ISSN 00329452, Journal of Ichthyology, 2013, Vol. 53, No. 9, pp. 687–701. © Pleiades Publishing, Ltd., 2013. Original Russian Text © E.M. Baykina, 2013, published in Voprosy Ikhtiologii, 2013, Vol. 53, No. 6, pp. 671–686.

Diagnostic Importance of Visceral Skull Bones of Recent and Fossil (Pisces, ) E. M. Baykina Moscow State University, Moscow, 119991 Russia email: [email protected] Received November 15, 2012

Abstract—An analysis of visceral skull bones morphology of six recent genera (, , , Sardina, Sardinops, and Sardinella) and three fossil species (Illusionella tsurevica, I. pshekhensis, and Clupea doljeana) of Clupeinae was carried out. Description of bones of maxillary and opercular regions was done for examined taxa subject to generic and infra and interspecific variability. Due to ascertained features of vis cerocranium morphology of Illusionella species, we can distinguish them from all of the recent European clu peins. Also there is a number of generic features in this article which give us a possibility to distinguish either recent or fossil forms, even in case of separate paleoichhthyological material. DOI: 10.1134/S0032945213050019 Keywords: Pisces, Clupeinae, Illusionella, Clupea doljeana, visceral skull, generic features, Europe

From Paleocene–Neogene deposits of Eastern cise drawings. Also rather valuable is the work of Phil Paratethys, a multitude of representatives of the sub lips (1942) dedicated to the osteology of one species of family Clupeinae are known. Most of them were dis the genus Sardinops—S. caerulea. However, typical of covered and described in the 19th–early 20th centu most descriptions is a situation when, in the diagnosis ries and are stored in museum funds of Europe under of this or another taxon, characters of different generic names Clupea and . In collections formed ranks—from subfamily to specific—appear. In addi from deposits of Ciscaucasia, there are also genera tion, the emphasis is on the structure of neurocranium Sardinella and Clupeonella rich in species composition of Clupeidae, while this information can be used with (Danil’chenko, 1980). Early researchers (Heckel, great limitations with respect to fossils. 1850; Kner, 1863; GorjanovicKramberger, 1884) The study performed demonstrated that visceral repeatedly noted that fossil Clupeidae are a very prob skull elements, namely big bones of the jaw apparatus lematic group since their diagnosis even up to species and opercular region clearly noticeable and recog is strongly hindered or impossible altogether. Similar nized on fossil material, even if it is separated, are far views are determined by the imperfection of the sys more informative for the systematic differentiation. tem of Clupeidae at the time and by specific features of On the basis of recent and fossil taxa, an attempt was proper fossil material. Its significance is affected by a made to order diagnostic characters of generic and multitude of facts: conditions of burial, the extent of specific ranks using the comparativeanatomical preservation and deformation, perspective of imprint method and the method of statistical analysis of cranio in a rock, etc. Thus, the primary assignment of Euro logical indices, as was, for instance, done in the paper pean fossil Clupeidae to the genera Clupea or Alosa of Vasil’eva (1996) for species of the genus Alosa (sub meant nothing but that this or that form should be family ). The unified system of characters will considered a . Many generic definitions of Clu permit comparison of fossil genera and species with peidae in collections of the 19th–early 20th centuries recent ones, as well as with each other, and obtainment are, as a rule, erroneous and should be revised. This of more precise definitions. This in turn will provide a can be aided by revealing diagnostic characters, pri possibility for a more efficient use of paleoichthyolog marily of the whole generic rank, used for both recent ical material, including fragmentary material, for pur and fossil Clupeinae. Craniological material can form poses of biostratigraphy. the basis for such work.

The skull osteology of recent representatives of MATERIAL AND METHODS Clupeinae is known due to works of Matthews (1887), Smitt (1895), Ridewood (1904), Regan (1917), Phil Skulls of recent and fossil representatives of the lips (1942), Svetovidov (1952), Whitehead (1973, subfamily Clupeinae served as material for the study. 1985), and Grande (1985). Of special note is the work The study was made of 20 specimens of Clupeonella of Ridewood (1904) provided with anatomically pre cultriventris cultriventris, Sprattus sprattus balticus,

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Clupea harengus (15 specimens of C. harengus haren addition, tilt angle (=deviation angle) of zygapophysis gus and 5 specimens of C. harengus membras), and (Amx)—angle between the axis of proper zygapophy Sardina pilchardus ; ten specimens of Sardi sis and the axis of the longitudinal bony rib of maxil nops melanostictus (after Whitehead et al., 1985); and lare—was determined. one specimen of Sardinella aurita (fixed in alcohol Supramaxillare posterior. For this sample from the collection 9318 of the sector of ich bone, three measurements were made and values of thyology of the Zoological Museum, Moscow State two indices were calculated: Lsmx—length of bone University). The fossil material includes: nine speci together with process; Hsmx—bone depth along its mens of Illusionella tsurevica Baykina (PIN dorsoventral axis; lsmx—length of process from the no. 5073—Konkian stage, northern vicinity of the vil anterior end of the bone to the point of bend of the sur lage of Tsurevskii, Pshekha River, Krasnodar krai), six face on the ventral side of the bone (Fig. 1b); Smx1— specimens of I. pschekhensis Baykina (PIN index of the length of process (ratio of the length of no. 5422—Sarmatian stage, 0.5 km northward the process of supramaxillare to Lsmx); Smx2—index of northern marginal area of the village of Tsurevskii, the bone body depth (ratio of the body depth and Pshekha River, Krasnodar krai), and six specimens of Lsmx). Clupea doljeana Kramberger (collection of D. Kram berger no. 27 “Sarmatian Fishes of Croatia and S u b o p e r c u l u m. Bone proportion was assessed Slavonia” from the Croatian Museum of Natural His from three measurements and two indices: Lsop— tory in the city of Zagreb—Sarmatian stage, localities maximum bone length along the craniocaudal axis; Dolye, Podsused, and Vranche, Croatia). Skulls of Hsop—maximum bone depth along the dorsoventral only adult fish were considered. axis; lsop—length of process along its axis from the dorsoventral end up to the point of bend at connection Recent material was processed by maceration of with the bone body on the posterior surface of subo salted heads in hot water, and fossil material was sub perculum (Fig. 1c); Sop1—index of the length of pro jected to mechanical preparation. In addition, for sev cess (ratio of the length of process and the bone eral samples of the genus Illusionella, the method of length); Sop2—index of the bone body depth (ratio of transfer of skeletal remains to epoxy resin was used to the bone body depth and its length). elucidate the details of skull structure. I n t e r o p e r c u l u m. For this bone, three mea For analysis, nine bones of visceral skull were cho surements were made and two indices were deter sen: maxillare, second supramaxillare, suboperculum, mined: Liop—bone length; Hiop—bone depth at its interoperculum, praeoperculum, operculum, last ray anterior end; H’iop—bone depth at posterior end of branchiostegal membrane, anguloarticulare, and (Fig. 1d); Iop —anterior index (ratio of interopercu dentale. These bones that are usually distinguishable 1 lum depth at anterior end to bone length); Iop2—pos on the skull of fossil forms also occur in an isolated terior index (ratio of interoperculum depth at poste form. In this case, taxon diagnosis becomes most dif rior end to bone length). ficult for the researcher. P r a e o p e r c u l u m. To assess habitus of this We provide methods of measuring bones and bone, six measurements were made because of its description of the system of indices accepted in the complicated form: Lpop—bone length from the ante given paper below. rior end of the bone to extreme point at posterior mar M a x i l l a r e. Bone sizes and proportions were gin along the axis via longitudinal crest of the horizon assessed according to three measurements and two tal branch; Hpop—bone depth from the dorsal end of indices: Lmx—bone length along the longitudinal axis the bone to the extreme point at ventral margin along without zygapophysis; Hmx—maximum bone depth the axis through the longitudinal crest of the vertical along its dorsoventral axis; lmx—length of zygapophysis branch; L’pop—length of horizontal branch from the from the extreme articular head until the point it interacts anterior end of the bone to the point of intersection with the longitudinal axis of maxillare (Fig. 1a); Mx1— with the longitudinal crest of the vertical branch; index of elongation of zygapophysis (ratio of zygapo H’pop—depth of vertical branch from the dorsal end physis length and the bone length); Mx2—index of of the bone to the point of intersection with the longi maxillare habitus (ratio of depth and bone length). In tudinal crest of the horizontal branch; lpop—length of

Fig. 1. Schemes of main measurements of bones of visceral skull of representatives of Clupeinae: (a) maxillare (Lmx—length along the longitudinal axis without zygapophysis; Hmx—maximum depth; lmx—length of zygapophysis; Amx—tilt angle of zyg apophysis), (b) supramaxillare posterior (Lsmx—length together with the process; Hsmx—bone depth; lsmx—process length), (c) suboperculum (Lsop—maximum bone length; Hsop—maximum bone depth; lsop—process length), (d) interoperculum (Liop—length; Hiop, H’iop—bone depth at anterior and posterior ends, respectively), (e) praeoperculum (L’pop, hpop—length and depth of horizontal branch; lpop, H’pop—length and depth of vertical branch; Apop—angle of convergence of bone branches), (f) operculum (Lop—bone length; Hop—total depth; hop—depth from extreme point of the bone at ventral margin to zygapophysis), (g) radius branchiostegi posterior (Lbr—length; Hbr—bone depth), (h) anguloarticulare (Laa—total length together with zygapophysis; Haa—depth; laa—length of zygapophysis), (i) dentale (Ld—total length; Hd—maximum depth; Ad—angle between bone axes).

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(а) (b) lmx

Hsmx A lmx Hmx mx Lmx Lsmx Lsmx Lmx lsmx lsmx Hmx Hsmx H’iop op (c) ls (d) Hsop Hiop Lsop lsop Liop Lsop Liop

Hsop H’iop Hiop p Hop Hpo op (e) H’p (f)

hop Lpop

Ap Lop op p lpo Lpop hpop L’ipop L’pop Lop

H’pop p Hpo Hop hop Hbr Haa

Lbr (h) (g)

Laa Lbr Laa laa laa Hbr Haa

Hd (i)

Ld Ad Ld

Hd

JOURNAL OF ICHTHYOLOGY Vol. 53 No. 9 2013 690 BAYKINA vertical branch from the point of intersection of the RESULTS bone crests to the extreme point at its posterior mar The values of indices of visceral skull bones in the gin; hpop—depth of horizontal branch from the point considered taxa of Clupeinae are provided in the table. of intersection of bone crests to the extreme point at its For this bone, no considerable diversity ventral margin. Five indices were used: Pop —ratio of Maxillare. 1 of the types of structure was revealed. During descrip the length of horizontal branch and the total bone tion of maxillare, one should take into account details length; Pop2—ratio of the length of vertical branch of morphology, such as general habitus, pattern of ven and the total bone length; Pop3—ratio of the length of tral margin, form of posterior end, presence or vertical branch and the total bone depth; Pop4—ratio absence of dentition, the angle of deviation of zyg of the depth of horizontal branch and the total bone apophysis, and Mx1 and Mx2 indices. In addition, an depth; Pop5—ratio of the depth of horizontal branch important characteristic is the level reached by the and the length of vertical branch. The internal angle of posterior end of maxillare with respect to the orbit. convergence of branches of praeoperculum (Apop) was In most representatives of Clupeinae, maxillare to also determined (Fig. 1e). one or another degree is saberlike (Fig. 2). Among the O p e r c u l u m. Bone proportions were assessed forms studied, a noticeable exception is the genus according to three measurements and two indices: Sprattus, which is characterized by a subrectangular lop—total bone length; Hop—total bone depth; outline of this bone (Fig. 2b). Habitus of maxillare hop—bone depth from the extreme point of the bone directly depends on the degree of convexity of the ven at ventral margin to articular head of operculum along tral margin of the bone. Convexity is common for all dorsoventral axis (Fig. 1f); Op —ratio of the total studied genera except for Sprattus with an almost 1 straight ventral margin. Convexity of the ventral mar length of the bone and its total depth; Op —ratio of 2 gin is most pronounced in fossil forms—representa the depth of operculum along anterior margin ( ) hop tives of the genus Illusionella and in Clupea doljeana. and its total depth (Hop). Generally, in representatives of Clupeinae, the ven Radius branchiostegi (posterior). In tral margin of maxillare is to one or another degree this bone, a high variability of the posterior margin is denticulated with small denticles, and this is a plesio observed; therefore, we made two measurements and morphic character (Svetovidov, 1952). For instance, in calculated one index: Lbr—bone length from the the genera Sprattus and Clupea, almost ¾ of the margin anterior end of the ray to the extreme point at posterior is denticulated; in Sardina, Sardinops, and Sardinella, margin; Hbr—bone depth at posterior margin; Br— dentition is concentrated mainly on the caudoventral ratio of Hbr and Lbr (Fig. 1g). surface of the bone; and in Sardinella, it is least devel oped (Fig. 2f). A smooth ventral margin is typical of Anguloarticulare—three measurements representatives of the genus Clupeonella and all fossil and two indices: Laa—total length together with zyg forms considered in the given paper. It is of interest apothysis along the craniocaudal axis of the bone; that, nevertheless, a small site of dentition was found Haa—bone depth between extreme points along the in the middle part of the ventral margin of maxillare in dorsoventral axis; laa—length of zygapophysis (Fig. 1h); 1 of 20 specimens of Clupeonella (Fig. 3a). Aa1—ratio of bone depth and its length; Aa2—ratio of The angle of deviation of zygapophysis (Amx) the length of zygapophysis and the length of anguloar turned out to be a variable magnitude even within one ticulare. species, but, on the whole, it does not exceed 138° in the studied representatives of Clupeinae. For instance, D e n t a l e. Bone habitus was assessed on the basis for the genus Clupeonella, the range of variation of of two measurements and one index: Ld—total bone Amx comprises 115°–135°; for Sprattus—126°–130°; length from the extreme anterior point to the extreme for Clupea—129°–138°; for Sardina—126°–128°; posterior point; Hd—maximum bone depth along its for Sardinops—136°–138°; for Sardinella—125°; for dorsoventral axis; D—ratio of the depth of dentale and Illusionella—124°–130°; and for C. doljeana— its length. In addition, the angle (Ad) between the 127°–135°. bone axis parallel to the anterior and posterior margins The posterior end of maxillare can be both sharp of the bone was measured (Fig. 1i). ened a little (the genera Clupea, Sardina, Sardinops, According to 19 craniological indices expressed in and Sardinella as well as Illuionella pshekhensis and percent of length (or depth) of bones, for recent taxa, C. doljeana) and rounded (the genera Clupeonella and standard statistical analysis of samples was performed Sprattus as well as Illusionella tsurevica) (Fig. 2). As for (Vasil’eva, 1996): M ± m—average value and relative its location with respect to orbit, in almost all dis cussed genera, the posterior end of maxillare is situ deviation (m = σ/ n, where σ is rootmeansquare ated between verticals passing through the anterior deviation and n is sample amount). Because of the margin of the orbit and through its middle or at the small samples of fossil forms, only average values of vertical through the anterior margin of the orbit. An indices were calculated for them. exception is made by the genus Clupea whose repre

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Indices of some bones of visceral skull of studied taxa of the subfamily Clupeinae, % of the bone length or depth Taxa (sample size, ind.) recent fossil Indices Clupeonella Sprattus Clupea Sardina Sardinops Sardinella Illusionella Illusionella Clupea cultriventris sprattus harengus pilchardus melanostictus aurita tsurevica pshekhensis doljeana (20) (20) (20) (20) (10) (1) (9) (6) (6) 53.5± 0.95 58.7± 1.06 40.2± 1.10 60.4± 0.73 42.4± 0.73 66.0 73.7 75.3 Mx 41 1 45–60 51–70 34–50 55–66 40–46 54–77 73–78 58–86 31.9± 0.48 36.9± 0.57 26.0± 0.29 30.9± 0.31 27.7± 0.40 44.6 46.3 46.0 Mx 40 2 29–36 34–42 24–28 29–34 26–30 40–50 42–50 43–53 39.9± 0.79 40.7± 0.48 45.0± 0.63 48.3± 0.54 47.5± 0.62 57.0 42.5 51.0 Smx 52 1 34–46 37–45 39–51 44–52 45–50 40–74 40–45 51 40.7± 0.58 33.4± 0.45 37.5± 0.71 40.2± 0.55 41.0± 0.67 49.0 48.0 48.0 Smx 48 2 35–45 28–36 31–43 38–47 38–44 45–51 45–51 45–51 9.9± 0.37 9.3± 0.29 15.7± 0.59 14.0± 0.29 39.9± 0.67 25.0 32.8 28.5 Sop 41 1 7–13 7–11 10–22 11–16 37–43 20–29 26–38 23–34 42.1± 0.59 35.4± 0.57 49.1± 2.13 47.9± 0.73 57.0± 1.06 54.0 43.0 42.5 Sop 66 2 38–48 31–40 34–62 42–53 52–62 38–70 39–53 40–45 17.3± 0.39 20.0± 0.27 25.0± 0.29 22.4± 0.37 26.5± 0.50 22.5 Iop 22 ? ? 1 14–20 18–22 23–27 19–25 25–30 20–25 36.8± 0.57 33.3± 0.31 43.4± 0.82 38.8± 0.31 51.1± 0.89 36.0 Iop 42 ? ? 2 33–42 30–35 37–49 36–41 48–55 35–37 61.0± 0.63 57.1± 0.47 47.3± 0.64 48.4± 0.44 43.6± 1.67 57.3 57.3 57.4 Pop 49 1 56–66 53–61 43–52 45–52 40–58 52–62 48–64 55–60 79.3± 0.50 80.7± 0.4 73.8± 0.61 77.9± 0.29 78.1± 0.35 76.2 74.5 74.6 Pop 79 2 76–83 79–85 68–79 76–80 77–80 71–82 67–80 70–80 32.5± 0.79 35.7± 0.52 43.0± 0.44 44.1± 0.42 54.6± 6.09 40.0 40.5 39.8 Pop 43 3 26–37 32–42 40–47 41–48 37–96 35–47 37–46 35–45 20.8± 0.56 19.3± 0.31 25.8± 0.70 21.8± 0.35 22.2± 0.47 23.8 25.2 23.8 Pop 20 4 17–25 19–22 20–32 19–24 20–25 18–29 18–33 20–30 65.0± 1.12 56.9± 1.73 70.7± 2.14 56.9± 1.09 53.6± 1.33 50.5 59.0 51.8 Pop 47 5 57–75 40–68 62–95 49–67 46–59 42–62 52–66 47–57 53.6± 0.78 61.6± 0.51 53.1± 0.69 52.3± 0.42 59.5± 0.86 58.0 50.8 54.5 Op 54 1 49–59 58–66 50–58 50–55 56–64 56–59 43–61 50–59 63.7± 0.81 62.9± 0.53 66.6± 0.57 57.8± 0.26 66.8± 0.61 79.0 71.2 74.5 Op 62 2 60–70 58–67 62–70 55–59 64–69 73–84 56–83 70–80 63.0± 2.03 44.6± 0.65 55.2± 0.75 45.6± 0.37 51.6± 0.87 41.3 59.3 50.4 Br 50 48–83 39–52 50–60 42–49 48–57 26–59 46–66 40–60 54.8± 0.68 59.7± 0.62 51.3± 0.57 52.8± 0.41 46.4± 0.68 60.0 75.3 64.4 Aa 54 1 50–60 55–64 48–56 50–56 43–50 34–90 60–85 45–80 12.7± 0.27 13.3± 0.17 11.3± 0.42 11.1± 0.22 13.2± 0.29 13.3 16.0 14.0 Aa2 8 11–14 12–15 9–14 10–13 12–15 11–16 14–17 13–16 ± 51.0± 0.48 49.1± 0.25 44.9± 0.30 46.3± 0.39 61.3 65.5 61.2 D 47.4 0.35 48 44–50 48–54 46–51 43–48 45–49 59–65 59–72 55–65 Mx1—index of zygapophysis of maxillare; Mx2—index of habitus of maxillare; Smx1—index of the length of process of supramaxillare; Smx2—index of body depth of supramaxillare; Iop1—anterior index of interoperculum; Iop2—posterior index of interoperculum; Pop1, Pop2—ratio between the length of horizontal and vertical branches of praeoperculum, respectively, and the total length of the bone; Pop3—ratio between the length of vertical branch of praeoperculum and the total depth of the bone; Pop4—ratio between the depth of horizontal branch of praeoperculum and the total depth of the bone; Pop5—ratio of the depth of horizontal branch and the length of vertical branch of praeoperculum; Op1, Op2—ratio between the length of operculum and its depth along the anterior margin and the total depth of the bone; Br—ratio between the depth of radius branchiostegi posterior and its length; Aa1—ratio between the depth of anguloarticulare and its length; Aa2—ratio between the length of zygapophysis and the length of anguloarticulare; D—ratio between the depth of dentale and its length. Above the line—average value of the index and relative deviation (for fossil species—only average value); below the line—limits of index variation; “?”—structure of interoperculum in the given species is unknown.

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cranial direction caudal direction

(а) (b) (c)

(d) (e) (f)

(g)

(h) (i)

Fig. 2. Shape of maxillare and supramaxillare posterior in various taxa of Clupeinae: (a) Clupeonella cultriventris, (b) Sprattus sprattus, (c) Clupea harengus, (d) Sardina pilchardus, (e) Sardinops melanostictus, (f) Sardinella aurita, (g) Illusionella tsurevica, (h) I. pshekhensis, (i) Clupea doljeana; (↑↑) distribution of dentition on the ventral margin of the bone; (  ) reconstructed sites of the bone. Here and in Figs. 4–7, homonymous bones are reduced to a unique scale.

sentatives have very long maxillare extending beyond of lines of dorsal and ventral margins, and Smx1 and the vertical through midorbit but not reaching the ver Smx2 indices, are most important. tical passing through its posterior margin. First of all, differences concern the general shape The individual variation of maxillare within species of the bone. For instance, genera Clupea, Sardinops, in the subfamily Clupeinae is low. The line of the pos and Sardinella are characterized by a subtriangular terior margin of the bone and the anterior boundary of shape of supramaxillare II, and this bone has more the body of maxillare (the prominence can be obtuse likely the shape of an incorrect rhomb in representa or strongly pronounced) are mainly subjected to vari tives of genera Clupeonella, Sprattus, Sardina, and ations. In Fig. 3a, the individual variation of this bone Illusionella as well as in C. doljeana (Fig. 2). in Clupeonella cultrivensis is shown as an example. Bone habitus is determined by the pattern of lines In general, typical for the two species of the genus of dorsal and ventral margins. In all the studied repre Illusionella and C. doljeana is maxillare with a smooth sentatives of Clupeinae, the dorsal and ventral margins ventral margin, greater depth, and longer zygapophy are to one or another degree convex, the ventral mar sis compared to all six studied recent genera. gin being bent more strongly. This regularity is partic Supramaxillare II (posterior). External differences ularly pronounced in genera Clupea, Sardinops, and in supramaxillare II in the considered are Sardinella, in which the dorsal margin of the bone is far variations of one general plan of the structure of this more gently sloping compared to the ventral (Figs. 2c, bone. Its parameters, such as general habitus, pattern 2e, 2f). In Clupeonella, Sprattus, I. pshekhensis, and

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* *

(b) (а)

* * (d)

(c) *

(e)

Fig. 3. Individual variation of bones of visceral skull of various taxa of Clupeinae: (a) variants of shape of maxillare in Clupeonella cultriventris ((→)—presence of dentition), (b) variants of shape of suboperculum in Clupea harengus, (c) variants of shape of sub operculum in Sardinops melanostictus, (d) variants of line of dorsal margin of interoperculum in Sprattus sprattus, (e) variants of shape of dorsal prominence of interoperculum in S. melanostictus; (*)—typical variants of bone morphotype.

C. doljeana, the arch of the ventral margin is bent only Zygapophysis of suboperculum, as a rule, is long slightly stronger than the arch of the dorsal margin; and well developed and this is evidently a plesiomor one can say that they are developed approximately phic character. It manifests itself in all the considered equally. taxa except for genera Clupeonella (process is devel The posterior end of supramaxillare II is mainly oped comparatively weakly) and Sprattus (process is subjected to individual variation. It can be sharpened very short) (Fig. 4). or rounded and directed upwards, upwards and down In some species, for instance, in Clupea and Sardi wards, or more frequently backwards. These variations nops, suboperculum is subjected to noticeable individ are found in all the considered herrings. ual variation (Figs. 3b, 3c). In all cases, changes con cern lines of ventral and dorsal margins of the bone, The representatives of the genus Illusionella and and also zygapophysis that can be thinner or thicker C. doljeana have a similar type of supramaxillare II, with respect to average values in Clupea. which in turn is almost identical to that in the genus Clupeonella. I. tsurevica has variations of the morpho Interoperculum. Morphotype of the given bone is type of this bone, in which it resembles supramaxillare II characterized by parameters such as general bone of the genus Sardina (Fig. 2). habitus and shape of dorsal prominence of interoper culum as well as Iop1 and Iop2 indices. Suboperculum. For this bone, there is a great vari The plan of structure of interoperculum is unique ety of the types of structure. The determining parame for all Clupeinae—long bone with deep and wide pos ters are general bone habitus and the extent of devel terior end, prominence at dorsal margin of anterior opment of zygapophysis pronounced in Sop1 and Sop2 end, and short process to fix ligaments coming from indices. lower jaw. Within the subfamily, taxa are distinguished Among the studied material, one can separate out according to the degree of bend of interoperculum and suboperculum morphotypes, such as an elongated the shape of the dorsal prominence. Among the genera parallelogram, including irregular shape (genera Clu considered in the paper, three (Clupeonella, Sprattus, peonella, Sardina, and Illusionella and rare specimens and Clupea) as well as C. doljeana have a weakly curved of Sardinops), longdroplike shape (Sprattus, C. dol interopercular bone; in Sardina and Sardinops, intero jeana), subrectangular shape (Sardinella), and subtri perculum is saberlike, and in Sardinella—droplike angular shape (Clupea, Sardinops) (Fig. 4). (Fig. 4). In representatives of the genus Illusionella, we

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caudal direction cranial direction

(а) (b) (c)

(d) (e) (f)

(g) (h) (i)

Fig. 4. Shape of suboperculum and interoperculum in various taxa of Clupeinae: (a) Clupeonella cultriventris, (b) Sprattus sprattus, (c) Clupea harengus, (d) Sardina pilchardus, (e) Sardinops melanostictus, (f) Sardinella aurita, (g) Illusionella tsurevica, (h) I. pshe khensis, (i) Clupea doljeana; ( ) reconstructed sites of the bone.

failed to distinctly determine the shape of this bone. In habitus of the bone is determined by indices Pop1, genera Sprattus and Clupea, interopercular bone has Pop2, Pop3, Pop4, and Pop5. an additional structure—a longitudinal bony crest (Figs. 4b, 4c). For all considered taxa, praeoperculum in which The dorsal prominence can be rounded and vertical branch is higher and considerably wider than directed upwards as in genera Sardina, Sardinops, and the horizontal is typical (Fig. 5). In only some Clupeo Sardinella; subrectangular and directed upwards as in nella, rarely in Sprattus, and regularly in Illusionella Clupeonella; or wedgeshaped and directed anteriorly and C. doljeana, there are specimens in which as in Sprattus, Clupea, and C. doljeana (Fig. 4). How branches of praeoperculum are comparable in length. ever, by itself (without consideration of direction) the shape of prominence is subjected to strong individual As for the angle of convergence of branches of variation, which can be seen in Fig. 3e with reference praeoperculum (Apop), the most typical is the situa to the genus Sardinops. The lines of ventral and dorsal tion when it varies in the range of 105°–116°: Clupeo margins of the bone can also slightly vary (Fig. 3d). nella—107°–111°, Sprattus—110°–112°, Sardina— Praeoperculum. Within the subfamily Clupeinae, 111°–116°, Sardinops—113°–116°; and Sardinella— uniformity of morphotypes is most pronounced in this 105°–110°. The exception is made by genera Clupea bone. During its description, one should pay attention and Illusionella as well as C. doljeana, in which this to the ratio of proportions of vertical and horizontal angle is noticeably bigger (120°–125°), because of branches and the angle of their convergence. General which their preopercles seem visually lower (Fig. 5).

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Thus, the angle between branches of the bone and there are differences. Representatives of the genus reciprocal lengths of branches are subjected to individ Clupeonella have a sabrelike last ray of branchiostegal ual variation. Values of Pop5 index also strongly vary for membrane with a weakly convex ventral margin and an the considered fossil forms, but it is more likely the abruptly bent upwards and backwards dorsal margin. result of the sample insufficiency. On the whole, habi Sprattus is characterized by having a branchiostegal tus of praeoperculum within each considered taxon is ray in the shape of an irregular weakly curved trapeze stable. with a direct ventral and weakly concave dorsal margin Operculum. Morphotype of this bone is subjected curved upwards very gently. In representatives of Clu to noticeable variation at a generic level. A common pea, branchiostegal ray is sabrelike with a weakly con feature for all considered forms is the fact that opercu vex ventral and strongly curved dorsal margins. lum is deep and bears on posterior margin concavity, The second group includes genera Sardina, Sardi more or less pronounced depending on genus (Fig. 5). nops, and Sardinella, in which caudodorsal angle of During diagnostics, one should pay attention to the the last ray of branchiostegal membrane is transformed presence/absence of sculpture on operculum, shape of into a lobe, like a heterocercal fin (Fig. 6). General posteroventral angle of this bone, and Op1 and Op2 bone habitus in these fish is different. Radius bran indices. chiostegi posterior in Sardina is sabrelike, with direct Of the studied taxa, Clupeonella, Sprattus, Illu or very weakly curved ventral margin, steeply curved sionella, and C. doljeana have similar habitus. The dorsal, and a long moderately wide lobe. Representa posterior margin of the bone has a deep notch, and the tives of the genus Sardinops have a sabrelike bran lower half of the bone is visually greater than the upper chiostegal ray with a direct ventral margin, steeply one. The opercles of fossil forms exhibit strong simi curved dorsal one, and a long wide lobe. Sardinella is larity between themselves and with operculum of rep characterized by branchiostegal ray with direct ventral resentatives of the genus Sprattus and, less frequently, and dorsal margins, the posterior third of the dorsal with Clupeonella. Operculum of the genus Clupea is margin steeply bends upwards; posterodorsal end of characterized by a very weakly pronounced (almost the bone is transformed into a narrow, sabrelike, lacking) notch at the posterior margin and a more sharpened lobe. developed lower half with respect to the upper one; in The third group is formed by fossil forms—repre genera Sardina and Sardinella, there is a notch of the sentatives of the genus Illusionella and C. doljeana. posterior margin, but it is gently sloping and pro They are an intermediate variant: the posterodorsal nounced weakly; in Sardina, the lower half of opercu end of their last ray of branchiostegal membrane bears lum is wider than the upper one, while in Sardinella, it a poorly pronounced lobe (Fig. 6). Rays of all three is developed on a parity basis, so that the bone assumes species are similar also to the remaining parameters: a rectangular habitus; operculum of Sardinops is char they are, on the whole, sabrelike, with a straight or acterized by a strong development of the upper half weakly bent ventral margin and an abruptly bent back with respect to the lower one and a noticeable gently wards dorsal margin; posterodorsal angle is thinner sloping notch at the posterior margin (Fig. 5). than posteroventral, bends backwards, and is sharp ened at the end. In almost all considered forms, posteroventral angle of operculum is obtuse or rounded. The excep Habitus of the bone stable. The width of posterior tion is the genus Clupea with a sharpened posteroven lobe (where it is present) and, to an inconsiderable tral angle. Except for genera Sardina and Sardinops, all degree, the line of the posterior margin of the bone can the studied taxa, including fossil ones, have smooth be subjected to individual variation. operculum. Operculum of representatives of the genus Anguloarticulare. Morphotype of the given bone is Sardina bears a sculpture in the shape of six to seven characterized by parameters such as general habitus of radial crests, and there are five such crests on operculum the bone, and shape of anterior margin as well as Aa1 of representatives of the genus Sardinops (Figs. 5d, 5e). and Aa2 indices. An important generic trait is also the level relative to orbit at which the lower jaw articulates Of the considered bones, operculum parallel to with the skull. dentale is least subjected to individual variation. The plan of structure of anguloarticulare is unique Radius branchiostegi posterior. For this element, for all representatives of Clupeinae—this is a subtrian manifestation of very high diversity on a generic level gular bone with a well developed, clearly pronounced is typical. First of all, this is determined by a strong zygapophysis. In almost all considered taxa, including variability of the general bone habitus. According to fossil ones, the lower jaw articulates with the skull the structure of the last ray of gill membrane, the con between verticals passing through the anterior margin sidered taxa can be arbitrarily subdivided into three of the orbit and through its middle or (in some speci groups. mens of Sprattus) at the vertical through the anterior The first group includes genera Clupeonella, margin of the orbit. The exception is made by genera tus, and Clupea that are united by the absence of lobe Sardinops (articulation of the lower jaw at the level of at the posterior margin of the ray of branchiostegal the middle of the orbit) and Clupea (articulation with membrane (Fig. 6). According to other parameters, the skull almost at the level of the posterior margin of

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caudal direction cranial direction

(а) (b) (c)

(d) (e) (f)

(g) (h) (i)

Fig. 5. Shape of praeoperculum and operculum in various taxa of Clupeinae; (a) Clupeonella cultrivensis, (b) Sprattus sprattus, (c) Clupea harengus, (d) Sardina pilchardus, (e) Sardinops melanostictus, (f) Sardinella aurita, (g) Illusionella tsurevica, (h) I. pshekhensis, (i) Clupea doljeana. the orbit). In addition, articularangular bones of In fossil forms, the index of the depth of anguloarticu these genera (if bones are reduced to one scale) look lare varies noticeably. However, this is more likely like visually lower and longer than in the remaining related to the insufficiency of the sample and to the considered Clupeinae. fact that it is not always possible to distinctly deter The pattern of the line of anterior margin is unique for mine the anterior boundary of the bone and, hence, to each species, and its variants are represented in Fig. 7. correctly measure its length. In recent forms, the bone is hardly subject to indi Dentale can be characterized by many parameters, vidual variation. Sometimes, the pattern of the line of the most important of which are: outline of the general anterior margin can vary to a very insignificant degree. profile of the lower jaw, presence or absence of denti

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caudal direction cranial direction

(а) (b) (c)

(d) (e) (f)

(g) (h) (i)

Fig. 6. Shape of the last ray of gill membrane in various taxa of Clupeinae: (a) Clupeonella cultriventris, (b) Sprattus sprattus, (c) Clupea harengus, (d) Sardina pilchardus, (e) Sardinops melanostictus, (f) Sardinella aurita, (g) Illusionella tsurevica, (h) I. pshekhensis, (i) Clupea doljeana. tion, pattern of line of antedorsal margin, angle of Sardinops, and Sardinella, the notch of the antedorsal convergence of axial rays of anterior margin, and pat margin is rounded and well pronounced; fossil forms tern of line of posterior margin as well as the degree of demonstrate an intermediate variant—a well notice prominence of the lower jaw beyond the snout limits. able, extended depression. The pattern of the line of General habitus of the bone is determined by the index the posterior margin is unique for each species, and its of the depth of dentale D. variants are provided in Fig. 7. General profile of the lower jaw (dentale + angu loarticulare) of the studied representatives of Clu The angle of convergence of axial rays of anterior peinae is trapezoid, and there are variations with both margin of dentale (Ad) turned out to be a universal an oblique dorsal margin (Clupeonella, Sprattus, Illu magnitude, and its values in most cases fit in the inter sionella, C. doljeana, and some specimens of Sardina) val 50°–64°: in Clupeonella it is 53°–58°; in Sprat and with an almost straight margin (Clupea, Sardi tus—57°–59°; in Clupea—51°–59°; in Sardina— nops, Sardinella). There are differences also in the 50°–56°; in Sardinops—57°–64°; in Sardinella— shape of the symphysis: in genera Sprattus and Clupea, 50°; in I. tsurevica—54°–60°; in I. pshekhensis— it is deep and short with a clearly pronounced 52°–58°; and in C. doljeana—50°–55°. anteroventral angle; for genera Sardinops and Sar dinella, a noticeably extended anteriad low symphysial Except for representatives of the genus Sardinella, region is typical, and symphysis of representatives of in which dentale is slightly protruded forward, in the Clupeonella, Sardina, Illusionella, and C. doljeana overwhelming majority of the considered forms, the occupies an intermediate position between the men lower jaw noticeably extends beyond the snout limits, tioned two types: it has moderate depth and length, particularly in the genus Clupea. and its anteroventral angle can be rounded. On the whole, the two species of the genus Illu Most of the considered genera have no teeth at the sionella and C. doljeana are characterized by a very anterodorsal end of dentale. The exception is made by deep (deepest in I. pshekhensis) and short dentale with genera Sprattus and Clupea. a shallow extended notch at the anterodorsal margin The anterodorsal margin of dental bone of all stud compared to all six studied recent genera. ied forms bears a notch whose outline can be different (Fig. 7). For instance, for the group of genera includ If one does not take into consideration variations of ing Clupeonella, Sprattus, and Clupea, a poorly pro the angle Ad, dentale, similar to operculum, is hardly nounced, gently sloping notch is typical; in Sardina, subject to individual variation.

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cranial direction caudal direction

(а) (b) (c)

(d) (e) (f)

(g) (h) (i)

Fig. 7. Shape of anguloarticulare and dentale in various taxa of Clupeinae: (a) Clupeonella cultriventris, (b) Sprattus sprattus, (c) Clupea harengus, (d) Sardina pilchardus, (e) Sardinops melanostictus, (f) Sardinella aurita, (g) Illusionella tsurevica, (h) I. pshekhensis, (i) Clupea doljeana; ( ) reconstructed sites of the bone.

DISCUSSION 50%). In the remaining forms, the values of this index Maxillare demonstrates the presence of diagnostic vary in the range 40 to 70%, and the ranges of values characters of various ranks. Generic characters for different taxa frequently overlap. The studied fossil include the presence or absence of dentition and the species have a very long, compared to recent, process level reached by the posterior end of maxillare with of maxillare. The range of values of the index Mx1 for respect to orbit. The ratio of the bone depth and its them is 66–75%. It is noteworthy that fossil species are clearly differentiated according to the length of the length (Mx2) can also be assigned to them. This is a safe and stable character, functioning, however, within process: the shortest process is in I. tsurevica (Mx1 54– the groups of genera. According to the range of values, 77%), I. pshekhensis occupies an intermediate posi tion (73–78%), and the longest process is in Mx of Clupeonella coincides with Sardina (29–36 and 2 (primary values 76–86%). 29–34%, respectively), Sprattus is close to Sardinella C. doljeana (34–42 and 40%), and Clupea is close to Sardinops The angle of deviation of the process of maxillare (24–28 and 26–30%). Thus, in groups Clupea–Cluo (Amx) in the group Clupeonella–Sprattus–Clupea is a peonella–Sprattus and Sprattus–Sardina–Sardinella, variable character unfit for distinguishing species since the depth of maxillare smoothly increases (according values of angles in various forms strongly overlap. In to sequence). The studied fossil forms have a very deep representatives of the group Sardina–Sardinops–Sar , this character is more or less constant within a maxillary bone compared to recent taxa (Mx2 40–50 dinella vs. 25–40%). No noticeable differences between the species. According to this character, Sardina (Amx three fossil species with respect to the given character 126°–128°) is well distinguished from Sardinops are recorded. (136°–138°). In fossil forms, values of Amx vary in a Specific characters in the structure of maxillare wide range (124°–135°), which does not permit dis include: shape of the posterior end, pattern of line of tinguishing individual species. ventral, dorsal, and posterior margins, length of zyga Supramaxillare. In the structure of this bone, only pophysis, and the angle of its deviation from the bone characters of species rank are present. They include: body. The overwhelming majority of these characters the shape of the posterior end of the bone, pattern of to this or another degree are subjected to individual line of dorsal and ventral margins, depth of supramax variation and are not very suitable for diagnostics. illare posterior, and the length of the anterior process For instance, for the index of the length of the pro of this bone. The first character can be individually variable, but the remaining are sufficiently stable. cess of maxillare (Mx1), wide ranges of values are com mon. C. harengus has the shortest process of maxillare The index of the depth of supermaxillare (Smx2) in of the studied recent species (34–43%, seldom up to the considered taxa demonstrates uniformity even at

JOURNAL OF ICHTHYOLOGY Vol. 53 No. 9 2013 DIAGNOSTIC IMPORTANCE OF VISCERAL SKULL BONES 699 an intergeneric level. In all studied recent forms, are typical for Atlantic C. harengus harengus (45– except for the genus Sprattus (28–36%), its values fit 49%). in the range 31–47% and almost completely overlap Praeoperculum. For this bone, it is difficult to each other. Supramaxillare posterior in the studied determine the rank of parameters characterizing it fossil forms on the whole is deeper than in recent since all of them, despite stability, to one or another forms. The range Smx2 45–51% without any species degree are unfit for diagnostics of taxa. Praeoperculum specifications corresponds to its depth. is described by five main indices (Pop1, Pop2, Pop3, The index of the length of the process of supramax Pop4, Pop5) and the angle of convergence of branches illare posterior (Smx1) is also uniform. In all studied (Apop). forms, including fossil forms, its values fit in the range In Clupea, Sardinops, Sardinella, and Sardina, val 35–50%. It is almost identical in Clupeonella and ues of index Pop1 vary in the range 40–55%. In Clupeo Sprattus (34–46 and 37–45%, respectively) and in nella, Sprattus, and fossil forms, the length of horizon Sardina and Sardinops (44–52 and 45–50%). tal branch of praeoperculum is on the whole greater: Suboperculum. In the structure of this bone, com 56–66% in Clupeonella, 53–61% in Sprattus, and 50– pared to all considered ones, most contrast characters 64% in C. doljeana and representatives of the genus are pronounced. On the one hand, almost all signifi Illusionella. Values of the index of the depth of vertical cant parameters, such as the pattern of lines of ventral, branch of praeoperculum (Pop2) in all studied forms dorsal, and interior margins and the depth of suboper are mainly within the interval 70–80% and strongly culum, are subjected to strong individual variation, overlap. It is also impossible to distinguish species which considerably depreciates them. For instance, using it. Values of the index of the length of vertical the index of the depth of the bone (Sop2) well charac branch of praeoperculum (Pop3) for Clupea, Sardi terizes genera Sprattus (mainly 33–39%) and Sardi nops, Sardinella, and Sardina are within the interval nops (mainly 54–60%), but that for Clupea is very vari 40–50%. In Clupeonella and Sprattus, values of Pop3 able (34–62%). Ranges of values of Sop2 of Clupeo overlap (26–37 and 32–42%, respectively). The range nella (38–48%), Sardina (42–53%), and fossil forms of values of Pop3 in the studied fossil forms (35–45%) (38–70%) overlap. occupies an intermediate position and intersects with On the other hand, there is a stable character that ranges of the first group of genera and of the second. can be considered as a generic one—the length of the Species differentiation is lacking. The index of depth process of suboperculum (index Sop1). According to it, of horizontal branch of praeoperculum (Pop4) is also almost all studied forms are well distinguished. In Clu not demonstrative. In all studied recent forms, except peonella and Sprattus, the values of this index fluctuate for Clupea (20–32%), its values are within the interval mainly in the range 8–11%; in Sardina: 13–15%; and 19–24% and strongly overlap. In the three studied fos in Sardinops and Sardinella: 37–43%. The range of sil forms, this index varies in a wide range of values values of Sop1 in Clupea is rather wide: 10–20% (20–30%) and cannot be used for comparison. The (mainly 15–18%). For fossil forms, it comprises 20– ratio of the depth of horizontal branch of praeopercu 38%, without the possibility to use it for subdivision lum and the length of vertical branch (Pop5), besides into species. being not demonstrative, is also a very variable index. Interoperculum. The presence or absence of longi In all studied forms, its values are within a wide inter tudinal crest (as in Clupea and Sprattus) can be val (47–80%) and strongly overlap. The angle of con assigned to the diagnostic character in the structure of vergence of branches of praeoperculum (Apop) is this bone. The species level is characterized by lines of rather stable; however, it cannot serve as a diagnostic ventral and dorsal margins, shape of prominence at the character either. In all studied forms, its values are anterior end and its direction, and bone depth at ante within the interval 105°–125° and strongly overlap. rior and posterior ends. The first two characters fre Operculum is characterized by the presence of quently manifest individual variation. diagnostic characters of various ranks. To generic As for indices of the bone depth (Iop1 and Iop2), characters, one can assign the presence or absence of they are usually not demonstrative. For all studied sculpture, shape of posteroventral angle of the bone, forms (including C. doljeana), except for genera Clu and the degree of development of notch at the poste peonella and Sprattus, the values of Iop1 are in the rior margin. range 20–30%. In the mentioned genera, the depth of Species characters include indices of the length of interoperculum at the anterior end is on the whole operculum (Op1) and its depth along the anterior mar smaller: 14–20% in Clupeonella and 18–22% in Sprat gin (Op2). The first of them is rather variable. In Clupeo tus. The values of index Iop2 for Clupeonella, Sprattus, nella, Clupea, Sardinella, Sardina, and studied fossil Sardina, and C. doljeana are within the interval 30– forms, the values of Op1 are in the interval 50–59%; in 40%. In Clupea, Sardinops, and Sardinella, the depth Sardinops and Sprattus, the values of Op1 are on the of interoperculum at the posterior end is on the whole whole greater, they strongly overlap and together com greater: 37–49, 48–55, and 42%. For Atlantic subspe prise an interval 56–66%. Index Op2 is more stable, cies Clupea harengus membras, smaller values of this though it is also not very suitable for diagnostics. Of index are typical (37–42%), and mainly greater values the whole mass, only the studied fossil forms with a

JOURNAL OF ICHTHYOLOGY Vol. 53 No. 9 2013 700 BAYKINA deep operculum (the range of index values mainly 70– bone body (dentition, sculpture, outgrowths, or 80%) and the genus Sardina with the lowest opercu notches). The position of bone with respect to other lum (55–59%) are distinguished. The remaining five elements and skull regions (orbit, snout, etc.) is recent genera are indistinguishable according to this important. It was found that the length of process of character, and its values vary in the range 60–70%. suboperculum and the body depth of maxillare can be Radius branchiostegi posterior. In the structure of also considered characters of generic rank. All that the last ray of branchiostegal membrane, one can dis concerns habitus of bones and the index of individual tinguish one generic character—the presence or measurements is related to species or sometimes sub absence of lobe at the posterior end of the bone. species characters or is a manifestation of individual The pattern of ventral and dorsal margins compos variation. It is important to consider the pattern of ing general habitus of the bone and width of posterior outline of bones—at similar indices, bones can look lobe as well as ray depth along the posterior margin like quite differently. During diagnostics, species char (index Br) represent characters of species rank. Values acters should be used only in a complex. of Br in all studied recent forms are in the interval 40– As analysis of cranyological data shows that the six 60% and strongly overlap. In the three studied fossil recent genera considered in the paper can be included forms, as in the genus Clupeonella, this index is into two clearly distinguished groups: herring (with strongly variable (the ranges of values 30–60 and 48– genera Clupeonella, Sprattus, and Clupea) and sardina 83%, respectively) and cannot be used for comparison. (with genera Sardina, Sardinops, and Sardinella). Anguloarticulare. The level with respect to orbit at Representatives of Sardina exhibit an unusual similar which the lower jaw articulates with the skull can be ity with representatives of Sardinops and Sprattus considered a generic character in the structure of the exhibit an unusual similarity with Clupea, which was given bone. repeatedly pointed out previously (Philips, 1942; There are several characters of species rank, Svetovidov, 1952; Whitehead et al., 1985). namely: shape of anterior margin of the bone, depth of Compared to recent forms inhabiting seas of anguloarticulare, and the length of zygapophysis. The Europe, the considered fossil forms have a deeper first is most diagnostic. Index Aa1 is rather stable but maxillare with a longer zygapophysis, last ray of bran not demonstrative. One can separate the genus Sardi chiostegal membrane with a weakly developed poste nops with low anguloarticulare (Aa1 43–50%). The rior lobe (intermediate position between the groups of remaining five recent genera are indistiguishable herring and sardine) as well as a shorter and deeper according to this character, its values vary within 48– dentale with a shallow extended notch at the antero 64%. In the three studied fossil forms, this index is dorsal margin. According to cranyological data, repre strongly variable (34–90%). The index of the length of sentatives of the genus Illusionella are much closely the process of anguloarticulare (Aa2) is also little suitable related to the group of herrings than to the group of for diagnostics. In all studied forms, its values are mainly . within the interval 9–15% and strongly overlap. Species C. doljeana needs careful revision. It Dentale is characterized by several stable charac strongly differs from typical representatives of the ters, among which one can separate two generic char genus Clupea in such characters as absence of denti acters—presence or absence of dentition of antero tion on jaw bones, short maxillare hardly extending dorsal end and the degree of prominence of the lower the vertical of the anterior margin of orbit (maxillare of jaw beyond the snout limits. Clupea reaches vertical of the posterior margin of Species characters include pattern of dorsal, orbit), rounded shape of posteroventral margin of anterodorsal, and posterior margins and the index of operculum (in Clupea, it is sharpened), development depth of dentale (D). For recent genera, the range of of a weak lobe on posterior margin of the last ray of values of D is rather narrow and comprises mainly 43– branchiostegal membrane (in Clupea, there is no 49%. It is noteworthy that fossil herrings considered in lobe), presence of seven gill rays (versus eight) and this paper have a very deep lower jaw: values of D vary presence of two elongated rays in anal fin as well as a in the range 55–65%. smaller number of vertebrae (44–46 vs. 52–60). At the The angle of convergence of rays of dentale cannot same time, C. doljeana demonstrates all diagnostic be considered to be a species character because of its characters, both cranyological and postcranial inher static nature. In all studied forms, its values are within ent to fossil genus Illusionella (Baykina, 2012) and the interval 50°–59° and strongly overlap. should be redescribed in its composition.

CONCLUSIONS ACKNOWLEDGMENTS Morphological analysis of some bones of visceral I am grateful to E.K. Sychevskaya (PIN RAS), skull of recent and fossil Clupeinae demonstrated that A.F. Bannikov (PIN RAS), and E.D. Vasil’eva (Zoo the level of generic characters begins mainly from the logical Museum of Moscow State University) for all appearance/disappearance of some structures on the round help in the work; and to S. Yapunzhich (Croat

JOURNAL OF ICHTHYOLOGY Vol. 53 No. 9 2013 DIAGNOSTIC IMPORTANCE OF VISCERAL SKULL BONES 701 ian Museum of Natural History) for the provided fossil Akad. Wiss. Math.Naturwiss. Kl., 1863, vol. 1, pp. 126– material from localities of Croatia. 148. The study was supported by the Russian Founda Matthews, J.D., Structure of the herring and other clu tion for Basic Research (grant no. 130500213). peids, Fifth Rept. Fish. Board. Scotl. Append. F. Sessial Papers. House of Commons, 1887, vol. 21, pp. 274–292. Phillips, J.B., Osteology of the sardine (Sardinops cae REFERENCES rulea), J. Morphol., 1942, vol. 70, no. 3, pp. 463–500. Baykina, E.M., A New clupeid genus (Pisces, Clupei Regan, C.T., A revision of the clupeid fishes of the genera formes, Clupeidae) from the Sarmatian of the eastern Sardinella, , etc., Ann. Mag. Natur. Hist., 1917, Parametethys, Krasnodar Region, Paleontol. J., 2012, no. 3, vol. 19, no. 8, pp. 377–395. pp. 302–312. Ridewood, W.G., On the cranial osteology of the clupeoid Danil’chenko, P.G., Order , in Tr. PIN AN fishes, Proc. Zool. Soc. L., 1904, vol. 2, pp. 448–493. SSSR (Proceedings of the Palentological Institute of the Smitt, F.A., A History of Scandivian Fihes, Vol. 2, Stock USSR), Vol. 178: Fossil Bony Fish of the USSR, Moscow: holm: P.A. Norstedt & Söner, 1895. Nauka, 1980, pp. 7–26. Svetovidov, A.N., The Clupeidae, in Fauna SSSR. Ryby GorjanovicKramberger, D., Die Jungtertiare Fischfauna (Fauna of the USSR: Fish), Moscow: AN SSSR, 1952. Croatiens, in Beiträge zur Paläontologie ÖsterreichUngarns Vasil’eva, E.D., On divergence of shads of genus Alosa from und des Orients, 1884, vol. 2, no. 3, pp. 65–86. the Azov Sea: cranyological findings, J. Ichthyol., 1996, Grande, L., Recent and fossil clupeomorph fishes with vol. 36, no. 2, pp. 139–145. materials for revision of the subgroups of clupeoids, Bull. Whitehead, P.J.P., Nelson, G.J., and Wongratana, T., Clu Amer. Mus. Natur. Hist., 1985, vol. 181, no. 2, pp. 231–372. peoid fishes of the world (suborder Clupeoidei). Pt 1. Chi Heckel, J.J., Beitrage zur Kenntnis der Fossilen Fische rocentridae, Clupeidae and Pristigasteridae, FAO Fish. Österreichs, Denkschr. Kais. Acad. Wiss. Math.Naturwiss. Synop., 1985, vol. 7, pp. 305–579. Kl., 1865, vol. 1, pp. 201–242. Whitehead, P.J.P., The clupeoid fishes of the Guianas, Bull. Kner, R., Ueber einige fossile Fische aus den Kreide und Brit. Mus. Nat. Hist. (Zool.), Suppl. 5, 1973, pp. 1–227. TertiarSchichten von Comen und Podused, Sitz.Ber. Translated by I. Pogosyants

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