◄ Carnets Geol. 24 (8) ►
Outline:
[1. Introduction]
[2. Material and methods]
[3. Geological background]
[4. Systematic vertebrate paleontology]
[5. Discussion and conclusions]
and ...
[Bibliographic references]
Museo Geologico "G. Cortesi", Via Sforza Caolzio,
57, 29014 Castell'Arquato, Piacenza (Italy)
Via Azzolini 12, Lesignano de Bagni, Parma (Italy)
Published online in final form (pdf) on July 24, 2024
DOI 10.2110/carnets.2024.2408
[Editor:
: Alberto Collareta; language editor: Stephen Carey;
technical editor: Bruno R.C. Granier]
We describe and analyze a rib fragment of a small cetacean from the Castell'Arquato Plio-Pleistocene Basin (Northern Apennines, Italy) that displays various tooth marks featuring parallel striations similar to those left by the serrated tooth of the extant white shark, Carcharodon carcharias. The discovery locality, known as "Buca della Balena", was an inner-shelf marine setting where sharks may have scavenged on drifting cetacean carcasses in Piacenzian times. The high number of marks found on the small bone fragment suggests multiple bites by one or more shark individuals. The rib fragment studied is one of the few osteological specimens from the Pliocene of the Mediterranean Basin to preserve white shark tooth marks.
• Pliocene;
• Piacenzian;
• Cetacea;
• Carcharodon
carcharias;
• great white shark;
• tooth marks;
• Castell'Arquato;
• Northern
Apennines
Freschi A. & Cau S. (2024).- Tooth marks of the Great White Shark from a Pliocene outcrop of the Northern Apennines (Castell'Arquato, Italy).- Carnets Geol., Madrid, vol. 24, no. 8, p. 135-141.
Traces de morsures de grand requin blanc provenant d'un affleurement pliocène des Apennins du Nord (Castell'Arquato, Italie).- Nous décrivons et analysons un fragment de côte d'un petit cétacé du bassin plio-pléistocène de Castell'Arquato (Apennins du Nord, Italie). Ce fragment présente diverses traces de morsures avec des stries parallèles similaires à celles laissées par la dent crénelée du grand requin blanc actuel, Carcharodon carcharias. Le site de la découverte, connu sous le nom de "Buca della Balena", est localisé dans la partie interne d'un plateau sous-marin où, au cours du Plaisancien, les requins pouvaient se nourrir de carcasses dérivantes de cétacés. Le grand nombre de marques relevées sur ce petit fragment d'os suggère de multiples morsures par un ou plusieurs individus. Le fragment de côte étudié est l'un des rares spécimens ostéologiques du Pliocène du bassin méditerranéen à conserver de telles marques de dents de grand requin blanc.
• Pliocène ;
• Plaisancien ;
• cétacés ;
• Carcharodon carcharias ;
• grand requin blanc ;
• marques de dents ;
• Castell'Arquato ;
• Apennins du Nord
Fossil evidence for the ancient trophic interactions between white sharks (Carcharodon carcharias Linnaeus, 1758) or other shark species (e.g., Cosmopolitodus hastalis) and large marine mammals is mostly represented by tooth marks on bone. These ichnofossils result from the impact of the shark teeth on the skeletal elements of prey or scavenged items (Jacobsen & Bromley, 2009; Pirrone et al., 2014; Collareta et al., 2017; Freschi, 2017; Zonneveld et al., 2022). In the case of the white shark, Carcharodon carcharias (Linnaeus, 1758), the tooth marks display a characteristic outline due to the marginally serrated tooth edges that produce parallel grooves on the bitten bones (Cigala-Fulgosi, 1990). To date, the fossil record of the Pliocene basins of the Mediterranean region has provided a few examples of trophic interaction between white sharks and cetaceans in which tooth marks are present (e.g., Bianucci et al., 2000; Bisconti, 2008).
This article describes some white shark tooth marks that were found on a single rib fragment of a small cetacean from the Pliocene of the North Apennines. This rib fragment has been mentioned by Cigala-Fulgosi (1990) and then figured by Collareta et al. (2023a: Fig. 5.C-D); however, it has only been described at some length in a conference paper in Italian (Freschi & Cau, 2020), hence our more complete characterization herein.
We describe the traces and assign a tooth-mark type based on the terminology proposed by Cigala-Fulgosi (1990) and subsequent studies (Bianucci et al., 2010; Collareta et al., 2017). The tooth marks are thus divided into five morphological-genetic types:
Type I: The tooth completely penetrates the bone, leaving a single, clean cut perpendicular to the bone;
Type II: The tooth penetrates the bone and then moves in a sawing fashion, producing a cut with light, jagged marks;
Type III: The tooth strikes the bone and then drags straight across the surface of the bone, producing shallow, parallel striae;
Type IV: The tooth strikes the bone and then drags in an undulating manner across the surface, producing shallow, wavy, parallel marks;
Type V: The tooth penetrates deep into the bone and carves out a prismatic or wedge-shaped indentation.
The fossil specimen described herein was found at the 'Buca
della Balena' locality (hereinafter, BDB), in the vicinity of the Osteria di
Montezago (GPS coordinates: 44°50'00"N,
9°46'58"E) (Fig. 1 
). The BDB section is 55
meters thick and consists of inner-shelf deposits of the Castell'Arquato
Plio-Pleistocene Basin (Roveri & Taviani,
2003).
These deposits are part of the Upper Pliocene (Piacenzian) Montezago Superiore
Unit (Freschi et al., 2019, and references therein) (Fig.
1.B-C ).
The BDB section shows a rhythmic alternation of ten depositional cycles, each of
which is 1–5 meters thick (Fig. 1.D ). These cycles are formed by hemicycles of
fine sandstone containing scarce macrobenthic fossils and poorly cemented
biocalcarenite hemicycles of coarse sandstone that are rich in skeletal remains
of macrobenthos. The bioclasts are unorganized and display abrasion and/or
bioencrustation by bryozoans and cirripedes. The presence of Discoaster
tamalis throughout the section indicates that the geological age of the BDB
section is within the 3.40–3.10 Ma time interval (Cau et al.,
2019, 2020; Freschi
et al., 2019).
|
Figure 1:
Geographical, stratigraphical, and lithological information of the Buca della
Balena (BDB) outcrop. A) Geographical position of the BDB fossiliferous locality
in Piacenza province (Italy); B) field photographs and corresponding line
drawings of the upper part of the section, featuring ten distinct
biocalcarenitic horizons; C) stratigraphic log of the BDB locality. Numbers in
panels B and C identify the ten biocalcarenitic horizons. PS = sandy pelites; SF
= fine sands; SM = medium sands. |
Order: CETACEA Brisson, 1762
Cetacea indet.
(Fig.
2 )
Referred material: VT0173, a rib fragment found at the 'Buca della Balena' locality, in the vicinity of the Osteria di Montezago. VT0173 is currently stored in the "G. Cortesi" Geological Museum in Castell'Arquato (Piacenza Province, Italy).
Description: The specimen is a medial rib fragment. It is 72 mm long and about 15 mm in maximum diameter, with an elliptical cross-section. The external surface of the bone is well preserved. The outer, compact bone is relatively thick, but the rib is neither osteosclerotic nor pachyostotic. Although a taxonomic assignment to any specific marine mammal taxon is difficult, we can exclude the sirenians based on their bone characteristics, and the pinnipeds based on the shape and overall size of the fragment. Owing to these observations, VT0173 is classified herein as belonging to a small, indeterminate cetacean.
Descriptive ichnology: Marks of various shapes and lengths
are visible on the rib fragment. Six such marks are located on the dorsal
surface of the rib, and another is located on the ventral central surface of the
rib (Fig. 2.A ). The incisions range from 5 to 29 mm in length and are often
associated with parallel streaks with spacings of about 0.5-1 mm. Four 'V-shaped',
type II incisions are prominent (Fig. 2.B ). One is particularly long and is
incised deeply into the bone ; its internal surface is scored with light,
parallel streaks (Fig. 2.C-D ). Near the anterior margin of the rib, type III and
IV surficial marks with deep, parallel grooves are also present (Fig.
2.D-E ). A
shallow type I mark occurs on the posterior margin of the rib (Fig.
2.A ).
Several type II marks are characterized by crenulations of the inner surface.
The edges of five type II marks are irregular and indicate the detachment of
small bone splinters caused by the impact of the tooth (Fig.
2.B ). The
'V-shaped'
marks are especially deep and cluster on the surface of the bone, exhibiting
both concave and convex morphologies.
|
Figure 2:
VT0173,
tooth-mark-bearing rib fragment of Cetacea indet. from the Buca della Balena
locality. A) The rib fragment in dorsal and ventral views (arrows indicate the
tooth marks); B) four different type II tooth marks; C) close-up of some clearly
serrated tooth marks; D) two tooth marks belonging to types III and IV; E) type
IV. Different tooth marks are identified by different lowercase letters. Scale
bars measure 10 mm. |
The tooth marks described in this study are interpreted to be the result of the bite of a selachian predator or scavenger. On the basis of morphological and dimensional considerations, the parallel grooves evident on the bone fragment studied indicate production by the large, coarsely serrated teeth of the white shark, Carcharodon carcharias (see also Cigala-Fulgosi, 1990; Jacobsen & Bromley, 2009; Schouten, 2017). From an ichnotaxonomic viewpoint (Jacobsen & Bromley, 2009), such tooth marks can be classified within the ichnogenus Linichnus, and specifically as Linichnus serratus.
The Piacenzian marine setting reflected by the BDB succession was offshore and neritic (Cau et al., 2019, 2020; Freschi et al., 2019). Thus, the BDB palaeoenvironment may have been: 1) frequented by white sharks (Chapple et al., 2011; Jorgensen et al., 2012) as well as by cetaceans (including both odontocetes and mysticetes), and 2) characterized by the transport and/or deposition of cetacean carcasses (Dominici et al., 2020; Moore et al., 2020). This scenario suggests that scavenging activity by mammalophagous sharks was likely to occur (Klimley, 1994; Long & Jones, 1996; Bianucci et al., 2010; Fallows et al., 2013; Collareta et al., 2017; Tucker et al., 2019).
Although VT0173 consists only of a small rib fragment, it exhibits several tooth marks. Similar traces have also been observed on more complete fossil cetacean skeletons, where more than ten tooth marks have been locally observed on a single rib (Cigala-Fulgosi, 1990; Bianucci et al., 2010). The rib from the BDB locality displays a high number of tooth marks with different orientations, which could indicate that the abdomen of the cetacean was bitten multiple times by one or more white sharks (Lea et al., 2018). The abdominal region of a small cetacean is the most voluminous part of the animal – one that comprises layers of fat, internal organs, and muscles (Litchfield et al., 1974). As scavengers, white sharks famously feed by drawing on highly nutritious food sources with minimal effort (Heithaus, 2004; Benites-Palomino, 2022).
white shark tooth marks are relatively rare compared to the abundance of cetacean finds from the Pliocene epoch, during which Carcharodon carcharias spread worldwide (Leone et al., 2020). In the Mediterranean Basin, only two other finds of fossil cetacean bones with tooth marks have been described so far, both originating from the Pliocene. The first consists of bite marks on the ulna of Eschrichtioides gastaldii (Bisconti, 2008; see also Portis, 1883) from the "Sabbie Gialle Astigiane" of Piedmont. The second such find is an almost complete skeleton belonging to Hemisyntrachelus cortesii (Del Prato, 1897; Bianucci, 1996), which was described in great detail by Cigala-Fulgosi (1990). This specimen, where 80 different white shark tooth marks were observed, was discovered at the Rio Stramonte locality, a few hundred meters from the BDB section.
Several bone fragments incised by white shark tooth marks have been documented from the southern Atlantic. Govender and Chinsamy (2013) and Govender (2015, 2019) reported on 14 fragmentary cetacean specimens showing abundant evidence of predation or scavenging from the South African Cape Basin. The concentration of discoveries in this specific area along the southeastern Atlantic coast suggests that white shark populations in the Cape Basin were abundant and engaged in the predation of marine mammals as early as Pliocene times.
Two additional discoveries from the northeastern and central-eastern Pacific margins contribute to the understanding of white shark tooth marks on fossil cetacean remains. Deméré and Cerutti (1982) described tooth marks attributed to a great white shark on a posterior portion of the mandibular ramus of a specimen of Herpetocetus, a small (~5 m long) baleen whale, from the San Diego Formation of California (Eastern USA). Cortés et al. (2019) documented remains of a fossil whale from Panama, specifically appendicular remains of a baleen whale belonging to the family Balaenopteridae. These remains were recovered from the sediments of the Upper Pliocene Burica Formation and, according to Cortés et al. (2019), they exhibit two distinct types of shark tooth marks on the whale forelimb bones, indicating scavenging activity by at least two great white shark individuals.
Continued research on white shark tooth marks contributes significantly to our knowledge of the paleoecology and distribution of this iconic shark species during the Neogene period. The roughly coeval appearance of teeth and tooth marks from different oceanic regions underscores the rapid dispersal of Carcharodon carcharias (Collareta et al., 2023a, 2023b). This dispersal was likely facilitated by the gradual disappearance and extinction of the megatoothed shark, Otodus megalodon, reducing ecological competition, and by favorable climatic conditions established around 3 million years ago that supported this cosmopolitan top predator (Ehret et al., 2012).
Special thanks are extended to Gianni Tagliaferri for discovering the specimen described in this work, and to Carlo Francou (Museo Geologico "G. Cortesi") for facilitating its study. Acknowledgments also go to Aldo Marcelo Benites-Palomino (University of Zürich) and Marco Merella (University of Pisa) for their valuable revisions of an early manuscript version that enhanced the significance of this research. Additionally, gratitude is expressed to Alberto Collareta (University of Pisa) for providing constructive feedback that improved the text, to Lesley McBride for language revision, and to Girolamo Lo Russo (Museo Civico di Storia Naturale di Piacenza) for outstanding photographs of the specimen.
Benites-Palomino A., Velez-Juarbe J., Altamirano-Sierra A., Collareta A., Carrillo-Briceño J.D. & Urbina M. (2022).- Sperm whales (Physeteroidea) from the Pisco Formation, Peru, and their trophic role as fat sources for late Miocene sharks.- Proceedings of the Royal Society B, vol. 289, no. 1977, 8 p.
Bianucci G. (1996).- The Odontoceti (Mammalia, Cetacea) from Italian Pliocene. Systematics and phylogenesis of Delphinidae.- Palaeontographia Italica, Pisa, vol. 83, p. 73-197.
Bianucci G., Bisconti M., Landini W., Storai T., Zuffa M., Giuliani S. & Mojetta A. (2000).- Trophic interaction between white shark, Carcharodon carcharias, and cetaceans: A comparison between Pliocene and recent data from central Mediterranean Sea. In: Vacci M., La Mesa G., Serena F. & Séret B. (eds.), 4th meeting of the European Elasmobranch Association, Livorno (Italy), 2000.- Proceedings, ICRAM, ARPAT & SFI, p. 33-48.
Bianucci G., Sorce B., Storai T. & Landini W. (2010).- Killing in the Pliocene: Shark attack on a dolphin from Italy.- Palaeontology, vol. 53, no. 2, p. 457-470.
Bisconti M. (2008).- Morphology and phylogenetic relationships of a new eschrichtiid genus (Cetacea: Mysticeti) from the Early Pliocene of northern Italy.- Zoological Journal of the Linnean Society, London, vol. 153, p. 161–186
Cau S., Laini A., Monegatti P., Roveri M., Scarponi D. & Taviani M. (2019).- Palaeocological anatomy of shallow-water Plio-Pleistocene biocalcarenites (northern Apennines, Italy).- Palæogeography, Palæoclimatology, Palæoecology, vol. 514, p. 838-851.
Cau S., Roveri M. & Taviani M. (2020).- Palaeobiology of Pliocene-Pleistocene shallow-water biocalcarenites (Northern Apennines, Italy) and their relationship with coeval sapropels.- Bollettino della Società Paleontologica Italiana, Modena, vol. 59, no. 1, p. 26.
Chapple T.K., Jorgensen S.J., Anderson S.D., Kanive P. E., Klimley A.P., Botsford L.W. & Block B.A. (2011).- A first estimate of white shark, Carcharodon carcharias, abundance off central California.- Biology Letters, London, vol. 7, no. 4, p. 581-583.
Cigala-Fulgosi F. (1990).- Predation (or possible scavenging) by a great white shark on an extinct species of bottlenose dolphin in the Italian Pliocene. - Tertiary Research, Leiden, vol. 12, no. 1, p. 17-36.
Collareta A., Casati S., Di Cencio A. & Bianucci G. (2023a).- The deep past of the white shark, Carcharodon carcharias, in the Mediterranean Sea: A synthesis of its palaeobiology and palaeoecology.- Life, Basel, vol. 13, no. 10, article 2085, 16 p.
Collareta A., Casati S., Di Cencio A. & Bianucci G. (2023b).- Quaternary records of Carcharodon carcharias (Linnaeus, 1758) in Tuscany (central Italy): Implications for the palaeobiology of Mediterranean white sharks. Neues Jahrbuch für Geologie und Paläontologie, Abhandlungen, Stuttgart, vol. 309, p. 65-76.
Collareta A., Lambert O., Landini W., Di Celma C., Malinverno E., Varas-Malca R., Urbina M. & Bianucci G. (2017).- Did the giant extinct shark Carcharocles megalodon target small prey? Bite marks on marine mammal remains from the late Miocene of Peru.- Palæogeography, Palæoclimatology, Palæoecology, vol. 469, p. 84-91.
Cortés D., De Gracia C., Carrillo-Briceño J.D., Aguirre-Fernández G., Jaramillo C., Benites-Palomino A. & Atencio-Araúz J.E. (2019).- Shark-cetacean trophic interactions during the late Pliocene in the Central Eastern Pacific (Panama).- Palaeontologia Electronica, Amherst - MA, vol. 22, no. 2, p. 1-13. DOI: 10.26879/953
Del Prato A. (1897).- Il Tursiops Capellini Sacco del Pliocene piacentino.- Palaeontographia Italica, Pisa, vol. 3, p. 1-14.
Demere T.A. & Cerutti R.A. (1982).- A Pliocene shark attack on a cethotheriid whale.- Journal of Paleontology, Cambridge (UK), vol. 56, p. 1480-1482.
Dominici S., Danise S., Cau S. & Freschi A. (2020).- The awkward record of fossil whales.- Earth-Science Reviews, vol. 205, article 103057, 20 p.
Ehret D.J., Macfadden B.J., Jones D.S., Devries T.J., Foster D.A. & Salas-Rismondi R. (2012).- Origin of the white shark Carcharodon (Lamniformes: Lamnidae) based on recalibration of the upper Neogene Pisco Formation of Peru.- Palaeontology, vol. 55. no. 6, p. 1139-1153.
Fallows C., Gallagher A.J. & Hammerschlag N. (2013).- White sharks (Carcharodon carcharias) scavenging on whales and its potential role in further shaping the ecology of an apex predator.- PLoS ONE, vol. 8., no. 4, article e60797, 10 p.
Freschi A. (2017).- New Carcharodon scavenging evidence on Pliocene whale bones remains from Northern Apennines.- Quaderni del Museo Civico di Storia Naturale di Ferrara, Ferrara, vol. 5, p. 33-36.
Freschi A. & Cau S. (2020).- New trophic interaction between Carcharodon carcharias and an odontocete in the Castell'Arquato Plio-Pleistocene Basin (Piacenza, Northern Apennines).- Parva Naturalia, Piacenza, vol. 15, p. 133–156.
Freschi A., Cau S., Monegatti P. & Roveri M. (2019).- Chronostratigraphic distribution of cetaceans in the Pliocene of Northern Apennines (Italy): Palaeoecological implications.- Palæogeography, Palæoclimatology, Palæoecology, vol. 526, p. 13-27.
Govender R. (2015).- Shark-cetacean trophic interaction, Duinefontein, Koeberg (5 Ma), South Africa.- South African Journal of Science, Pretoria, vol. 111, no. 11-12, p. 1-7.
Govender R. (2019).- Early Pliocene fossil cetaceans from Hondeklip Bay, Namaqualand, South Africa.- Historical Biology, vol. 33, no. 4, p. 574-593.
Govender R. & Chinsamy A. (2013).- Early Pliocene (5 Ma) shark-cetacean trophic interaction from Langebaanweg, western coast of South Africa.- Palaios, Lawrence – KS, vol. 28, no. 5, p. 270-277.
Heithaus M.R. (2004).- Predator–prey interactions. In: Carrier J.C., Simpfendorfer C.A., Heithaus M.R. & Yopak K.E. (eds.), Biology of sharks and their relatives.- CRC Press, Boca Raton, p. 487–521.
Jacobsen A.R. & Bromley R.G. (2009).- New ichnotaxa based on tooth impressions on dinosaur and whale bones.- Geological Quarterly, Warsaw, vol. 53, no. 4, p. 373-382.
Jorgensen S.J., Arnoldi N.S., Estess E.E., Chapple T.K., Rückert M., Anderson S.D. & Block B.A. (2012).- Eating or meeting? Cluster analysis reveals intricacies of white shark (Carcharodon carcharias) migration and offshore behavior.- PloS ONE, vol. 7, no. 10, article e47819, 10 p.
Klimley A.P. (1994).- The predatory behavior of the white shark.- American Scientist, New Haven, vol. 82, p. 122–133.
Lea J., Daly R., Leon C., Daly C. & Clarke C. (2018).- Life after death: Behavior of multiple shark species scavenging a whale carcass.- Marine and Freshwater Research, Clayton, vol. 70, p. 302–306.
Leone A., Puncher G.N., Ferretti F., Sperone E., Tripepi S., Micarelli P., Garibaldi F., Bressi N., Dall'Asta A., Minelli D., Cilli E., Vanni S., Serena F., Diaz-Jaimes P., Baele G., Cariani A. & Tinti F. (2020).- Pliocene colonization of the Mediterranean by great white shark inferred from fossil records, historical jaws, phylogeographic and divergence time analyses.- Journal of Biogeography, vol. 47, no. 5, p. 1119-1129.
Litchfield C., Greenberg A.J., Caldwell D.K., Caldwell M.C, Sipos J.C. & Ackman R.G. (1975).- Comparative lipid patterns in acoustical and nonacoustical fatty tissues of dolphins, porpoises and toothed whales.- Comparative Biochemistry and Physiology Part B, vol. 50, p. 591–597.
Long D.J. & Jones R.E. (1996).- White shark predation and scavenging on cetaceans in the eastern North Pacific Ocean. In: Klimley A.P. & Ainley D.G. (eds.), Great white sharks: The biology of Carcharodon carcharias.- Academic Press, San Diego, p. 293-307.
Moore M.J., Mitchell G.H., Rowles T.K. & Early G. (2020).- Dead cetacean? Beach, bloat, float, sink.- Frontiers in Marine Science, vol. 7, article 333, 6 p.
Pirrone C.A., Buatois L.A., Bromley R.G. (2014).- Ichnotaxobases for bioerosion trace fossils in bones.- Journal of Paleontology, Cambridge (UK), vol. 88, on. 1, p. 195-203.
Portis A. (1883).- Nuovi studi sulle tracce attribuite all'uomo pliocenico.- Memorie Regia Accademia delle Scienze di Torino, vol. 35, p. 3-27.
Roveri M. & Taviani M. (2003).- Calcarenite and sapropel deposition in the Mediterranean Pliocene: Shallow- and deep-water record of astronomically driven climatic events.- Terra Nova, vol. 15, no. 4, p. 279-286.
Schouten S. (2017).- De witte haai (Carcharodon carcharias Linnaeus, 1758) in het (Vroeg) Holoceen van de Noordzee?- Cranium, Leiden, vol. 34, no. 1, p. 68-73.
Tucker J.P., Vercoe B., Santos I.R., Dujmovic M. & Butcher P.A. (2019).- Whale carcass scavenging by sharks.- Global Ecology and Conservation, vol. 19, article e00655, 11 p.
Zonneveld J.P., Fiorillo A.R., Hasiotis S. & Gingras M.K. (2022).- Tooth marks, gnaw marks, claw-marks, bite marks, scratch marks, etc.: Terminology in ichnology.- Ichnos, vol. 29, no. 2, p. 93-101.
