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Feeding habits of the Oligocene bristlemouth fish Scopeloides glarisianus (Teleostei: Stomiiformes: Gonostomatidae)
Geobios 45 (2012) 377–386
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Original article
Feeding habits of the Oligocene bristlemouth fish Scopeloides glarisianus (Teleostei: Stomiiformes: Gonostomatidae)§ Toma´sˇ Prˇikryl a,*,b, Arte´m M. Prokofiev c,d, Wiesław Krzemin´ski e a
Institute of Geology, Academy of Sciences of the Czech Republic, v.v.i., Rozvojova´ 269, 16500 Prague 6, Czech Republic Institute of Geology and Palaeontology, Charles University in Prague, Albertov 6, 12843 Prague 2, Czech Republic c A.N. Severtsov’s Institute of Ecology and Evolution, Russian Academy of Science, Leninski Prospekt, 33, 119071 Moscow, Russia d Paleontological Institute, Russian Academy of Science, Profsoyuznaya ul., 123, 117997 Moscow, Russia e Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, ul. S´w. Sebastiana 9, 31049 Krako´w, Poland b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 5 September 2011 Accepted 20 October 2011 Available online 16 July 2012
The dietary habits of the Oligocene fish Scopeloides glarisianus (Agassiz) are presented on the basis of functional morphology, in comparison with their recent relatives (Gonostoma spp.) as well as fossil materials from localities in Poland (Lubenia, Błaz˙ova), Ukraine (Ljubizhnja), the Czech Republic (Loucˇka), and the northern Caucasus in Russia and Abkhazia. Analogous to the recent relatives from the genus Gonostoma, S. glarisianus fed on crustaceans such as ostracods and copepods, the larger specimens preying on small fishes. Fishes remains preserved within the alimentary canal region are usually represented by smaller individuals of the same species; accordingly, the cannibalistic behaviour of the adult S. glarisianus is thereby documented. The remains of the alimentary canal and the peritoneum are identified. ß 2012 Elsevier Masson SAS. All rights reserved.
Keywords: Teleostei Gonostomatidae Functional morphology Feeding habits Cannibalism Palaeoecology Palaeogene
1. Introduction Scopeloides glarisianus was first described by Louis Agassiz (1833–1844), in his famous monograph on fossil fishes, as Osmerus glarisianus from Oligocene deposits in Switzerland. This fish of the family Gonostomatidae (order Stomiiformes) was either mesopelagic (Prokofiev, 2005a) or bathypelagic (Jerzman´ska, 1968), and its ecological demands were probably similar to recent species of the genus Gonostoma. No information has been published on its feeding habits, except for one theoretical note mentioned by Kalabis (1948). The recent deep-water fishes are ecomorphologically well adapted for predatory lives. In particular, these adaptations include large jaws capable of catching larger prey, and are morphological results of evolutionary processes. Such features can also be traced in the fossil representations of various predatory fish species. In recent fishes, the feeding and dietary habits are possible to study in two different ways. There are direct and indirect evidences, which can be used for the reconstruction of their feeding. Direct evidences are presented by the remnants of prey in
§
Corresponding editor: Gilles Escarguel. * Corresponding author. E-mail address: [email protected] (T. Prˇikryl).
0016-6995/$ – see front matter ß 2012 Elsevier Masson SAS. All rights reserved. http://dx.doi.org/10.1016/j.geobios.2011.10.012
the stomach or alimentary canal of the predators; indirect evidences could be from the information provided through comparative anatomy and functional morphology (Wootton, 1998). Indirect methods could also show the feeding modus (Gartner et al., 1997). In recent deep-water fishes it is quite difficult to study the feeding habits, especially from the physiological point of view, due to many methodological limitations; moreover, many predators only feed infrequently, making difficult to decide if the predator is a ‘‘selective’’ or ‘‘generalized’’ feeder (Gartner et al., 1997). On the basis of both types of indices (direct and indirect), the possible dietary habits can also be reconstructed in the fossil record; however, it is clear that only direct evidences specifically show the original food. The predatory feeding habits of fossil fishes were recognized in various stratigraphic positions (Viohl, 1990; Maisey, 1994), but many of them were only noted as interesting palaeoecological facts, without larger ecological and anatomical contexts. Not only ‘‘general’’ feeding behaviours, but also highly specific habits, such as cannibalism, were certainly recognized record in the fossil (Watson, 1927; Pauca˘, 1934; Case, 1982; Maisey, 1994; Prˇikryl and Novosad, 2009). In the fossil record, the feeding habits of ‘‘deep-water fishes’’ are principally deduced on the basis of functional anatomy (e.g., Carnevale, 2002, 2008), although several cases of direct evidence have also been published (one such case is the viper fish Chauliodus eximius (Jordan and
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Gilbert, 1925) from southern California Miocene deposits (Crane, 1966: text-fig. 13)). A general review of the dietary habits in fossil fishes was published by Boucot (1990). In 1948, Kalabis stated that almost all specimens of S. glarisianus studied by him were fossilized with full stomachs. He had interpreted a dark pigmented zone behind the head, which tapers posteriorly, as the stomach. About their feeding habits, he wrote that Scopeloides were predators with distinctly toothed jaws, but did not comment further on the feeding habits of this species. This short note was just one published mention about the possible feeding habits for this taxon. However, true remnants of the alimentary canal cannot be recognized in these specimens. It is our opinion that these structures were misinterpreted by Kalabis, and are herein properly identified. The first direct evidence of the diet of the adult S. glarisianus is preserved in several fossil specimens we have studied and present here. 2. Material and methods Specimen Lit2006/44a was prepared by thin needles under a binocular microscope; the other specimens studied were either left unprepared or had been prepared before this investigation. In order to extricate artefacts from real trophic records, digested specimens can be separated by the following rationale: the prey lies inside the rib cage (i.e., prey is situated between the ribs of both sides of the body); the position of the digested fish, in general, agrees with the orientation of the predator’s digestive tract; the digested specimens are never positioned perpendicular nor under a distinct angle to the longitudinal axis of predator’s digestive tract; the digested specimens never retain natural articulation of the skull, ribs, and intermusculars, nor well-preserved and naturally expanded fins, especially unpaired ones; their vertebral columns are usually distorted (some pieces of column can be separated, or some vertebrae can be close-set to one another, and some of them are spaced away from each other); the skeleton elements of the digested fish never cross the skeleton elements of the predator, viewed from the side; the outer surface of the digested specimens can be corroded by the digestive processes. Institutional abbreviations: AtlantNIRO: Atlantic Research Institute of Fishery and Oceanography; Kaliningrad; Russia; IGP: Institute of Geology and Palaeontology; Faculty of Sciences; Charles University; Prague; Czech Republic; IORAS: Institute of Oceanology; Russian Academy of Sciences; Moscow; Russia; MRV: Museum of Valasˇsko region; Vsetı´n; Czech Republic; NMP: National Museum; Prague; Czech Republic; PAS: Institute of Systematics and Evolution of Animals; Polish Academy of Sciences; Krakow; Poland; PIN: Paleontological Institute; Russian Academy of Sciences; Moscow; Russia. Anatomical abbreviations: SL: standard length; P-V distance: distance between the pectoral and ventral fins. 2.1. Scopeloides glarisianus (Agassiz, 1844) PAS: Specimen Pi-F/MP/2/1510/08; Lubenia locality (Southeastern Poland, naer Rzeszo´w); Oligocene; entire specimen, SL 154 mm. Specimen Pi-F/MP/4/1483/08; Błaz˙ova locality (Southeastern Poland, near Rzeszo´w); Oligocene; almost complete specimen, without posterior-most extremity of the body, estimated SL about 75 mm. PIN: Specimen Nr. 4841/64; Ljubizhnja (Ukraine); lower Oligocene, lower menilithic shales; complete skeleton with
counterpart (same number), SL 84 mm. Specimens Nos. 4841/66 and 70; Krasnodarski Krai, Belaya River (Russia); lower Oligocene, Pshekha Formation, amphisilian layers; nearly complete skeletons and fragmentary (middle part of body), respectively (SL ca. 70 mm and estimated SL ca. 76 mm). NMP: Specimen Pc 2863 (counterpart No. Pc 2862); Loucˇka locality (Czech Republic, near Valasˇske´ Mezirˇı´cˇı´); Oligocene; part of the body without head and caudal fin, estimated SL ca. 170 mm. IGP: Specimen 2007/07, coll. Prˇikryl; Błaz˙ova 3 locality (Southeastern Poland, near Rzeszo´w); Oligocene; anterior part of the body with head, estimated SL ca. 40 mm. In addition, 16 specimens (complete and incomplete skeletons, partially with counterparts) were studied from the Czech Republic, Poland, Russia, and Abkhazia. These possess the remains of the peritoneum as a black triangular area in the abdominal region. PIN: Nos.1413/30 (complete skeleton, SL 100 mm), 4841/72 (fragmentary, middle part of body, estimated SL ca. 65 mm), 275 (nearly complete skeleton, SL ca. 52 mm), 276 (fragmentary, middle part of body with counterpart, estimated SL ca. 65 mm); Abkhazia, Gumista River, lower Oligocene, analogues of Pshekha Formation, amphisilian layers; Nos. 1413/667 (fragmentary, anterior two-thirds of body, estimated SL ca. 63 mm), 668 (complete skeleton, SL 42 mm) and 4841/21 (complete, SL 55 mm), 74 (complete, SL 52 mm), 286 (complete, SL 60 mm) from Russia, Krasnodarski Krai, Belaya River, lower Oligocene, Pshekha Formation, amphisilian layers. MRV: No. 7620 (entire specimen, SL 130 mm); unnumbered specimens: nearly complete skeleton, estimated SL ca. 70 mm; nearly complete skeleton, SL ca. 55 mm; fragmentary, anterior part of body, estimated SL ca. 55 mm; fragmentary, anterior part of body, estimated SL ca. 65 mm, from Kelcˇ locality, near Valasˇske´ Mezirˇı´cˇı´, Czech Republic. IGP: No. 2007/08, nearly complete skeleton (estimated SL ca. 50 mm) from Błaz˙ova locality, near Rzeszo´w, Poland. No. Lit2006/ 44a, coll. Prˇikryl, entire young specimen (SL 30 mm) from Litencˇice locality, Czech Republic. 2.2. Comparative recent specimens Gonostoma atlanticum Norman, 1930: 2 specimens, SL 40 and 56 mm, R/V Dm. Mendeleev, cruise 18, sta. 1489, 01.17.1977, IORAS, uncatalogued. Gonostoma elongatum Gu¨nther, 1878: 1 specimen, SL 190 mm, R/V Ak. Kurchatov, cruise 17, sta. 1462, IKTM Nr. 43, 02.16.1974; 10 specimens, SL 90–105 mm, R/V Ak. Kurchatov, cruise 17, sta. 1459, IKTM Nr. 30, 01.31.1974; 4 specimens, SL 200–215 mm, R/V Ak. Kurchatov, cruise 17, sta. 1456, IKTM Nr. 12, 01.23.1974; 1 specimen, SL 90 mm, R/V Dm. Mendeleev, cruise 18, sta. 1489, 01.17.1977; all from IORAS, uncatalogued. Gonostoma denudatum Rafinesque, 1810: 4 specimens, SL 100– 130 mm, mid-Atlantic ridge, AtlantNIRO, uncatalogued. Diplophos taenia Gu¨nther, 1873: 3 specimens, SL 142–147 mm, R/V Ak. Kurchatov, cruise 17, sta. 1461, IKTM Nr. 35, 02.03.1974. Phosichthys argenteus Hutton, 1872: 5 specimens, SL 162– 223 mm, R/V Dm. Mendeleev, cruise 16, sta. 1374, 02.29.1976. Astronesthes similis Parr, 1927: 1 specimen, SL 119 mm, R/V Petr Lebedev, 208300 N, 608400 W, dip-net surface, 03.12.1964, IORAS, uncatalogued. Stomias lampropeltis Gibbs, 1969: 1 specimen, SL 270 mm, FRV Zvezda Kryma, sta. 261, off coast of West Africa, IORAS, uncatalogued. 3. Systematic palaeontology Order STOMIIFORMES sensu Fink and Weitzman, 1982 Family GONOSTOMATIDAE Gill, 1893
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Genus Scopeloides Wettstein, 1886 Scopeloides glarisianus (Agassiz, 1844) Description: Six specimens clearly show prey remains preserved inside the body cavity. Specimen Pi-F/MP/2/1510/08 (Fig. 1) represents almost a complete fish, SL 154 mm. The skull bones are crushed so it is impossible to recognize most of separated bones (except maxillary, dentary, frontal, posttemporal, opercle, and cleitrum). The caudal and pelvic fins are not preserved completely; others are preserved in good condition. This specimen is especially interesting because of the well-preserved imprint of the body cavity in which the prey can be identified. The imprint was probably created by perforation of the gut wall and leakage of the contents of digestive tract into the abdominal cavity. The imprint stretches from the head to the level of the 16th vertebra and is 39 mm long (i.e., ca. a quarter of the entire length of the specimen). Its greatest width takes up almost the full width of the body, and narrows posteriorly. A row of left ribs is laid out on the surface of the imprint. Within the area of imprint, the remains of the prey are partly preserved, consisting of ostracod shells and fragments of fish bones in the posterior portion. Unfortunately, the state of preservation of these partly digested remains does not allow for a more precise taxonomic identification. Specimen Pi-F/MP/4/1483/08 (Fig. 2) represents an almost complete fish without the caudal extremity; estimated SL ca. 75 mm. The skeleton is preserved on the surface of the light sediments. The dorsal part of the skull and caudal extremity of the body are missing. The remains of the skull are relatively well
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preserved, with visible dentition on the jaws. The vertebral column is covered by sediment in the caudal portion, and two vertebrae behind the head are missing. The pectoral fin is turned to the ventral position, so it is exposed at the lateral part of the body. A remnant of the dorsal fin is preserved in the same level, like an anal fin. The ventral fin is situated between the pectoral and the anal fin. There is a row of dark points preserved at the ventral portion of the body, between the pectoral and anal fins. These dark points represent the remains of the photophores. In the abdominal cavity, it is possible to recognize the prey remains, situated immediately behind the head up to the level of the 10th rib. Crushing of the skull bones is present in the cranial part of the body cavity. The state of preservation does not allow for the recognition of each bone. Posteriorly from this bone cluster, there are the preserved remains of the vertebral column, which is twisted anterodorsaly. The vertebral column consists of 20 vertebrae (five of them are fossilized, others just as imprints) with the following morphology: anterior part of the vertebra is shorter than the posterior one, which is slightly conical (extended towards the posterior); the vertebral column is bent; the neural and haemal spines are relatively long (about three times longer than the size of vertebra, measured in the 2nd preserved vertebra). The systematic position of the prey is uncertain; however, on the basis of general vertebrae similarity (especially their elongated shape), it can be tentatively identified as the genus Scopeloides. Specimen Pc 2863 (Fig. 3) is preserved as a body torso without a head, tail or pectoral fin; estimated SL ca. 170 mm. The vertebral column (well-preserved 32 vertebrae) is preserved on the stone
Fig. 1. Scopeloides glarisianus (Agassiz, 1844). A. Specimen Pi-F/MP/2/1510/08 with imprint of body cavity. B. Schematic drawing of the same specimen. Scale bars: 10 mm.
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Fig. 2. Scopeloides glarisianus (Agassiz, 1844). Specimen Pi-F/MP/4/1483/08. A. Specimen with prey skeleton in the body cavity. B. Detail of the prey skeleton. Scale bars: 10 mm.
surface. The dorsal fin starts in the same level as the anal fin. The prey remains (represented by a fish vertebral column) are preserved in the middle part of the body cavity. The prey consists of 24 vertebrae (estimated SL ca. 45 mm). The centra of the vertebrae are slightly elongated, and the distal parts of their neural and haemal spines are turned posteriorly. The prey vertebral column is twisted to the ventral side in the posterior quarter. Stripes are preserved along the prey skeleton, and are slightly darker than the surrounding sediment; these are probably remnants of the stomach wall (Fig. 3(C)). Similarly, as in the previous specimen, the prey can be tentatively identified as the genus Scopeloides. Specimen PIN 4841/64 (Fig. 4) represents an almost complete fish preserved in good condition (only a few parts of the caudal fin are not preserved), with a poorly preserved although complete counterpart; SL 84 mm. The skull elements are somewhat displaced in the sagittal plane, whereas the postcranial elements are naturally articulated; the scales and photophores are missing. This exemplar contains another smaller fish specimen (estimated SL ca. 30 mm) in the abdominal region. The prey specimen can also undoubtedly be identified as S. glarisianus, based on the osteological characteristics. The digested specimen is, in general, positioned slightly closer to the ventral contour of the body than to the vertebral column (between the 5th and 16th or 17th vertebrae). Its cranial elements are pressed slightly dorsoventrally, and somewhat more distinctly displaced in the sagittal plane;
the pectoral girdle is inclined backward by its ventral portion and the pelvic girdle is moved anteriorly and dorsally. The vertebrae of the prey specimens are characteristically distorted (some neural spines are close-set to one another; others are spaced further from the others). The vertebral column is broken not far behind the mid-body; the poorly preserved remains of the caudal portion are folded backwards, and are observable between the anterior portion of the digested specimen and the vertebral column of a large fish. Specimen PIN 4841/66 represents a nearly complete skeleton (only the tip of the snout is missing) of SL ca. 70+ mm, which contains the remains of unidentified fish vertebrae in the abdominal region, at the level of the anterior tip of the pelvis. Specimen PIN 4841/70 represents an incomplete skeleton (anterior part of head and most of caudal portion are absent) of an estimated SL ca. 76 mm, which contains the remains of poorly preserved bones of an unidentified teleost taxon in a P-V distance close to the vertebral column. Remarks: The fossils are known from Oligocene localities in the Alps (Agassiz, 1833–1844; Wettstein, 1886), Carpathians (Pauca˘, 1931; Kalabis, 1938–1940, 1948, 1975a, 1975b; Jerzman´ska, 1968; Ciobanu, 1977; Gregorova´, 1989, 1997; Prokofiev, 2005a), Caucasus (Daniltshenko, 1960; Prokofiev, 2005a), and Iran (Arambourg, 1967). From the systematic point of view, most authors agree that its closest recent relative is the species Gonostoma denudatum (Kalabis, 1938–1940, 1948; Daniltshenko, 1960; Arambourg,
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Fig. 3. Scopeloides glarisianus (Agassiz, 1844). Specimen Pc 2863. A. Specimen with prey skeleton in the body cavity. B. Detail of the prey skeleton. C. Schematic drawing of probably preserved stomach wall; light grey area represents the preserved part of the body. Scale bars: 10 mm.
Fig. 4. Scopeloides glarisianus (Agassiz, 1844). Specimen PIN 4841/64. A. Specimen with prey skeleton in the body cavity. B. Detail of the prey skeleton. Scale bars: 10 mm (A) and 2 mm (B).
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1967). The complex osteological description with full synonymy and a cladistic analysis have been provided by Prokofiev (2005a). 4. Discussion 4.1. Feeding habits in Gonostoma As the closest living relatives of Scopeloides, the genus Gonostoma was chosen for comparison of feeding habits. Hopkins et al. (1996) stated that members of the family Gonostomatidae generally are zooplanktivorous fishes with small crustaceans as the main components of their diet. Fish were recognized as a minor dietary component (about 8%). The feeding habits of the recent genus Gonostoma were studied in Gonostoma gracile Gu¨nther, 1878, by Gordon et al. (1985), Kawaguchi (1969), and Uchikawa et al. (2001); in G. elongatum by Lancraft et al. (1988), and they were also mentioned by Guschin (1982). Information about the diet of other species of this genus is lacking. The dominant foods of G. gracile from the Pacific coast of Hokkaido are euphausiids and copepods (Ostracoda and Mysidacea were rarely identified; Gordon et al., 1985). Kawaguchi (1969) examined 216 specimens of G. gracile from the Kuroshio Area and Suruga Bay (North-western Pacific Ocean), and among the recognized preys are: copepods, euphasiids, amphipods, mysids, chaetognaths, and rarely fishes; informational details on the types or sizes of the fish preys was not provided. Copepods and ostracods dominated among the prey remains (approximately 70%) in the stomach of G. gracile, of a body length of 19–116 mm (Northwestern North Pacific; Uchikawa et al., 2001). These authors described an ontogenetic dietary shift: the size range of the prey increased with the growth of the fish. The prey of G. elongatum is mainly composed of crustaceans, copepods, and ostracods in the early juvenile stages, and of euphasiids in larger-sized individuals; very rarely is it composed of fish: leptocephalus larvae and other unidentifiable types of fish remains (Lancraft et al., 1988). These authors recognized changes in the diet between different size classes: growing individuals change their prey from copepods and ostracods to mainly euphasiids. In addition, Guschin (1982) mentioned pisces preys found in the digestive tract of two specimens in G. elongatum: in the first specimen (SL 160 mm), the prey was Maurolicus muelleri (Gmelin, 1789), and its length was estimated at about 50 mm; in the second specimen (SL 180 mm), fishes were identified without any more definitive determination. Within 22 specimens of G. denudatum, G. elongatum and G. atlanticum that we examined, only one specimen of G. elongatum was found with prey in the stomach; the others had empty stomachs. The stomach of a fish (SL 190 mm) contains a single euphausiid crustacean, ca. 25 mm in length (from tip of the rostrum to tip of the telson). This prey is headed anteriorly in the stomach (Fig. 5). It can be concluded that Gonostoma is a typical crustacean feeder with an opportunistic connection to the fish prey.
Fig. 5. Gonostoma elongatum Gu¨nther, 1878. Content of digestive tract. Detail of an uncatalogued specimen, SL 190 mm. Scale bar: 10 mm.
(Pi-F/MP/2/1510/08), the body cavity contained ostracods and an unrecognizable type of fish bones (Fig. 6). The ostracods, as well as the fish skull bones, are fragmentarily preserved. The poor preservation of the remains is probably partly caused by the fossilization processes, and partly by digestion. It is highly improbable that the prey were chewed or crushed by the force of the jaw, because this jaw type with long sharp fangs is not functional for the mastication of prey. Furthermore, Gartner et al. (1997) proposed that many mid-water fishes have been shown to be swallowers. Fish skull elements preserved in the abdominal cavity are unusable for a taxonomic determination of the prey, due to their poor state of preservation. Problems with the digested portions, during the study of the feeding habits in recent fishes, where mentioned by Gerking (1994). The five other specimens (Pc 2863, Pi-F/MP/4/1483/08, PIN 4841/64, 66 and 70) contain the remains of teleost fishes. In three cases (Pc 2863, Pi-F/MP/4/1483/08, and PIN 4841/64), the digested fish specimens can be identified as the same species. In the remaining two cases the prey remains are too incomplete or poorly preserved; therefore, they cannot be identified any closer than as Teleostei. In specimens Pc 2863, Pi-F/MP/4/1483/08, and PIN 4841/ 64, prey’s orientation in the predator is with the head anteriorly (Figs. 2(B), 3(B), 4(B)). In the remaining two specimens (PIN 4841/ 66 and 70), the preys are represented only by some separated bones or their fragments; thus, it is not possible to identify this position. However, as the remnants lie in the area of stomach, we can consider that a large part of the digestion process appears in the stomach.
4.2. Probable feeding habits in Scopeloides The study of the preserved anatomic structures of S. glarisianus allows for speculation about the feeding habits of this fossil species. The heavy jaws are the main functional unit for catching, holding, and transporting the prey; the length of the lower jaw is about 70% that of the head length. The structure of the dentition in S. glarisianus was described in detail by Prokofiev (2005a). The presence of fang-like teeth in the jaws clearly shows a predatory feeding modus. We have examined six specimens of S. glarisianus possessing fossilized preys in their alimentary canal. In the first case
Fig. 6. Scopeloides glarisianus (Agassiz, 1844). Content of digestive tract in the abdominal cavity, detail of specimen Pi-F/MP/2/1510/08. Scale bar: 10 mm.
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In specimens Pi-F/MP/4/1483/08 and PIN 4841/64, the caudal portions of the digested fishes are folded backwards, which may indicate that they were caught by their sides, close to the tail, and further that they were folded during swallowing. In contrast to these specimens, the prey’s head orientation is anterior, in a similar way to its caudal extremity in specimen Pc 2863. Apparently, S. glarisianus is a predator which typically swallowed their prey tail-first. The only two taxa of Palaeogene fishes with the prey headed anteriorly were noted by Viohl (1990: table 23); both were from the Italian locality of Monte Bolca (Eocene). The position of the prey inside the predator’s body may well illustrate some interesting information about the types of feeding habits. Hoogland et al. (1957) studied Perca and Esox feeding habits, and found a correlation between the prey’s orientation in the predator’s stomach and the presence of special morphological features (spines) of the prey’s body. L’Abe´e-Lund et al. (1996) showed that Salmo trutta change their feeding behaviour depending on the prey species, size, as well as the number of prey eaten. Boucot (1990) presented the major facts about prey orientation, and briefly discussed the possibility whether the swallowing of the prey headfirst could be a learned behaviour or not. There is no possibility to decide any such significance from the prey position in our case. Our primary focus is on the body of Scopeloides (as the probable congeneric prey), as there are no spines present, which could cause any problems during tail-first swallowing. Based on the examination of G. elongatum with prey in situ, we can conclude that tail-first swallowing is also characteristic for the members of this genus. As Gonostoma are mainly crustacean feeders, this mode of swallowing possibly represents an adaptation to safe swallowing of large crustacean prey, such as euphausiids and mysids for example, which possess the long and sometimes spined antennae, legs, and rostrum, making tail-first swallowing more successful. Despite the probability of stronger connections to the fish prey in Scopeloides compared with Gonostoma (see below), its feeding behaviour retains the general adaptations of the gonostomatids. In this connection, it should be noted that the ichthyophagous predator Holosteus mariae (Menner, 1948) was a head-first swallower, despite the fact that Myctophidae and Argentinidae, its documented preys (Prokofiev, 2005b;
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Fig. 7. Scopeloides glarisianus (Agassiz, 1844). Preserved remains of the peritoneum, detail of the specimen MRV 7620. Scale bar: 10 mm.
Bien´kowska-Wasiluk, 2010), lacked spines or other structures prohibiting tail-first swallowing. The aforementioned specimens of S. glarisianus clearly show the trophic relationship of the vertebrate prey. Furthermore, in at least three specimens the remains of the prey probably represent congeneric specimens. Cannibalistic behaviour has been described in three marine Oligocene fishes within the Carpathian region: Oligoserranoides (syn.: Serranus, Oliganodon) budensis by Pauca˘ (1934) and Bien´kowska-Wasiluk (2010) from Romania and Poland; Anenchelum glarisianum by Prˇikryl and Novosad (2009) from the Czech Republic; and Trachinus minutus by Bien´kowska-Wasiluk (2010) from Poland. The possibility of cannibalistic behaviour in Scopeloides is presented for the first time herein. Moreover, congeneric prey is documented in 50% of cases having the presence of fish preys; however, this ratio could be underestimated as in other cases the remains of the teleost preys cannot be identified more precisely. This may indicate that cannibalism had a rather important role in the feeding behaviour of S. glarisianus. Although the relatively low number of specimens with preserved preys do not allow for the reconstruction of their feeding habits more precisely, on the basis of the above-mentioned specimens the functional anatomy and information on recent relatives make it possible to state that S. glarisianus was a predator consuming crustaceans and fishes. The fishes that made up their prey appear to have attained an SL of over 70 mm, and apparently,
Fig. 8. Scopeloides glarisianus (Agassiz, 1844). A. Juvenile specimen with preserved remains of the peritoneum. B. Detail of (A). C. Adult or subadult specimen with preserved stomach and anterior part of intestine. D. Detail of (C). A, B, specimen Lit2006/44a; C, D, specimen 2007/07. Scale bars: 5 mm.
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individuals had fish preys not only in exceptional cases. Although we cannot estimate the ratio between the invertebrate and vertebrate preys in S. glarisianus (due to the processes of fossilization, invertebrate preys appear to be extremely rarely preserved in fossils), the quite frequent presence of fish preys in the abdominal cavity of S. glarisianus, which even occurs in rather small individuals (70–84 mm SL), indicates a stronger connection with the consumption of fish preys than in the strategy of those representatives of the recent genus Gonostoma (see above). It also seems that Scopeloides becomes ichthyophagous before maturity, which is a characteristic of mainly ichthyophagous predators, as pointed out earlier by Lebedev and Spanovskaya (1983) for asp-like cyprinids, by Tankevitsch et al. (1989) for toothfishes (Dissostichus, Nototheniidae), by Kornilova and Portsev (1989) for cutlassfishes (Trichiuridae), and by Prokofiev and Kukuev (2009) for chiasmodontids. However, it should be noted that the feeding habits are only known for a few species of Gonostoma, and the interspecific differences are still awaited. 4.3. Preservation of soft tissues in Scopeloides A closer examination of S. glarisianus specimens in many collections has shown that the structure described by Kalabis
(1948) as the remains of the stomach cannot be identified with a real oesophagus nor stomach full of food. This is not possible for general anatomical reasons, as in stomiiforms a stomach is an elongate tube with a gently narrowed, pointed, or obtuse posterior tip. The tapering shape, size, position, and marked colour of the dark pigment in many fossil specimens instead apparently indicates the imprints of the peritoneum. This structure is relatively frequently preserved, not only in adults (Fig. 7; Gregorova´, 1989: pl. 7), but also in young individuals (Fig. 8 (A, B)). In all mentioned specimens it originates immediately behind the head, between the vertebral column and a point above the flexion of the cleithrum, tapering and gently declining posteriorly; the caudal tip of this organ is terminated at a level slightly behind (about one vertebra) the end of the pelvic bone. Comparisons with recent Gonostoma (Fig. 9) species shows that the rather constant triangular and tapering shape of this dark zone can be explained by the quite rapid decrease of the height of the abdominal cavity in the post-pelvic portion of the body. In recent fishes we can easily observe almost the same form when we remove the peritoneum from the body wall during preparation (a similar stratification can be expected during decomposition of the dead Scopeloides specimens). It is possible that the terminal
Fig. 9. Gonostoma elongatum Gu¨nther, 1878. A. Digestive tract and associated structures in abdominal cavity; uncatalogued specimen, SL 205 mm. B. Prepared digestive tract in outer view; uncatalogued specimen, SL 210 mm. C. Same specimen as in (B) but in inner view. D. Digestive tract and associated structures in abdominal cavity with prey preserved in situ; uncatalogued specimen, SL 190 mm. Scale bars: 10 mm.
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ending of the peritoneum is not preserved, as it can become too thin during the decomposing process. A true imprint of the fish’s alimentary canal is only exceptionally preserved in fossils (e.g., Zhang and Jin, 2003: text-fig. 96). This rare situation is observed in specimen 2007/07, in which the greater part of the digestive duct is preserved (Fig. 8(C, D)). The digestive tract is obviously empty, but the anatomical position of its anterior part is clearly recognizable. The oesophagus is not recognizable due to the covering of bones of the opercular series and the pectoral girdle, but is apparently short. The stomach is in an almost horizontal position, and it expands to the eighth rib. Its dorsal contour is somewhat concave at the level between the second and third rib, which may indicate the position of the pylorus, and a border between the anterior and posterior (caecal) portions of the stomach. The tip of the caecal part of the stomach is bluntly rounded. The beginning of the intestine is well preserved along the ventral contour of the caecal portion of the stomach, but its posterior portion cannot be reconstructed. In contrast to the very well preserved alimentary canal, the liver is not preserved. The shape of the stomach can also be reconstructed on the basis of specimen Pc 2863, where slightly darker stripes than the surrounding sediment are preserved; these are probably remnants of the caecal part of the stomach (Fig. 3(C)). The wall of this part of the stomach was relatively thick and probably elastic. The remains of dark pigmentation could indicate that the walls of the stomach were darkly pigmented, similar to various recent deep-water teleost taxa, like many stomiiforms (see below), some lizardfishes (Prokofiev, 2006), deep-sea eels (Fishelson, 1994), or cardinal fishes (Fishelson et al., 1997). This characteristic in recent fishes is supposed to be an adaptation to prevent bioluminescence for illuminating the predator, if a bioluminescent prey fish is swallowed (Fishelson, 1994). The darkly coloured peritoneum probably has a similar function. In recent Gonostoma species, the oesophagus is a very short and rather broad tube lying under the basioccipital bone, and between the pectoral-fin girdles. It is separated from the stomach by a clearly marked constriction, indicating the oesophagus-gastric sphincter. The stomach is an elongate tube with thick muscular walls. The dorsal contour of the stomach is indistinctly concave at mid-length; on the ventral surface the pylorus is separated. The posterior portion of the stomach is caecal, with a pointed or bluntly rounded distal tip. In most of the examined specimens, the length of the stomach is about one-half of the P-V distance, rarely slightly longer (about two-thirds of P-V). The pyloric caeca are not numerous, moderately large, elongate, and finger-like. The colour of the peritoneum is dark brown to blackish; the oesophagus and stomach (including pylorus) are jet-black; and the pyloric caeca and intestine are yellowish or white. The walls of the intestine sometimes have the aggregations of greyish and blackish melanophores on some portion of them. The liver is rather small, consists of two lobes, in which the inner lobe is always smaller than the outer ones; lobes with a more or less distinct incision along their posterior margin are much better developed in the outer lobe. The length of the outer lobe of liver is (usually) about one-quarter to one-third of the stomach length. The intestine is nearly straight, and the anus is located not far in front of the analfin origin (distance between anus and anal-fin origin is 20–25% of the P-V distance). The same configuration and colouration of the viscera is observed in Phosichthys; while in Diplophos the viscera have a similar size and structure, but all parts of the alimentary duct are light in colour. Within the representatives of the closely related family Sternoptychidae, the pigmentation of the various parts of the alimentary canal are variable within the species (Parin and Kobyliansky, 1993). Additionally, the colour of the peritoneum can be variable within the species of the recent phosichthyid genus
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Polymetme (Parin and Borodulina, 1991). We also checked two specimens of the deep-water family Stomiidae. Both Astronesthes similis and Stomias lampropeltis have the same general plan of structure and colouration of the viscera as described above for the Gonostoma spp.; however, the stomach is much more elongated (especially in Stomias), which corresponds with the markedly elongated abdominal region. Thus, the structure of the viscera observable in S. glarisianus is almost the same as in recent members of the genus Gonostoma, and shows the general plan characteristic for all stomiiforms. 5. Conclusions The probable feeding habits of S. glarisianus are briefly sketched on the basis of the studied specimens from the Russia, Ukraine, Poland, and the Czech Republic. On the basis of the preserved preys within the alimentary-canal, S. glarisianus appears as predatory fish with a dietary connection to crustaceans and fishes, similar to recent relatives of the genus Gonostoma, although an ichthyophagous predation seems to be more characteristic for Scopeloides, in contrast with Gonostoma. The fish preys appear in individuals of 70–75 mm SL. Cannibalistic behaviour is proposed for the first time. All identified fish remains in the alimentary canal belong to the same species. The preserved soft tissues also allow for a brief discussion of some anatomical and eco-morphological features. Acknowledgments We are grateful to M. Pozˇa´r and K. Pavelka for access to the MRV collection; to B. Ekrt (NMP) for access to the specimen under his care; to N. Kubricky and P.R. Lemkin who kindly made linguistic improvements; to D.A. Astakhov for assistance in the photographing of recent specimens; to G. Escarguel for his valuable notes; and finally to the reviewers A.M. Murray and G. Carnevale for their comments, which improved the quality of the manuscript. This work was supported by institutional project AVOZ30130516 of the Institute of Geology AS CR, v.v.i. References Agassiz, L., 1833–1844. Recherches sur les poissons fossiles. Petitpierre, Neuchaˆtel. Arambourg, C., 1967. Re´sultats scientifiques de la mission C. Arambourg en Syrie et en Iran (1938–1939). II : Les Poissons oligoce`ne de l’Iran. Notes et Me´moires sur le Moyen-Orient 8, 11–210. Bien´kowska-Wasiluk, M., 2010. Taphonomy of Oligocene teleost fishes from the Outer Carpathians of Poland. Acta Geologica Polonica 60, 479–533. Boucot, A.J., Ed. 1990. Evolutionary paleobiology of behavior and coevolution. Elsevier, London. Carnevale, G., 2002. A new barbeled dragonfish (Teleostei: Stomiiformes: Stomiidae) from the Miocene of Torricella Peligna, Italy: Abruzzoichthys erminioi gen. and sp. nov. Eclogae geologicae Helvetiae 95, 471–479. Carnevale, G., 2008. Miniature deep-sea hatchetfish (Teleostei: Stomiiformes) from the Miocene of Italy. Geological Magazine 145, 73–84. Case, G.R., 1982. A pictorial guide to fossils. Van Nostrand Co, New York. Ciobanu, M., 1977. Fauna fosila˘ din Oligocenul de la Piatra Neamt¸. Editura Academiei Republicii Socialiste Romaˆnia, Bucuresti. Crane, J.M., 1966. Late Tertiary radiation of viperfishes (Chauliodontidae) based on a comparison of recent and Miocene species. Los Angeles County Museum of Natural History, Contributions in Science 115, 1–29. Daniltshenko, P.G., 1960. Bony Fish from Maikop Deposits in the Caucasus. Trudy Paleontologicheskogo Instituta AN SSSR 78, 1–208 (in Russian). Fink, W.L., Weitzman, S.H., 1982. Relationships of the stomiiform fishes (Teleostei), with a description of Diplophos. Bulletin of the Museum of Comparative Zoology 150, 31–93. Fishelson, L., 1994. Comparative internal morphology of deep-sea eels, with particular emphasis on gonads and gut structure. Journal of Fish Biology 44, 75– 101. Fishelson, L., Goren, M., Gon, O., 1997. Black gut phenomenon in cardinal fishes (Apogonidae, Teleostei). Marine Ecology Progress Series 161, 295–298. Gartner Jr., J.V., Crabtree, R.E., Sulak, K.J., 1997. Feeding at depth. In: Randall, D.J., Farrell, A.P. (Eds.), Deep-Sea Fishes. Academic Press, San Diego, pp. 115–193. Gerking, S.D., 1994. Feeding Ecology of Fish. Academic Press, San Diego.
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Original article
Feeding habits of the Oligocene bristlemouth fish Scopeloides glarisianus (Teleostei: Stomiiformes: Gonostomatidae)§ Toma´sˇ Prˇikryl a,*,b, Arte´m M. Prokofiev c,d, Wiesław Krzemin´ski e a
Institute of Geology, Academy of Sciences of the Czech Republic, v.v.i., Rozvojova´ 269, 16500 Prague 6, Czech Republic Institute of Geology and Palaeontology, Charles University in Prague, Albertov 6, 12843 Prague 2, Czech Republic c A.N. Severtsov’s Institute of Ecology and Evolution, Russian Academy of Science, Leninski Prospekt, 33, 119071 Moscow, Russia d Paleontological Institute, Russian Academy of Science, Profsoyuznaya ul., 123, 117997 Moscow, Russia e Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, ul. S´w. Sebastiana 9, 31049 Krako´w, Poland b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 5 September 2011 Accepted 20 October 2011 Available online 16 July 2012
The dietary habits of the Oligocene fish Scopeloides glarisianus (Agassiz) are presented on the basis of functional morphology, in comparison with their recent relatives (Gonostoma spp.) as well as fossil materials from localities in Poland (Lubenia, Błaz˙ova), Ukraine (Ljubizhnja), the Czech Republic (Loucˇka), and the northern Caucasus in Russia and Abkhazia. Analogous to the recent relatives from the genus Gonostoma, S. glarisianus fed on crustaceans such as ostracods and copepods, the larger specimens preying on small fishes. Fishes remains preserved within the alimentary canal region are usually represented by smaller individuals of the same species; accordingly, the cannibalistic behaviour of the adult S. glarisianus is thereby documented. The remains of the alimentary canal and the peritoneum are identified. ß 2012 Elsevier Masson SAS. All rights reserved.
Keywords: Teleostei Gonostomatidae Functional morphology Feeding habits Cannibalism Palaeoecology Palaeogene
1. Introduction Scopeloides glarisianus was first described by Louis Agassiz (1833–1844), in his famous monograph on fossil fishes, as Osmerus glarisianus from Oligocene deposits in Switzerland. This fish of the family Gonostomatidae (order Stomiiformes) was either mesopelagic (Prokofiev, 2005a) or bathypelagic (Jerzman´ska, 1968), and its ecological demands were probably similar to recent species of the genus Gonostoma. No information has been published on its feeding habits, except for one theoretical note mentioned by Kalabis (1948). The recent deep-water fishes are ecomorphologically well adapted for predatory lives. In particular, these adaptations include large jaws capable of catching larger prey, and are morphological results of evolutionary processes. Such features can also be traced in the fossil representations of various predatory fish species. In recent fishes, the feeding and dietary habits are possible to study in two different ways. There are direct and indirect evidences, which can be used for the reconstruction of their feeding. Direct evidences are presented by the remnants of prey in
§
Corresponding editor: Gilles Escarguel. * Corresponding author. E-mail address: [email protected] (T. Prˇikryl).
0016-6995/$ – see front matter ß 2012 Elsevier Masson SAS. All rights reserved. http://dx.doi.org/10.1016/j.geobios.2011.10.012
the stomach or alimentary canal of the predators; indirect evidences could be from the information provided through comparative anatomy and functional morphology (Wootton, 1998). Indirect methods could also show the feeding modus (Gartner et al., 1997). In recent deep-water fishes it is quite difficult to study the feeding habits, especially from the physiological point of view, due to many methodological limitations; moreover, many predators only feed infrequently, making difficult to decide if the predator is a ‘‘selective’’ or ‘‘generalized’’ feeder (Gartner et al., 1997). On the basis of both types of indices (direct and indirect), the possible dietary habits can also be reconstructed in the fossil record; however, it is clear that only direct evidences specifically show the original food. The predatory feeding habits of fossil fishes were recognized in various stratigraphic positions (Viohl, 1990; Maisey, 1994), but many of them were only noted as interesting palaeoecological facts, without larger ecological and anatomical contexts. Not only ‘‘general’’ feeding behaviours, but also highly specific habits, such as cannibalism, were certainly recognized record in the fossil (Watson, 1927; Pauca˘, 1934; Case, 1982; Maisey, 1994; Prˇikryl and Novosad, 2009). In the fossil record, the feeding habits of ‘‘deep-water fishes’’ are principally deduced on the basis of functional anatomy (e.g., Carnevale, 2002, 2008), although several cases of direct evidence have also been published (one such case is the viper fish Chauliodus eximius (Jordan and
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Gilbert, 1925) from southern California Miocene deposits (Crane, 1966: text-fig. 13)). A general review of the dietary habits in fossil fishes was published by Boucot (1990). In 1948, Kalabis stated that almost all specimens of S. glarisianus studied by him were fossilized with full stomachs. He had interpreted a dark pigmented zone behind the head, which tapers posteriorly, as the stomach. About their feeding habits, he wrote that Scopeloides were predators with distinctly toothed jaws, but did not comment further on the feeding habits of this species. This short note was just one published mention about the possible feeding habits for this taxon. However, true remnants of the alimentary canal cannot be recognized in these specimens. It is our opinion that these structures were misinterpreted by Kalabis, and are herein properly identified. The first direct evidence of the diet of the adult S. glarisianus is preserved in several fossil specimens we have studied and present here. 2. Material and methods Specimen Lit2006/44a was prepared by thin needles under a binocular microscope; the other specimens studied were either left unprepared or had been prepared before this investigation. In order to extricate artefacts from real trophic records, digested specimens can be separated by the following rationale: the prey lies inside the rib cage (i.e., prey is situated between the ribs of both sides of the body); the position of the digested fish, in general, agrees with the orientation of the predator’s digestive tract; the digested specimens are never positioned perpendicular nor under a distinct angle to the longitudinal axis of predator’s digestive tract; the digested specimens never retain natural articulation of the skull, ribs, and intermusculars, nor well-preserved and naturally expanded fins, especially unpaired ones; their vertebral columns are usually distorted (some pieces of column can be separated, or some vertebrae can be close-set to one another, and some of them are spaced away from each other); the skeleton elements of the digested fish never cross the skeleton elements of the predator, viewed from the side; the outer surface of the digested specimens can be corroded by the digestive processes. Institutional abbreviations: AtlantNIRO: Atlantic Research Institute of Fishery and Oceanography; Kaliningrad; Russia; IGP: Institute of Geology and Palaeontology; Faculty of Sciences; Charles University; Prague; Czech Republic; IORAS: Institute of Oceanology; Russian Academy of Sciences; Moscow; Russia; MRV: Museum of Valasˇsko region; Vsetı´n; Czech Republic; NMP: National Museum; Prague; Czech Republic; PAS: Institute of Systematics and Evolution of Animals; Polish Academy of Sciences; Krakow; Poland; PIN: Paleontological Institute; Russian Academy of Sciences; Moscow; Russia. Anatomical abbreviations: SL: standard length; P-V distance: distance between the pectoral and ventral fins. 2.1. Scopeloides glarisianus (Agassiz, 1844) PAS: Specimen Pi-F/MP/2/1510/08; Lubenia locality (Southeastern Poland, naer Rzeszo´w); Oligocene; entire specimen, SL 154 mm. Specimen Pi-F/MP/4/1483/08; Błaz˙ova locality (Southeastern Poland, near Rzeszo´w); Oligocene; almost complete specimen, without posterior-most extremity of the body, estimated SL about 75 mm. PIN: Specimen Nr. 4841/64; Ljubizhnja (Ukraine); lower Oligocene, lower menilithic shales; complete skeleton with
counterpart (same number), SL 84 mm. Specimens Nos. 4841/66 and 70; Krasnodarski Krai, Belaya River (Russia); lower Oligocene, Pshekha Formation, amphisilian layers; nearly complete skeletons and fragmentary (middle part of body), respectively (SL ca. 70 mm and estimated SL ca. 76 mm). NMP: Specimen Pc 2863 (counterpart No. Pc 2862); Loucˇka locality (Czech Republic, near Valasˇske´ Mezirˇı´cˇı´); Oligocene; part of the body without head and caudal fin, estimated SL ca. 170 mm. IGP: Specimen 2007/07, coll. Prˇikryl; Błaz˙ova 3 locality (Southeastern Poland, near Rzeszo´w); Oligocene; anterior part of the body with head, estimated SL ca. 40 mm. In addition, 16 specimens (complete and incomplete skeletons, partially with counterparts) were studied from the Czech Republic, Poland, Russia, and Abkhazia. These possess the remains of the peritoneum as a black triangular area in the abdominal region. PIN: Nos.1413/30 (complete skeleton, SL 100 mm), 4841/72 (fragmentary, middle part of body, estimated SL ca. 65 mm), 275 (nearly complete skeleton, SL ca. 52 mm), 276 (fragmentary, middle part of body with counterpart, estimated SL ca. 65 mm); Abkhazia, Gumista River, lower Oligocene, analogues of Pshekha Formation, amphisilian layers; Nos. 1413/667 (fragmentary, anterior two-thirds of body, estimated SL ca. 63 mm), 668 (complete skeleton, SL 42 mm) and 4841/21 (complete, SL 55 mm), 74 (complete, SL 52 mm), 286 (complete, SL 60 mm) from Russia, Krasnodarski Krai, Belaya River, lower Oligocene, Pshekha Formation, amphisilian layers. MRV: No. 7620 (entire specimen, SL 130 mm); unnumbered specimens: nearly complete skeleton, estimated SL ca. 70 mm; nearly complete skeleton, SL ca. 55 mm; fragmentary, anterior part of body, estimated SL ca. 55 mm; fragmentary, anterior part of body, estimated SL ca. 65 mm, from Kelcˇ locality, near Valasˇske´ Mezirˇı´cˇı´, Czech Republic. IGP: No. 2007/08, nearly complete skeleton (estimated SL ca. 50 mm) from Błaz˙ova locality, near Rzeszo´w, Poland. No. Lit2006/ 44a, coll. Prˇikryl, entire young specimen (SL 30 mm) from Litencˇice locality, Czech Republic. 2.2. Comparative recent specimens Gonostoma atlanticum Norman, 1930: 2 specimens, SL 40 and 56 mm, R/V Dm. Mendeleev, cruise 18, sta. 1489, 01.17.1977, IORAS, uncatalogued. Gonostoma elongatum Gu¨nther, 1878: 1 specimen, SL 190 mm, R/V Ak. Kurchatov, cruise 17, sta. 1462, IKTM Nr. 43, 02.16.1974; 10 specimens, SL 90–105 mm, R/V Ak. Kurchatov, cruise 17, sta. 1459, IKTM Nr. 30, 01.31.1974; 4 specimens, SL 200–215 mm, R/V Ak. Kurchatov, cruise 17, sta. 1456, IKTM Nr. 12, 01.23.1974; 1 specimen, SL 90 mm, R/V Dm. Mendeleev, cruise 18, sta. 1489, 01.17.1977; all from IORAS, uncatalogued. Gonostoma denudatum Rafinesque, 1810: 4 specimens, SL 100– 130 mm, mid-Atlantic ridge, AtlantNIRO, uncatalogued. Diplophos taenia Gu¨nther, 1873: 3 specimens, SL 142–147 mm, R/V Ak. Kurchatov, cruise 17, sta. 1461, IKTM Nr. 35, 02.03.1974. Phosichthys argenteus Hutton, 1872: 5 specimens, SL 162– 223 mm, R/V Dm. Mendeleev, cruise 16, sta. 1374, 02.29.1976. Astronesthes similis Parr, 1927: 1 specimen, SL 119 mm, R/V Petr Lebedev, 208300 N, 608400 W, dip-net surface, 03.12.1964, IORAS, uncatalogued. Stomias lampropeltis Gibbs, 1969: 1 specimen, SL 270 mm, FRV Zvezda Kryma, sta. 261, off coast of West Africa, IORAS, uncatalogued. 3. Systematic palaeontology Order STOMIIFORMES sensu Fink and Weitzman, 1982 Family GONOSTOMATIDAE Gill, 1893
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Genus Scopeloides Wettstein, 1886 Scopeloides glarisianus (Agassiz, 1844) Description: Six specimens clearly show prey remains preserved inside the body cavity. Specimen Pi-F/MP/2/1510/08 (Fig. 1) represents almost a complete fish, SL 154 mm. The skull bones are crushed so it is impossible to recognize most of separated bones (except maxillary, dentary, frontal, posttemporal, opercle, and cleitrum). The caudal and pelvic fins are not preserved completely; others are preserved in good condition. This specimen is especially interesting because of the well-preserved imprint of the body cavity in which the prey can be identified. The imprint was probably created by perforation of the gut wall and leakage of the contents of digestive tract into the abdominal cavity. The imprint stretches from the head to the level of the 16th vertebra and is 39 mm long (i.e., ca. a quarter of the entire length of the specimen). Its greatest width takes up almost the full width of the body, and narrows posteriorly. A row of left ribs is laid out on the surface of the imprint. Within the area of imprint, the remains of the prey are partly preserved, consisting of ostracod shells and fragments of fish bones in the posterior portion. Unfortunately, the state of preservation of these partly digested remains does not allow for a more precise taxonomic identification. Specimen Pi-F/MP/4/1483/08 (Fig. 2) represents an almost complete fish without the caudal extremity; estimated SL ca. 75 mm. The skeleton is preserved on the surface of the light sediments. The dorsal part of the skull and caudal extremity of the body are missing. The remains of the skull are relatively well
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preserved, with visible dentition on the jaws. The vertebral column is covered by sediment in the caudal portion, and two vertebrae behind the head are missing. The pectoral fin is turned to the ventral position, so it is exposed at the lateral part of the body. A remnant of the dorsal fin is preserved in the same level, like an anal fin. The ventral fin is situated between the pectoral and the anal fin. There is a row of dark points preserved at the ventral portion of the body, between the pectoral and anal fins. These dark points represent the remains of the photophores. In the abdominal cavity, it is possible to recognize the prey remains, situated immediately behind the head up to the level of the 10th rib. Crushing of the skull bones is present in the cranial part of the body cavity. The state of preservation does not allow for the recognition of each bone. Posteriorly from this bone cluster, there are the preserved remains of the vertebral column, which is twisted anterodorsaly. The vertebral column consists of 20 vertebrae (five of them are fossilized, others just as imprints) with the following morphology: anterior part of the vertebra is shorter than the posterior one, which is slightly conical (extended towards the posterior); the vertebral column is bent; the neural and haemal spines are relatively long (about three times longer than the size of vertebra, measured in the 2nd preserved vertebra). The systematic position of the prey is uncertain; however, on the basis of general vertebrae similarity (especially their elongated shape), it can be tentatively identified as the genus Scopeloides. Specimen Pc 2863 (Fig. 3) is preserved as a body torso without a head, tail or pectoral fin; estimated SL ca. 170 mm. The vertebral column (well-preserved 32 vertebrae) is preserved on the stone
Fig. 1. Scopeloides glarisianus (Agassiz, 1844). A. Specimen Pi-F/MP/2/1510/08 with imprint of body cavity. B. Schematic drawing of the same specimen. Scale bars: 10 mm.
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Fig. 2. Scopeloides glarisianus (Agassiz, 1844). Specimen Pi-F/MP/4/1483/08. A. Specimen with prey skeleton in the body cavity. B. Detail of the prey skeleton. Scale bars: 10 mm.
surface. The dorsal fin starts in the same level as the anal fin. The prey remains (represented by a fish vertebral column) are preserved in the middle part of the body cavity. The prey consists of 24 vertebrae (estimated SL ca. 45 mm). The centra of the vertebrae are slightly elongated, and the distal parts of their neural and haemal spines are turned posteriorly. The prey vertebral column is twisted to the ventral side in the posterior quarter. Stripes are preserved along the prey skeleton, and are slightly darker than the surrounding sediment; these are probably remnants of the stomach wall (Fig. 3(C)). Similarly, as in the previous specimen, the prey can be tentatively identified as the genus Scopeloides. Specimen PIN 4841/64 (Fig. 4) represents an almost complete fish preserved in good condition (only a few parts of the caudal fin are not preserved), with a poorly preserved although complete counterpart; SL 84 mm. The skull elements are somewhat displaced in the sagittal plane, whereas the postcranial elements are naturally articulated; the scales and photophores are missing. This exemplar contains another smaller fish specimen (estimated SL ca. 30 mm) in the abdominal region. The prey specimen can also undoubtedly be identified as S. glarisianus, based on the osteological characteristics. The digested specimen is, in general, positioned slightly closer to the ventral contour of the body than to the vertebral column (between the 5th and 16th or 17th vertebrae). Its cranial elements are pressed slightly dorsoventrally, and somewhat more distinctly displaced in the sagittal plane;
the pectoral girdle is inclined backward by its ventral portion and the pelvic girdle is moved anteriorly and dorsally. The vertebrae of the prey specimens are characteristically distorted (some neural spines are close-set to one another; others are spaced further from the others). The vertebral column is broken not far behind the mid-body; the poorly preserved remains of the caudal portion are folded backwards, and are observable between the anterior portion of the digested specimen and the vertebral column of a large fish. Specimen PIN 4841/66 represents a nearly complete skeleton (only the tip of the snout is missing) of SL ca. 70+ mm, which contains the remains of unidentified fish vertebrae in the abdominal region, at the level of the anterior tip of the pelvis. Specimen PIN 4841/70 represents an incomplete skeleton (anterior part of head and most of caudal portion are absent) of an estimated SL ca. 76 mm, which contains the remains of poorly preserved bones of an unidentified teleost taxon in a P-V distance close to the vertebral column. Remarks: The fossils are known from Oligocene localities in the Alps (Agassiz, 1833–1844; Wettstein, 1886), Carpathians (Pauca˘, 1931; Kalabis, 1938–1940, 1948, 1975a, 1975b; Jerzman´ska, 1968; Ciobanu, 1977; Gregorova´, 1989, 1997; Prokofiev, 2005a), Caucasus (Daniltshenko, 1960; Prokofiev, 2005a), and Iran (Arambourg, 1967). From the systematic point of view, most authors agree that its closest recent relative is the species Gonostoma denudatum (Kalabis, 1938–1940, 1948; Daniltshenko, 1960; Arambourg,
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Fig. 3. Scopeloides glarisianus (Agassiz, 1844). Specimen Pc 2863. A. Specimen with prey skeleton in the body cavity. B. Detail of the prey skeleton. C. Schematic drawing of probably preserved stomach wall; light grey area represents the preserved part of the body. Scale bars: 10 mm.
Fig. 4. Scopeloides glarisianus (Agassiz, 1844). Specimen PIN 4841/64. A. Specimen with prey skeleton in the body cavity. B. Detail of the prey skeleton. Scale bars: 10 mm (A) and 2 mm (B).
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1967). The complex osteological description with full synonymy and a cladistic analysis have been provided by Prokofiev (2005a). 4. Discussion 4.1. Feeding habits in Gonostoma As the closest living relatives of Scopeloides, the genus Gonostoma was chosen for comparison of feeding habits. Hopkins et al. (1996) stated that members of the family Gonostomatidae generally are zooplanktivorous fishes with small crustaceans as the main components of their diet. Fish were recognized as a minor dietary component (about 8%). The feeding habits of the recent genus Gonostoma were studied in Gonostoma gracile Gu¨nther, 1878, by Gordon et al. (1985), Kawaguchi (1969), and Uchikawa et al. (2001); in G. elongatum by Lancraft et al. (1988), and they were also mentioned by Guschin (1982). Information about the diet of other species of this genus is lacking. The dominant foods of G. gracile from the Pacific coast of Hokkaido are euphausiids and copepods (Ostracoda and Mysidacea were rarely identified; Gordon et al., 1985). Kawaguchi (1969) examined 216 specimens of G. gracile from the Kuroshio Area and Suruga Bay (North-western Pacific Ocean), and among the recognized preys are: copepods, euphasiids, amphipods, mysids, chaetognaths, and rarely fishes; informational details on the types or sizes of the fish preys was not provided. Copepods and ostracods dominated among the prey remains (approximately 70%) in the stomach of G. gracile, of a body length of 19–116 mm (Northwestern North Pacific; Uchikawa et al., 2001). These authors described an ontogenetic dietary shift: the size range of the prey increased with the growth of the fish. The prey of G. elongatum is mainly composed of crustaceans, copepods, and ostracods in the early juvenile stages, and of euphasiids in larger-sized individuals; very rarely is it composed of fish: leptocephalus larvae and other unidentifiable types of fish remains (Lancraft et al., 1988). These authors recognized changes in the diet between different size classes: growing individuals change their prey from copepods and ostracods to mainly euphasiids. In addition, Guschin (1982) mentioned pisces preys found in the digestive tract of two specimens in G. elongatum: in the first specimen (SL 160 mm), the prey was Maurolicus muelleri (Gmelin, 1789), and its length was estimated at about 50 mm; in the second specimen (SL 180 mm), fishes were identified without any more definitive determination. Within 22 specimens of G. denudatum, G. elongatum and G. atlanticum that we examined, only one specimen of G. elongatum was found with prey in the stomach; the others had empty stomachs. The stomach of a fish (SL 190 mm) contains a single euphausiid crustacean, ca. 25 mm in length (from tip of the rostrum to tip of the telson). This prey is headed anteriorly in the stomach (Fig. 5). It can be concluded that Gonostoma is a typical crustacean feeder with an opportunistic connection to the fish prey.
Fig. 5. Gonostoma elongatum Gu¨nther, 1878. Content of digestive tract. Detail of an uncatalogued specimen, SL 190 mm. Scale bar: 10 mm.
(Pi-F/MP/2/1510/08), the body cavity contained ostracods and an unrecognizable type of fish bones (Fig. 6). The ostracods, as well as the fish skull bones, are fragmentarily preserved. The poor preservation of the remains is probably partly caused by the fossilization processes, and partly by digestion. It is highly improbable that the prey were chewed or crushed by the force of the jaw, because this jaw type with long sharp fangs is not functional for the mastication of prey. Furthermore, Gartner et al. (1997) proposed that many mid-water fishes have been shown to be swallowers. Fish skull elements preserved in the abdominal cavity are unusable for a taxonomic determination of the prey, due to their poor state of preservation. Problems with the digested portions, during the study of the feeding habits in recent fishes, where mentioned by Gerking (1994). The five other specimens (Pc 2863, Pi-F/MP/4/1483/08, PIN 4841/64, 66 and 70) contain the remains of teleost fishes. In three cases (Pc 2863, Pi-F/MP/4/1483/08, and PIN 4841/64), the digested fish specimens can be identified as the same species. In the remaining two cases the prey remains are too incomplete or poorly preserved; therefore, they cannot be identified any closer than as Teleostei. In specimens Pc 2863, Pi-F/MP/4/1483/08, and PIN 4841/ 64, prey’s orientation in the predator is with the head anteriorly (Figs. 2(B), 3(B), 4(B)). In the remaining two specimens (PIN 4841/ 66 and 70), the preys are represented only by some separated bones or their fragments; thus, it is not possible to identify this position. However, as the remnants lie in the area of stomach, we can consider that a large part of the digestion process appears in the stomach.
4.2. Probable feeding habits in Scopeloides The study of the preserved anatomic structures of S. glarisianus allows for speculation about the feeding habits of this fossil species. The heavy jaws are the main functional unit for catching, holding, and transporting the prey; the length of the lower jaw is about 70% that of the head length. The structure of the dentition in S. glarisianus was described in detail by Prokofiev (2005a). The presence of fang-like teeth in the jaws clearly shows a predatory feeding modus. We have examined six specimens of S. glarisianus possessing fossilized preys in their alimentary canal. In the first case
Fig. 6. Scopeloides glarisianus (Agassiz, 1844). Content of digestive tract in the abdominal cavity, detail of specimen Pi-F/MP/2/1510/08. Scale bar: 10 mm.
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In specimens Pi-F/MP/4/1483/08 and PIN 4841/64, the caudal portions of the digested fishes are folded backwards, which may indicate that they were caught by their sides, close to the tail, and further that they were folded during swallowing. In contrast to these specimens, the prey’s head orientation is anterior, in a similar way to its caudal extremity in specimen Pc 2863. Apparently, S. glarisianus is a predator which typically swallowed their prey tail-first. The only two taxa of Palaeogene fishes with the prey headed anteriorly were noted by Viohl (1990: table 23); both were from the Italian locality of Monte Bolca (Eocene). The position of the prey inside the predator’s body may well illustrate some interesting information about the types of feeding habits. Hoogland et al. (1957) studied Perca and Esox feeding habits, and found a correlation between the prey’s orientation in the predator’s stomach and the presence of special morphological features (spines) of the prey’s body. L’Abe´e-Lund et al. (1996) showed that Salmo trutta change their feeding behaviour depending on the prey species, size, as well as the number of prey eaten. Boucot (1990) presented the major facts about prey orientation, and briefly discussed the possibility whether the swallowing of the prey headfirst could be a learned behaviour or not. There is no possibility to decide any such significance from the prey position in our case. Our primary focus is on the body of Scopeloides (as the probable congeneric prey), as there are no spines present, which could cause any problems during tail-first swallowing. Based on the examination of G. elongatum with prey in situ, we can conclude that tail-first swallowing is also characteristic for the members of this genus. As Gonostoma are mainly crustacean feeders, this mode of swallowing possibly represents an adaptation to safe swallowing of large crustacean prey, such as euphausiids and mysids for example, which possess the long and sometimes spined antennae, legs, and rostrum, making tail-first swallowing more successful. Despite the probability of stronger connections to the fish prey in Scopeloides compared with Gonostoma (see below), its feeding behaviour retains the general adaptations of the gonostomatids. In this connection, it should be noted that the ichthyophagous predator Holosteus mariae (Menner, 1948) was a head-first swallower, despite the fact that Myctophidae and Argentinidae, its documented preys (Prokofiev, 2005b;
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Fig. 7. Scopeloides glarisianus (Agassiz, 1844). Preserved remains of the peritoneum, detail of the specimen MRV 7620. Scale bar: 10 mm.
Bien´kowska-Wasiluk, 2010), lacked spines or other structures prohibiting tail-first swallowing. The aforementioned specimens of S. glarisianus clearly show the trophic relationship of the vertebrate prey. Furthermore, in at least three specimens the remains of the prey probably represent congeneric specimens. Cannibalistic behaviour has been described in three marine Oligocene fishes within the Carpathian region: Oligoserranoides (syn.: Serranus, Oliganodon) budensis by Pauca˘ (1934) and Bien´kowska-Wasiluk (2010) from Romania and Poland; Anenchelum glarisianum by Prˇikryl and Novosad (2009) from the Czech Republic; and Trachinus minutus by Bien´kowska-Wasiluk (2010) from Poland. The possibility of cannibalistic behaviour in Scopeloides is presented for the first time herein. Moreover, congeneric prey is documented in 50% of cases having the presence of fish preys; however, this ratio could be underestimated as in other cases the remains of the teleost preys cannot be identified more precisely. This may indicate that cannibalism had a rather important role in the feeding behaviour of S. glarisianus. Although the relatively low number of specimens with preserved preys do not allow for the reconstruction of their feeding habits more precisely, on the basis of the above-mentioned specimens the functional anatomy and information on recent relatives make it possible to state that S. glarisianus was a predator consuming crustaceans and fishes. The fishes that made up their prey appear to have attained an SL of over 70 mm, and apparently,
Fig. 8. Scopeloides glarisianus (Agassiz, 1844). A. Juvenile specimen with preserved remains of the peritoneum. B. Detail of (A). C. Adult or subadult specimen with preserved stomach and anterior part of intestine. D. Detail of (C). A, B, specimen Lit2006/44a; C, D, specimen 2007/07. Scale bars: 5 mm.
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individuals had fish preys not only in exceptional cases. Although we cannot estimate the ratio between the invertebrate and vertebrate preys in S. glarisianus (due to the processes of fossilization, invertebrate preys appear to be extremely rarely preserved in fossils), the quite frequent presence of fish preys in the abdominal cavity of S. glarisianus, which even occurs in rather small individuals (70–84 mm SL), indicates a stronger connection with the consumption of fish preys than in the strategy of those representatives of the recent genus Gonostoma (see above). It also seems that Scopeloides becomes ichthyophagous before maturity, which is a characteristic of mainly ichthyophagous predators, as pointed out earlier by Lebedev and Spanovskaya (1983) for asp-like cyprinids, by Tankevitsch et al. (1989) for toothfishes (Dissostichus, Nototheniidae), by Kornilova and Portsev (1989) for cutlassfishes (Trichiuridae), and by Prokofiev and Kukuev (2009) for chiasmodontids. However, it should be noted that the feeding habits are only known for a few species of Gonostoma, and the interspecific differences are still awaited. 4.3. Preservation of soft tissues in Scopeloides A closer examination of S. glarisianus specimens in many collections has shown that the structure described by Kalabis
(1948) as the remains of the stomach cannot be identified with a real oesophagus nor stomach full of food. This is not possible for general anatomical reasons, as in stomiiforms a stomach is an elongate tube with a gently narrowed, pointed, or obtuse posterior tip. The tapering shape, size, position, and marked colour of the dark pigment in many fossil specimens instead apparently indicates the imprints of the peritoneum. This structure is relatively frequently preserved, not only in adults (Fig. 7; Gregorova´, 1989: pl. 7), but also in young individuals (Fig. 8 (A, B)). In all mentioned specimens it originates immediately behind the head, between the vertebral column and a point above the flexion of the cleithrum, tapering and gently declining posteriorly; the caudal tip of this organ is terminated at a level slightly behind (about one vertebra) the end of the pelvic bone. Comparisons with recent Gonostoma (Fig. 9) species shows that the rather constant triangular and tapering shape of this dark zone can be explained by the quite rapid decrease of the height of the abdominal cavity in the post-pelvic portion of the body. In recent fishes we can easily observe almost the same form when we remove the peritoneum from the body wall during preparation (a similar stratification can be expected during decomposition of the dead Scopeloides specimens). It is possible that the terminal
Fig. 9. Gonostoma elongatum Gu¨nther, 1878. A. Digestive tract and associated structures in abdominal cavity; uncatalogued specimen, SL 205 mm. B. Prepared digestive tract in outer view; uncatalogued specimen, SL 210 mm. C. Same specimen as in (B) but in inner view. D. Digestive tract and associated structures in abdominal cavity with prey preserved in situ; uncatalogued specimen, SL 190 mm. Scale bars: 10 mm.
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ending of the peritoneum is not preserved, as it can become too thin during the decomposing process. A true imprint of the fish’s alimentary canal is only exceptionally preserved in fossils (e.g., Zhang and Jin, 2003: text-fig. 96). This rare situation is observed in specimen 2007/07, in which the greater part of the digestive duct is preserved (Fig. 8(C, D)). The digestive tract is obviously empty, but the anatomical position of its anterior part is clearly recognizable. The oesophagus is not recognizable due to the covering of bones of the opercular series and the pectoral girdle, but is apparently short. The stomach is in an almost horizontal position, and it expands to the eighth rib. Its dorsal contour is somewhat concave at the level between the second and third rib, which may indicate the position of the pylorus, and a border between the anterior and posterior (caecal) portions of the stomach. The tip of the caecal part of the stomach is bluntly rounded. The beginning of the intestine is well preserved along the ventral contour of the caecal portion of the stomach, but its posterior portion cannot be reconstructed. In contrast to the very well preserved alimentary canal, the liver is not preserved. The shape of the stomach can also be reconstructed on the basis of specimen Pc 2863, where slightly darker stripes than the surrounding sediment are preserved; these are probably remnants of the caecal part of the stomach (Fig. 3(C)). The wall of this part of the stomach was relatively thick and probably elastic. The remains of dark pigmentation could indicate that the walls of the stomach were darkly pigmented, similar to various recent deep-water teleost taxa, like many stomiiforms (see below), some lizardfishes (Prokofiev, 2006), deep-sea eels (Fishelson, 1994), or cardinal fishes (Fishelson et al., 1997). This characteristic in recent fishes is supposed to be an adaptation to prevent bioluminescence for illuminating the predator, if a bioluminescent prey fish is swallowed (Fishelson, 1994). The darkly coloured peritoneum probably has a similar function. In recent Gonostoma species, the oesophagus is a very short and rather broad tube lying under the basioccipital bone, and between the pectoral-fin girdles. It is separated from the stomach by a clearly marked constriction, indicating the oesophagus-gastric sphincter. The stomach is an elongate tube with thick muscular walls. The dorsal contour of the stomach is indistinctly concave at mid-length; on the ventral surface the pylorus is separated. The posterior portion of the stomach is caecal, with a pointed or bluntly rounded distal tip. In most of the examined specimens, the length of the stomach is about one-half of the P-V distance, rarely slightly longer (about two-thirds of P-V). The pyloric caeca are not numerous, moderately large, elongate, and finger-like. The colour of the peritoneum is dark brown to blackish; the oesophagus and stomach (including pylorus) are jet-black; and the pyloric caeca and intestine are yellowish or white. The walls of the intestine sometimes have the aggregations of greyish and blackish melanophores on some portion of them. The liver is rather small, consists of two lobes, in which the inner lobe is always smaller than the outer ones; lobes with a more or less distinct incision along their posterior margin are much better developed in the outer lobe. The length of the outer lobe of liver is (usually) about one-quarter to one-third of the stomach length. The intestine is nearly straight, and the anus is located not far in front of the analfin origin (distance between anus and anal-fin origin is 20–25% of the P-V distance). The same configuration and colouration of the viscera is observed in Phosichthys; while in Diplophos the viscera have a similar size and structure, but all parts of the alimentary duct are light in colour. Within the representatives of the closely related family Sternoptychidae, the pigmentation of the various parts of the alimentary canal are variable within the species (Parin and Kobyliansky, 1993). Additionally, the colour of the peritoneum can be variable within the species of the recent phosichthyid genus
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Polymetme (Parin and Borodulina, 1991). We also checked two specimens of the deep-water family Stomiidae. Both Astronesthes similis and Stomias lampropeltis have the same general plan of structure and colouration of the viscera as described above for the Gonostoma spp.; however, the stomach is much more elongated (especially in Stomias), which corresponds with the markedly elongated abdominal region. Thus, the structure of the viscera observable in S. glarisianus is almost the same as in recent members of the genus Gonostoma, and shows the general plan characteristic for all stomiiforms. 5. Conclusions The probable feeding habits of S. glarisianus are briefly sketched on the basis of the studied specimens from the Russia, Ukraine, Poland, and the Czech Republic. On the basis of the preserved preys within the alimentary-canal, S. glarisianus appears as predatory fish with a dietary connection to crustaceans and fishes, similar to recent relatives of the genus Gonostoma, although an ichthyophagous predation seems to be more characteristic for Scopeloides, in contrast with Gonostoma. The fish preys appear in individuals of 70–75 mm SL. Cannibalistic behaviour is proposed for the first time. All identified fish remains in the alimentary canal belong to the same species. The preserved soft tissues also allow for a brief discussion of some anatomical and eco-morphological features. Acknowledgments We are grateful to M. Pozˇa´r and K. Pavelka for access to the MRV collection; to B. Ekrt (NMP) for access to the specimen under his care; to N. Kubricky and P.R. Lemkin who kindly made linguistic improvements; to D.A. Astakhov for assistance in the photographing of recent specimens; to G. Escarguel for his valuable notes; and finally to the reviewers A.M. Murray and G. Carnevale for their comments, which improved the quality of the manuscript. This work was supported by institutional project AVOZ30130516 of the Institute of Geology AS CR, v.v.i. References Agassiz, L., 1833–1844. Recherches sur les poissons fossiles. Petitpierre, Neuchaˆtel. Arambourg, C., 1967. Re´sultats scientifiques de la mission C. Arambourg en Syrie et en Iran (1938–1939). II : Les Poissons oligoce`ne de l’Iran. Notes et Me´moires sur le Moyen-Orient 8, 11–210. Bien´kowska-Wasiluk, M., 2010. Taphonomy of Oligocene teleost fishes from the Outer Carpathians of Poland. Acta Geologica Polonica 60, 479–533. Boucot, A.J., Ed. 1990. Evolutionary paleobiology of behavior and coevolution. Elsevier, London. Carnevale, G., 2002. A new barbeled dragonfish (Teleostei: Stomiiformes: Stomiidae) from the Miocene of Torricella Peligna, Italy: Abruzzoichthys erminioi gen. and sp. nov. Eclogae geologicae Helvetiae 95, 471–479. Carnevale, G., 2008. Miniature deep-sea hatchetfish (Teleostei: Stomiiformes) from the Miocene of Italy. Geological Magazine 145, 73–84. Case, G.R., 1982. A pictorial guide to fossils. Van Nostrand Co, New York. Ciobanu, M., 1977. Fauna fosila˘ din Oligocenul de la Piatra Neamt¸. Editura Academiei Republicii Socialiste Romaˆnia, Bucuresti. Crane, J.M., 1966. Late Tertiary radiation of viperfishes (Chauliodontidae) based on a comparison of recent and Miocene species. Los Angeles County Museum of Natural History, Contributions in Science 115, 1–29. Daniltshenko, P.G., 1960. Bony Fish from Maikop Deposits in the Caucasus. Trudy Paleontologicheskogo Instituta AN SSSR 78, 1–208 (in Russian). Fink, W.L., Weitzman, S.H., 1982. Relationships of the stomiiform fishes (Teleostei), with a description of Diplophos. Bulletin of the Museum of Comparative Zoology 150, 31–93. Fishelson, L., 1994. Comparative internal morphology of deep-sea eels, with particular emphasis on gonads and gut structure. Journal of Fish Biology 44, 75– 101. Fishelson, L., Goren, M., Gon, O., 1997. Black gut phenomenon in cardinal fishes (Apogonidae, Teleostei). Marine Ecology Progress Series 161, 295–298. Gartner Jr., J.V., Crabtree, R.E., Sulak, K.J., 1997. Feeding at depth. In: Randall, D.J., Farrell, A.P. (Eds.), Deep-Sea Fishes. Academic Press, San Diego, pp. 115–193. Gerking, S.D., 1994. Feeding Ecology of Fish. Academic Press, San Diego.
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