included two groups: Brevidoma, with a short body with a similar or identical stratigraphic position in the chamber (180°–360°) and Longidoma, with a long Upper Bathonian (Gulyaev and Kiselev, 1999; Mitta, body chamber (over 360°). The formal classification of 2005; Kiselev, Rogov, 2007). BCL was proposed by Krimholz (1960), who recog- For some genera the variability was not studied at nized three groups—with a short BC (up to 180°), the species level because of insufficient material. In medium BC (180°–360°) and long BC (more than such cases results are given for the entire genus, for 360°). Informal classifications wherever possible use example the following genera: less subjective boundaries between the groups. Wester- Cranocephalites mann (1996) accepts angular values of BCL as bound- 1. Spath including C. vulgaris vul- aries, near which shell hydrostatics and apertural ori- garis Spath, C. vulgaris var. densicostata Spath, C. vul- entation differ considerably. Westermann recognized garis var. compressa Spath, C. pompeckji (Madsen) var. three groups of body chambers according to their laevis Spath, C. costidensus (Imlay), C. rotundum length: brevidomes (less than 220°), mesodomes (Imlay), C. alaskanus Imlay, and C. cf. ignekensis (220°–320°), and longidomes (over 320°). Lukeneder Imlay. (2015) recognized groups of body chambers using the 2. Arctocephalites Spath including A. arcticus same criteria, but his system is to some extent contro- (Newton), A. elegans Spath, A. nudus Spath, A. spathi versial, as it contains gaps between the groups (Fig. 1c, Poulton, A. callomoni Poulton, A. praeishmae Poulton, column 3). A. amundseni Poulton, and A. kigilakhensis Voronetz. Eckhardites Objective boundaries between groups can be 3. Mitta including E. pavlowi (Smoro- emended or verified using statistical criteria. The dina), E. menzeli (Mönnig), and E. dietli Mitta. This cumulative curve (Fig. 1b) shows critical points (203° genus, the position of which in the family Cardiocer- and 340°), based on which the recognition of three atidae is debated (Kiselev and Rogov, 2007; Mitta, groups is possible: brevidomic (less than 203°), 2009), is formally included in this list. mesodomic (203°–340°), and longidomic (more than 340°). This grouping is most similar to Westermann’s RESULTS classification but differs due to the specifics of the selected material. Since the position of critical points Variations within Genera and Subgenera on the cumulative curve in Fig. 1b is unstable and can The total distribution of BCL in early cardiocer- depend on the size of the sample, in this paper I use atids is a normal distribution (Fig. 1a) and shows a Westermann’s classification developed based on vari- wide range of variations from 137° to 420°. The mean ous hydrostatic simulations of ammonite shells (after value is 268°, therefore, all body chambers with a Saunders and Shapiro, 1986, and Ebel, 1990). smaller BCL can be considered as short and vice versa. Most specimens of the studied cardioceratids However, for further analysis of diversity it is neces- belong to the mesodomic group (69.2%). The brevid- sary to use grouping of body chambers in length based omic and longidomic groups are approximately on a less formalized principle. equally represented, and occur in low numbers Several classifications of the ammonite body (16.4 and 14.4%). It is possible to determine to which chamber length have been proposed. The first of extent this distribution reflects the intraspecific vari-

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540 120 (a) (b) 120 520 100 500 80 120 480 460 60 120 440 40 Sample no. 420 20 400 100

0 Longidomes 380 100 150 200 250 300 350 400 450 360 (L) body chamber angular length, deg 80 340

320 double by are shown mic classes, circles:

60 istribution; (b) classification of body cham-

300 ers. Classification of body chambers (on the 280 40 260 240 theoret- of BCL from deviations curvethe shows gray Mesodomes 220 20 200

(L) body chamber angular length, deg length, angular (L) body chamber 180 0 160 140 –20 120 100

–40 Brevidomes 80 Ranked genus 60 1234 (c) 420 400

380 long Very Longidomes 360 Longidomes Longidomes 340 mesodomic, boundaries and brevidomic, longido indicating between 320 300 280

260 Mesodomes Long

240 Mesodomes Brevidomes 220 (L) body chamber angular length, deg length, angular (L) body chamber 200 180

160 Brev. Brevidomes Short 140

0 20 40 60 80 100 120 140 160 180 200 220 240 d (a) density length, body chamber the for relative and arctocephalitins) (cadoceratins specimens Distribution of cardioceratid Shell diameter, mm Fig. 1. bers for critical points in the range distribution of 273 specimens. Black curve is a theoretical curve of range distribution, curve is Black a theoretical specimens. points in the range distributionbers critical of 273 for of linear points regression. values Critical calculated ically (c) body chamb show intermediate last show circles body white chambers, circles Black values. distribution of the diameter shell (4). (3); Haug, 1898 2015 (2); Lukeneder, 1996 (1); Westermann, Krimholz,right) is 1960 after

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4.0

3.5

3.0

2.5

2.0

1.5 (D/T) relative shell height shell (D/T) relative 1.0

0.5 Brevidomes Mesodomes Longidomes 0 140 160 180 200 220 240 260 280 300 320 340 360 380 400 420 440 (L) body chamber angular length, deg

Fig. 2. Correlation of the relative body chamber length and relative shell height (shell diameter to whorl width) in cardioceratids. Black circles show last body chambers, white circles show intermediate body chambers. Lines of the exponential trend are given for all specimens (R2 = 0.45) and for the last body chambers (R2 = 0.5). ability and is connected with taxonomic diversity by observed in most known genera and subgenera of car- studying the correlation of BCL with other characters. dioceratids. Arctocephalites, Cadoceras s.str., C. (Para- cadoceras), C. (Catacadoceras), Cadochamoussetia, A correlation of BCL with the shell diameter has Chamoussetia, and Funiferites (Fig. 4) occupy a single not been observed in either the total sample or within morphospace. Cranocephalites, Arcticoceras and to a the brevidomic, mesodomic, and longidomic groups lesser extent, Eckhardites are in a different morpho- analyzed separately (Fig. 1c). This means that there is space. no morphogenetic trend in all the examined cardioc- eratids. The absence of any kind of correlation is Therefore, it is virtually impossible to establish tax- observed in both the terminal and intermediate body onomic similarity or disparity or phylogenetic rela- chambers. tions between taxa based on similarity or differences in BCL. Likewise, it is difficult to determine continuity A slight correlation is observed between BCL and of taxa judging from their stratigraphic succession and relative shell height or width (Fig. 2). This reveals a similarity of the body chamber distribution (Fig. 3). trend toward a decrease in the body chamber length in discoconic, oxyconic, and platyconic shells and an General shape and shell proportions are known to increase in BCL in cadicones or pachycones. The first influence shell hydrodynamics and consequently three shell types are characteristic of the genera Cha- affect its adaptation capacities. Such parameters moussetia, Cadochamoussetia, Funiferites, Arcticoceras, include relative shell height, which as shown above, and Eckhardites, whereas other shell types are more does not show a distinctive correlation with BCL. common in Cadoceras, Arctocephalites, and Crano- The whorl expansion rate (W), which is another cephalites. Nevertheless, the observed correlation is so extremely important parameter of shell geometry is small that it is unlikely to be used as evidence of a cor- definitely correlated with BCL in Cretaceous ammo- relation between the characters. The BCL values nites and nautilids (Okamoto, 1996) and Devonian within genera are so diverse that eight of 11 studied ammonoids (Klug, 2001). These characters show a genera and subgenera show specimens with body negative correlation, i.e., the BCL value is highest in chambers of all three types, and in three cases of the species with lower values of the whorl expansion rate. 11, of two types (Table 3, Fig. 3). None of the genera In cadoceratins and arctocephalitins, there is almost have a body chamber of only a single type, which is no correlation between these values (Fig. 5). These

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12345678910 100

90

80

70

60

50

40

30

20

10 Number of specimens with different type of body chamber, % typechamber, of body with different of specimens Number 0 ) ) ) ) Funiferites Cadoceras Arcticoceras Rondiceras . ( Chamoussetia . ( Arctocephalites C Catacadoceras Paracadoceras C Cranocephalites ( . ( Cadochamoussetia C. C Brevidomes Mesodomes Longidomes

Fig. 3. Quantitative correlation with a different type of the body chamber in genera and subgenera cardioceratids. Numbers 1 to 10 show the relative age of taxa corresponding to their stratigraphic succession. groups are characterized by a W value in the range any correlation between W and L°. All examples of 1.1–1.5, which corresponds to a very low whorl negative correlation of these characters are shown in expansion rate (Klug et al., 2015, p. 7). It is possible a wide range invariably above the values of W = 1.5 that this range of very low values is too small to show (Okamoto, 1996, text-fig. 6).

Table 3. Percentage of specimens with different types of the body chamber length in different genera and subgenera of car- dioceratids Body chamber Genera (subgenera) brevidomic mesodomic longidomic Cranocephalites 45 55 0 Arctocephalites 5.3 84.2 10.5 Arcticoceras 40 60 0 Cadoceras (Catacadoceras) 24 76 0 Cadoceras (Paracadoceras) 10 88 2 Cadoceras (Cadoceras) 46531 Cadoceras (Rondiceras) 17 63 20 Cadochamoussetia 11.2 80.5 8.3 Chamoussetia 35.8 42.8 21.4 Funiferites 27.3 31.8 40.9

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440 1—Cranocephalites 2—Arctocephalites 420 3—Arcticoceras 4—Catacadoceras 400 5—Paracadoceras 8 6—Cadochamoussetia 380 6 7—Chamoussetia 8—Cadoceras 360 9—Funiferites 7 4 10—Eckhardites 340 5 320 300 6 280 260 2 240 10 220 (L) Body chamber angular length, deg length, angular chamber (L) Body 200 8 1 3 180 9 7

160 Brevidomes Mesodomes Longidomes 140 0 20 40 60 80 100 120 140 160 180 200 220240 260 Shell diameter, mm

Fig. 4. Distribution of the body chamber angular length and shell diameter in genera and subgenera of cardioceratids. Each taxon is characterized by a range of morphological space. Position of most specimens is shown in Figs. 6–8.

1.55

1.50

2 1.45 R = 0.1953

1.40

1.35

1.30

1.25

(W) whorl expansion rate (W) whorl 1.20

1.15 Brevidomes Mesodomes Longidomes 1.10 140 160 180 200 220 240 260 280 300 320 340 360 380 400 (L) body chamber angular length, deg

Fig. 5. Relationships between the body chamber angular length and whorl expansion rate in cardioceratids.

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Arcticoceras Chamoussetia C. (Catacadoceras) C. (Cadoceras) and C. (Rondiceras) 350 C. (Paracadoceras) Funiferites Longidomes 330 Cadochamoussetia

310

290 L 270 i family

250

230

i 210

(L) body chamber angular length, deg length, angular (L) body chamber 190

170 Brevidomes Mesodomes 150 calyx frearsi F. allae F. elatmae sokolovi infimum sublaeve .) variabile geerzense barnstoni F. patruus F. catostoma P .) tscheffkini .) .) multiforme A. ischmae .) F. funiferus F. .) anabarense .) P C .) milaschevici . ( C .) C Cad. surensis Cad. .) ex gr. gr. .) ex .) . ( C C . ( Ch. buckmani .) Cat . ( nordenskjoeldi Cat C P . ( C quenstedtiforme Cat C R C . ( Cad. subpatruus Cad. .) ex gr. gr. .) ex . ( .) C . ( . ( . ( Ch. hyperbolicum .) C . ( . ( C C .) ex gr. gr. .) ex C C A. cranocephaloide P C C Cat Cad. tschernyschewi Cad. Cat P . ( . ( . ( . ( C C C C

Fig. 6. Ranked distribution of the body chamber angular length in cardioceratids.

The BCL distribution in species of most genera and Chamoussetia, which occur in the middle of the range subgenera of cardioceratids can in general be charac- and are mainly in the mesodomic range of the BCL terized as eurymorphic, i.e., in a wide morphological values (Fig. 6). Note that C. (Catacadoceras) and Cha- range, and isomorphic (overlapping in most taxa). moussetia occur both in the mesodomic and brevidomic This suggests a lack of prominent differences of these range, whereas C. (Paracadoceras) and Cadochamous- characters in supraspecific taxa of cadoceratins and setia are completely within the mesodomic range. A arctocephalitins. The widest and most equally distrib- narrower range of BCL values is observed in the species uted overlap is observed in species of Cadoceras (Para- of Arcticoceras and Funiferites, morphologies of which cadoceras), C. (Catacadoceras), Cadochamoussetia and occupy the marginal field of the total morphospace.

Explanation of Plate 3 Explanations here and below: (TBC) temporary body chamber, (LBC) last body chamber, (YarGPU) A.N. Ivanov Geological Museum (Yaroslavl State Pedagogical University). Asterisks mark the beginning of the body chamber, crosses mark apertures, and arrows show an apertural constriction. Numbers near the dashes show a relative thickness of the umbilical shoulder (US) near the aperture, in per cent from the maximum US in TBC. Scale bar 10 mm. Figs. 1 and 2. Cadoceras (Catacadoceras) barnstoni (Meek): (1a, 1b) LBC, specimen YarGPU ZFI/M-1. Franz Josef Land, Hooker Island, Medvezhii Cape, Upper Bathonian, Barnstoni Zone (coll. by V.D. Dibner, 1957); (2) LBC, specimen YarGPU LRJ4/3; Yakutia, Lena River, Chekurovka Village, talus of the Tochinsk Formation (Upper Bathonian) (coll. by M.A. Rogov, 2009). Fig. 3. Cadoceras (Catacadoceras) infimum Gulyaev et Kiselev. LBC, YarGPU 6/3. Previously figured by Gulyaev and Kiselev (1999a, pl. 2, fig. 6). Nizhny Novgorod Region, Prosek Village, Upper Bathonian, Calyx Zone, infimum Biohorizon. Fig. 4. Cadoceras (Rondiceras) milaschevici milaschevici (Nik.). TBC with an apertural margin at the pre-Cadoceras stage, left side, specimen YarGPU 3/12. The same specimen illustrated from the right in Pl. 3, fig. 4. Kostroma Region, Unzha River, Cher- menino Village, Middle Callovian, Jason Zone, Medea Subzone. Figures 1–3 have the same scale.

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Plate 3

+

1a 1b

220°*

2

+ +

+

4 3

199° * *

PALEONTOLOGICAL JOURNAL Vol. 52 No. 13 2018 1528 KISELEV

C. (P.) frearsi (Orb.) C. (P.) ex gr. multiforme Imlay C. (P.) elatmae (Nik.) C. (P.) ex gr. suevicum (Call. et Dietle) 370 C. (Catacadoceras) the Arctic C. (Catacadoceras) Middle Volga Region 350 C. (P.) breve Blake

330

310

290

270

250

230

(L) body chamber angular length, deg length, angular (L) body chamber 210

190

170 Brevidomes Mesodomes Longidomes

150 40 60 80 100 120 140 160 Shell diameter, mm

Fig. 7. Distribution of the body chamber angular length and shell diameter in specimens of various species of Cadoceras (Cataca- doceras) and C. (Paracadoceras).

The study of variability of the body chamber length body chambers are completely mesodomic, whereas allows the covariation of this character with other shell Cad. subpatruus 50% of specimens are mesodomic, features in various phylogenetic lineages to be esti- while the remaining specimens belong to the brevid- mated. It is shown above (Fig. 2) that in early cardioc- omic group. eratids the covariation of BCL with the whorl shape Shells of Chamoussetia are characterized by a more (negative correlation) is too weak to be considered sig- strongly oxyconic and carinate morphotype than Cad. nificant, along with other rules of covariation (1 and subpatruus, but the mean BCL values in this genus are 2 Buckman’s rules of covariation). Below, the mani- higher (248.2°). This is related to the fact that the body festation of this character is considered in the phyloge- chambers of Chamoussetia are distributed in all three netic lineage Cadochamoussetia-Chamoussetia, the types – longidomic (21.4%), mesodomic (42.8%) and terminal members of which have a discoconic and brevidomic (35.8%). Long body chambers are gener- oxyconic shell. It is generally accepted, based on ally characteristic of Ch. hyperbolicum (Buckm.) actual observations (Mitta, 2005; Mitta, 2016), and on (=Ch. phillipsi Call. et Wright, pars.), which have a theoretical calculations (Hammer and Bucher, 2006), more inflated shell morphotype (Pl. 4, fig. 1). In that an increase in lateral compression should be Ch. buckmani Call. et Wright, body chambers are most accompanied by BCL. In general, this is manifested in commonly brevidomic (Pl. 4, fig. 3); nevertheless, the the genus Cadochamoussetia by a decrease in the mean sample also contains mesodomic morphotypes, with values of BCL (along with increase in lateral compres- BCL up to 280° (Pl. 4, fig. 2). In the relative range of sion of the shell) in the phylogenetic lineage Cad. variation, (V ) the variability of species of Chamousse- Tschernyschewi–Cad. Surensis–Cad. subpatruus: r 290°–279.4°–240°. However, variations in each spe- tia is the highest among cardioceratids (Pl. 4). This is cies result in the essential overlap of the morphospaces probably related to the small size of the sample, which of these species (Fig. 8). The body chambers of Cad. accidentally included only marginal specimens. tschernyschewi are mainly mesodomic (86%) and to a A similar situation is observed in the genus lesser extent longidomic (14%). In Cad. surensis, the Funiferites: F. patruus is markedly different from

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410 Cadoch. tschernyschewi (Sok.) 390 Cadoch. surensis (Nik.) Cadoch. subpatruus (Nik.) 370 Chamoussetia

350 Longidomes 330

310

290

270

250

230 (L) body chamber angular length, deg length, angular (L) body chamber 210

190

170 Brevidomes Mesodomes

150 0 20 40 60 80 100 120 140 160 Shell diameter, mm

Fig. 8. Distribution of the relative angular length of the body chamber and shell diameter in specimens of Chamoussetia and var- ious species of Cadochamoussetia. Dots show intermediate body chambers; solid figures show last body chambers.

F. allae in the whorl shape and proportions, although LBC). The remaining specimens in the sample belong the proportions of longidomic and mesodomic speci- to a longidomic class (33%). The minimal value of mens in the samples of this species are almost the BCL for the adult whorls is 266°, and the maximum same. Only F. funiferus, the terminal species of this value is 397° (Pl. 5, fig. 5). In the adult whorls preced- genus, is represented by only brevidomic morpho- ing the last body chamber, the length of the body types. chamber is generally shorter than that in the terminal In the phylogenetic succession, Cadochamoussetia- whorl, hence there is a slight trend toward an increase Chamoussetia and the genus Funiferites the covariation of the body chamber length in morphogenesis (Fig. 9). of BCL and the whorl height is inconsistent; therefore This trend is disrupted by the presence of a few longi- its diagnostic value appears to be low. domic specimens. In the intermediate stage with later- ally compressed or sometime discoconic shells (pre- Cadoceras stage according to Ivanov, 1960), BCL is Intraspecific Variability considerably smaller (up to 180°–200°) than in adult Intraspecific variability will only be discussed in cadiconic whorls, i.e., in this stage, the body cham- those species which are represented by relatively large ber was brevidomic (40% of specimens of this stage) samples (Pl. 4). These samples are dominated by last or shortened mesodomic (60% of specimens) (Pl. 5, body chambers; hence this material allows the vari- fig. 4). ability of the terminal ontogenetic stage to be esti- Thus the morphogenesis of C. milaschevici shows a mated. correlation between whorl height and BCL, which is In C. milaschevici, the length of the body chamber characterized by a considerably high correlation index could be more than one whorl; nevertheless, most (r = 0.73). This is the only species of cadoceratins in samples of the adult whorls (Cadoceras and terminal which the morphological trend of the BCL variation is stage) represent the mesodomic class (67% of all distinctly expressed. These differences can be

PALEONTOLOGICAL JOURNAL Vol. 52 No. 13 2018 1530 KISELEV

Plate 4

* 328°

1b 1a

2b 277° *

2a

3b 3a * ~180°

PALEONTOLOGICAL JOURNAL Vol. 52 No. 13 2018 VARIABILITY OF RELATIVE BODY CHAMBER LENGTH IN JURASSIC AMMONITES 1531

450 C. milaschevici (Nik.) R2 = 0.67 2 430 C. tscheffkini(Orb.) R = 0.48 C. sokolovi Kiselev R2 = 0.06 410 C. sublaeve (Sow.) R2 = 0.78 390 370 350 330 310 290 270 250 230 (L) body chamber angular length, deg length, angular (L) body chamber 210 190 170 Brevidomes Mesodomes Longidomes 150 0 20 40 60 80 100 120 140160 180 200 220 Shell diameter, mm

Fig. 9. Distribution of the angular length of the body chamber and shell diameter in various species of Cadoceras (Cadoceras) and C. (Rondiceras). Dots show intermediate body chambers; solid figures show last body chambers. explained by the relative whorl height being the great- chamber: the maximum body chamber length is most est among cadoceratins (D/T = 2.73) in the pre- common in dwarf individuals with relatively high pro- Cadoceras stage in this species, whereas at the Cadoc- portions of the terminal shell (Pl. 5, fig. 1), whereas eras stage it is as low as in other species that develop a larger, bradygerontic individuals, with relatively wide cadicone at the adult stage (D/T = 1.1–1.5). In whorls, have a longer body chamber (Pl. 5, figs. 2, 3). C. tscheffkini, the phylogenetic predecessor of A general trend toward an increase in the body cham- C. milaschevici, BCL at the pre-Cadoceras stage ber length with age in C. milaschevici, suggests that in (D/T = 2.48) is also shorter than at the terminal stage dwarf (tachygerontic) individuals bradymorphy is (last body chamber), but the difference between them expressed in the length of the body chamber. Individ- is less noticeable than in C. milaschevici (Fig. 9). uals with a slower development retain a shorter body In other cadoceratins, the length of BC remains chamber in adult stages, which is not much longer that more or less consistent in the morphogenesis, e.g., in in the pre-Cadoceras stage. Bradymorphic individuals C. elatmae (Bodylevsky, 1925), or varies randomly to a in the size range D = 90–130 mm represent an interval varying extent. The latter is also observed in of the co-occurrence of tachygerontic, normogeron- C. sokolovi, the basal species in the phylogenetic lin- tic, and bradygerontic individuals (Fig. 9, dashed zone eage Cadoceras s. str.—C. (Rondiceras) (Fig. 9). of overlap). Some cadoceratins, e.g., C. milaschevici, show a Among C. elatmae (mean L° = 258° = middle of correlation between shell size and BCL in the last body the lower half of the mesodomic group) there are

Explanation of Plate 4 Figs. 1a and 1b. Chamoussetia hyperbolicum (Buckm.) TBC, specimen YarGPU 6/32: Kostroma Region, Unzha River, Kolokhta Village, Lower Callovian, Koenigi Zone, Curtilobus Subzone. Figs. 2 and 3. Chamoussetia buckmani Callomon et Wright: (2a, 2b) TBC, specimen YarGPU 6/34; (3a, 3b) LBC, specimen YarGPU 6/33; Kostroma Region, Unzha River, Kolokhta Village, Lower Callovian, Koenigi Zone, Curtilobus Subzone. All fig- ures have the same scale.

PALEONTOLOGICAL JOURNAL Vol. 52 No. 13 2018 1532 KISELEV extremely brevidomic specimens (L° = 170°–200°) very clearly, in C. sokolovi: 50% of middle whorls and and longidomic specimens (L° = 350°). This distribu- only 25% of terminal whorls are longidomic. tion does not show a correlation of the body chamber Thus, the specific characters of BCL at various length either with a total shell shape or cross-section stages of cadoceratin morphogenesis are rarely and shape. However a decrease in BCL is recorded in indistinctly manifested. Ontogenetic trend of the BCL specimens with bradymorphic ornamentation (Pl. 6, changes, rather than the measured BCL, seem to be fig. 1). The body chamber of tachymorphic and nor- more reliable characters. The trends are observed in a momorphic individuals is usually longer, and reaches few species that show a pronounced contrast between the maximum size (Pl. 6, fig. 2). whorl shape at different stages of ontogeny. The vari- The body chamber length of adult whorls of Cado- ability of this character is so high in most that it can chamoussetia tschernyschewi is also quite variable only be used for diagnosis in some rare cases. (Fig. 8). The last body chamber shows a trend toward a decrease in BCL in relatively high shells (Pl. 6, DISCUSSION figs. 3–5), although no significant correlation is observed between these characters. The morphogene- The body chamber length in all studied species of sis of this species shows a continuous weak trend cardioceratids shows continuous variation. This sug- toward a decrease in BCL with age: intermediate gests that BCL is not a polymorphic or polytypic char- whorls are mesodomic (62.5% of the sample) and lon- acter. In general, this conclusion is valid when using a gidomic (37.5%), whereas all measured LBCs are in “splitted” model of taxonomy (as in this paper). If the mesodomic morphospace. The observed inverse some species are accepted within wider limits, with correlation (r = 0.45) is quite weak, but can be better correspondingly wider geographical ranges, the distri- examined in a more complete sample. However, even bution in the sample by BCL may become discrete. In limited material distinctly shows that it is opposite to this case, the variability will be interpreted as poly- the correlation described for C. milaschevici. In typic, as was shown above for the Arctic species Cad. surensis, the same kind of correlation is readily C. (Catacadoceras) barnstoni and its vicariants from observed even based on limited material: a specimen at European Russia. the pre-Cadoceras stage has a longidomic TBC (Pl. 7, The discrete variability of BCL can only be estab- fig. 3), while the last body chambers are mainly lished in species with a wide range of variation, with mesodomic (Pl. 7, fig. 1). In tachygerontic specimens series dominated by specimens with marginal values of of this species, BCL is usually longer than in brady- the body chamber length. As a result, the mean varia- gerontic specimens, and sometimes longidomic (Pl. 7, ° tion range of species (Vi ) can exceed such for the fig. 2). Therefore it is possible that the elongation of entire family, whereas the relative variation range (Vr) the body chamber in the dwarf adults is a manifesta- in this species is certainly below the much lower values tion of bradymorphosis, i.e. deceleration of develop- of the family (100%). Such species include Chamous- ment like in C. milaschevici. If that is the case, the setia buckmani, Ch. hyperbolicum, and Funiferites allae change in the rate of character development in differ- (Pl. 4; Fig. 10). At present it is premature to draw a ent individuals is different: some characters develop conclusion on the discrete nature of the variability of faster than the others, and any combinations of accel- these species, because estimates of their ranges are erated and decelerated rates of character development made based on small samples. If the distribution pat- are possible in different individuals. In C. milaschevici tern remains the same after the study of the BCL of and Cad. Surensis, bradymorphosis of BCL is com- these species based on more representative material, it bined with tachygerontic and tachymorphic develop- will be possible to state that Chamoussetia in fact ment of the umbilicus, whereas in C. elatmae the exhibits a distribution grouped into discrete categories bradymorphosis of BCL could be simultaneous with a (polymorphism). retarded development of ornamentation irrespective How high is the variability value of BCL in car- of the final shell size. dioceratid species? Its coefficient of variation (mean An inverse correlation of BCL and shell diameter is Cv = 9.68% for the species) is completely compatible also observed in C. sublaeve (Fig. 9): all specimens of with that of other shell characters. In taxonomy, the the body chambers at an middle whorls belong to a answer to this question depends on how criteria of spe- longidomic type. This trend is observed, albeit not cific identification are valued by a taxonomist. As spe-

Explanation of Plate 5 Figs. 1–5. Cadoceras (Rondiceras) milaschevici milaschevici (Nik.): (1a, 1b) tachygerontic bradymorph, LBC, specimen YarGPU E/К-46. Previously figured by Ivanov (1975, text-fig. 2, 3). Ryazan Region, Elatma, Middle Callovian, Jason Zone and Subzone; (2a, 2b) LBC, specimen YarGPU Ch1/4-2; (3a, 3b) LBC, specimen YarGPU 3/56; (4a, 4b) TBC at the pre-Cadoceras stage, specimen YarGPU 3/12. Kostroma Region, Unzha River, Chermenino Village, Middle Callovian, Jason Zone, Medea Subzone; (5) LBC, MHC-NC 27, A.A. Mironenko; Ryazan Region, Nikitino Village, Jason Zone, Medea Subzone. Figures 1–3 have the same scale.

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Plate 5

+ + 373° 73 *

5

* 270°

1b 1a +

316° * 85

+

* ° 2a 4b 4a 199 2b +

328° 84 *

3b

PALEONTOLOGICAL JOURNAL Vol. 52 No. 13 2018 1534 KISELEV

Area of continuous variability Area of discrete variability 100 Cadoceratinae Cardioceratidae 90 Cadoceras R2 = 0.61

80 Cadoceras s. str. Funiferites Chamoussetia C. milaschevici 70 Cadochamoussetia 2 C. elatmae C. (Paracadoceras) R = 0.95 60 Arctocephalitinae C. tscheffkini Ch. hyperbolicum Cad. tschernyschewi C. (Catacadoceras) 50 C. sokolovi Ch. buckmani Eckhardites Arctocephalites Cad. subpatruus 40 C. ex gr. multiforme F. patruus F. allae ) relative variation range, % variation ) relative

r C. variabile 30 Cranocephalites C. geerzense (V C. sublaeve C. ex gr. calyx Arcticoceras 20 C. anabarense Cad. surensis Group with samples of over 10 specimens 10 A. cranocephaloide A. ischmae Group with samples of less than 10 specimens 0 C. catostoma 0 20406080100120140 (Vi) mean variation range of the body chamber angular length, deg

Fig. 10. Correlation between different parameters of BCL variability of cardioceratid taxa. Relative range of variation (Vr) (vari- ation range of the subdominant taxon to the variation range of all studied cardioceratids (subfamilies cadoceratins and arctoceph- ° alitins) ratio in percent) shows a comparative value of variability of all taxa, when Vr family = 100%. The mean variation range (Vi ) (difference between the statistical mean and minimum of values) allows the recognition of taxa with discrete variability, in which Vr species, genus > Vr family. Genera and subgenera are shown by areas of morphospace. The dashed lines show a critical level for the family-rank values.

cies or genera descriptions usually contain one fixed In various species, Vr can reach up to 70%. The maxi- value of the body chamber as a diagnostic character, mum values of this character are displayed by variability of BCL should be considered as significant C. milaschevici (73%), C. tscheffkini (52.6%), C. sokolovi in relation to such values. Studies of variability in car- (51.2%), Cad. tschernyschewi (51.9%), Cad. subpatruus dioceratids show that this approach can be used in (41.3%), Ch. buckmani (47.7%), and Ch. hyperbolicum specimen descriptions, but is completely unsuitable (54.7%). For these species, BCL is a taxonomic char- for descriptions of species, let alone of genera. acter that cannot be used only as a fixed value, but also In estimating the taxonomic value of the variation expressed as a mean value. In other species, Vr is in the of the body chamber length, the best marker is the rel- range 1–35%, there, at the first glance, the use of the ative range of variation (Vr) expressed as a ratio (in %) BCL for their diagnostics can be more appropriate. of the total amplitude of the BCL values in a genus or However, it should be noted that the group of species species to the total range of the BCL values in a family. with a low Vr is also characterized by a smaller sample

Explanation of Plate 6 Figs. 1 and 2. Cadoceras (Paracadoceras) elatmae (Nik.): (1) normogerontic bradymorph LBC, specimen YarGPU VP1896/10; (2) normogerontic normomorph, LBC (lateral part of the apertural margin is partly broken off), specimen YarGPU VP-1896/9. Nizhny Novgorod Region, Prosek Village; Lower Callovian, Elatmae Zone and Subzone. Figs. 3–6. Cadochamoussetia tschernyschewi (Sok.): (3a, 3b) LBC, specimen YarGPU 5/4; (4a, 4b) LBC, specimen YarGPU 5/2; (5a, 5b) TBC, penultimate whorl, specimen YarGPU 5/9; (6a, 6b) TBC at a pre-Cadoceras stage, specimen YarGPU 5/11; Kostroma Region, Unzha River, mouth of the Pezhenga River, Lower Callovian, Subpatruus Zone, tschernyschewi Biohorizon.

PALEONTOLOGICAL JOURNAL Vol. 52 No. 13 2018 VARIABILITY OF RELATIVE BODY CHAMBER LENGTH IN JURASSIC AMMONITES 1535

Plate 6 + +

350°

∗ 202°

+

2 1

280°∗

+ 6a 6b

320°∗ 65

380°∗

3a 3b 5a

73 122

4a 4b 5b 220°*

PALEONTOLOGICAL JOURNAL Vol. 52 No. 13 2018 1536 KISELEV

Plate 7

153 332° ∗

3b 3a

325°*

58

2b 2a

85

1a ∗ 1b 240°

PALEONTOLOGICAL JOURNAL Vol. 52 No. 13 2018 VARIABILITY OF RELATIVE BODY CHAMBER LENGTH IN JURASSIC AMMONITES 1537

90 R2 = 0.7 80 r = 0.83 70 R2 = 0.46 60 r = 0.66

50

40

30 ) relative variation range, % variation ) relative r 20

(V Species 10 Genera, subgenera 0 102030405060 Sample size, number of specimens

Fig. 11. Correlation between the BCL variation value of species and genera of cardioceratids and the sample size. The variability indicator is shown by a relative range of variation (Vr) the ratio of the variation range of a subdominant taxon to the variation range of all studied cardioceratids (subfamilies Cadoceratinae and Arctocephalitinae) in per cents.

(less than 10 specimens). These two parameters are ity observed in cardioceratid species can be considered reasonably well correlated (Fig. 11), hence the range of as relatively high. This conclusion contradicts some variation of many species is clearly reduced and can be postulates, which serve as the basis for some concepts reliably estimated only in samples including at least of theoretical morphology, or allows them to be 10 specimens. Apparently, if more representative viewed from new perspectives. Most these concepts material is used, the relative range of variation in species (Truemann, 1941; Saunders and Shapiro, 1986; Ebel, of the second group will increase. Therefore the estima- 1990; etc.) conclude that the body chamber length tion of variability should be restricted to the species indirectly influenced the hydrostatic stability, aper- with the most representative samples. The sample size ture, locomotion, and consequently the lifestyle of of most genera and subgenera exceeds the threshold ammonites. Hence, species with short and long body value designated above, hence the Vr for these taxa can chambers should have occupied different ecological be considered more adequately representative than in niches. As shown above, the variability of BCL in the species. Nevertheless, in the case of the genera and some cardioceratids is so high that populations of the same species can contain both brevidomic, and subgenera, the dependence of Vr on the sample size exists (Fig. 11), and therefore it can be expected that mesodomic, or even longidomic individuals. Conse- the true range of variation in some taxa is somewhat quently one species of ammonite would have included higher. The highest values of V are observed in the different morphotypes with a different life style. If that r was the case, the ecological niche of ammonites would subgenus Cadoceras s. str.—81.3%, and the lowest in have been extremely wide and could include both Cranocephalites—26.5%. The remaining genera and planktonic and nektonic adaptive types. Such capacity subgenera are in the intermediate range of values, of an ecological niche appears to be rather extreme, from 45% and above. This means that BCL values are because it suggests an unspecified lifestyle of ammo- similar in most genera, and so cannot be confidently nites, which is unlikely. used for their identification. The cited reconstructions of ammonite hydrostat- In the context of paleobiological interpretations ics and hydrodynamics are based on the assumption based on theoretical shell morphology and calculated that the ammonite body chamber was entirely filled buoyancy and locomotion of ammonites, the variabil- with the soft body. Therefore the BCL and the length

Explanation of Plate 7 Figs. 1–3. Cadochamoussetia surensis (Nik.): (1) LBC, specimen YarGPU U-10. Nizhny Novgorod Region, Uzhovka Village; (2) tachygerontic bradymorph, LBC, specimen YarGPU VP-1896/12; Nizhny Novgorod Region, Isady Village; (3) TBC, speci- men YarGPU VP-1896/13; Nizhny Novgorod Region, Isady Village. All: Lower Callovian, Subpatruus Zone, surensis Biohori- zon. All figures are in the same scale.

PALEONTOLOGICAL JOURNAL Vol. 52 No. 13 2018 1538 KISELEV of the soft body coincided as in modern Nautilus. If The expansion of the adaptive zones of cardiocer- that was the case, the presence of high variability in atids correlates with an increase of the size of their ammonites leads to conclusions, some of which are geographical range and development of the Middle mutually exclusive: Jurassic transgressions. (1) The relative length and proportions of the (5) Alternative conclusion: the existing models of ammonite soft body strongly varied within species: the the ammonite shell hydrodynamics and hydrostatics maximum angular length of the soft body could be need to be reconsidered. Despite the aforementioned twice the minimal length (Vt, Pl. 4). concepts of theoretical morphology, the aperture ori- (2) Ammonites with different lengths and propor- entation and stability of ammonite shells did not sig- tions of the soft body should have maintained different nificantly influence their lifestyle and change the life styles, considering that the existing theoretical parameters of ecological niches (for species) and models of ammonites are correct. adaptive zone (for genera). Consequently, individu- als with a different soft body length and proportions (3) Species with insignificant variability of BCL had approximately the same lifestyle. Therefore the were stenobiontic, and those with high values of BCL variability of the ammonite soft body was not con- were eurybiontic. The BCL variability range less than trolled by stabilizing evolutionary factors, and was 100° can be considered as an indication of low vari- therefore high. ability. With that value of variability, the maximum body chamber length (and that of the soft body) could It is also possible that in the ammonites, the soft exceed the minimal by not more than 1.5 times body was shorter than the body chamber and could (Fig. 12a). This range embraces all species of Arcticoc- move within it, as suggested by some authors (Monks eras and C. (Catacadoceras), and a third or half of spe- and Young, 1998; Kröger, 2002). It is known that the cies from other genera or subgenera (Fig. 12b). Low- ammonite mantle could from time to time become specialized taxa with the BCL variation range from unattached from the shell wall or could stretch (Dogu- 100° to 180° and specialized taxa (V° > 180°) can be zhaeva and Mapes, 2015). Hence, ammonites could considered as eurybiontic. The variation rates in these regulate and change their buoyancy and locomotion groups are as follows: maximum BCL and soft body type by moving their soft body within the body cham- length exceed the minimal more than 1.5 times, and in ber. The soft body length was more or less constant, the non-specialized twice or more. These include all whereas the BCL varied significantly. Chamoussetia, most Cadochamoussetia and represen- High variability of the ammonite body chamber tatives of other genera and subgenera. The subgenus length can also be explained by a different hypothesis, C. (Rondiceras) shows the minimal level of specializa- according to which the ammonite soft body was longer tion. As most species (20 of 27) were studied from than the body chamber, so ammonites were negatively small samples, it is most likely that if the sample sizes buoyant, and mainly belonged to the benthic adaptive become larger, some species will be moved to the low- zone (Ebel, 1992; 1993). Accordingly, the shell func- specialized groups. The non-specialized group tion was limited, which should have increased its vari- includes C. elatmae and C. milaschevici, which domi- ability. nate (almost totally, up to 100%) in ammonite assem- blages of most Lower Callovian (elatmae biohorizon) and Middle Callovian (milaschevici milaschevici bio- Body Chamber Length and Systematic horizon). Therefore, a high plasticity of these species of Early Cardioceratids can be related to the absence of interspecific competi- Some publications, which propose a new phyloge- tion pressure in the ammonite communities where netic reconstruction of the Late Bathonian–Callovian they prevailed. cardioceratids (Mitta, 2005, Mitta, 2016), contain (4) If the variation rates of BCL reflect the diversity indications of a specific length of the body chamber of the soft body length, and accordingly, the adaptive for the genera Cranocephalites, Arctocephalites, Arcti- possibilities, the same parameter can characterize the coceras, Greencephalites, Cadoceras, Rondiceras, Para- level of specialization and the capacity of the adaptive cadoceras, Chamoussetia, Cadochamoussetia, Eckhar- zone of supraspecific taxa (genera and subgenera) dites, and Platychamoussetia (=Funiferites). These (Fig. 12c). Genera of arctocephalitins were the most interpretations of the differences and similarities of the specialized and stenobiontic, whereas in cadoceratins, body chamber in different genera were largely the basis most taxa were non-specialized. In general, the adap- for the concept of the “main cadiconic evolutionary tive zones of genera and subgenera of expand from the trend in Cadoceratinae” (Mitta, 2016). According to Bajocian–Bathonian to the Late Callovian cardiocer- that concept, this lineage represents a phylogenetic atids, which can be considered as a regular pattern. succession of three genera with a “long body cham- This means that cadoceratins species occupied differ- ber”: Greencephalites–Cadoceras (including Rondi- ent parts of the adaptive zones of genera and subgen- ceras)–Longaeviceras. This phylogenetic lineage gave era, whereas in arctocephalitin species occurred in the rise to three iterative blind branches of cadoceratins same part of the adaptive space. with an oxyconic shell and a “short body chamber”:

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2.6 (a) R2 = 0.9569 2.4 Non-specialized 2.2 R2 = 0.9081

2.0

1.8 Low-specialized

1.6

1.4 High-specialized Species 1.2 Genera, subgenera

1.0 0 20 40 60 80 100 120 140 160 180 200 220 240 260 280 (V) variation range of the body chamber angular length, deg (b) (c) Arcticoceras C. (Paracadoceras) bj-bth 2.5 C. (Catacadoceras) Cadochamoussetia cll1 2.4 Chamoussetia Funiferites cll2–3-cl3 2.3 C. (Cadoceras) and C. (Rondiceras) 2.2 2.1 Non-specialized ) variation rate of the body chamber length of the rate body chamber ) variation t 2.0 (V 1.9 1.8 Low-specialized 1.7 1.6 1.5 1.4 High-specialized 1.3 1.2 1.1

1.0 Stenobiontic Eurybiontic 0.9 ) ) ) allae calyx . frearsi F elatmae sokolovi infimum .) sublaeve variabile geerzense barnstoni F. patruus F. catostoma P .) tscheffkini .) Funiferites .) multiforme A. ischmae .) F. funiferus F. Cadoceras .) anabarense .) P .( C Eckhardites .) milaschevici Arcticoceras ( .) C C .( Cad. surensis Cad. C .( .) ex gr. gr. .) ex .) .( C Chamoussetia Ch. buckmani .) Cat nordenskjoeldi .( C Arctocephalites Cat C C P C. Catacadoceras Paracadoceras .( C quenstedtiforme Cat R Cranocephalites .( Cad. subpatruus Cad. C .) ex gr. gr. .) ex ( ( .( .) .( .( C .( Ch. hyperbolicum C .) . ( Cad. tscherischevi Cad. C C C Cadochamousettia .) ex gr. gr. .) ex A. cranocephaloide C P C. C. C Cat Cat P .( .( .( .( C C C C

Fig. 12. Distribution of species and supraspecific taxa of cardioceratids for the BCL variation rate: (a) correlation between the BCL variation rate and range; (b, c) ranked distribution of the BCL variation rate in species (b) and supraspecific taxa (c) and their classification according to the specialization level. See explanations in the text.

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Eckhardites, Chamoussetia, and Platychamoussetia. A group of species from the Upper Bathonian of The genus Paracadoceras, which also had a short body the Middle Volga Region (Nizhny Novgorod Region, chamber, represents a blind branch, which in Mitta’s Mordovia), which includes C. (Cat.) infimum, opinion ceased to exist in the Late Bathonian. C. (Cat.) keuppi, C. (Cat.) nageli, C. (Cat.) efimovi is distinct among Catacadoceras species. In general, they The BCL distribution of most species belonging to are characterized by a brevidomic body chamber and the above-mentioned genera and subgenera allows the only some specimens belong to the mesodomic size diagnoses of some taxa to be refined, especially those class. Statistically, this separates these specimens from with debatable assignment. Such taxa include a group the Arctic specimens of Catacadoceras (Fig. 7), but it of cadoceratins that retained ribbing on the last body is possible that the Central Russian group may contain chamber up to the terminal aperture, similar to Cadoc- specimens with a longer BCL. Nevertheless, the cur- eras barnstoni (Meek.) (Tables 2, 4). These species are rently existing sample of specimens with a complete here assigned to the subgenus Catacadoceras Bodyl- body chamber suggests that a short body chamber is evsky, 1960 (type species Ammonites barnstoni Meek, not accidental in this group and reflects real geograph- 1859). Meledina (1977, 1999) understands this species ical differences, which are not only restricted to BCL. in approximately the same way. Mitta (2005, 2016) This is supported by the fact that most specimens from accepted a different view, and interpreted this ammo- Central Russia are small, sometime dwarfish in size, nite as a blind branch of arctocephalitins within the whereas the Arctic specimens on average reach a larger genus Paracadoceras Crickmay, 1930 (type species final diameter. This is clearly shown by a comparison Cadoceras harveyi Crickmay, 1930). In Mitta’s inter- by adult specimen (with a preserved terminal aper- pretation the genus Paracadoceras includes some spe- tures) of C. (Cat.) infimum and C. (Cat.) barnstoni, cies of Catacadoceras Bodylevsky, 1960, emend Mele- with a very similar morphotype, but differing in size dina, 1977 and Paracadoceras Crickmay, 1930, (Pl. 3, figs. 1–3). The morphological similarity emend. Imlay, 1953, while the characteristic paraca- between these is quite high, and therefore in the first doceratin species C. elatmae (along with other species publication illustrating these specimens from the Pro- of the same phylogenetic lineage) he assigned not only sek section, they were assigned to C. (Cat.) barnstoni to a different genus, but also a different subfamily (Gulyaev and Kiselev, 1999, pl. 2, fig. 6). It is possible (Cadoceratinae). This separation of closely related that all Central Russian species or at least some of species between the different subfamilies is largely them based on limited material are geographic varia- based in Mitta’s view, on differences in the body tions, of C. (Cat.) barnstoni, as was suggested by Guly- chamber length. BCL is considered by Mitta (2016, aev (2009). Hence, all statistically mean differences in p. 42) as a very essential taxonomic character: the the terminal size and in BCL in the Arctic and Central genus Paracadoceras, characterized by a “relatively Russian specimens should be considered as manifesta- smaller shell and body chamber, a higher whorl cross- tions of polytypical variability. section, usually finer ornamentation, often also devel- The problem of the taxonomic position of Cataca- oped on the relatively short body chamber,” i.e., “0.5– doceras from Central Russia can be solved after exam- 0.6 whorls” (Mitta, 2005) or 180°–216°. This defini- ination of supplementary material. However, it should tion seems very strange, since this author in an earlier be accepted, that the similarity or disparity in the work (Mitta, 2005) noted that the BCL of the type length of the body chamber should not affect the species of Paracadoceras is 7/8 of the whorl, i.e., choice of a preferred taxonomic model. The compari- around 315°. son of the distributions of this character in Catacadoc- eras and Paracadoceras clearly demonstrate (Fig. 6) Consider variability of BCL in various representa- that both subgenera have the same range of values irre- tives of Cadoceras (Catacadoceras) (Table 4). Most spective of shell diameter. In general, the two genera specimens of both Catacadoceras and Paracadoceras in are not distinguished by BCL, and this pattern will not the sample, have a body chamber length in the mesod- be affected by any subjective reshuffling of taxa of omic size class. Within this size class, the BCL varies early cardioceratids. widely, both within the subgenus and at the species level. The longest body chambers are characteristic of the Arctic species C. (Cat.) nordenskjoeldi in East CONCLUSIONS Greenland, and C. (Cat.) catostoma in South Alaska. The body chamber length in Jurassic ammonites is In other Arctic species C. (Cat.) barnstoni and C. (Cat.) strongly variable within species and genera, which sig- variabile the mean values of BCL are somewhat nificantly limits its diagnostic possibilities. Fixed val- smaller (Table 2), but the samples of these species ues of BCL should not be used for ammonite identifi- contain both specimens with a very short, and quite a cation. Statistically mean values of this character can long body chamber. This shows that the length of the have taxonomic value only for some ammonite spe- body chamber is not a decisive character for assigning cies, and are of little use for identification of genera, members of this group to a subfamily or phylogenetic subgenera, and species. Therefore the conclusions on lineages. relationships between taxa, as well as phylogenetic

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Table 4. Body chamber length of specimens of Cadoceras (Catacadoceras) from various collections. Explanations:: YarGPU—geological museum of YarGPU; GMC—Geological Museum of Copenhagen. Nomenclatural types: HT—holo- type; PT—paratype; TT—topotype Species of Cadoceras Nomenclatural types Locality D L° (Catacadoceras) C. (Cat.) barnstoni (Meek) YarGPU: ZM-1 Franz Josef Land 130 225 C. (Cat.) barnstoni (Meek) Meledina, 1999, pl. 1, fig. 2 Kotelnyi Island 95 268 C. (Cat.) barnstoni (Meek) TT: Poulton, 1987, pl. 25, fig. 1 Yukon 115 286 C. (Cat.) barnstoni (Meek) GMC: 3267-f 21 East Greenland 95 251 C. (Cat.)barnstoni (Meek) YarGPU: LRJ4/1 lower reaches of the Lena River 132 300 C. (Cat.)barnstoni (Meek) YarGPU: L267 lower reaches of the Lena River 112 252 C. (Cat.) subcatostoma Voronetz HT: Voronetz, 1962, pl. 25, fig. 1 lower reaches of the Lena River 100 270 C. (Cat.) perrarum Voronetz TT: Meledina et al., 1991, pl. 9, lower reaches of the Lena River 140 230 fig. 1 C. (Cat.) aff. perrarum Voronetz Mitta, 2011, text-fig. 4 Northern Caucasus 94 270 C. (Cat.) catostoma Pomp. sensu TT: Imlay, 1953, pl. 34, fig. 12 Southern Alaska 105 285 Imlay C. (Cat.) catostoma Pomp. sensu TT: Imlay, 1953, pl. 34, fig. 1 Southern Alaska 88.1 281 Imlay C. (Cat.) nordenskjoeldi Callomon HT: Callomon, 1985, pl. 1, fig. 4 East Greenland 125 310 C. (Cat.) nordenskjoeldi Callomon PT: Callomon, 1985, pl. 4, fig. 1 East Greenland 99,8 272 C. (Cat.) nordenskjoeldi Callomon PT: Callomon, 1985, pl. 4, fig. 3 East Greenland 129 263 C. (Cat.) nordenskjoeldi Call. var. α TT: GMC: 3565-f29 East Greenland 84,5 294 C. (Cat.) variabile Spath PT: Spath, 1932, pl. 18, fig. 1 East Greenland 140 240 C. (Cat.) variabile Spath GMC: 4444-f 20 East Greenland 110 240 C. (Cat.) variabile Spath GMC: 3116-f 20 East Greenland 107 238 C. (Cat.) variabile Spath var. β GMC: 3267-f 21 East Greenland 111 287 C. (Cat.) infimum PT: Kiselev and Rogov, 2007, Central Russia 75 222 Gulyaev & Kiselev pl. 2, fig. 2. C. (Cat.) keuppi (Mitta) PT: Mitta, 2005, pl.5, f. 3 Central Russia 94 170 C. (Cat.) keuppi (Mitta) PT: Mitta, 2005, pl.8, fig. 3 Central Russia 82 173 C. (Cat.) keuppi (Mitta) HT: Mitta, 2005, pl. 4, fig. 2 Central Russia 106 190 C. (Cat.) nageli (Mitta) HT: Mitta, 2005, pl. 4, fig. 1 Central Russia 107 163 C. (Cat.) nageli (Mitta) PT: Mitta, 2005, pl. 5, fig. 2 Central Russia 117 200 C. (Cat.) efimovi (Mitta) HT: Mitta, 2005, pl. 6, fig. 1 Central Russia 105 180 reconstructions and macrotaxonomic models based terminal stage are weakly coherent or incoherent with on the similarities and differences in BCL, can be a the variability of other morphological characters of the source of major errors. shell. In some cases the variability of the body cham- A general trend of BCL changes in the morphogen- ber length is determined by morphogenetic rates, esis of species is more suitable for taxonomic identifi- hence BCL values are different in bradymorphic and cations. It is more prominent in species in which mid- tachymorphic shells. It is quite likely that this charac- dle and later whorls are very different. This character ter does not have much influence on the ammonite varies within genera, hence does not have taxonomic shell hydrodynamics or hydrostatics. significance for this taxonomic rank. The body chamber length only slightly correlates with the morphological parameters of an ammonite ACKNOWLEDGMENTS shell, such as the shape of the whorl cross-section or the whorl shape. Variations in BCL within species at The study was supported by the Russian Founda- different morphogenetic stages and especially at the tion for Basic Research, project 18-05-01070.

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