Trophic interaction between white shark (Carcharodon carcharias

Trophic interaction between white shark (Carcharodon
carcharias) and cetaceans: a comparison between Plioceene
and Recent data from central Mediterranean Sea
Giovanni Bianucci (1), Michelangelo Bisconti (1), Walter Landini (1), Tiziano Storai
(2), Marco Zuffa (3), Silvia Giuliani (4), Angelo Mojetta (5)
(1)
Dipartimento di Scienze della Terra, Università di Pisa, via Santa Maria 53,
56126, Pisa (Italy). E-mail: [email protected]; [email protected];
[email protected].
(2)
Museo Civico di Scienze Naturali della Valdinievole, P.zza Leonardo da Vinci
1, 51017, Pescia, Pistoia (Italy). E-mail: [email protected].
(3)
Museo "Luigi Donini", Via F.lli Canova 49, 40068, San Lazzaro di Savena,
Bologna (Italy).
(4)
C.I.B.M. Centro Interuniversitario di Biologia Marina, Piazzale Mascagni 1,
57100, Livorno (Italy).
(5)
Civica Stazione Idrobiologica e Acquario di Milano, viale Gadio 2, 20121,
Milano (Italy). E- mail: [email protected].
1
Abstract
Evidences of white shark-cetacean trophic interactions from Pliocene and Recent central
Mediterranean Sea are examined. The analysis of Recent data (stomach content reports,
eyewitnesses' depositions about predation on living cetaceans and scavenging signs on
the carcasses) shows that cetaceans represent a significant component of the diet of
Carcharodon carcharias. Fossil evidences (cetacean bones marked by white shark bites
and white shark teeth in close relation with skeletal remains of cetaceans) suggest
sharks-cetaceans trophic interaction in the Pliocene too. A comparison between Recent
and fossil data lets us presume that in the Pliocene both Mysticeti and Odontoceti were
equally represented in the Carcharodon carcharias diet. On the contrary in the Recent
the white shark interaction is principally directed to little-sized toothed whales and just
rarely to mysticetes baleen whales. This change could be due to both the general
reduction of the living white shark body size and the diminished diversity of the
cetacean assemblage.
Key words
White sharks, Cetaceans, Mediterranean Sea, Pliocene, Recent, Trophic interactions.
Introduction
2
Predation events on cetaceans are principally due to white sharks (Carcharodon
carcharias) and killer whales (Orcinus orca) (Tomilin, 1967; Philo et al., 1993). The
interactions between predators and preys are not completely cleared by behavioural
studies and a pacific coexistence of both is sometimes recorded (Tomilin, 1967). In
general, white sharks attack preferably toothed whales (Slipp and Wilke, 1953; Day and
Fisher, 1954; Arnold, 1972; Corkeron et al., 1987; Cockcroft et al., 1989; Cliff et al.,
1989; Long, 1991; Bruce, 1992; Long and Jones, 1996) while the interaction with
baleen whales is limited to scavenging actions (Long and Jones, 1996).
The whale population of the Mediterranean Sea is formed by several species of toothed
whales and essentially one gigantic baleen whale (the fin whale: Balaenoptera
physalus). Other mysticetes are occasionarily observed. Some authors reported that the
Mediterranean whales are sometimes engaged in predatory interactions due to white
sharks (Cigala-Fulgosi, 1990; Fergusson, 1996; Mojetta et al., 1997). The fossil record
relative to the time interval between about 5 to 1.6 million years (spanning to the
Pliocene time) suggests that this trophic relationship could be relatively old.
Carcharodon carcharias fossil remains consist primarily of teeth that are frequently
found in the Pliocene outcrops of the Italian peninsula. They are sometimes found in
direct association to whale remains suggesting ancient interactions. Cigala-Fulgosi
(1990) described in great detail the bite marks made by a white shark on a Pliocene
dolphin providing an experimental paradygm to diagnosize white shark bites on fossil
bones in absence of shark's teeth. His work supplements the initial attempt by Deméré
and Cerutti (1982) that documents a white shark attack on a little late Pliocene
mysticete. Other reports are older and involve both mysticetes and odontocetes of Italy
(Portis, 1883) and Southern Argentine (Frenguelli, 1928). Purdy (1996) extends the
likelihood of direct interactions analyzing the contemporaneous presence of white shark
3
teeth and cetacean remains in North Atlantic geological formations characterized by
both reduced temporal and areal extension.
In this work, a new analysis of fossil cetaceans is carried out to search clues of
interactions with white sharks in the Pliocene time. The study was made in the light of
the current evidence about Carcharodon carcharias predation on Mediterranean
whales. A comparison between Recent and Pliocene data was made to hypothesize
possible changes in the diet of the white shark in the last five million years.
Materials and methods
Recent data
Several kinds of sources were employed to gather evidences on the interactions between
white sharks and cetaceans in the living population of the central Mediterranean Sea: a)
scientific publications; b) non-specialistic publications on newspapers and other
journals; c) communications by eyewitnesses. In general, the likelihood of the data
obtained by scientific publications (point a) is considered high; about the likelihood of
the data obtained by sources as those in points b and c, here, just some informations
were considered useful for the investigation. These are the ones that were supported by
evidence as photographies, multiple verifications and expertise of the witnesses.
Pliocene data
Informations on interactions between Pliocene white sharks and cetaceans were
obtained by analysis of both literature and skeletal remains. Three criteria were chosen
to evaluate the grade of likelihood of the hypothesized interactions: a) presence of bite
4
marks on the whale bones (Portis, 1883; Frenguelli, 1928; Cigala-Fulgosi, 1990;
Deméré and Cerutti, 1982); b) direct association of white shark teeth and cetacean
bones, that means the teeth were found over or in close proximity of the cetacean bones
(Borselli and Cozzini, 1992; Capellini, 1865); c) coexistence of both shark teeth and
cetacean remains within the same deposit (Purdy, 1996).
The first criterion is presumed to provide the highest likelihood but it does not clear the
kind of interaction (attack or scavenging). Moreover, the signs on the bones allow to
identify the shark just when supplementary informations are available, as those due to
the marginally serrated teeth belonging to Carcharodon carcharias (Deméré and
Cerutti, 1982; Cigala-Fulgosi, 1990).
About the second criterion, current evidence discussed later will show that predatory
interactions exist in which the shark does not leave bite marks on the bones of the prey;
for this reason, the finding of shark's teeth in close association with cetacean remains
should be considered as an evidence of interaction. In general, the fossilization process
is a rare fact; to assume that a shark tooth and some cetacean bones have been fossilized
in different times within the same few m2 is an unlikely event. Cetacean bones and
closely associated shark's teeth could be the remains of an ancient predatory or
scavenging interaction even if the bones of the prey are not marked by bite signs. A
single bite on the ventral addominal portion as that in Fig. 1 does not leave bite marks
on the cetacean bones and similar attacks are presumed to have been possible also
during Pliocene.
The third criterion provides the lesser likelihood to interpret interaction types between
cetaceans and white sharks. In general, it is difficult to evaluate the contemporaneous
presence of both vertebrates when they are found in weak association. The main part of
the fossil specimens are difficult to place chronologically within the stratigraphic
5
frameworks of deposits that span for some million years. Moreover, the finding of
shark's teeth and cetacean remains on the same stratigraphical horizon but not in close
association should be considered a clue of coexistence but not of interaction.
Results
Interactions in Recent central Mediterranean Sea
In Table 1, events are described showing that both toothed (21 records) and baleen
whales (2 records) are alimentary items for Carcarodon carcharias. The geographical
distribution of these records is reported in Fig. 2.
Mediterranean interactions between mysticetes and white sharks are rare and their
reports are old. Parona (1896) wrote about close associations of many white sharks to
some carcasses of probable Balaenoptera musculus (blue whale) or Balaenoptera
physalus (fin whale). This pattern is known in other seas but it appears as exceptional in
Mediterranean, where just one or two white sharks are seen together. Damiani (1911)
reported a probable attack on a rorqual stranded at Marciana Marina; this is the first
time in which an interaction between white shark and a living mysticete is observed. It
must be remarked that the rorqual was possibly suffering and unable to escape. Parona's
(1896) and Damiani's (1911) identifications of predators and preys are reasonable but
not completely sure.
Relatively to the 21 toothed whale records, the involved species are the following:
Delphinus (Postel, 1958), Tursiops (Marcantonio and Cataldo, pers. comm., 1980;
Centro Studi Cetacei, 1988; Vanadie, pers. comm., 1988), Stenella (Centro Studi
Cetacei, 1999), Physeter (Fergusson, 1996), and maybe Phocoena (Moreau, 1892).
6
All the attacks in which the predator's size is known are referable to very large white
sharks (>400 cm in length). This consideration induces to hypothesize that cetaceans
represent a trophic target for white sharks near to the sexual maturity or completely
mature (range of sexual maturity lenght by Casey and Pratt, 1985).
The reference database for white sharks/cetaceans trophic interactions uses the
following sources: a) stomach contents reports; b) eyewitnesses' depositions about
predation on living cetaceans; c) scavenging signs on the carcasses.
Stomach contents - An extensive bibliographic search provided 274 records relative to
several aspects of the Mediterranean Carcharodon carcharias life cycle ( Mojetta et al.,
1997; Storai et al., in press; Storai and Zuffa, unpublished data). Among these, 33
records are reports on stomach contents whose analysis furnished data on the relative
presence of a given item in the white shark diet. From a quantitative viewpoint, the
cetacean component of the white shark diet is highly significant and it covers as much
as one-third (17 specimens found into white shark stomaches: 28.91%; total items
found: 59) of the whole diet of the white shark. It is remarkable that one-third of the
examined sharks beard cetaceans into their stomachs (11 cases on 33).
Unfortunately, the sample is statistically too little to allow inferences with high degree
of confidence. Moreover, the data from literature are too generic (the authors wrote
about the presence of large items as tunas, swordfish, tortoises, other sharks, humans
etc., but they did not describe every other little things they found within the stomachs).
For this reason, lacking supporting evidence, every detailed inference on the diet of the
Mediterranean white shark risks to be deceptive.
However, based on the current database, to hypothesize a wide trophic range for the
Mediterranean Carcharodon carcharias appears correct. Possibly, this wide trophic
range should result from the difference between the Mediterranean biota and other
7
biotas around the world, where white sharks show certain trophic specializations. In
fact, non-Mediterranean Carcharodon carcharias populations seem closely associated
to large low-diversity communities of marine mammals or other vertebrates while in
Mediterranean sea the prey availability is characterized by many highly diversified
alimentary items.
Eyewitnesses' depositions about predation on living cetaceans - Just one report
exists that documents an attack on a living cetacean (Condorelli Francavilla and
Ferrando, 1909): during the first attack, a large white shark excided the caudal fin of a
little Delphinidae caught by fishmen, in the second attack, the same shark scoffed the
entire whale. From this description it is impossible to establish a pattern attack to a
living whale due to the handicapped situation of the prey. Spoken reports documented
the presence within white shark's stomachs of odontocetes whose body was cut in two
pieces, but it is not possible to discriminate between predation and scavenging events
(Abela, pers. comm., 1987; Giudici and Fino, 1989).
Scavenging marks on carcasses - Several elasmobranches perform scavenging
operations on floating cetacean carcasses (Long and Jones, 1996), but the records listed
in table 1 are reasonably ascribed to Carcharodon carcharias due to the descriptions of
bite morphology and dimension (Centro Studi Cetacei, 1988, 1999; Vanadie, pers. com.,
1988; Babboni, pers. com., 1995). All of the bites are found in the abdominal zone of
the cetacean body. This observation suggests a kind of attack to a prey too large to be
scoffed as a whole (Anonymus, 1967; Terrasa, 1988; Chiocca, pers. com., 1990; Lipey,
1994).
The comparison between the Mediterranean data and the ones obtained from the
Sarasota bay (Florida) Tursiops population (Bortolotto, 1998) shows a difference. In
fact, the Florida white sharks seem to attack Tursiops from a craniodorsal direction.
8
However, due to the fact that the main part of the Sarasota bay Tursiops were living
after the attack, it is likely that the Florida data are to refer to failed attacks.
Vanadie (pers. com., May, 1988) described a 3-meter-long Tursiops carcass showing a
wide injury clearly due to a large shark attack near to Bovo Marina (Fig. 1). The bite
dimension (diameter about 50 cm) implies, with an high degree of confidence, the
involvement of a white shark. Thorough this attack the shark extracted a large portion of
both abdominal muscles and bowel without damaging the cetacean skeleton.
Interactions in Pliocene central Mediterranean Sea
Fossil teeth of Carcharodon carcharias are known from many Pliocene Italian localities
both from paleotyrrenian and paleoadriatic areas, even if they are less abundant than
other shark teeth, as those referred to Isurus spp. and Carcharinus spp. (Cigala-Fulgosi,
1990, Landini, 1977).
Fossil cetaceans are relatively frequent in the marine Pliocene sediments of Italy,
particularly in Piedmont, Emilia Romagna and Tuscany regions (Bianucci, 1996,
1997a,b,c; Bianucci and Landini, 1999; Bianucci et al. 1998; Bisconti, 2000) and often
they have been collected in the same deposits of white shark teeth.
In some cases direct interactions of shark and both odontocete and mysticete cetaceans
are documented by fossil data. Bibliographical and new records are listed in Tab. 2 and
discussed below. The geographical distribution of these records is reported in Fig. 3.
White shark-odontocete interactions - Portis (1883) examined five odontocete records
from Pliocene sediments of Piedmont with supposed bite marks of Carcharodon or
generic "shark" teeth. Evident signs on the ribs and vertebrae of a delphinid skeleton
collected from Bagnasco (Asti province) were reported. The specimen was originally
9
described (Portis, 1886) as the holotype of the species Steno bellardii but recently it has
been referred (Bianucci,1996) to Astadelphis gastaldii. We have examined in detail the
signs on the bones of this delphinid and no trace of serration, both in cutting and
scraping action as described by Deméré and Cerutti (1982) and Cigala-Fulgosi ( 1990)
for white shark attack, have been observed. Consequently the attack is not referable to a
white shark, as supposed by Portis (1883), but probably to an isurid shark, whose teeth
have not serrations. Regarding the bite marks on the other odontocete records described
by Portis (1883), we doubt that these are consequences of shark attacks, and
particularly the signs on a lumbar vertebra of a supposed delphinid are probably
invertebrate bioerosion.
Cigala-Fulgosi (1990) described in great detail an almost complete skeleton belonging
to a Delphinidae in which he found several signs of attack or scavenging by a Pliocene
white shark. The specimen comes from the Rio Stramonte Piacenzian (Piacenza, Emilia
Romagna) and was referred to Tursiops cortesii capellini by Pilleri (1987) and CigalaFulgosi (1990) and to Hemisyntrachelus cortesii by Bianucci (1996). There are evident
bite signs on the bones of this specimen. Cigala-Fulgosi (1990), analysing the marks,
hypothesized that the shark attacked or scavenged the ventrolateral portion of the whale.
Based on the particular serrated signs, he proposed that a Carcharodon carcharias was
the predator or the scavenger. Together with the attacked or scavenged
Hemisyntrachelus cortesii, other cetacean remains were found, among which the
Hemisyntrachelus cortesii holotype (Cuvier, 1823), an incomplete Hemisyntrachelus sp.
skull (Bianucci, 1997b), and the dentary, ribs and the vertebra that constitute the
Balaena paronai holotype (Del Prato, 1900). White shark's teeth from the Rio
Stramonte Pliocene sediments (spanning from 3.2-3.0 million years; see Bianucci et al.,
1998) were described by De Stefano (1912). This finding is an indirect evidence for a
10
coexistence between white sharks and toothed whales in this area of the Paleoadriatic
sea. It can be hypothesized that the highly diffuse Hemisyntrachelus was an alimentary
source for Carcharodon carcharias.
Cigala-Fulgosi (1990) discussed also another specimen bearing bite marks. It is a single
Delphinidae rib on which there are signs made by a white shark.
In one case, an odontocete skeleton was found in close association with two white
shark's teeth but its bones did not bear bite marks. The specimen belongs to
Hemisyntrachelus cortesii (Bianucci, 1997a) and it comes from the Campore quarry
near Salsomaggiore (Parma province, Emilia Romagna). The skeleton lacks the arms,
many lumbar and all of the caudal vertebrae; the skeletal remains are almost completely
articulated but a disarticulation pattern is observed among the anteriormost portion of
the postcranial skeleton (Fig. 4). Particularly, the anterior dorsal vertebrae are dislocated
and the ribs are dispersed and cracked. Within the cervical-anterothoracic area, on the
right side of the whale body, two Carcharodon carcharias teeth were found that were
very near to the ribs. A random association between the teeth and the cetacean remains
should be considered very unlikely. The depth of the bottom on which the dolphin was
deposed is esteemed to be 200-400 m (upper epibathyal; Bianucci, 1997a) is in the
range of occurrence of living white sharks. However, Carcharodon carcharias makes
rarely scavenging onto preys deposed on the bottom. For this reason, it is reasonable to
suppose that the white shark attacked the living dolphin or its floating carcass. The
lacking of the arms and the caudal region of the body supports the hypothesis of floating
transport of the carcass because these portions could be detached during decomposition
before the deposition of the cetacean on the bottom (Shäfer, 1972).
11
White shark-mysticete interactions - Records from Tuscany are noteworthy and
comprehend essentially balaenids. Capellini (1876) described bite signs on the ribs and
fragments of vertebrae of dwarf balaenids that he identified as Balaenotus found from
Poggiarone (Siena province) and S. Murino (Pisa province) near Siena. He supposed
that the signs were due to human activities on the bones. After some years, Portis (1883)
identified the marks as evidence of interaction with Carcharodon sharks. We consider
correct the attribution of these signs to shark bites but we believe that they are not the
result of white shark attack because completely different from signs described and
illustrated by Cigala-Fulgosi (1990) and Deméré and Cerutti (1982).
From the San Miniato basin (including an area between Florence and Pisa, Tuscany),
two other balaenids were found in close association to white shark's teeth. Borselli and
Cozzini (1992) described the excavation of a large bowhead whale (Balaena sp.)
bearing eight white shark's teeth in close proximity. The whale was represented by an
almost articulated skeleton whose arms and scapulae were shifted at the level of the
lumbar vertebrae. It is likely that the decomposed whale went under a taphonomic
process that shifted anteriorly the axial body (skull and vertebral spine) leaving the arms
behind. A single white shark tooth was found between the scapula's glenoid cavity and
the distal epiphysis of the disassociated ulna (Fig. 5). It is likely that the very close
association between shark's teeth and the skeletal remains constitutes a real clue of
direct interaction between the large bowhead whale and a white shark. The cetacean
body was deposited on a bottom which was not more than 30 m in depth, (Borselli and
Cozzini, 1992), and for this reason, a scavenging option cannot be excluded.
Within the same basin, a disassociated Eubalaena glacialis skull was found and initially
identified as Physeter by Pilleri (1987). Recently, Bisconti (unpublished data)
redescribed the specimen and found apomorphies of Eubalaena glacialis. The skull was
12
composed by three disassociated pieces dispersed on several-m2; among the cranial
remains, a single triangular white shark's tooth was found. The evidence to hypothesize
an interaction is too weak because the lack of a close proximity between the tooth and
the cranial remains
In his detailed work, Portis (1883) described the bite marks on the bones of some
Mysticeti from Pliocene sediments of Piedmont (four records) and Liguria regions (one
records). Among these records, only the "Balaenoptera" gastaldii holotype shows bite
marks on its ulna that are homogeneous to the experimental paradigm provided by
Cigala-Fulgosi (1990) and Deméré and Cerutti (1982) (Fig. 6). For this reason, it is
hypothesizable that a white shark attacked or scavenged on the fin of the whale.
Three Pliocene rorquals were found in Emilia Romagna that were associated to shark's
teeth. Capellini (1865) stated that the rorqual remains found at S. Lorenzo in Collina
(Bologna province) were strictly associated to some shark's teeth among which a single
Carcharodon carcharias specimen. A balaenopterid skeleton has been recently found
near Vignola (Modena province) in weak relation with a single large tooth belonging to
a white shark. Unfortunately, the complete disassociation of the skeletons prevents an
analysis of the kind of interactions between the sharks and the baleen whales. It can be
stated just that some kind of interaction really happened. A large Piacenzian rorqual-like
whale was found near Salsomaggiore Terme (Parma province; Bianucci, 1997a) bearing
three white shark's teeth. The specimen was found in the same quarry of the
Hemisyntrachelus cortesii discussed below. The shark teeth were closely associated to
the skeleton; one of them was found under a lumbar vertebra and the others were in the
anterior portion of the whale. The whale was deposited on its back and the abdomen
was exposed to scavenging. Due to the enormous body size of the cetacean, it is
hypothesized that the white shark scavenged on the floating carcass of this whale.
13
Discussion
The analysis of trophic interactions between white sharks and cetaceans in the Recent
central Mediterranean shows that cetaceans represent a significant component of the
diet of large size (> 4 m) Carcharodon carcharias. The available data do not allow to
assess which part of this interaction is due to scavenging and which to predation on
living animals. However, the involved cetaceans are prevalently small and medium size
delphinids which represent, still living, potential preys for these sharks (Casey and Pratt,
1985).
The fossil record shows interactions between white sharks and whales also during the
Pliocene. In particular, evidence of interaction is documented in three toothed whales
and six baleen whales. Even if, on the basis of fossil data, it is not possible to
distinguish scavenging from predation with an higher degree of confidence, considering
that the estimated body size of the Mediterranean Pliocene Carcharodon carcharias
was larger than the extant one (Cigala-Fulgosi, 1990), we can hypothesize that
predation was possible on small and medium size delphinids and small Mysticeti as
some cetotheriids and balaenids (Balaenula, Balaenotus). In light of the gathered
evidences, the reason of death of the Hemisyntrachelus cortesii from Rio Stramonte and
the "Balaenoptera" gastaldii from Cordandone could have been a white shark attack.
Both specimens are 4.5-5 m long and show bite marks on the bones. It is hypothesizable
that larger toothed and baleen whales could have been a trophic source for white sharks
just when died. The finding of Carcharodon carcharias teeth in close proximity to
14
rorquals (Salsomaggiore Terme, about 8 m in length) and balaenids (Ponte a Elsa, about
10 m in length) is a clue of such a scavenging interaction.
The comparison between Pliocene and Recent data shows that in the Recent central
Mediterranean Sea, the interactions are principally directed to little-sized odontocetes
and just rarely to mysticetes, while in the Pliocene, both toothed whales and baleen
whales are presumed to have been equally represented in the Carcharodon carcharias
diet (Fig. 7). It is remarkable that the diversity of living Mediterranean mysticetes is
lower than the Pliocene one and that the living baleen whales from Mediterranean are
represented just by larger species. In summary, a change occurred in the diet of white
shark through time. This change could be due to both the general reduction of the living
white shark body size and the diminished diversity of the cetacean assemblage. Within
this context, the extinction of dwarf balaenids could have played a significant role.
Acknowledgements
We are very grateful to the following people for their courtesy, help and for granting us
access to fossil collections: Carlo Francou (Geological Museum of Castell'Arquato);
Raffaele Quarantelli (Gruppo Paleontologico Salsese); Berselli Renato and Miria Burani
(Gruppo "Al Palesi", Vignola); Paul Mazza (Paleontological Museum, University of
Florence); Daniele Ormezzano (Geological and Paleontological Museum, University of
Torino).
We also thank Chiara Sorbini (Dipartimento di Scienze della Terra, Università di Pisa)
for her valuable help.
15
References
ANONYMUS, 1967. - Squalo nelle reti a Porto Santo Stefano. La Nazione Sera,
Firenze, 24/7/1967.
ARNOLD P. W., 1972. - Predation on harbour porpoise, Phocoena phocoena, by a
white shark, Carcharodon carcharias. J. Fish. Res. Board Can., 29: 1213-1214.
AZZAROLI A & M.B. CITA, 1980. - Geologia stratigrafica. Vol. III. CisalpinoGoliardica, Milano.
BIANUCCI G., 1996. - The Odontoceti (Mammalia, Cetacea) from Italian Pliocene.
Systematics and Phylogenesis of Delphinidae. Palaeont. Ital., 83: 73-167.
BIANUCCI G., 1997. - Hemisyntrachelus cortesii (Cetacea, Delphinidae) from the
Pliocene sediments of Campore Quarry (Salsomaggiore Terme, Italy). Boll. Soc.
Paleont. It., 36(1-2): 75-83.
BIANUCCI G., 1997b. - A new find of Hemisyntrachelus (Cetacea, Delphinidae) from
Piacenzian sediments of Rio Stramonte (Northern Appenines, Italy). Riv. ital. Paleont.
Stratigr., 103(2): 259-262.
BIANUCCI G., 1997c. - The Odontoceti (Mammalia, Cetacea) from Italian Pliocene.
The Ziphiidae. Palaeont. Ital., 84: 163-192.
BIANUCCI G. & W. LANDINI, 1999. - Kogia pusilla from Middle Pliocene of
Tuscany (Italy) and a phylogenetic analysis of family Kogiidae (Odontoceti, Cetacea)
Riv. ital. Paleont. Stratigr., 105(3): 445-453.
BIANUCCI G., SARTI G., CATANZARITI R. & U. SANTINI, 1998. - Middle
Pliocene cetaceans from Monte Voltraio (Tuscany, Italy). Biostratigraphical,
paleoecological and paleoclimatic observations. Riv. Ital. Paleont. Stratig., 104: 123130.
16
BISCONTI M., in press. - New description, character analysis and preliminary phyletic
assessment of two Balaenidae skulls from the Italian Pliocene. Palaeont. Ital.
BORSELLI V. & F. COZZINI, 1992. - Il recupero di un cetaceo fossile in località Ponte
a Elsa (Pisa). Museol. Sci., 8: 9-22.
BORTOLOTTO A., 1998. - Interazioni fra squali e cetacei. Cetacea Informa, 13: 28-29.
BRUCE B.D., 1992. - preliminary observations on the biology of the white shark,
Carcharodon carcharias, in South Australian waters. Austr. J. Mar. Freshwater Res.,
43: 1-11.
CAPELLINI G., 1865. - Balenottere fossili del Bolognese. Mem. R. Acc. Sci. Ist.
Bologna, 4: 3-24.
CAPELLINI G., 1905. - Balene fossili toscane. III. Idiocetus guicciardinii. Mem. R.
Acc. Sci. Ist. Bologna, 2: 71-83.
CASEY J.C.H. & PRATT L. JR., 1985. - Distribution of the white shark Carcharodon
carcharias in the Western North Atlantic. Mem. South Calif. Acc., 9: 2-14.
CENTRO STUDI CETACEI, 1988. - Cetacei spiaggiati lungo le coste italiane. II
Rendiconto 1987. Atti Soc. It. Sci. Nat., 129(4): 411-432.
CENTRO STUDI CETACEI, 1991. - Cetacei spiaggiati lungo le coste italiane. IV
Rendiconto 1989. Atti Soc. It. Sci. Nat., 131(27): 413-432.
CENTRO STUDI CETACEI, 1999. - Cetacei spiaggiati lungo le coste italiane. XII
Rendiconto 1997. Atti Soc. It. Sci. Nat., 139(2): 213-226.
CIGALA-FULGOSI F., 1990. - Predation (or possible scavenging) by a great white
shark on an extinct species of bottlenosed dolphin in the Italian Pliocene. Tertiary Res.,
12(1): 17-36.
17
COCKCROFT V.G., DUNDLEY S.F.J. & DAVIS B., 1989. - Shark predation on
Indian Ocean bottlenose dolphins Tursiops truncatus off Natal, South Africa. S. Afr. J.
Zool., 24: 305-310.
CONDORELLI FRANCAVILLA M. & FERRANDO G.G., 1909. - Notizie sul
carcharodon carcharias L. 1758 catturato nelle acque di Augusta e considerazioni
medico legali sui resti umani trovati nel suo tubo digerente. Boll. Soc. Zool. Ital., 10:
164-183.
CORKERON P.J., MORRIS R.J. & BRYDEN M.M., 1987. - Interaction between
bottlenose dolphin and sharks in Moreton Bay, Queensland. Aquat. Mammal., 13: 109113.
CROWLEY T.J., 1991. - Modeling Pliocene warmth. In: DOWSETT H.J. & CRONIN
T.M. (eds.) - Pliocene climates, Quat. Sc. Rev., 10: 147-162.
CUVIER G., 1823. - Recherches sur les ossements fossiles, où l'on rètablit les caractèrs
du plusieurs animaux dont les révolution du Globe ont détruit les espéces. Tome
Cinquième, I Partie., Dufour et E. D'Ocagne libraires, Paris.
DAMIANI G., 1911. - Sovra una Balenoptera del Novembre 1910 a Marciana Marina,
Boll. Soc. Zool. It., 1911: 50-57.
DAY L.R. & FISHER H.D., 1954. - Notes on the great white shark, Carcharodon
carcharias, in Canadian waters. Copeia, 4: 295-296.
DELL'OMODARME F., 1976. - Studio di un cetaceo villafranchiano di Montopoli
(Valdarno inferiore). Thesis, 55 pp. Univ. Firenze.
DEMÉRÉ T.A. & R.A. CERUTTI, 1982. - A Pliocene shark attack on a Cetotheriid
whale. J. Paleont., 56(6): 1480-1482.
DE STEFANO 1912. - Appunti sulla ittiofaunafossile dell'emilia conservata nel Museo
Geologico dell'Università di Parma. Boll. Soc. Geol. It., 31: 35-78.
18
DEL PRATO A., 1897. - Il Tursiops Capellinii Sacco del Pliocene Piacentino.
Palaeont. ital., 3: 1-14.
DEL PRATO A., 1900. - Balena fossile del Piacentino. Riv. ital. Paleont., 6(3): 136142.
FERGUSSON J.K., 1996. - Distribution and autoecology of the white shark in the
Eastern North Atlantic Ocean and the Mediterranean Sea. Pp. 321-345 in KRIMLEY
A.P. & AINLEY D.G. (eds.): Great White Sharks, The biology of Carcharodon
carcharias.
FRENGUELLI G., 1928. - A proposito di alcune incisioni sull'omero di uno
Squalodonte del Miocene superiore della Patagonia. Boll. Soc. Geol. Ital., 47(1): 1-9.
GIUDICI A. & FINO F., 1989. - Squali del Mediterraneo. Atlantis, Roma.
LANDINI W., 1977. - Revisione degli "ittiodontoliti pliocenici" della collezione
Lawley. Palaeont. ital., 70: 92-134.
LIPEY L., 1994. - Se o izolskem belem morskem volku. Proteus, 56: 208-209.
LONG D.J., 1991. - Apparent predation by a white shark Carcharodon carcharias on a
pygmy whale Kogia breviceps. Fishery Bull., 89(3): 538-540.
LONG D.J. & JONES R.E., 1996. - White shark predation and scavengin on cetaceans
in the Eastern North Pacific Oceans: 293-307.
MARTINI A., 1989. - Quella volta che all'improvviso ci sono apparsi davanti. Nature
Oggi, 8: 40-41.
MOJETTA A., STORAI T. & ZUFFA M., 1997. - Segnalazioni di Carcharodon
carcharias in acque italiane. Quad. Civ. Staz. Idrobiol. Milano, 22: 23-38.
MOREAU E., 1982. - Manual d'ichtyologie française. Pp. 15-16, Masson, Paris.
NOTARBARTOLO DI SCIARA G. & BIANCHI I., 1998. - Guida degli squali e delle
razze del Mediterraneo. Franco Muzzio Editore, pp. 388, Padova.
19
PARONA C., 1896. - Notizie storiche sopra i grandi cetacei nei mari italiani e in
particolare sulle quattro balenottere catturate in Liguria nell'autunno del 1896. Atti Soc.
It. Sci. Nat., 36: 297-373.
PHYLO L.M., SHOTTS E.B. JR. & J.C. GEORGE, 1993. - Morbidity and mortality.
In: The Bowhead Whale (Burns J.J., Montague J.J., & C.J. Cowles, eds.), Spec. Pub.,
Soc. Mar. Mam., 2: 275-312.
PORTIS A., 1883. - Nuovi studi sulle traccie attribuite all'uomo pliocenico. Mem. R.
Acc. Sci. Torino, 35: 3-27.
PORTIS A., 1886. - Catalogo descrittivo dei Talassoterii rinvenuti nei terreni terziari
del Piemonte e della Liguria. Mem. R. Acc. Sci. Torino, 37, 247-365.
PURDY R.W., 1996. - Paleoecology of fossil white sharks. In: Great white sharks: 6778, Academic Press, London.
POSTEL E., 1958. - Sur la presence de Carcharodon carcharias (L. 1758) dans les
eaux tunisiennes. Bull. Mus. Nation. Hist. Nat. Paris, 30:342-344.
SHÄFER W, 1972. - Ecology and Palaeocology of marine environments. (G.Y. Craig,
ed.), The University of Chicago Press.
SLIPP J.W. & WILKE F., 1953. - the beaked whale Berardius on the Washington coast.
J. Mammal., 34: 105-113.
STORAI T., MOJETTA A., ZUFFA M. & GIULIANI S., in press. - Nuove
segnalazioni di Carcharodon carcharias (L.) nel Mediterraneo Centrale. Atti Soc. Tosc.
Sci. Nat.
TERRASA S., 1988. - Tiburones en Mallorca. Brisas, 55: 6-12.
TOMILIN A.G., 1967. - Cetacea. In: HEPTNER V.G. (ed.) - Mammals of the U.S.S.R.
and adjacent countries. Israel Program for Scientific Translations, 9: 1-756, Jerusalem.
20
21
FIGURE CAPTIONS
Fig. 1 - Carcass of Tursiops trucatus from Bovo Marina, showing a wide injury
(diameter about 50 cm) clearly due to a large shark.
Fig. 2 - Geographical distribution of the evidence of interactions between Carcarodon
carcharias and cetaceans in the Recent central Mediterranean Sea. Circle: odontocetes;
squares: mysticetes; questionmark: geographical placing not precisely known. For
numbers and referred records see Tab. 1.
Fig. 3 - Geographical distribution of the evidence of interactions between Carcarodon
carcharias and cetaceans in the Pliocene central Mediterranean Sea. Circle:
odontocetes; squares: mysticetes. For numbers and referred records see Tab. 2.
Paleogeographical reconstruction after Azzaroli and Cita (1980).
Fig. 4 - Outline skeletal plan of Hemisyntrachelus cortesii from Pliocene sediments of
Salsomaggiore Terme (Parma, Emilia Romagna). Md, mandible; Rb, rib; Sk, skull; St,
stern; Tt, tooth; Vc, cervical vertebra; Vd, dorsal vertebra; Vl, lumbar vertebra. The
arrow indicates the two associated Carcharodon carcharias teeth.
Fig. 5 - Balaena sp. from Pliocene sediments of Ponte a Elsa (Pisa, Tuscany). A:
disarticulated right arm; B detail of A with associated Carcharodon carcharias tooth.
The arrows indicate the position of the tooth.
22
Fig. 6 - Ulna of the Balaenoptera gastaldii holotype from Pliocene sediments of
Cortandone (Asti, Piedmont) with bite marks of white shark (1-3). A: lateral view.; B:
detail of A.
Fig. 7 - Hypothetical trophic interaction between Carcharodon carcharias and
cetaceans in the Pliocene (A) and Recent (B) central Mediterranean Sea. 1: delphinid
(odontocete); 2: ziphiid (odontocete); small cethotherid/balaenopterid (mysticete); 4:
small balaenid (mysticete); large balaenopterid (mysticete); large balaenid (mysticete);
physeterid (odontocete). Solid arrows indicate sure interaction based on data discussed
in this paper; broken arrows indicate possible interactions based on the presence of this
cetacean group in the central Mediterranean Sea.
23
TABLE CAPTIONS
Tab. 1 - Evidences of the interactions between Carcharodon carcharias and cetaceans
in the central Mediterranean Sea; Recent data (1889-1997).
Tab. 2 - Evidences of the interactions between Carcharodon carcharias and cetaceans
in the central Mediterranean Sea; fossil data (Pliocene).
24
Date
Place
Cetaceans
Species involved
Cetacean
length (cm)
Cetacean
weight (kg)
Shark
Length (cm)
Shark
Weight (kg)
1
Oct. 1889
Toulon (F)
Pochoena pochoena ?
2
1896
Liguria (It)
400
-
3
26/1/1909
Augusta (It)
Balenoptera musculus
or
B. physalus
Indet. small delphinid
-
4
13/11/1910
Marciana Marina
I. d’Elba (It)
50
700-800
-
450
800
-
(Condorelli and
Perrando, 1909)
(Damiani, 1911)
5
Aug. 1938
6
16/5/1956
Enfola
I. d’Elba (It)
Capo Bon (Tun)
Jun. 1958
Estaque (F)
Indet. large delphinid
8
Aug. 1960
Indet. small delphinid
9
22/10/1963
I. d’Elba, Rio Marina
(It)
Isola (Slo)
10
1964
Italian coasts
11
1967
12
22/07/1967
C. Ferrutx, Mallorca
(E)
I. del Giglio (It)
Physeter
macrocephalus
Indet. delphinid
13
Jun. 1978
Lido di Venezia (It)
Tursiops sp.?
14
Jun. 1979
Capo Bon (Tun)
Indet. delphinid
15
24/04/1980
Favignana (It)
Tursiops sp.
600
1.800
520
1.800
Wide Shark
500
1.000
600?
1.100
1.500
900
500
520
540
1.500
(Chiocca, 1990
Pers. Com.)
(Postel, 1958)
7
15
200
-
16
17/04/1987
Filfla (Malta)
Indet. delphinid
08/05/1987
Favignana (It)
Indet.
18
31/07/1987
Ganzirri (It)
Tursiops sp.
19
04/05/1988
Bovo Marina (It)
Tursiops sp.
20
Jun. 1989
Capo Spartivento (It)
Indet. delphinid
21
Jan. 1991
Sete (F)
Indet. delphinid
22
04/06/1995
Follonica (It)
Indet. delphinid
23
11/06/1997
Is. Salina (It)
Stenella sp.
200
100
250
310
120
150
150
-
714?
535
2.000
550
450
400
-
17
Balenoptera physalus
or
B. acutorostrata
Indet. small delphinid
Delphinus sp.
Indet. delphinid
Indet. delphinid
References
(Moreau, 1892)
(Parona, 1896)
(Damonte, 1993)
(Chiocca, 1994
Pers. Com.)
(Lipey, 1994)
(Fergusson, 1996)
(Terrasa, 1988)
(Anonimo, 1967)
(Martini, 1989)
(Fergusson, 1996)
(Marcantonio &
Cataldo, 1980 Pers.
Com.)
Abela, 1987 Pers.
Com.)
(Giudici & Fino,
1989)
(CSC, 1988)
(Vanadie, 1988
Pers. Com.)
(CSC, 1991)
(Fergusson, 1996)
(Babboni, 1995
Pers. Com.)
(CSC, 1999)
25
"Berardiopsis"
"Berardiopsis"
Delphinid
Hemisyntrachelus
cortesii
Delphinid
Hemisyntrachelus
cortesii
Balenopterid
Balaenoptera
cortesii
Piedmont
"Balaenoptera"
gastaldii
Balenopterid
Balaenopterid
Balenopterid
Balenopterid
(2) Calunga (Asti)
(3) "Sabbie gialle" sediments (Asti
province)
(4) "Sabbie gialle" sediments (Asti
province)
(5) "Sabbie gialle" sediments (Asti
province)
Shar
k teeth
References
Portis, 1883
?
?
?
no
Portis, 1883
Portis, 1883
Portis, 1883
Portis, 1883
Cigla-Fulgosi,
1990
Cigla-Fulgosi,
1990
(6) Stramonte river (Piacenza)
(7) Piacenza province
(8) Salsomaggiore Terme
(Parma)
New data
(9) Poggiarone (Siena)
Portis, 1883
(10) S. Murino (Pisa)
Portis, 1883
Borsellii and
Cozzini, 1992
(11) Ponte a Elsa (Pisa)
(12) Ricavo, near Caslelfranco
(Florence)
Eubalena sp.
Emilia-R.
Mysticeti
Balaena sp.
Tuscany
Balaenotus
Balaenotus
Shark
bites
(1) Bagnasco (Asti)
Piedmont
Astadelphis
gastaldii
Astadelphis
gastaldii
Locality
Emila-R.
Odontoceti
Cetacean records
New data
Portis, 1883
(13) Cortandone (Asti)
(14) Calunga, near S. Damiano
(Asti)
(15) Asti province
(16) "Sabbie gialle" sediments
(Asti province)
(17) S. Lorenzo in Collina
(Bologna)
(18) Salsomaggiore Terme
(Parma)
(19) Vignola (Modena)
?
?
?
Portis, 1883
Portis, 1883
Portis, 1883
Capellini, 1865
New data
New data
26
27
28
29
30
31