Content uploaded by Peter Lewis Falkingham
Author content
All content in this area was uploaded by Peter Lewis Falkingham on Oct 20, 2021
Content may be subject to copyright.
Biting in the Miocene seas: estimation of the bite force of the macroraptorial sperm
whale Zygophyseter varolai using nite element analysis
Emanuele Peri
a,b,c
, Peter L. Falkingham
b
, Alberto Collareta
c
and Giovanni Bianucci
c
a
Dottorato Regionale Pegaso in Scienze Della Terra, Università Di Pisa, Pisa, Italy;
b
School of Biological and Environmental Sciences, Liverpool John
Moores University, Liverpool, UK;
c
Dipartimento Scienze Della Terra, Università Degli Studi Di Pisa, Pisa, Italy
ABSTRACT
Diering from the extant physeteroids, macroraptorial sperm whales are currently regarded as apex
predators of the Miocene seas based on several morphofunctional observations. Here, we estimate the
bite force of Zygophyseter varolai, a macroraptorial physeteroid from lower upper Miocene strata of the
Pietra leccese formation (Apulia, Italy) using the nite element analysis (FEA). To explore multiple bite
scenarios, we set four dierent load cases on a 3D model of the cranium obtained via digital photogram-
metry, considering the temporalis and masseter muscles as jaw adductors. Our FEA simulations indicate that
Z. varolai exerted an anterior bite force of more than 4000 N and a posterior bite force of more than 10000 N.
These values are similar to those estimated for other marine predators known for their powerful bite. This
suggests that Z. varolai might have fed upon medium-sized marine vertebrates like other odontocetes.
Considering the signicant dierence observed between the anterior and posterior bite forces, Z. varolai
likely fed via ‘grip-and-shear’ feeding, snapping the food items with an anterior bite and then cutting them
with a powerful posterior bite. Other macroraptorial sperm whales such as the roughly coeval Acrophyseter
from Peru likely employed the same feeding technique.
ARTICLE HISTORY
Received 20 August 2021
Accepted 20 September 2021
KEYWORDS
Physeteroidea; apex
predator; biomechanics; FEA;
feeding strategy;
palaeoecology
Introduction
Since the earliest predator–prey interaction, oceans have always had
their sea monsters. Once jaws had evolved, bite force became
a defining characteristic of predators. During the Late Devonian,
the top predator of the seas was the placoderm Dunkleosteus, an
armoured, jawed fish more than 8 m long, and calculated to have
had a bite force of 7495 N at the rear gnathal plates (Anderson and
Westneat 2009; Ferrón et al. 2017). From the late Triassic to the late
Cretaceous, the role of marine apex predators was mainly played by
marine reptiles such as the Pliosauroidea (Plesiosauria,
Sauropterygia) (Foffa et al. 2014). Pliosauroids included large-
sized predators like Kronosaurus queenslandicus, with a total body
length of 9–10.9 m and an estimated bite force of more than
27000 N (McHenry 2009; Foffa et al. 2014). Near the end of the
Cretaceous period (98–65.5 Ma), Mosasauroidea (Squamata)
roamed the seas together with Pliosauroidea and ruled the aquatic
environments till the end of the Mesozoic (Polcyn et al. 2014;
Madzia and Cau 2017). Mosasauroids were marine reptiles with
a lacertiform appearance, and the largest species exceeded 10 m in
length (Bullard and Caldwell 2010; Driscoll et al. 2019). After the
K-Pg boundary, during the Palaeocene and part of the Eocene, the
role of apex predator in oceans was still occupied by reptiles, with
large marine crocodiles like the genera Thoracosaurus (Danian,
Palaeocene) and Dyrosaurus (Ypresian, Eocene) (Gallagher 2003;
Jouve et al. 2005; Puértolas-Pascual et al. 2015). Besides crocodiles,
the selachian family Otodontidae provided important marine pre-
dators in the Palaeogene with the megatoothed shark species
Otodus obliquus (Palaeocene) and Carcharocles auriculatus
(Eocene) (Ehret and Ebersole 2014; Perez et al. 2018). From the
middle Eocene, marine mammals became the new top predators in
seas thanks to the radiation of the Archaeoceti (Fordyce 2018; Uhen
2018). This group includes some of the most impressive fossil
marine predators like Basilosaurus (Basilosauridae), a huge archaic
whale (total body length 17–20 m) with serrated teeth and a bone-
crushing bite (Snively et al. 2015; Uhen 2018; Voss et al. 2019). Near
the end of the Eocene, cetaceans radiated into the modern Mysticeti
and Odontoceti lineages (forming the Neoceti clade) and new
predator taxa with various morphologies and feeding strategies
occupied the top of the trophic chain (Boessenecker et al. 2020).
Nowadays, the cetacean apex predator is the killer whale (Orcinus
orca; Delphinidae, Odontoceti), which thanks to its large size and
coordinated hunting strategies can feed upon sperm whales as well
as large baleen whales (mysticetes) like common minke whales
(Balaenoptera acutorostrata), calves of humpback whales
(Megaptera novaeangliae), and grey whales (Eschrichtius robustus)
(Pitman et al. 2001, 2015; Barrett-Lennard et al. 2011; Ford 2018).
In modern oceans, the killer whale shares the top position of the
trophic chains with the great white shark (Carcharodon carcharias),
whose predatory activity on diminutive marine mammals is widely
known (Compagno 1984; Heithaus 2001; Brown et al. 2010; Skomal
et al. 2017; Moro et al. 2020).
In the Miocene epoch, sharks belonging to the family
Otodontidae roamed the oceans covering the ecological role
of apex predators (Ehret and Ebersole 2014; Collareta et al.
2017a; Perez et al. 2018; Boessenecker et al. 2019).
Carcharocles megalodon (total body length up to 20 m; Perez
et al. 2021) was the most impressive representative of the
otodontid family, and it likely fed upon small to medium-
sized baleen whales (Collareta et al. 2017a; Boessenecker
et al. 2019; Cooper et al. 2020; Shimada et al. 2020). During
the same epoch, high trophic levels of predation like those of
the modern killer whale have been proposed for some fossil
CONTACT Emanuele Peri emanuele.peri@phd.unipi.it Dottorato Regionale Pegaso in Scienze Della Terra, Università Di Pisa, Via S. Maria 53, Pisa 56126, Italy
HISTORICAL BIOLOGY
https://doi.org/10.1080/08912963.2021.1986814
© 2021 Informa UK Limited, trading as Taylor & Francis Group
Published online 20 Oct 2021
relatives of the modern sperm whales (superfamily
Physeteroidea) (Bianucci and Landini 2006; Lambert et al.
2008, 2010, 2017). Differently from the extant physetheroids
(i.e., the sperm whale Physeter macrocephalus, the dwarf sperm
whale Kogia sima, and the pygmy sperm whale K. breviceps),
which feed nearly exclusively upon cephalopods by suction
generated through the mouth in Kogia and directly within
the oropharynx in Physeter (Werth 2004, 2006a, 2006b;
Bloodworth and Marshall 2005), these putatively macroraptor-
ial, extinct forms likely preyed upon marine vertebrates using
robust jaws and large teeth to grasp their food items (Bianucci
and Landini 2006; Lambert et al. 2008, 2010, 2014, 2017;
Hocking et al. 2017; Lambert and Bianucci 2019; Peri et al.
2020). This hypothesis is based on various cranial features
displayed by the macroraptorial Physeteroidea, including
a wide temporal fossa, well-developed maxillary teeth (only
mandibular teeth are functional in extant sperm whales) and,
as observed on the holotype of Acrophyseter robustus, bony
exostoses in correspondence of upper cheek teeth (Bianucci
and Landini 2006; Lambert et al. 2008, 2010, 2014; Lambert
and Bianucci 2019; Peri et al. 2020). Furthermore, the teeth of
these fossil sperm whales exhibit deep occlusal facets, which
are sulci on the tooth surface produced by repeated tooth-to-
tooth contacts (attritional wear), and fractures attributed to
strong occlusion or to the contact with hard material (e.g.,
bone) (Bianucci and Landini 2006; Lambert et al. 2017;
Lambert and Bianucci 2019; Peri et al. 2020). Taxonomically
diagnostic fossil remains of macroraptorial physeteroids have
been retrieved in several localities all around the world, both
in the middle Miocene (Albicetus oxymycterus, California,
USA; Brygmophyseter shigensis, Japan) and in the upper
Miocene (Acrophyseter deinodon, Acrophyseter robustus and
Livyatan melvillei, Peru; Zygophyseter varolai, Italy) (Bianucci
and Landini 2006; Kimura et al. 2006; Lambert et al. 2008,
2010, 2017; Boersma and Pyenson 2015). One of the best
known macroraptorial physeteroids, Z. varolai from
Tortonian strata of the Pietra leccese formation (Salento
Peninsula, southern Italy), is characterised by having a dorsal
concavity on the skull (i.e., supracranial basin) that is wide
and hemispherical, an extremely elongated zygomatic process
(probably supporting a developed masseter muscle), and sev-
eral dental features associated to a strong occlusion and repe-
titive use of the bite (e.g. occlusal facets, lowering of the
gingival collar due to the deepening of the associate occlusal
facet, and lateral wear of the enamel layer) (Bianucci and
Landini 2006). The holotype of Z. varolai is complete enough
to provide reliable estimations of both the condylobasal length
(148 cm) and the total body length (650–700 cm). All these
elements led to the hypothesis that Z. varolai preyed upon
small- to medium-sized marine vertebrates using a powerful
bite (Bianucci and Landini 2006).
Here, we use the ‘dry-skull’ method and the finite element
analysis (FEA) to estimate the bite force of Z. varolai and test the
bite performances of this extinct macroraptorial sperm whale. FEA
has proven to be a powerful tool to investigate form and function of
extinct vertebrates (Rayfield et al. 2001; Hassan et al. 2002;
McHenry et al. 2007; Wroe et al. 2007; Bell et al. 2009; Oldfield
et al. 2012; Foffa et al. 2014; Snively et al. 2015), but such
a biomechanical approach has never been used before on
a macroraptorial sperm whale. The results obtained from the FEA
bite simulations provide informative clues about the palaeoecology
of this top predator from the late Miocene, and open new intriguing
research horizons concerning the macroraptorial physeteroids and
their trophic role in the Miocene global ocean.
Materials and methods
Institutional abbreviations
MAUS, Museo dell’Ambiente, Università del Salento, Lecce, Italy;
MNHN, Muséum National d’Histoire Naturelle, Paris, France;
MSNUP, Museo di Storia Naturale dell’Università di Pisa, Calci,
Italy; MUSM, Museo de Historia Natural, Universidad Nacional
Mayor de San Marcos, Lima, Peru.
Examined specimen
The specimen used in this study is a cast of the cranium and the
mandibles of the holotype of Zygophyseter varolai (MSNUP
I-16828). The holotype (MAUS 229, a replacement number for
MAUL 229/1 reported in Bianucci and Landini 2006) also includes
most of the postcrania and was collected from the uppermost strata
of the Cisterna quarry of Salento peninsula (Lecce Province, south-
ern Italy) (Bianucci and Landini 2006; Bianucci and Varola 2014).
The cranium lacks the right lacrimo-jugal complex and the poster-
odorsal portion of the supracranial basin. These cranial parts were
included in stone slabs that were not collected from the quarry (the
right lacrimo-jugal complex) or were lost before the fossil could be
stored at the MAUS (the posterodorsal portion of the supracranial
basin). The mandibles are virtually complete, although the right
coronoid process appears slightly deformed.
Digital acquisition
We acquired a 3D model of the cranium and mandibles of Z. varolai
through digital photogrammetry of the holotype cast accomplished
with the software Agisoft Metashape (1.7.0) (Petti et al. 2008;
Falkingham 2012; Falkingham et al. 2014, 2018, 2020; Mallison
and Wings 2014; Fahlke and Autenrieth 2016; Fau et al. 2016;
Díez Díaz et al. 2021). The camera used for the photographic
acquisition was a Sony a6000 equipped with a Sigma 30 mm F1.4
lens. We performed two separate acquisitions for the cranium (94
photos) and the mandibles (134 photos). To reconstruct the missing
parts, we imported the digital model of the cranium into Blender
(2.91.0) (https://www.blender.org/) and digitally rebuilt the poster-
odorsal portion of the cranium and the missing right lacrimojugal
complex. Our reconstruction of the missing posterodorsal portion
of the cranium was based on observations made in the quarry
during the collection of the fossil by one of us (G.B.) as well as on
comparisons with the holotypes of Acrophyseter deinodon (MNHN
SAS 1626) and Acrophyseter robustus (MUSM 1399) (which, among
the physeteroid species, are the phylogenetically and morphologi-
cally closest to Zygophyseter according to Lambert et al. 2017). The
missing right lacrimojugal complex was digitally rebuilt by mirror-
ing its well-preserved left antimere. Concerning the 3D mesh of the
mandibles, we retrodeformed the right coronoid process in Blender
in light of careful comparations with the substantially undeformed
left coronoid process. Since we acquired both the 3D model of the
cranium and of the mandible by digital photogrammetry, the inter-
nal geometry of the Z. varolai skull is missing. The only way to
obtain the internal geometry of a vertebrate skull is via computed
axial tomography (CT scan). However, we used digital photogram-
metry here because moving the holotype specimen would have
seriously threatened its integrity; moreover, the large size and
weight of the Z. varolai skull would have made the acquisition
through conventional CT scans very difficult. Although the lack of
the internal cranial geometry may affect the results of biomechani-
cal simulations, previous studies have demonstrated that surface
meshes and simplified 3D geometries can provide reliable
2E. PERI ET AL.
estimations of reaction forces associated with biting actions (which
are the focus of the present work) and allow for general analyses of
stress distribution (Rayfield et al. 2007; Snively et al. 2015).
Reconstruction of the muscles
To estimate the bite force of Z. varolai we followed the methods
proposed by Snively et al. (2015) for investigating the bite of
Basilosaurus isis: the bite was considered static, where the velocity
of muscles is 0 m/s and exerting isometric force. In this condition,
the muscle force is equal to the anatomical cross-section of the
muscle multiplied by the specific muscular tension. In several
studies, the specific tension of the mammalian musculature has
been set to 30 N/cm
2
(e.g., Weijs and Hillen 1985; Thomason
1991; Wroe et al. 2005; Snively et al. 2015); however, factors like
the pennation of the muscle and changes in the fibre length could
increase this value (Koolstra et al. 1988; Wroe et al. 2005; McHenry
et al. 2007; Snively et al. 2015). Considering the significant penna-
tion of the mammalian temporalis muscle as well as the available
data in literature on the muscular anatomy of extant odontocetes
(Von Schulte and De Forest Smith 1918; Seagars 1982), in our
model we considered a specific muscular tension value of 37 N/
cm
2
, as already done elsewhere (Christiansen 2007; Snively et al.
2015).
In order to estimate the anatomical cross-section of the tempor-
alis muscle, we used the ‘dry-skull’ method (Thomason 1991): in
the Blender workspace, we modelled a polygon having the shape of
the area described by the zygomatic arch (which is defined by the
zygomatic process of the squamosal and lacrimo-jugal complex)
and the lateral wall of the temporal fossa as appearing in ventral
view. Considering the strong asymmetry that affects the cranium of
physeteroids (Bianucci and Landini 2006; Lambert et al. 2017, 2020;
Collareta et al. 2020b), we repeated the process on both the right
and left sides of the skull. The cross-section of the masseter was
harder to estimate than that of the temporalis, due to the lack of
clear bony constraints for this muscle. Following what was done by
Snively et al. (2015) in their study about the bite force of
Basilosaurus isis, we assumed the cross-section of the masseter to
be equal to 10% of that of the temporalis. To substantiate this
assumption, we observed that both Z. varolai and B. isis display
a wide cross-section of the temporalis muscle and elongated zygo-
matic arches (Bianucci and Landini 2006; Snively et al. 2015). This
is apparent by studying the ratio between the length of the zygo-
matic arch and the distance measured from the tip of the rostrum to
the posteriormost point of the temporal fossa: this ratio equals 0.28
in B. isis, 0.20 in Z. varolai, and 0.06 in Physeter macrocephalus.
Such values indicate that B. isis and Z. varolai bear similarly elon-
gated zygomatic arches, thus greatly differing from
P. macrocephalus in this respect. Based on these considerations,
the assumption of a cross-section area of the masseter equalling
10% of that of the temporalis is here regarded as reasonable for
Z. varolai. Subsequently, we digitally coupled the skull with the
mandibles in Blender and determined the direction of the muscular
vectors. We calculated the latter at two mouth gape angles (20° and
35°) in order to estimate the bite force exerted on different bite
scenarios. We chose such gape angles as they were selected for
carrying out the FEA analyses on B. isis (ca. 20°, measured from
Snively et al. 2015: Figure 1a) and Carcharodon carcharias (35°;
Wroe et al. 2008), thus allowing for robust comparisons of bite force
values in these marine predator species. As origin of the temporalis
muscle, we chose the entire surface of the temporal fossa (Figure 1),
following the reconstruction proposed by Lambert et al. (2014) for
Acrophyseter robustus and the muscular anatomy of extant odonto-
cetes (Von Schulte and De Forest Smith 1918; Seagars 1982).
Concerning the masseter muscle, we placed the origin of the pars
superficialis on the lacrimo-jugal complex, whereas the origin of the
pars profunda was reconstructed as distributed between the
lacrimo-jugal complex and the zygomatic process (Figure 1) (Von
Schulte and De Forest Smith 1918; Seagars 1982). Zygophyseter
varolai displays a keel along the anterior crest of the coronoid
process that we tentatively interpreted as marking the anterior
limit of the temporalis muscle insertion. We based our reconstruc-
tion of the masseter insertion on the observation of a low but well-
defined crest paralleling the ventral margin of the mandible and
projecting anteriorly from the mandibular condyle. Moreover, to
rebuild the masseter architecture of Z. varolai, we also followed
previous reconstructions for the holotype of A. deinodon (MNHN
SAS 1626) and anatomical data from extant odontocetes (Von
Schulte and De Forest Smith 1918; Seagars 1982; Lambert et al.
2008, 2017).
Simulating a biting action in a fossil mammal can prove
a challenging task: one of the most crucial phases is reconstructing
the jaw adduction muscle architecture of the species under exam-
ination. However, muscles are soft tissues that are only rarely
preserved in the fossil record; thus, researchers often base their
assumptions on soft-tissue anatomical data from extant taxa
(which are often quite rare in literature). Therefore, a future devel-
opment of physiological and anatomical studies aimed at increasing
our knowledge of muscle architecture and its functions in living
taxa is desirable (Bates and Falkingham 2018). In a mammalian
biting action, at least three muscular groups are involved: tempor-
alis, masseter, and pterygoid (Weijs 1985; Thomason 1991). For our
purposes, we did not estimate any force for the pterygoid because,
in mammals, the contribution of this muscle group to the mandible
adduction can be regarded as irrelevant (Snively et al. 2015).
Simulating a bite
We used the software GOM Inspect 2019 (https://www.gom.com/
it/software-3d.html) to reduce the polygon count and to optimise
the topology of the high-density photogrammetry mesh into
a cleaner, smaller mesh appropriate for FEA. The final result was
a 3D. stl model of the Zygophyseter cranium having 10000 vertices
and 20008 faces (Figure 1). To perform the bite simulations, we
used Autodesk Inventor 2020 (https://www.autodesk.it/products/
Figure 1. Reconstruction of the Zygophyseter varolai skull and mandibles in lateral
view, based on the cast of the holotype (MSNUP I-16828), and schematic recon-
struction of the temporalis (red) and masseter (including the pars superficialis and
pars profunda) (yellow).
HISTORICAL BIOLOGY 3
inventor/overview), the finite element (FE) solver of the Autodesk
suite. In Autodesk Inventor, the model was converted to a FE mesh
consisting of 100076 nodes and 60327 elements. We set the material
as isotropic, and trade-off values between the mammalian compact
bone and dentine were adopted to describe the elastic behaviour of
the Z. varolai cranium (elastic modulus E = 17.4 GPa and Poisson’s
ratio = 0.34) (Martin et al. 2015; Snively et al. 2015). Concerning the
volumetric density, we assigned a value (1.38 gr/cm
3
) averaging the
density of the maxilla and occipital in the common dolphin
(Delphinus delphis) (de Buffrénil and Sire J-Y 1986). It is worth
mentioning here that the cranium of the extant sperm whale
P. macrocephalus displays an amphitheatre-shaped supracranial
basin formed by a macroporous lamina between two denser bony
layers (Alam et al. 2016). Such a peculiar osteoanatomical structure
likely results in a lower bone density compared to other toothed
whales. However, based on the observation of broken bone surfaces
in the holotypes of Z. varolai and A. deinodon, we contend that
macroraptorial sperm whales did not display a macroporous
lamina.
To simulate the mandibular joints, we placed a fixed constraint
on each squamosal at level of the mandibular fossa; in addition,
a third fixed constraint was placed alternatively on the posterior-
most and anteriormost upper left teeth, thus simulating the resis-
tance of a food item during posterior and anterior biting actions,
respectively. The reaction force generated at the dental constraint
represents the bite force exerted in that specific point (following
Snively et al. 2015). Varying the position of the dental constraint
and the gape angle of the mouth, we made four simulations corre-
sponding to four load cases:
●20° gape angle, constraint at the anteriormost teeth (anterior
bite)
●20° gape angle, constraint at the posteriormost tooth (poster-
ior bite)
●35° gape angle, constraint at the anteriormost tooth (anterior
bite)
●35° gape angle, constraint at the posteriormost tooth (poster-
ior bite)
Finally, we compared the von Mises stress patterns obtained for the
four loading cases, to explore how stress distribution varies during
an anterior and posterior biting actions.
Comparative palaeoecology
In order to compare the bite force of Z. varolai with that exerted by
an extant marine apex predator in a comparative palaeoecological
framework, we estimated the body mass of a hypothetical great white
shark (Carcharodon carcharias) that could generate the same bite
forces estimated for Zygophyseter at 35° gape angle by following the
equation proposed by Wroe et al. (2008). Furthermore, we applied
the equation provided by Kohler et al. (1996) to calculate the total
length of such a hypothetical great white shark. We did not perform
this calculation for the bite force at 20° gape angle because Wroe et al.
(2008) proposed their bite force estimation at a gape angle of 35°.
Consequently, doing the same calculation with the Z. varolai bite
force at 20° would produce misleading data.
Results
The bite force results obtained from our FE simulations in this
study are reported in Table 1 . Considering a specific muscular
tension of 37 N/cm
2
, we calculated a force of 18645 N for the left
temporalis muscle and 18780 N for the right one. According to
previous assumptions, we estimated that the masseter muscles
exerted a force of 1864 N (left) and 1878 N (right). At a gape
angle of 20°, the FE simulation generated an anterior bite force of
4312 N, and a posterior bite force of 10103 N. The bite simulation at
a greater gape angle (35°) yielded slightly higher values of 4812 N at
the anterior end of the dental row and 10823 N at its posterior end.
We calculated that a posterior bite force of 10823 N would be
generated by a great white shark having a body mass of 1542.5 kg
and a total length of 536.3 cm. Similarly, an anterior bite force of
4812 N would be generated by a great white shark reaching a body
mass of 1249.6 kg and a total length of 501.3 cm.
Based on the FE simulations we also obtained the resulting von
Mises stress distributions on the cranium of Z. varolai during
a biting action (Figure 2). At the two different gape angles (20°
and 35°), the stress patterns are almost indistinguishable from each
other. The stress values affecting the cranium are between 4 MPa
and 19 MPa, with higher values being located in correspondence of
the lacrimo-jugal complex and the dental constraints (Figure 2). In
the posterior bite simulations (Figure 2a, b, c, d), the stress mainly
affects the supracranial basin, with three major peaks being located
medial to the left antorbital notch, in correspondence of an ante-
roposteriorly elongated ridge that is grossly aligned with the right
antorbital notch and on the left lateral border of the supracranial
basin. The anterior bite load cases exhibit a von Mises stress pattern
that is anteriorly projected, involving the rostrum for most of its
length (Figure 2e, f, g, h). The von Mises stress values are higher at
the base of the rostrum and decrease forward. As we used a cavity-
filling 3D mesh, the resulting stress distribution across the supra-
cranial basin could be slightly affected by the lack of modelling of
the hollow spaces that are found in this region of the neurocranium
(e.g. the facial terminations, the infraorbital canal branches and the
nasal cavity). However, this issue should not affect the stress pattern
on the rostrum, which appears to be a rather massive structure,
lacking apparent foramination.
Discussion
Comparing bite force magnitudes
Much of the biomechanic studies on cetaceans (both extant and
extinct) have been focussed on motion, physical properties of
tissues, hearing, and sound production; analyses of the feeding
mechanics are quite scarce in literature (Fish 1998; de Buffrénil
et al. 2000; Rohr and Fish 2004; Yamato et al. 2008; Bagnoli et al.
2011; Loch et al. 2013; Loch and van Vuuren 2016; Tubelli and
Ketten 2019). In one of the few investigations about this issue, the
bite force of the archaeocete Basilosaurus isis was estimated at the
specific tension of 37 N/cm
2
(Snively et al. 2015). The posterior and
anterior bite forces estimated for Zygophyseter varolai at 20° gape
angle are, respectively, 39.6% and 66.3% weaker than the
Table 1. Input muscular data and resulting forces obtained from the biting
simulation at 20° and 35° gape angle. Note that all the results have been calculated
at a specific tension of 37 N/cm
2
.
Gape angle 20° Gape angle 35°
Cross-section of the left temporalis muscle 503.93 cm
2
503.93 cm
2
Cross-section of the left masseter muscle 50.39 cm
2
50.39 cm
2
Cross-section of the right temporalis muscle 507.56 cm
2
507.56 cm
2
Cross-section of the right masseter muscle 50.76 cm
2
50.76 cm
2
F temporalis left muscle 18645 N 18645 N
F masseteric left muscle 1864 N 1864 N
F temporalis right muscle 18780 N 18780 N
F masseteric right muscle 1878 N 1878 N
Anterior bite force 4312 N 4812 N
Posterior bite force 10103 N 10823 N
4E. PERI ET AL.
corresponding values in B. isis (Snively et al. 2015). We only
compared the Z. varolai bite force at 20° because this gape angle
is similar to that used for the B. isis bite simulations (measured from
Snively et al. 2015: Figure 1a). The disparity of bite force values
between Z. varolai and B. isis is not surprising: indeed, Z. varolai
displays a smaller cross-section of the temporalis muscle, and con-
sequently, a less developed mandible adduction power.
Furthermore, Z. varolai bears a proportionally more elongated
rostrum than B. isis; this is clear when comparing the ratios between
the length of the rostrum and the distance between the tip of the
rostrum and the posteriormost point of the temporal fossa in
Z. varolai (0.56) and B. isis (0.51). This morphological difference
may contribute to the large gap between the anterior bite force of
Z. varolai and that of B. isis.
We calculated the hypothetical body length (501.3–536.3 cm) and
mass (1249.6–1542.5 kg) of a great white shark (Carcharodon carch-
arias) that would exert the same bite force as estimated for Z. varolai
at a gape angle of 35°. We noted a slight discrepancy between the
datum calculated for the anterior and posterior bite forces; this can be
easily explained by considering that the force dispersion is greater
along the elongated rostrum of Z. varolai than along the short and
rounded mouth arch of C. carcharias. Regardless for this, our results
suggest that Z. varolai generated the same bite force as a fully adult
great white shark (Long and Jones 1996; Estrada et al. 2006).
We also compared the biting performances of Z. varolai with
those of the extant saltwater crocodile (Crocodylus porosus, the
largest living reptile) at the caniniform and molariform teeth
(Read et al. 2007). Saltwater crocodiles grow throughout their life
Figure 2. Distribution patterns of the von Mises stress (s
vM
) on the Zygophyseter varolai skull obtained by FEA simulations. a,c) s
vM
distribution for a posterior bite simulation
at 35° gape angle (a, anterolateral view; c, dorsal view). b,d) s
vM
distribution for a posterior bite simulation at 20° gape angle (b, anterolateral view; d, dorsal view). e,g) s
vM
distribution for an anterior bite simulation at 35° gape angle (e, anterolateral view; g, dorsal view). f,h) s
vM
distribution for an anterior bite simulation at 20° gape angle (f,
anterolateral view; h, dorsal view).
HISTORICAL BIOLOGY 5
span, and consequently, their bite force greatly increases with age
(Erickson et al. 2012). The highest bite force recorded by Erickson
et al. (2012) for a saltwater crocodile is 11216 N (at the caniniform
tooth) and 16414 N (at the molariform tooth) in a 459 cm long
individual with a skull length of 65 cm; these results are higher than
the bite forces estimated for Z. varolai and place C. porosus near to
B. isis (Erickson et al. 2012). This is even more surprising consider-
ing that Z. varolai exhibits a body that is about 1.5 times longer and
a cranium that is more than twice as long than the tested individual
of C. porosus (Bianucci and Landini 2006; Erickson et al. 2012). The
reason behind these exceptional values in C. porosus could be
searched in the reptilian cranial and muscular architecture.
Indeed, reptiles have laterally unconstrained pterygoid muscles
and highly pennate temporalis muscles that exert a higher specific
tension than mammals. Thus, the lack of bony restrictions, and the
resulting greater space available for the muscle expansion in reptiles
might explain the high bite force values observed in C. porosus
(Thomason 1991; Christiansen 2007; Erickson et al. 2012; Snively
et al. 2015).
According to an estimation made via the ‘dry-skull’ method and
adjusted for the pennation of the mammalian musculature, the lion
(Panthera leo) can exert a bite force of 3388 N at the canine
(McHenry et al. 2007). The lion is one of the largest extant felids
and is known to use a powerful bite to hold and kill its prey
(Sunquist and Sunquist 2002; McHenry et al. 2007; Schaller 2009).
In felids, the canine tooth is placed in an anterior position along the
tooth row, thus we compared the canine bite force of P. leo with the
anterior bite force estimated for Z. varolai. Despite the long ros-
trum, and thus the relative force dispersion, Z. varolai results in
having a 21.4–29.6% higher anterior bite force value than the canine
bite force of P. leo (McHenry et al. 2007).
According to our simulation, in condition of static bite, Z. varolai
can generate a force of more than 10000 N at the posteriormost tooth,
depending on the gape angle. It has been calculated that 7000–9000 N
are needed to break a long bone of a large ungulate (Tanner et al.
2008). In addition, Erickson et al. (1996) estimated that the giant
theropod dinosaur Tyrannosaurus rex had to generate at least 6410 N
to damage a Triceratops ilium. Based on these lines of evidence,
Z. varolai was likely able to break or seriously damage the bones of
a prey by using its powerful posterior bite. Given all these considera-
tions, we hypothesise that Z. varolai was able to generate a great bite
force, even compared with other marine and terrestrial vertebrate
predators known to use biting actions for capturing, killing, and
sometimes processing (i.e., cutting or tearing) their prey items.
Feeding strategy by biomechanics
The high bite force values associated to Zygophyseter varolai are in
good agreement with several osteomorphological and dental char-
acters of this extinct sperm whale, including a wide temporal fossa,
a well-developed zygomatic process of the squamosal, and the
presence of deep occlusal facets on teeth suggesting a strong degree
of occlusion during bite (Bianucci and Landini 2006).
The mouth gape angle and the point where the reaction force is
measured are two important factors in a FE bite simulation (Bourke
et al. 2008; Wroe et al. 2008). Our results reveal that the bite force
estimated at 35° gape angle is higher than that at 20° gape angle
(both anteriorly and posteriorly); probably, 35° is close to the angle
at which the highest bite force is generated (i.e., the optimum of the
mechanical advantage) (Bourke et al. 2008; Wroe et al. 2008).
Future research efforts might investigate the variation of bite force
values with the gape angle increase, which is especially relevant in
the light of the wide mouth opening hypothesised for Z. varolai
(Bianucci and Landini 2006).
In our simulations, we recorded a higher bite force at the poster-
ior most dental constraint relative to the anteriorly positioned
constraint. This trend is not unexpected, because the posteriormost
tooth is closer to the rotation centre of the mandible (mandibular
fossa), and as such, to the lever fulcrum. Consequently, the huge
disparity between the anterior and posterior bite forces is a direct
consequence of the mandible lever mechanics (Wroe et al. 2008;
Lambert et al. 2014). Interestingly, bony outgrowths that have been
detected along the upper dental row in MUSM 1399, the holotype of
Acrophyseter robustus (a macroraptorial sperm whale phylogeneti-
cally and morphologically close to Z. varolai; Lambert et al. 2014,
2017), are especially developed nearby the posteriormost teeth.
These bony outgrowths have been interpreted as resulting from
the occlusal stress increase close to the rotation centre of the
mandible lever system (Lambert et al. 2014). Thus, the bony exo-
stoses observed in A. robustus and their functional interpretation
further support the bite force trend described by our bite simula-
tions in Z. varolai. Such a variation of bite force along the upper jaw
provides some clues about the feeding strategy of Z. varolai: this
macroraptorial sperm whale likely captured large food items with
an anterior bite and then cut them into pieces with a powerful
posterior bite. The anteriorly tapered rostrum and the procumbent
conical anterior teeth could have been used to efficiently grab
motile preys (Bianucci and Landini 2006). On the other hand, the
posterior mandibular teeth (the sole that were found within the
corresponding alveoli) display an obvious degree of mediolateral
compression of the root portion placed above the gingival collar
that possibly facilitated the shearing of food items (Bianucci and
Landini 2006). Even though this character could simply reflect the
accommodation of the voluminous lower cheek teeth within the
narrow space left by the large mandibular canal running through
the posterior portion of the dentary, the mediolateral compression
of the posterior postcanines might still represent an exaptation
facilitating the shearing of prey items.
Many morphological features among those listed above (e.g., the
anteriorly tapered rostrum, the wide temporal fossa, the procum-
bent anterior teeth) are shared between Z. varolai and Acrophyseter
spp.; in addition, both Z. varolai and A. deinodon display
a mediolateral compression of the posterior mandibular teeth
(Bianucci and Landini 2006; Lambert et al. 2008, 2017). Based on
these shared morphological characters, we propose for Zygophyseter
and Acrophyseter a ‘grip-and-shear’ feeding strategy consisting of
three phases: 1) grasping and piercing of the prey with the anterior
teeth, 2) moving the food item backward along the mouth, and 3)
cutting it with the posterior teeth. In Figure 3, this hypothetical
trophic behaviour is integrated within the framework of feeding
strategies proposed for extant marine mammals by Kienle et al.
(2017) and Berta and Lanzetti (2020). It is our content that such
a feeding strategy was also used by heterodont basilosaurids having
anterior conical teeth (canine and incisors) and even more medio-
laterally compressed posterior teeth (premolars and molars) (Uhen
2004; Fahlke 2012; Fahlke et al. 2013; Loch et al. 2015; Snively et al.
2015) and, as a plesiomorphic condition, by several heterodont
basal neocetes (e.g., squalodontids; see Loch et al. 2015; Collareta
et al. 2020a). Nevertheless, the trophic strategy of Zygophyseter and
Acrophyseter can hardly be considered as plesiomorphic. Indeed,
neither Eudelphis motzelensis nor the recently described Raphicetus
valenciae, both of which appear to have branched earlier than
Acrophyseter spp. and Z. varolai, display any osteological or dental
feature that could be positively associated with a macropredator
ecology (Lambert 2008; Lambert et al. 2020). Considering also the
incipient homodonty observed in all physeteroids (in which all
teeth feature one root and no accessory cusps), we interpret the
feeding strategy of Zygophyseter and Acrophyseter as a secondary re-
6E. PERI ET AL.
adaptation driven by a selective pressure towards a diet consisting
of large-bodied prey. A tooth morphology roughly similar to that of
Z. varolai and Acrophyseter spp. is also observed in some fossil
homodont odontocetes, e.g. the early Miocene Furcacetus exiros-
trum, which is characterised by large and procumbent upper inci-
sors (Bianucci et al. 2020). However, based on the delicate
sigmoidal rostrum and the moderately expanded temporal fossa,
F. exirostrum is believed to have used the anterolaterally oriented
teeth to catch quickly moving prey items such as shrimps and small
fishes (Bianucci et al. 2020). Similarly, the living river dolphin
Platanista gangetica uses the large and pointed (but not procum-
bent) anterior teeth and slender rostrum to grab and pierce small
preys, the latter being subsequently moved towards the throat with-
out being sheared (Pilleri 1970; McCurry et al. 2017).
The grip-and-shear feeding technique is not observed among
extant sarcophagous predators, since they hold and shake their prey
with the jaws to tear off large pieces of flesh (Figure 3), without
a proper cutting action (Werth 2000; Berta and Lanzetti 2020). This
shark-like feeding strategy is known as grip-and-tear (Figure 3), and
the sole extant cetaceans that use it are the killer whale (Orcinus
orca) and the false killer whale (Pseudorca crassidens) (Ford 2018;
Berta and Lanzetti 2020; Galatius et al. 2020). These large-sized
delphinids have a blunt and robust rostrum as well as cheek teeth
that are not laterally compressed (Werth 2006a; McCurry et al.
2017; Ford 2018; Berta and Lanzetti 2020; Galatius et al. 2020),
thus differing from the putative grip-and-shear feeders like
Z. varolai and B. isis (Uhen 1996; Bianucci and Landini 2006).
Regardless of the differences between the aforementioned trophic
strategies, the teeth of O. orca display long occlusion facets (pers.
obs. on MSNUP C298 and MSNUP C301) that are reminiscent of
the condition observed in Z. varolai and Acrophyseter spp.
(Bianucci and Landini 2006; Lambert et al. 2008, 2014, 2017).
However, the presence of well-developed occlusal facets is only
indicative of a strong dental occlusion and an extensive use of the
biting action during feeding (Bianucci and Landini 2006; Lambert
et al. 2017; Lambert and Bianucci 2019; Peri et al. 2020).
Furthermore, during a grip-and-tear feeding event, the predator
tears its prey into pieces with large bites, thus exerting a somewhat
ripping action (Werth 2006a; Berta and Lanzetti 2020). According
to our hypothesis, a grip-and-shear feeder would rather use
a posterior bite to cut its prey after capturing it with an anterior
bite. Therefore, the fundamental difference between these two feed-
ing strategies relies on how the biting action is used for prey
processing.
Thus, during the first phase of a grip-and-shear feeding action,
the prey is grabbed with an anterior bite; during the second phase, it
is moved posteriorly along the mouth towards the posterior tooth
rows; finally, during the third phase, it is sheared with a powerful
posterior bite. In our simulations of the anterior bite of Z. varolai
(Figure 2e, f, g, h), the stress pattern appears as projected towards
the tip of the rostrum, and the higher values are placed at the
rostrum base. This is a consequence of the mechanical response of
an elongated body being subjected to a force application at one of its
ends. In these conditions, the base of an elongated rostrum is
a ‘bending point’ where the tensile stress accumulates.
Consequently, the von Mises stress pattern resulting from our FE
model replicates well the first phase of a grip-and-shear feeding
action. After capture, the wounded prey was likely transported
towards the posterior portion of the mouth, possibly by means of
suction. Interestingly, the living sperm whale P. macrocephalus can
create a powerful suction at level of the gular cavity (Werth 2006a),
thus evoking the possibility that extinct physeteroids were also
capable of applying some degree of suction. Moreover, a phase of
transport of the food items by means of suction is observed in
extant raptorial longirostrine odontocetes (e.g., Inia georensis) as
well as in the more stoutly snouted Tursiops (Werth 2000, 2006a,
2006b; Bloodworth and Marshall 2005). In the posterior bite simu-
lations, the rostrum does not appear as stressed, except for its very
basal portion, close to the constraint at the posteriormost tooth
(Figure 2a, b, c, d). Here, the FEA shows an evident stress peak that
is probably related to the contact between the tooth and the food
item during the third phase of a grip-and-shear feeding action.
Based on these observations, the stress patterns resulting from our
FEA simulations appear as consistent with the feeding strategy
hypothesised above for Z. varolai. Interestingly, there is a peak of
stress insisting on the right side of the supracranial basin, in corre-
spondence of an evident ridge. This structure might counteract the
bending of the rostrum during a biting action, and especially in
occasion of an anterior bite (Figure 2). However, as already men-
tioned, the lack of modelling of the internal cranial geometry of the
cranium of Z. varolai prevents us from further anatomical and
functional interpretations of specific stress peaks while allowing
for a more general discussion of stress distribution on the neuro-
cranium and, especially, the rostrum.
Palaeoecological role and diet of Zygophyseter varolai
According to our estimates, Zygophyseter varolai was able to gen-
erate the same bite force as a great white shark individual well
beyond sexual maturity (Kohler et al. 1996; Wroe et al. 2008).
Extant Carcharodon carcharias is known as a highly generalist
predator that mainly feeds upon diminutive and fat-rich marine
mammals, such as fur seals and small toothed whales (Compagno
1984; Heithaus 2001; Brown et al. 2010; Skomal et al. 2017; Moro
et al. 2020). Several field studies and laboratory analyses have
demonstrated that extant white sharks prey upon marine mammals
Figure 3. Feeding strategies of marine mammal predators. Modified from Berta and Lanzetti (2020), with the addition of the grip-and-shear feeding (illustration of
Zygophyseter varolai modified from Bianucci and Landini 2006).
HISTORICAL BIOLOGY 7
in adulthood, when they reach a body length of 300–400 cm (Long
and Jones 1996; Estrada et al. 2006). Considering that the body
length of the holotype of Z. varolai was likely 650–700 cm (Bianucci
and Landini 2006), its ecology might have been somewhat similar to
that of an adult C. carcharias, and its diet mainly consisting of
medium-sized marine vertebrates. As already mentioned,
Z. varolai was retrieved from the Tortonian strata of the Cisterna
quarry (Lecce), which also provided remains of several other mar-
ine vertebrates, such as Messapicetus longirostris (Ziphiidae,
Cetacea), Metaxytherium medium (Dugongidae, Sirenia), Makaira
cf. M. nigricans (Istiophoriade, Perciformes) and Acanthocibius cf.
A. solandri (Scombridae, Perciformes) (Bianucci et al. 1992, 2003,
2016a; Carnevale et al. 2002); all of them would have been potential
prey items for Z. varolai. Besides Z. varolai, the Tortonian strata of
the Pietra leccese formation have yielded fossils of other marine
macropredators, including an unnamed macroraptorial sperm
whale found at approximately the same horizon as the holotype of
Z. varolai (Peri et al. 2020) and several large-sized sharks (e.g.,
Anotodus agassizi, Carcharocles megalodon, Cosmopolitodus hasta-
lis, Parotodus benedeni) (Menesini 1969). Such an abundance of
high trophic-level predators in the Mediterranean Basin during the
early late Miocene starkly contrasts with the present-day situation,
which sees the great white shark and occasionally the killer whale as
the sole apex predators to be found in the Mediterranean trophic
chains (Notarbartolo di Sciara et al. 1993; Morey et al. 2003;
Abdulla 2004; Notarbartolo di Sciara and Reeves 2006;
Notarbartolo di Sciara 2016). The late Miocene presence of multiple
top predators has previously been explained with high productivity
conditions that led to a high availability of food items for a broad
spectrum of marine vertebrates (Peri et al. 2020). Sedimentologic
evidence of high productivity, such as phosphate-rich levels asso-
ciated with glauconite, has been reported from several localities of
the central Mediterranean (Salento Peninsula, Sicily, Malta and
Crete) (Föllmi et al. 2008, 2015; Catanzariti and Gatt 2014;
Vescogni et al. 2018). This suggests the presence of nutrient-laden
currents from the eastern Mediterranean that replenished the cen-
tral basin and supported the late Miocene macropredator guild
retrieved from the Pietra leccese formation (Menesini 1969;
Bianucci and Landini 2006; Peri et al. 2020).
Remarks on the Miocene marine macropredators
The results obtained in this study need to be framed in the context
of the complex ecology of Miocene seas. Indeed, besides a number
of genera and species that are based on taxonomically diagnostic
skeletal materials, isolated teeth referable to macroraptorial physe-
teroids have been reported from middle and upper Miocene depos-
its of several localities of the Americas, Asia and Europe (e.g.,
Kimura et al. 2006; Hasegawa et al. 2006; Marra et al. 2016;
Reumer et al. 2017; Piazza et al. 2018; Lambert and Bianucci
2019). As already mentioned, the chronostratigraphic and geo-
graphic distribution of the published remains of macroraptorial
sperm whales suggests that this group impressively radiated during
the middle and late Miocene (Lambert et al. 2017). In the light of
the presence of at least six species of macropredator sperm whales
(Acrophyseter deinodon, A. robustus, Livyatan melvillei,
Zygophyseter varolai, and two unnamed taxa identified from iso-
lated dental remains by Marra et al. 2016 and Peri et al. 2020)
during the late Miocene, the present-day stock of high-trophic
level odontocete predators appears greatly depleted, with two del-
phinids – i.e., the killer whale (Orcinus orca) and the false killer
whale (Pseudorca crassidens) – being the sole macropredators
among living toothed whales (Baird et al. 2008; Barrett-Lennard
et al. 2011; Ford et al. 2011; Pitman et al. 2015; Ford 2018; Baird
2018; Galatius et al. 2020). Considering the taxonomic composition
of the highest trophic levels, a shift likely occurred in Plio-
Pleistocene epochs, with sperm whales (acting as apex consumers
in the late Miocene) being replaced in this trophic position by large-
sized delphinids. Besides macroraptorial sperm whales, large-sized
elasmobranchs like Anotodus agassizii, Carcharocles megalodon,
Cosmopolitodus hastalis and C. plicatilis roamed the seas as apex
predators during the middle and late Miocene (Menesini 1969;
Purdy et al. 2001; Collareta et al. 2017a, 2017b; Boessenecker et al.
2019; Landini et al. 2017; Perez et al. 2018). On the other hand,
large-sized extant lamnid and carcharhinid sharks (e.g.,
Carcharhinus leucas, Carcharodon carcharias and Galeocerdo
cuvier) are often regarded as top predators within their habitats
(Long and Jones 1996; Simpfendorfer et al. 2001; Estrada et al. 2006;
Kim et al. 2012; Heupel et al. 2014); however, they do not reach the
giant size of mega-toothed sharks of the Miocene (Collareta et al.
2017a; Boessenecker et al. 2019).
All things considered, the late Miocene oceans displayed
a greater diversity of large-sized macropredators than today; in
addition, several such forms have been retrieved in the same sedi-
mentary bodies, thus suggesting a cohabitation in the same marine
areas (e.g. Carnevale et al. 2002; Bianucci et al. 2016; Peri et al. 2020;
Bosio et al. 2021). Nowadays, macroraptorial sperm whales are
extinct, and the reasons behind this disappearance are tentatively
traced back to the late Neogene establishment of gigantism as the
size standard among baleen whales (Lambert et al. 2010; Marx and
Fordyce 2015; Slater et al. 2017; Bianucci et al. 2019). Furthermore,
a global cooling occurred at the end of the Miocene (about 7–
5.4 Ma) may have reduced the geographical range of these macro-
raptorial physeteroids and led to the disappearance of medium-
sized baleen whale faunas (Lambert et al. 2010; Herbert et al. 2016;
Tanner et al. 2020). Similar biotic and abiotic drivers, together with
the emergence of modern ecomorphotypes such as those repre-
sented by the great white shark and the killer whale, have been
evoked for explaining the decline and the extinction of the otodon-
tid lineage in the early Pliocene (ca. 5.3–3.5 Ma) (Collareta et al.
2017a; Boessenecker et al. 2019; Pimiento et al. 2019).
Conclusions and perspectives
We used the ‘dry skull’ method and the finite element analysis
(FEA) to estimate the bite force of the macroraptorial sperm
whale Zygophyseter varolai from the late Miocene of southern
Italy. We set four different load cases to obtain anterior and poster-
ior bite force estimated at 20° and 35° gape angles. From the FEA
simulation, we obtained an estimation of 4312 N (20° gape angle)
and 4812 N (35° gape angle) for the anterior bite. We also estimated
that Z. varolai generated 10103 N (20° gape angle) and 10823 N (35°
gape angle) at the posterior bite.
Through mathematical formulas, we calculated that Z. varolai
exerted the same bite force of an adult great white shark reaching
more than 500 cm of body length. Extant white sharks begin to prey
upon marine mammals when they reach 300–400 cm of body length.
Consequently, we hypothesise that Z. varolai had an analogous diet
and that it fed upon the small and medium-sized marine vertebrate
fauna retrieved from the Tortonian strata of the Pietra leccese
formation.
The obtained bite force results are similar to, though somewhat
lower than, those estimated in the basilosaurid archaeocete
Basilosaurus isis in a previous study. According to our estimations,
Z. varolai exerted a high bite force, most likely sufficient to break
the bones of its prey. Based on the bite force variations along the
maxilla and the teeth and cranial morphology of Z. varolai, we
hypothesise that this extinct sperm whale grasped its food item
8E. PERI ET AL.
with an anterior bite, moved it backward along the mouth and
finally cut it with a powerful posterior bite. This hypothetic feeding
strategy, here named ‘grip-and-shear’, was likely shared by the
phylogenetically and morphologically close sperm whale genus
Acrophyseter. Some modern odontocetes use slightly different feed-
ing strategies as they grab and tear apart large-sized food items
(grip-and-tear feeding), snap small preys with anterior pointed
teeth to swallow them entirely (pierce feeding) or smash them
with their posterior teeth (crushing feeding). The stress patterns
derived from the FEA appear as consistent with the grip-and-shear
feeding strategy proposed for Z. varolai: the anterior bite simula-
tions show a stress pattern that is anteriorly projected on the
rostrum, while the posterior bite simulations reveal a stress peak
at the rostrum base that replicates the contact between the posterior
cutting tooth and the food item.
This is the first study that investigates the bite mechanics of
a macroraptorial physeteroid using FEA. Such a biomechanical
approach might be applied to shed new light on the trophic spectrum
and the feeding strategies of other macroraptorial sperm whales,
including the giant putative whale-eater Livyatan melvillei. A better
understanding of these aspects will greatly contribute to unravel the
complex trophic relationships in the Miocene oceans, which were
home to a surprisingly high diversity of large-sized predators.
Acknowledgments
We are grateful to Chiara Sorbini for providing access to the palaeontological
material studied in the present work. We also thank Olivier Lambert and
Toshiyuki Kimura who greatly contributed to improve the quality of this
paper with their useful advice. Not least, we are grateful to Gareth Dyke for
his expert editorial support.
Disclosure statement
No potential conflict of interest was reported by the author(s).
ORCID
Emanuele Peri http://orcid.org/0000-0001-8635-5379
Peter L. Falkingham http://orcid.org/0000-0003-1856-8377
Alberto Collareta http://orcid.org/0000-0002-6513-8882
Giovanni Bianucci http://orcid.org/0000-0001-7105-0863
References
Abdulla A. 2004. Status and conservation of sharks in the Mediterranean Sea.
IUCN Tech Pap. 144:1–6.
Alam P, Amini S, Tadayon M, Miserez A, Chinsamy A. 2016. Properties and
Architecture of the Sperm Whale Skull Amphitheatre. Zoology. 119(1):42–
51. https://doi.org/10.1016/j.zool.2015.12.001
Anderson PSL, Westneat MW. 2009. A biomechanical model of feeding kine-
matics for Dunkleosteus terrelli (Arthrodira, Placodermi). Paleobiology. 35
(2):251–269. doi:10.1666/08011.1.
Bagnoli P, Cozzi B, Zaffora A, Acocella F, Fumero R, Laura Costantino M. 2011.
Experimental and computational biomechanical characterisation of the
tracheo-bronchial tree of the bottlenose dolphin (Tursiops truncatus) during
diving. J Biomech. 44(6):1040–1045.
Baird RW. 2018. False Killer Whale: pseudorca crassidens. In: Würsig B, Jgm T,
Km K, editors. Encyclopedia of Marine Mammals. Third Edition ed. San
Diego (CA): Academic Press; p. 347–349.
Baird RW, Gorgone AM, McSweeney DJ, Webster DL, Salden DR, Deakos MH,
Ligon AD, Schorr GS, Barlow J, Mahaffy SD. 2008. False killer whales
(Pseudorca crassidens) around the main Hawaiian Islands: long-term site
fidelity, inter-island movements, and association patterns. Mar Mammal
Sci. 24(3):591–612.
Barrett-Lennard LG, Matkin CO, Durban JW, Saulitis EL, Ellifrit D. 2011. Predation
on gray whales and prolonged feeding on submerged carcasses by transient killer
whales at Unimak Island, Alaska. Mar Ecol Prog Ser. 421:229–241.
Bates KT, Falkingham PL. 2018. The importance of muscle architecture in
biomechanical reconstructions of extinct animals: a case study using
Tyrannosaurus rex. J Anat. 233(5):625–635.
Bell PR, Snively E, Shychoski L. 2009. A comparison of the jaw mechanics in
hadrosaurid and ceratopsid dinosaurs using finite element analysis. Anat Rec.
292(9):1338–1351.
Berta A, Lanzetti A. 2020. Feeding in marine mammals: an integration
of evolution and ecology through time. Palaeontol Electron. 23(2):1–42.
Bianucci G, Collareta A, Post K, Varola A, Lambert O. 2016a. A new record of
Messapicetus from the Pietra Leccese (late Miocene, Southern Italy): anti-
tropical distribution in a fossil beaked whale (Cetacea, Ziphiidae). Riv Ital
Paleontol S. 122(1):63–74.
Bianucci G, De Muizon C, Urbina M, Lambert O. 2020. Extensive diversity and
disparity of the early Miocene platanistoids (Cetacea, odontoceti) in the
Southeastern Pacific (Chilcatay Formation, Peru). Life. 10. doi:10.3390/
life10030027.
Bianucci G, Di Celma C, Landini W, Post K, Tinelli C, De Muizon C,
Gariboldi K, Malinverno E, Cantalamessa G, Gioncada A, et al. 2016.
Distribution of fossil marine vertebrates in Cerro Colorado, the type locality
of the giant raptorial sperm whale Livyatan melvillei (Miocene, Pisco
Formation, Peru). J Maps. 12(3):543–557.
Bianucci G, Landini W. 2006. Killer sperm whale: a new basal physeteroid
(Mammalia, Cetacea) from the Late Miocene of Italy. Zool J Linn Soc-
Lond. 148(1):103–131.
Bianucci G, Landini W, Varola A. 1992. Messapicetus longirostris, a new genus
and species of Ziphiidae (Cetacea) from the late Miocene of ‘Pietra leccese’
(Apulia, Italy). Boll Soc Paleontol I. 31(2):261–264.
Bianucci G, Landini W, Varola A. 2003. New records of Metaxytherium
(Mammalia: Sirenia) from the late Miocene of Cisterna quarry (Apulia,
southern Italy). Boll Soc Paleontol I. 42(1–2):59–63.
Bianucci G, Marx FG, Collareta A, Di Stefano A, Landini W, Morigi C, Varola A.
2019. Rise of the titans: baleen whales became giants earlier than thought.
Biol Letters. 15:5. doi:10.1098/rsbl.2019.0175
Bianucci G, Varola A. 2014. I cetacei fossili della Pietra leccese nei musei del
Salento [Fossil cetaceans from the Pietra leccese formation in the Salento
museums]. Museol Sci Mem. 13:130–134.
Bloodworth B, Marshall CD. 2005. Feeding kinematics of Kogia and Tursiops
(Odontoceti: cetacea): characterization of suction and ram feeding. J Exp
Biol. 208(19):3721–3730.
Boersma AT, Pyenson ND. 2015. Albicetus oxymycterus, a new generic name and
redescription of a basal physeteroid (Mammalia, Cetacea) from the Miocene
of California, and the evolution of body size in sperm whales. PLoS One. 10
(12):e0135551.
Boessenecker RW, Churchill M, Buchholtz EA, Beatty BL, Geisler JH. 2020.
Convergent Evolution of Swimming Adaptations in Modern Whales
Revealed by a Large Macrophagous Dolphin from the Oligocene of South
Carolina. Curr Biol. 30(16):3267–3273.e2.
Boessenecker RW, Ehret DJ, Long DJ, Churchill M, Martin E, Boessenecker SJ.
2019. The early Pliocene extinction of the mega-toothed shark Otodus mega-
lodon: a view from the eastern North Pacific. PeerJ. 7(2):e6088.
Bosio G, Collareta A, Di Celma C, Lambert O, Marx FG, De Muizon C,
Gioncada A, Gariboldi K, Malinverno E, Varas-Malca R, et al. 2021.
Taphonomy of marine vertebrates of the Pisco Formation (Miocene, Peru):
insights into the origin of an outstanding Fossil-Lagerstätte. PLoS One. 16
(17):e0254395. doi:10.1371/journal.pone.0254395.
Bourke J, Wroe S, Moreno K, McHenry C, Clausen P. 2008. Effects of gape and
tooth position on bite force and skull stress in the dingo (Canis lupus dingo)
using a 3-dimensional finite element approach. PLoS One. 3(5):e2200.
doi:10.1371/journal.pone.0002200.
Brown AC, Lee DE, Bradley RW, Anderson S. 2010. Dynamics of white shark
predation on pinnipeds in California: effects of prey abundance. Copeia. 2010
(2):232–238.
Bullard TS, Caldwell MW. 2010. Redescription and rediagnosis of the tylosaur-
ine mosasaur Hainosaurus pembinensis Nicholls, 1988, as Tylosaurus pembi-
nensis (Nicholls, 1988). J Vertebr Paleontol. 30(2):416–426.
Carnevale G, Sorbini C, Landini W, Varola A. 2002. Makaira cf. M. nigricans
Lacepede, 1802 (Teleostei: Perciformes: istiophoridae) from the Pietra
Leccese, Late Miocene, Apulia, Southern Italy. Palaeontogr Ital. 88:63–75.
Catanzariti R, Gatt M. 2014. Calcareous nannofossil biostratigraphy from the
middle/late Miocene of Malta and Gozo (Central Mediterranean).
Stratigraphy. 11(18):303–336.
Christiansen P. 2007. Comparative bite forces and canine bending strength in
feline and sabretooth felids: implications for predatory ecology. Zool J Linn
Soc-Lond. 151(2):423–437.
Collareta A, Di Cencio A, Ricci R, Bianucci G. 2020a. The shark-toothed dolphin
Squalodon (Cetacea: odontoceti) from the remarkable montagna della
Majella marine vertebrate assemblage (Bolognano formation, Central Italy).
HISTORICAL BIOLOGY 9
Carnets Geol. 20(2):19–28.
Collareta A, Lambert O, De Muizon C, Palomino AMB, Urbina M, Bianucci G.
2020b. A new physeteroid from the late Miocene of Peru expands the
diversity of extinct dwarf and pygmy sperm whales (Cetacea: odontoceti:
kogiidae). C R Palevol. 95(5):79–100.
Collareta A, Lambert O, Landini W, Di Celma C, Malinverno E, Varas-Malca R,
Urbina M, Bianucci G. 2017a. Did the giant extinct shark Carcharocles
megalodon target small prey? Bite marks on marine mammal remains from
the late Miocene of Peru. Palaeogeogr Palaeocl. 469:84–91.
Collareta A, Landini W, Chacaltana C, Valdivia W, Altamirano-Sierra A,
Urbina-Schmitt M, Bianucci G. 2017b. A well preserved skeleton of the fossil
shark Cosmopolitodus hastalis from the late Miocene of Peru, featuring fish
remains as fossilized stomach contents. Riv Ital Paleontol S. 123(1):11–22.
doi:10.13130/2039-4942/8005.
Compagno LJV 1984. FAO species catalogue. Vol. 4. Sharks of the world. An
annotated and illustrated catalogue of shark species known to date. Part 2.
Carcharhiniformes FAO Fish Synopsis. 251–655.
Cooper JA, Pimiento C, Ferrón HG, Benton MJ. 2020. Body dimensions of the
extinct giant shark Otodus megalodon: a 2D reconstruction. Sci Rep.
10:14596. doi:10.1038/s41598-020-71387-y
de Buffrénil V, Sire J-Y SD. 1986. Comparaison de la structure et du volume
squelettiques entre un delphinidé (Delphinus delphis L.) et un mammifère
terrestre (Panthera leo L.) [Comparison of skeletal structure and volume
between a delphinid (Delphinus delphis L.) and a land mammal (Panthera
leo L.)]. Can J Zool. 64(8):1750–1756.
de Buffrénil V, Zylberberg L, Traub W, Casinos A. 2000. Structural and mechan-
ical characteristics of the hyperdense bone of the rostrum of Mesoplodon
densirostris (Cetacea, Ziphiidae): summary of recent observations. Hist Biol.
14(1–2):57–65.
Díez Díaz V, Mallison H, Asbach P, Schwarz D, Blanco A. 2021. Comparing
surface digitization techniques in palaeontology using visual perceptual
metrics and distance computations between 3D meshes. Palaeontology. 64
(2):179–202.
Driscoll DA, Dunhill AM, Stubbs TL, Benton MJ. 2019. The mosasaur fossil
record through the lens of fossil completeness. Palaeontology. 62(1):51–75.
Ehret DJ, Ebersole J. 2014. Occurrence of the megatoothed sharks
(Lamniformes: otodontidae) in Alabama, USA. PeerJ. 2(1):1–18.
Erickson GM, Gignac PM, Steppan SJ, Lappin AK, Vliet KA, Brueggen JD,
Inouye BD, Kledzik D, Webb GJW. 2012. Insights into the ecology and evolu-
tionary success of crocodilians revealed through bite-force and tooth-pressure
experimentation. PLoS One. 7(3):e31781. doi:10.1371/journal.pone.0254395.
Erickson GM, Van Kirk SD, Su J, Levenston ME, Caler WE, Carter DR. 1996.
Bite-force estimation for Tyrannosaurus rex from tooth-marked bones.
Nature. 382(6593):706–708.
Estrada JA, Rice AN, Natanson LJ, Skomal GB. 2006. Use of isotopic analysis of
vertebrae in reconstructing ontogenetic feeding ecology in white sharks.
Ecology. 87(4):829–834.
Fahlke JM. 2012. Bite marks revisited – evidence for middle-to-late Eocene
Basilosaurus isis predation on Dorudon atrox (both Cetacea,
Basilosauridae). Palaeontol Electron. 15(3):32A. doi:10.26879/341.
Fahlke JM, Autenrieth M. 2016. Photogrammetry vs. Micro-CT scanning for 3D
surface generation of a typical vertebrate fossil - a case of study. J Paleontol
Tech. 14:1–18.
Fahlke JM, Bastl KA, Semprebon GM, Gingerich PD. 2013. Paleoecology of
archaeocete whales throughout the Eocene: dietary adaptations revealed by
microwear analysis. Palaeogeogr Palaeocl. 386:690–701.
Falkingham PL. 2012. Acquisition of high resolution three-dimensional models
using free, open-source, photogrammetric software. Palaeontol Electron. 15
(1):1T. doi:10.26879/264.
Falkingham PL, Bates KT, Avanzini M, Bennett M, Bordy EM, Breithaupt BH,
Castanera D, Citton P, Díaz-Martínez I, Farlow JO, et al. 2018. A standard
protocol for documenting modern and fossil ichnological data.
Palaeontology. 61(4):469–480.
Falkingham PL, Bates KT, Farlow JO. 2014. Historical photogrammetry: bird’s
Paluxy River dinosaur chase sequence digitally reconstructed as it was prior
to excavation 70 years ago. PLoS One. 9(4):e93247. doi:10.1371/journal.
pone.0093247.
Falkingham PL, Turner ML, Gatesy SM. 2020. Constructing and testing hypoth-
eses of dinosaur foot motions from fossil tracks using digitization and
simulation. Palaeontology. 63(6):865–880.
Fau M, Cornette R, Houssaye A. 2016. Photogrammetry for 3D digitizing bones
of mounted skeletons: potential and limits. C R Palevol. 15(8):968–977.
Ferrón HG, Martínez-Pérez C, Botella H. 2017. Ecomorphological inferences in
early vertebrates: reconstructing Dunkleosteus terrelli (Arthrodira,
Placodermi) caudal fin from palaeoecological data. PeerJ. 5(12):1–20.
Fish FE. 1998. Comparative kinematics and hydrodynamics of odontocete
cetaceans: morphological and ecological correlates with swimming
performance. J Exp Biol. 201(20):2867–2877.
Foffa D, Cuff AR, Sassoon J, Rayfield EJ, Mavrogordato MN, Benton MJ. 2014.
Functional anatomy and feeding biomechanics of a giant Upper Jurassic
pliosaur (Reptilia: sauropterygia) from Weymouth Bay, Dorset, UK. J Anat.
225(2):209–219.
Föllmi KB, Gertsch B, Renevey J-P, De Kaenel E, Stille P. 2008. Stratigraphy
and sedimentology of phosphate-rich sediments in Malta and
south-eastern Sicily (latest Oligocene to early Late Miocene).
Sedimentology. 55(4):1029–1051.
Föllmi KB, Hofmann H, Chiaradia M, De Kaenel E, Frijia G, Parente M. 2015.
Miocene phosphate-rich sediments in Salento (southern Italy). Sediment
Geol. 327:55–71.
Ford JKB. 2018. Killer Whale: orcinus orca. In: Würsig B, Jgm T, Km K, editors.
Encyclopedia of Marine Mammals. Third Edition ed. San Diego (CA):
Academic Press; p. 531–537.
Ford JKB, Ellis GM, Matkin CO, Wetklo MH, Barrett-Lennard LG, Withler RE.
2011. Shark predation and tooth wear in a population of northeastern Pacific
killer whales. Aquat Biol. 11(3):213–224.
Fordyce RE. 2018. Cetacean Evolution. In: Würsig B, Thewissen JGM,
Kovacs KM, editors. Encyclopedia of Marine Mammals (Third Edition).
San Diego (CA): Academic Press; p. 180–185.
Galatius A, Racicot R, McGowen M, Olsen MT. 2020. Evolution and
Diversification of Delphinid Skull Shapes. iScience. 23(10):101543.
doi:10.1016/j.isci.2020.101543.
Gallagher WB. 2003. Oligotrophic oceans and minimalist organisms: col-
lapse of the Maastrichtian marine ecosystem and Paleocene recovery in
the Cretaceous-Tertiary sequence of New Jersey. Neth J Geosci.
82:225–231.
Hasegawa Y, Kimura T, Koda Y. 2006. Fossil physeterid from the Miocene
Urizura Formation, Taga Group, Ibaraki, Japan. Bull Gunma Museum Nat
Hist. 10:25–36.
Hassan MA, Westermann GEG, Hewitt RA, Dokainish MA. 2002. Finite-element
analysis of simulated ammonoid septa (extinct Cephalopoda): septal and
sutural complexities do not reduce strength. Paleobiology. 28(1):113–126.
Heithaus MR. 2001. Predator-prey and competitive interactions between sharks
(order Selachii) and dolphins (suborder Odontoceti): a review. J Zool. 253
(1):53–68.
Herbert TD, Lawrence KT, Tzanova A, Peterson LC, Caballero-Gill R, Kelly CS.
2016. Late Miocene global cooling and the rise of modern ecosystems. Nat
Geosci. 9(11):843–847.
Heupel MR, Knip DM, Simpfendorfer CA, Dulvy NK. 2014. Sizing up the
ecological role of sharks as predators. Mar Ecol Prog Ser. 495:291–298.
Hocking DP, Marx FG, Park T, Fitzgerald EMG, Evans AR. 2017. A behavioural
framework for the evolution of feeding in predatory aquatic mammals. P Roy
Soc B. 284:20162750. doi:10.1098/rspb.2016.2750
Jouve S, Bouya B, Amaghzaz M. 2005. A short-snouted dyrosaurid
(Crocodyliformes, Mesoeucrocodylia) from the Palaeocene of Morocco.
Palaeontology. 48(2):359–369.
Kienle SS, Law CJ, Costa DP, Berta A, Mehta RS. 2017. Revisiting the beha-
vioural framework of feeding in predatory aquatic mammals. P Roy Soc B.
284(1863):20171035. doi:10.1098/RSPB.2017.1035.
Kim SL, Tinker MT, Estes JA, Koch PL. 2012. Ontogenetic and
among-individual variation in foraging strategies of northeast Pacific white
sharks based on stable isotope analysis. PLoS One. 7(9):e45068. doi:10.1371/
journal.pone.0045068.
Kimura T, Hasegawa Y, Barnes LG. 2006. Fossil sperm whales (Cetacea,
Physeteridae) from Gunma and Ibaraki prefectures, Japan; with observations
on the Miocene fossil sperm whale Scaldicetus shigensis Hirota and Barnes,
1995. Bull Gunma Museum Nat Hist. 10:1–23.
Kohler NE, Casey JG, Turner PA. 1996. Length-length and length-weight rela-
tionships for 13 shark species from the Western North Atlantic. In: NOAA
Tech Rep Memo. NMMFS-NE. 110:1–22.
Koolstra JH, Tmgj VE, Weijs WA, Naeije M. 1988. A three-dimensional math-
ematical model of the human masticatory system predicting maximum
possible bite forces. J Biomech. 21(7):563–576.
Lambert O. 2008. Sperm whales from the Miocene of the North Sea: a
re-appraisal. Bull Inst R Sc N B. 78:277–316.
Lambert O, Bianucci G. 2019. How to break a sperm whale’s teeth: dental
damage in a large Miocene physeteroid from the North Sea Basin. J Vertebr
Paleontol. 39(4):e1660987. doi:10.1080/02724634.2019.1660987.
Lambert O, Bianucci G, Beatty BL. 2014. Bony outgrowths on the jaws of an
extinct sperm whale support macroraptorial feeding in several stem
physeteroids. Naturwissenschaften. 101(6):517–521.
Lambert O, Bianucci G, De Muizon C. 2008. A new stem-sperm whale (Cetacea,
Odontoceti, Physeteroidea) from the Latest Miocene of Peru. C R Palevol. 7
(6):361–369.
Lambert O, Bianucci G, De Muizon C. 2017. Macroraptorial sperm whales
(cetacea, odontoceti, physeteroidea) from the Miocene of Peru. Zool J Linn
Soc-Lond. 179(2):404–474.
10 E. PERI ET AL.
Lambert O, Bianucci G, Post K, De Muizon C, Salas-Gismondi R, Urbina M,
Reumer J. 2010. The giant bite of a new raptorial sperm whale from the
Miocene epoch of Peru. Nature. 466(7302):105–108.
Lambert O, De Muizon C, Urbina M, Bianucci G. 2020. A new longirostrine
sperm whale (Cetacea, Physeteroidea) from the lower Miocene of the Pisco
Basin (southern coast of Peru). J Syst Palaeontol. 18(20):1707–1742.
Landini W, Altamirano-Sierra A, Collareta A, Di Celma C, Urbina M, Bianucci
G. 2017. The late Miocene elasmobranch assemblage from Cerro Colorado
(Pisco Formation, Peru). J S Am Earth Sci. 73:168–190
Loch C, Kieser JA, Fordyce RE. 2015. Enamel Ultrastructure in Fossil Cetaceans
(Cetacea: archaeoceti and Odontoceti). PLoS One. 10(1):e0116557.
doi:10.1371/JOURNAL.PONE.0116557.
Loch C, Swain MV, Van Vuuren LJ, Kieser JA, Fordyce RE. 2013. Mechanical
properties of dental tissues in dolphins (Cetacea: delphinoidea and Inioidea).
Arch Oral Biol. 58(7):773–779.
Loch C, van Vuuren LJ. 2016. Ultrastructure, biomechanical and chemical
properties of the vestigial dentition of a Cuvier’s beaked whale. New Zeal
J Zool. 43(2):171–178.
Long DJ, Jones RE. 1996. White shark predation and scavenging on cetaceans in
the eastern North Pacific Ocean. In: Klimley AP, Ainley DG, editors. Great
White Sharks: the Biology of Carcharodon carcharias. San Diego (CA):
Academic Press; p. 293–307.
Madzia D, Cau A. 2017. Inferring ‘weak spots’ in phylogenetic trees: application
to mosasauroid nomenclature. PeerJ. 5(9):e3782. doi:10.7717/peerj.3782.
Mallison H, Wings O. 2014. Photogrammetry in paleontology-a practical guide.
J Paleontol Tech. 12:1–31.
Marra AC, Carone G, Bianucci G. 2016. Sperm whale teeth from the late
Miocene of Cessaniti (Southern Italy). Boll Soc Paleontol I. 55(3):223–225.
Martin RB, Burr DB, Sharkey NA, Fyhrie DP. 2015. Skeletal Tissue Mechanics.
New York (NY): Springer New York.
Marx FG, Fordyce RE. 2015. Baleen boom and bust: a synthesis of mysticete
phylogeny, diversity and disparity. R Soc Open Sci. 2:140434. doi:10.1098/
rsos.140434
McCurry MR, Fitzgerald EMG, Evans AR, Adams JW, McHenry CR. 2017. Skull
shape reflects prey size niche in toothed whales. Biol J Linn Soc. 121
(4):936–946.
McHenry CR. 2009. ‘Devourer of Gods’ The palaeoecology of the Cretaceous
pliosaur Kronosaurus queenslandicus [dissertation]. Newcastle upon Tyne
(NE): University of Newcastle.
McHenry CR, Wroe S, Clausen PD, Moreno K, Cunningham E. 2007.
Supermodeled sabercat, predatory behavior in Smilodon fatalis revealed by
high-resolution 3D computer simulation. Proc Natl Acad Sci USA. 104
(41):16010–16015.
Menesini E. 1969. Ittiodontoliti miocenici di Terra d’Otranto [Miocene ichthyo-
dontolites from Terra d’Otranto]. Palaeontogr Ital. 65:1–61.
Morey G, Martìnez M, Massutì E, Moranta J. 2003. The occurrence of white
sharks, Carcharodon carcharias, around the Balearic Islands (western
Mediterranean Sea). Environ Biol Fish. 68(4):425–432.
Moro S, Jona-Lasinio G, Block B, Micheli F, De Leo G, Serena F, Bottaro M,
Scacco U, Ferretti F. 2020. Abundance and distribution of the white shark in
the Mediterranean Sea. Fish Fish. 21(2):338–349.
Notarbartolo di Sciara G. 2016. Chapter One - Marine Mammals in the
Mediterranean Sea: an Overview. In: Notarbartolo Di Sciara G, Podestà M,
Curry BE, editors. Mediterranean Marine Mammal Ecology and Conservation,
Advances in Marine Biology 75. San Diego (CA): Academic Press; p. 1–36.
Notarbartolo di Sciara G, oMC V, Zanardelli M, Bearzi G, FJ B, Cavalloni B.
1993. Cetaceans in the central Mediterranean Sea: distribution and sighting
frequencies. Ital J Zool. 60(1):131–138.
Notarbartolo di Sciara G, Reeves R 2006. The status and distribution of
Cetaceans in the Black Sea and Mediterranean sea. Málaga; IUCN Centre
for Mediterranean Cooperation, p. 142.
Oldfield CC, McHenry CR, Clausen PD, Chamoli U, Parr WCH, Stynder DD,
Wroe S. 2012. Finite element analysis of ursid cranial mechanics and the
prediction of feeding behaviour in the extinct giant Agriotherium africanum.
J Zool. 286(2):171.
Perez VJ, Godfrey SJ, Kent BW, Weems RE, Nance JR. 2018. The transition
between Carcharocles chubutensis and Carcharocles megalodon (Otodontidae,
Chondrichthyes): lateral cusplet loss through time. J Vertebr Paleontol. 38(6):
e1546732. doi:10.1080/02724634.2018.1546732.
Perez VJ, Leder RM, Badaut T. 2021. Body length estimation of Neogene macro-
phagous lamniform sharks (Carcharodon and Otodus) derived from associated
fossil dentitions. Palaeontol Electron. 24(1):a09. doi:10.26879/1140.
Peri E, Collareta A, Bianucci G. 2020. A new record of physeteroidea from the
upper Miocene of the pietra leccese (southern Italy): systematics, paleoecol-
ogy and taphonomy of a fossil macroraptorial sperm whale. Riv Ital Paleontol
S. 126(3):751–769.
Petti FM, Avanzini M, Belvedere M, De Gasperi M, Ferretti P, Girardi S,
Remondino F, Tomasoni R. 2008. Digital 3D modelling of dinosaur foot-
prints by photogrammetry and laser scanning techniques: integrated
approach at the Coste dell’Anglone tracksite (Lower Jurassic, Southern
Alps, Northern Italy). Studi Trent Sci Nat, Acta Geol. 83:303–315.
Piazza DS, Agnolin FL, Lucero S. 2018. First record of a macroraptorial sperm
whale (Cetacea, Physeteroidea) from the Miocene of Argentina. Rev Bras
Paleontolog. 21(3):276–280.
Pilleri G. 1970. Observation on the behavior of Platanista gangetica in the Indus
and Brahmaputra rivers. Investig Cetacea. 2:27–60.
Pimiento C, Cantalapiedra JL, Shimada K, Field DJ, Smaers JB. 2019.
Evolutionary pathways toward gigantism in sharks and rays. Evolution. 73
(3):588–599.
Pitman RL, Ballance LT, Mesnick SI, Chivers SJ. 2001. Killer whale predation on
sperm whales: observations and implications. Mar Mammal Sci. 17
(3):494–507.
Pitman RL, Totterdell JA, Fearnbach H, Ballance LT, Durban JW, Kemps H.
2015. Whale killers: prevalence and ecological implications of killer whale
predation on humpback whale calves off Western Australia. Mar Mammal
Sci. 31:629–657. doi:10.1111/mms.12182
Polcyn MJ, Jacobs LL, Araújo R, Schulp AS, Mateus O. 2014. Physical drivers of
mosasaur evolution. Palaeogeogr Palaeocl. 400:17–27.
Puértolas-Pascual E, Blanco A, Brochu CA, Canudo JI. 2015. Review of the late
cretaceous-early Paleogene crocodylomorphs of Europe: extinction patterns
across the K-Pg boundary. Cretaceous Res. 57:565–590.
Purdy RW, Schneider VP, Applegate SP, McLellan JH, Meyer RL, Slaughter BH.
2001. The Neogene sharks, rays, and bony fishes from Lee Creek Mine,
Aurora, North Carolina. Sm C Paleob. 90:71–202.
Rayfield EJ, Milner AC, Xuan VB, Young PG. 2007. Functional morphology of
spinosaur ‘crocodile-mimic’ dinosaurs. J Vertebr Paleontol. 27(4):892–901.
Rayfield EJ, Norman DB, Horner CC, Horner JR, Smith PM, Thomason JJ,
Upchurch P. 2001. Cranial design and function in a large theropod dinosaur.
Nature. 409(6823):1033–1037.
Read MA, Grigg GC, Irwin SR, Shanahan D, Franklin CE. 2007. Satellite tracking
reveals long distance coastal travel and homing by translocated estuarine
crocodiles, Crocodylus porosus. PLoS One. 2(9):e949.
Reumer JWF, Mens TH, Post K. 2017. New finds of giant raptorial sperm whale
teeth (Cetacea, Physeteroidea) from the Westerschelde Estuary (province of
Zeeland, the Netherlands). Deinsea. 17:32–38.
Rohr JJ, Fish FE. 2004. Strouhal numbers and optimization of swimming by
odontocete cetaceans. J Exp Biol. 207(10):1633–1642.
Schaller GB. 2009. The Serengeti lion: a study of predator-prey relations.
Chicago (IL): University of Chicago Press.
Seagars DJ. 1982. Jaw structure and functional mechanics of six delphinids
(Cetacea: odontoceti). San Diego (CA): San Diego State University. master’s
thesis.
Shimada K, Becker MA, Griffiths ML. 2020. Body, jaw, and dentition lengths
of macrophagous lamniform sharks, and body size evolution in
Lamniformes with special reference to ‘off-the-scale’ gigantism of the
megatooth shark, Otodus megalodon. Hist Biol. 1–17. doi:10.1080/
08912963.2020.1812598
Simpfendorfer CA, Goodreid AB, Mcauley RB. 2001. Size, sex and geographic
variation in the diet of the tiger shark, Galeocerdo cuvier, from Western
Australian waters. Environ Biol Fish. 61(1):37–46.
Skomal GB, Braun CD, Chisholm JH, Thorrold SR. 2017. Movements of the
white shark Carcharodon carcharias in the North Atlantic Ocean. Mar Ecol
Prog Ser. 580:1–16.
Slater GJ, Goldbogen JA, Pyenson ND. 2017. Independent evolution of baleen
whale gigantism linked to Plio-Pleistocene ocean dynamics. P Roy Soc B.
284:20170546. doi:10.1098/rspb.2017.0546
Snively E, Fahlke JM, Welsh RC. 2015. Bone-breaking bite force of Basilosaurus
isis (Mammalia, Cetacea) from the late Eocene of Egypt estimated by finite
element analysis. PLoS One. 10(2):e0118380. doi:10.1371/JOURNAL.
PONE.0118380.
Sunquist M, Sunquist F. 2002. Wild Cats of the World. Chicago (IL): University
of Chicago Press.
Tanner JB, Dumont ER, Sakai ST, Lundrigan BL, Holekamp KE. 2008. Of arcs
and vaults: the biomechanics of bone-cracking in spotted hyenas (Crocuta
crocuta). Biol J Linn Soc. 95(2):246–255.
Tanner T, Hernández-Almeida I, Drury AJ, Guitián J, Stoll H. 2020. Decreasing
atmospheric CO2 during the late Miocene cooling. Paleoceanogr
Paleoclimatology. 35(12):2020PA003925. doi:10.1029/2020PA003925.
Thomason JJ. 1991. Cranial strength in relation to estimated biting forces in
some mammals. Can J Zool. 69(9):2326–2333.
Tubelli AA, Ketten DR. 2019. The role of material properties in cetacean hearing
models: knowns and unknowns. Aquat Mamm. 45(6):717–732.
HISTORICAL BIOLOGY 11
Uhen MD. 1996. Dorudon atrox (Mammalia, Cetacea): form, function, and
phylogenetic relationships of an archaeocete from the late middle
Eocene of Egypt [dissertation]. Ann Arbor (MI): University of
Michigan.
Uhen MD. 2004. Form, function, and anatomy of Dorudon atrox (Mammalia,
Cetacea): an archaeocete from the Middle to Late Eocene of Egypt. Pap
Palaeontol. 34:1–238.
Uhen MD. 2018. Basilosaurids and Kekenodontids. In: Würsig B,
Thewissen JGM, Kovacs KM, editors. Encyclopedia of Marine Mammals
(Third Edition). San Diego (CA): Academic Press; p. 78–80.
Vescogni A, Vertino A, Bosellini FR, Harzhauser M, Mandic O. 2018. New
paleoenvironmental insights on the Miocene condensed phosphatic layer of
Salento (southern Italy) unlocked by the coral-mollusc fossil archive. Facies.
64(2):1–21.
Von Schulte HW, De Forest Smith M. 1918. The external characters, skeletal
muscles, and peripheral nerves of Kogia breviceps (Blainville). B Am Mus Nat
Hist. 38:7–72.
Voss M, Antar MSM, Zalmout IS, Gingerich PD. 2019. Stomach contents of the
archaeocete Basilosaurus isis: apex predator in oceans of the late Eocene.
PLoS One. 14(1):e0209021. doi:10.1371/JOURNAL.PONE.0209021.
Weijs WA, Hillen B. 1985. Cross-sectional areas and estimated intrinsic strength
of the human jaw muscles. Acta Morphol Neer Sc. 23(3):267–274.
Werth AJ. 2000. Feeding in Marine Mammals. In: Schwenk K, editor. Feeding.
San Diego (CA): Academic Press; p. 487–526.
Werth AJ. 2004. Functional Morphology of the Sperm Whale Physeter macrocepha-
lus Tongue, with Reference to Suction Feeding. Aquat Mamm. 30(3):405–418.
Werth AJ. 2006a. Mandibular and dental variation and the evolution of suction
feeding in odontoceti. J Mammal. 87(3):579–588.
Werth AJ. 2006b. Odontocete suction feeding: experimental analysis of water
flow and head shape. J Morphol. 267(12):1415–1428.
Wroe S, Clausen P, McHenry C, Moreno K, Cunningham E. 2007.
Computer simulation of feeding behaviour in the thylacine and dingo
as a novel test for convergence and niche overlap. P Roy Soc B. 274
(1627):2819–2828.
Wroe S, Huber DR, Lowry M, McHenry C, Moreno K, Clausen P, Ferrara TL,
Cunningham E, Dean MN, Summers AP. 2008. Three-dimensional computer
analysis of white shark jaw mechanics: how hard can a great white bite?
J Zool. 276(4):336–342.
Wroe S, McHenry C, Thomason J. 2005. Bite club: comparative bite force in big
biting mammals and the prediction of predatory behaviour in fossil taxa.
P Roy Soc B. 272(1563):619–625.
Yamato M, Ketten DR, Arruda J, Cramer S. 2008. Biomechanical
and structural modeling of hearing in baleen whales. Bioacoustics.
17(1–3):100–102.
12 E. PERI ET AL.
