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Results from this study of the white shark Carcharodon carcharias include measurements obtained using a novel photographic method that reveal significant differences between the sexes in the relationship between tooth cuspidity and shark total length, and a novel ontogenetic change in male tooth shape. Males exhibit broader upper first teeth and increased distal inclination of upper third teeth with increasing length, while females do not present a consistent morphological change. Substantial individual variation, with implications for pace of life syndrome, was present in males and tooth polymorphism was suggested in females. Sexual differences and individual variation may play major roles in ontogenetic changes in tooth morphology in C. carcharias, with potential implications for their foraging biology. Such individual and sexual differences should be included in studies of ontogenetic shift dynamics in other species and systems.
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Journal of Fish Biology (2017) 91, 1032–1047
doi:10.1111/jfb.13396, available online at
The tooth, the whole tooth and nothing but the tooth: tooth
shape and ontogenetic shift dynamics in the white shark
Carcharodon carcharias
G. C. A. F*, M. S*, S. R,J.H.VW,
D. E§, R. W. D§, S. P. W,A.V.T§
W. O. H. H*
*School of Life Sciences, University of Sussex, Brighton, BN1 9QG, U.K., Department of
Botany and Zoology, Stellenbosch University, Stellenbosch, 7600, South Africa, §Dyer Island
Conservation Trust, Kleinbaai, South Africa and KwaZulu-Natal Sharks Board and
Biomedical Resource Unit, University of KwaZulu-Natal, Durban, 4000, South Africa
(Received 20 January 2017, Accepted 18 July 2017)
Results from this study of the white shark Carcharodon carcharias include measurements obtained
using a novel photographic method that reveal signicant differences between the sexes in the rela-
tionship between tooth cuspidity and shark total length, and a novel ontogenetic change in male tooth
shape. Males exhibit broader upper rst teeth and increased distal inclination of upper third teeth
with increasing length, while females do not present a consistent morphological change. Substan-
tial individual variation, with implications for pace of life syndrome, was present in males and tooth
polymorphism was suggested in females. Sexual differences and individual variation may play major
roles in ontogenetic changes in tooth morphology in C. carcharias, with potential implications for their
foraging biology. Such individual and sexual differences should be included in studies of ontogenetic
shift dynamics in other species and systems.
© 2017 The Fisheries Society of the British Isles
Key words: apex predator; Carcharodon carcharias; ontogenetic dietary shift; phenotypic polymor-
phism; sexual variation.
Ontogenetic shifts in ecological niche are widespread across the animal kingdom and
represent changes in resource use with size, from birth/hatching to maximum size
(Werner & Gilliam, 1984). In some species, ontogenetic shifts in diet are generally
characterized by a change from smaller size classes consuming a limited range of rela-
tively small prey species, to larger size classes consuming a wider range of prey items
with a larger mean body size (Wilson, 1975). Such shifts in diet can be accompanied, or
even made possible, by allometric scaling of morphological features, in which one mor-
phological feature changes disproportionately to general body growth. In some species,
there may be phenotypic polymorphism in the ontogenetic change in morphology and
Author to whom correspondence should be addressed. Tel.: +44 (0)1202 682514; email: geor-
© 2017 The Fisheries Society of the British Isles
diet, resulting in trophic polymorphism (Hutchinson, 1957; Van Valen, 1965; Meyer,
1989, 1990).
The ecological importance of ontogenetic dietary shifts and associated morpho-
logical changes, and of sexual or individual variation in them, may be particularly
signicant in marine apex predators such as sharks because of their often keystone
ecology and vulnerable conservation status (Matich & Heithaus, 2015). It is becoming
increasingly clear that sharks exhibit sexual and individual differences in diet and
habitat use, and allometric scaling of morphological features through ontogeny. For
example, bull sharks Carcharhinus leucus (Valenciennes 1839), tiger sharks Galeo-
cerdo cuvier (Péron & LeSueur 1822) and other large pelagic sharks show individual
variation in diet (Heithaus et al., 2002; Matich et al., 2011; Kiszka et al., 2015), and
female scalloped hammerheads Sphyrna lewini (Grifth & Smith 1834) shift to off-
shore habitats at a smaller size than males, where access to pelagic prey and improved
foraging success allow them to grow faster than their male counterparts (Klimley,
1987). Bull, tiger, blacktip Carcharhinus limbatus (Valenciennes 1839) and horn
sharks Heterodontus francisci (Girard 1855) show allometric changes in head shape
and musculature (Huber et al., 2006; Kolmann & Huber, 2009; Habegger et al., 2012;
Fu et al., 2016), and C. limbatus and white sharks Carcharodon carcharias (L. 1758)
show this with caudal-n shape (Lingham-Soliar, 2005; Irschick & Hammerschlag,
2014). Allometric scaling of mouth length and width is also evident in the viper
dogsh Trigonognathus kabeyai Mochizuki & Fumio, 1990 (Yano et al., 2003).
Individual variation in tooth morphology, a mechanistic facilitator of shark diet
(Frazzetta, 1988; Compagno, 1990) has been reported for sand tiger Carcharias taurus
Ranesque 1810, blue Prionace glauca (Linnaeus 1758) and porbeagle Lamna nasus
(Bonnaterre 1788) sharks (Litvinov, 1983; Shimada, 2002a; Lucifora et al., 2003;
Litvinov & Laptikhovsky, 2005). Sexual dimorphism in tooth shape has been linked
to different diets (Litvinov & Laptikhovsky, 2005), but can also be an adaptation
that gives males greater purchase when holding on to females during copulation
(Kajiura & Tricas, 1996). Quantifying ontogenetic change is logistically challenging
in large pelagic elasmobranchs due to their intolerance of captivity, cryptic habitat
use, wide-ranging movements, relatively low abundance and handling difculty.
Consequently, many ontogeny studies have been limited to dead specimens.
Carcharodon carcharias is a classic example of a morphological, diet-related change
through ontogeny. Carcharodon carcharias is a member of the Lamniformes, an order
for which tooth morphology is an informative dening character (Compagno, 1990).
It is widely accepted that C. carcharias undergo an ontogenetic shift in prey prefer-
ence (Cliff et al., 1989; Bruce, 1992; Compagno, 2001; Estrada et al., 2006; Hussey
et al., 2012). Stomach-content and stable-isotope analyses indicate that this shift con-
stitutes a change in trophic level, from a predominantly piscivorous diet when young,
to marine mammals making up the major component of diet when older (Tricas &
McCosker, 1984; Klimley, 1985; Cliff et al., 1989; Estrada et al., 2006; Hussey et al.,
2012). The estimated length at which they undergo this dietary shift varies between 2
and 3·4 m total length (LT) (Cliff et al., 1989; Bruce, 1992; Compagno, 2001; Malcolm
et al., 2001; Bruce, 2006; Estrada et al., 2006; Hussey et al., 2012) and is generally
considered to occur in both sexes at the same size, despite the fact that C. carcharias
are sexually dimorphic, with males reaching maturity at c.3·5 m and females at 4·5m
in LT(Francis, 1996; Pratt, 1996; Compagno, 2001; Bruce & Bradford, 2012). This
dietary shift is widely accepted to be facilitated by a change in tooth morphology,
© 2017 The Fisheries Society of the British Isles, Journal of Fish Biology 2017, 91, 1032–1047
1034 G. C. A. FRENCH ET AL.
(a) (b)
F. 1. Illustrations of variation in Carcharodon carcharias tooth breadth and cuspidity: (a) a broad and (b) a
cuspidate tooth.
from relatively pointed (cuspidate) teeth with serrational cusplets adapted to puncturing
piscivorous prey, to broader teeth lacking serrational cusplets that are better suited
to handling mammalian prey (Tricas & McCosker, 1984; Frazzetta, 1988; Hubbell,
1996; Whitenack & Motta, 2010; Bemis et al., 2015) (Fig. 1). However, the primary
reliance of adult C. carcharias on marine mammal prey is arguably overstated (Fer-
gusson et al., 2009) and there is mounting evidence of individual dietary variation that
does not appear to be related to sex or age (Estrada et al., 2006; Carlisle et al., 2012;
Hussey et al., 2012; Kim et al., 2012; Hamady et al., 2014; Pethybridge et al., 2014;
Christiansen et al., 2015; Towner et al., 2016). Individual and sexual differences in
foraging strategy have been found (Huveneers et al., 2015; Towner et al., 2016), and
there are questions over whether it occurs at all for some individuals (Estrada et al.,
2006; Hussey et al., 2012). Tooth shape in adult C. carcharias has also been reported
as highly variable, with some large sharks retaining the more cuspidate tooth shape of
juveniles (Hubbell, 1996; Castro, 2012). The only previous explicit investigations of
tooth morphometrics in relation to sex and body length, however, included only tooth
height (Randall, 1973, 1987; Mollet et al., 1996; Shimada, 2002b), a metric which
does not capture tooth cuspidity. As tooth cuspidity is considered to play an important
role in the ontogenetic dietary shift, this leaves a substantial gap in understanding the
dynamics of this shift, including within and between the sexes.
Morphological changes through ontogeny are difcult to measure in wild animals,
especially those inhabiting marine environments and even more so in wide-ranging
apex predators. Carcharodon carcharias provide an excellent opportunity to study
these changes because their predictable aggregation at certain pinniped colonies,
and the ease with which they can be lured to boats and photographed, makes pho-
tographic analysis of live sharks a potentially valuable source of information on
tooth morphology. Here, the ontogenetic change in tooth cuspidity was examined by
integrating published data and tooth measurements from jaws of dead sharks with
a new non-invasive method of quantifying tooth morphology for live sharks from
photographs. How the ontogenetic change in tooth morphology differs between sexes
and individuals was also examined.
Teeth are described following the system of Bemis et al. (2015) and Moyer et al. (2015), in
which teeth are given a code based on their location in the left or right side of the jaw (L and R,
© 2017 The Fisheries Society of the British Isles, Journal of Fish Biology 2017, 91, 1032–1047
(a) (b)
(c) (d)
Crown width
Palatoquadrate symphysis
F. 2. (a) Position of rst (1) and second (2) right (R) palatoquadrate (P) teeth in Carcharodon carcharias from
a jaw held in the KwaZulu-Natal Sharks Board jaw collection, with (b) an enlarged view of RP1 and RP2
showing crown height and base length measurements. (c) Photograph of a live C. carcharias showing left
(L) P1 and LP2 teeth with (d) an enlarged view of the teeth showing height and base length measurements
of the LP2 tooth.
respectively), in Meckel’s or palatoquadrate cartilage (M and P, respectively) and then numbered
distally to medially, relative to the appropriate symphysis [Figs 2(a) and 3(a)]. Measurements
of tooth crown height and width, as described in Hubbell (1996), were used to calculate tooth
cuspidity, dividing the crown height by the crown width to produce what is termed the tooth
index value [IT; Fig. 2(a)]. The presence of serrational cusplets is not mentioned in the pub-
lished datasets and were not observed in any of the specimens that were measured in this study.
For analyses of the relationship between tooth cuspidity and LT, all tooth measurements were
taken from RP1 or LP1 teeth (Fig. 2). P1 tooth data were used from 23 live sharks in Gansbaai,
South Africa (34·58S; 19·35E), using a novel photographic method and ImageJ software
(; Abramoff et al., 2004) described below. Measurements were also taken
© 2017 The Fisheries Society of the British Isles, Journal of Fish Biology 2017, 91, 1032–1047
1036 G. C. A. FRENCH ET AL.
(a) (b)
(c) (d)
Tooth angle
F. 3. (a) Derivation of Carcharodon carcharias tooth angle from the third (3) left (L) palatoquadrate (P) 3
tooth from a jaw held in the KwaZulu-Natal Sharks Board jaw collection, with (b) an enlarged view of
LP2 and LP3 teeth showing the tooth midpoint and tooth angle on the LP3 tooth. (c) Photograph of a live
C. carcharias showing RP3 and RP4 teeth of a live shark with (d) an enlarged view of the teeth showing
tooth angle measurement of the LP3 tooth.
manually from teeth of 50 jaws in the jaw collection held by the KwaZulu-Natal Sharks Board
(KZNSB) (Appendix SI), South Africa and P1 crown height and width data from 55 sharks,
published by Hubbell (1996) and Mollet et al. (1996; where in the latter, crown height was
termed ‘UA1E2’ and crown width ‘UA1W’). KZNSB C. carcharias were caught as part of a
bather-safety programme and jaws either dried or frozen at time of measurement. The Gans-
baai and KZNSB sharks all came from the same South Africa population. The C. carcharias
in Hubbell (1996) and Mollet et al. (1996) came from multiple populations (Australia New
Zealand, South Africa, North-east Pacic Ocean, North-west Atlantic Ocean).
© 2017 The Fisheries Society of the British Isles, Journal of Fish Biology 2017, 91, 1032–1047
The intermediate upper tooth (RP3 or LP3; Fig. 3) is markedly different in shape from the P1
and P2 teeth, in that it typically displays asymmetry and an approximately straight medial edge
(Applegate & Espinosa-Arrubarrena, 1996; Hubbell, 1996). The angle of the tip of the crown
in comparison with the tooth midpoint shows greater variation in this tooth than the equivalent
angles of the P1 and P2 teeth (Hubbell, 1996) and was therefore selected as another potential
metric for analysing relationships between tooth morphology and LT[Fig. 3(b), (d)]. One P3
tooth per shark was selected and ImageJ software was used to measure the angle (lateral or
medial) of the tip of the tooth crown in relation to the midpoint of the tooth base [Hubbell (1996);
Fig. 3(b), (d)]. Medial inclinations were denoted by positive angles and distal inclinations as
negative [Fig. 3(b)]. P3 angle measurements derived from photographs of live sharks (see below)
and photographs of jaws held by the KZNSB were combined with data published by Hubbell
C. carcharias LTwas directly measured for sharks in the KZNSB and published datasets.
For live C. carcharias in Gansbaai, LTwas estimated in the eld by visually comparing the
free-swimming sharks to an object of known length (a 4·7 m length divers shark cage), xed to
the side of the boat, as has been done in many previous studies (Kock et al., 2013; Towner et al.,
2013a, 2016).
Measurements were taken of crown height, width and angle from photographs of both live
C. carcharias and KZNSB jaws [Figs 2(c), (d), 3 and 4]. Live C. carcharias were photographed
from a cage diving vessel operated by Marine Dynamics, based in Gansbaai, South Africa. The
photographs were taken when C. carcharias were interacting with stimuli (salmon head bait
and a wooden seal decoy), during three eld trips: August to October 2014, February to April
2015 and June 2015. Sharks were individually identied using photographs of the rst dorsal
n and DARWIN photo-identication software (, with digital traces
of the outline of the n being matched by the software and conrmed by eye (Stanley, 1995;
Tow ner et al., 2013b). Tooth images were given a quality score rating of 1– 6, based on their
resolution, clarity and angle relative to the camera, and only images with a score of 4 or above
were included in analyses, based on the results of the repeatability of the method, described
below. These images were imported into ImageJ software where measurements of crown height,
crown width and tooth angle were taken in pixels. Height and width measurements were taken
three times and averages used in the calculation of ITvalues.
To investigate scaling relationships between C. carcharias LTand P1 IT, both variables were
log10 transformed, sorted into male and female datasets and analysed with linear regression.
Log10 transformations are typically used to increase linearity of allometric relationships, which
tend to form curves as they are a power function (Huber et al., 2006; Kolmann & Huber, 2009;
Habegger et al., 2012). If the predicted isometric slope of 1 fell outside of the 95% .. of the
regression slope, the relationship was considered allometric (Sokal & Rohlf, 1995). To identify
discrete ITgroupings (e.g. pre and post ontogenetic shift and polymorphs) in P1 teeth, hier-
archical cluster analyses were applied to P1 ITdata. The NbClust function in R 3.2.4 (www was used to identify the optimal number of clusters with which to perform the
cluster analyses apriori. A Mann–Whitney U-test and one-way ANOVA were applied to data
from males and females, respectively, to test for differences in C. carcharias LTbetween tooth
clusters (male data were non-normal; female data had more than two clusters). Linear regression
analyses were further applied separately to male and female P3 tooth angle and shark LTand an
isometric slope of 1 used to determine allometry. Log10 transformations were not used for these
data, as they included negative and positive values.
© 2017 The Fisheries Society of the British Isles, Journal of Fish Biology 2017, 91, 1032–1047
1038 G. C. A. FRENCH ET AL.
F. 4. Photographs taken on (a) 15 March 2015 (K. Baker, and (b) 24 March 2015 showing
position of rst (1) and second (2) left (L) palatoquadrate (P) teeth in the individually identied Carcharodon
carcharias ‘Rosie II’ used in the repeatability test of the photographic method.
Tests of both accuracy and repeatability were conducted to determine the robustness of the
photographic methodology (Jeffreys et al., 2013). The C. carcharias jaw collection held by the
KZNSB was used to assess the accuracy of the photographic method for measuring tooth cus-
pidity [Fig. 2(a), (b)]. LM1 and LM2 teeth of 35 jaws were measured using a tape measure in
situ and photographs of the same jaws were used to measure the same teeth digitally, in pixels,
using ImageJ software. Linear regression were used to compare the ITvalues produced from
manual and digital measurements. Furthermore, digital measurements, obtained from multiple
photographs of the same teeth of live Gansbaai sharks, were compared to assess the repeatability
of the photographic method (Fig. 4). This dataset included teeth from both the upper and lower
jaw, in any position visible, provided the quality of the image met the requirements described
above. The teeth of 11 individual sharks, totalling 12 unique teeth, each measured at least twice,
were included in a repeatability calculation described by Lessells & Boag (1987). This cal-
culation uses the mean-square values produced by ANOVA (SPSS 22;; SW,
within group variance and SA, among group variance). Repeatability (R)=SA2(S2)1+SA2,
where S2=SW,SA2=(SASW)n0
1,wheren0=[1(a1)][nini2ni)1], a=number of
groups and ni=sample size of the ith group. Two repeatability scores were calculated: using
teeth with a quality score of 3 and above (n=46), or 4 and above (n=25).
© 2017 The Fisheries Society of the British Isles, Journal of Fish Biology 2017, 91, 1032–1047
LT (m)
Tooth angle
2·5 4·5 5·5
3·52·5 4·5 5·5
F. 5. Relationship between log10 P1 tooth index (IT)andlog
10 total body length (LT) for (a) male and (b) female
Carcharodon carcharias. Broad and cuspidate tooth types are illustrated on the y-axes. Males formed two
clusters, with teeth that were relatively cuspidate ( ) or relatively broad ( ), whereas females formed three
clusters, with teeth that were relatively cuspidate ( ), intermediate ( ) or relatively broad ( ). (c) The
relationships between the angle of the third palatoquadrate (P3) tooth and total body length (LT) for male
and (d) female C. carcharias.
P1 ITin male C. carcharias was signicantly related to LT(y=−0·119x+0·131;
F1,55 =20·6, P<0·001, 95% .. on slope 0·17 and 0·07, r2=0·25, n=57) and was
negatively allometric, with the predicted isometric slope of 1 being outside the 95%
.. of the regression slope [Fig. 5(a)]. Female ITalso decreased signicantly with
LT(y=−0·0226x+1·28; F1,61 =4·0, P<0·05, 95% .. on slope 0·14 and 1·23,
r2=0·05, n=71), but showed isometry [predicted isometric slope of 1 was inside of the
95% ..; Fig. 5(b)]. Additionally, there was much greater variability in the relationship
for females than for males [r2=0·05 and r2=0·25, respectively; Fig. 4(b)].
The angle of the P3 tooth was signicantly related to LTin male C. carcharias
(y=−3·075x+7·205, F=6·85, P<0·05; 95% .. on slope 0·94 and 0·1,
r2=0·31, n=17) in an isometric relationship, as the predicted isometric slope
was 1 [Fig. 5(c)]. In female C. carcharias, the angle of the P3 tooth was not related
to LT[y=−0·617x5·1663, F=2·62, P>0·05, 95% .. on slope 4·35 and 0·69,
© 2017 The Fisheries Society of the British Isles, Journal of Fish Biology 2017, 91, 1032–1047
1040 G. C. A. FRENCH ET AL.
1·10·9 1·3 1·5
1·10·9 1·3 1·5
F. 6. Relationship between Carcharodon carcharias tooth index values (IT) from (a) measurements from pho-
tographs of rst (1) and second (2) palatoquadrate (P) teeth from photographs and (b) manual measurement
of PI teeth of only C. carcharias caught by the KwaZulu-Natal Sharks Board.
r2=0·05, n=22; Fig. 5(d)]. The P1 teeth of males formed two clusters; one where
teeth were relatively cuspidate and another where teeth were broader [Fig. 5(a)]). The
lengths of sharks in the two tooth clusters were signicantly different (Mann– Whitney
U=191, P<0·001). Female P1 teeth separated into three clusters that represented
cuspidate, intermediate and broad teeth [Fig. 5(b)] and LTdid not signicantly differ
between these clusters (one-way ANOVA, F1,62 =0·234, P>0·05, 95% .. on slope
0·14 and 0·22, r2=0·01).
There was a signicant, positive relationship between the measurements taken
directly from teeth and from photographs [P1 and P2: y=0·6928x+0·4457,
F1,34 =43·02, P<0·001, 95% ..: 0·57–1·08, r2=0·57, n=55; P1 only: y=0·8009x+
0·2996, F1,16 =61·0, P<0·001, 95% .. 0·731·27, r2=0·8, n=18; Fig. 6(a) and (b),
respectively). Digital images of only the P1 tooth were therefore substantially more
accurate than those of the P2 tooth. Tooth measurements showed high repeatability,
which was substantially greater when using images ranked 4 or more (Table I) and
therefore only those were considered in analyses of tooth index and shark length.
The results show that C. carcharias exhibit an ontogenetic shift in tooth shape, but
that this relationship differs between sexes and shows substantial individual variation.
T I. Repeatability (R) of tooth index (IT) values obtained from photographs of teeth with
image quality scores (Q)3and4
QnGroup mean ITd.f. .. (%) 95% .. RP
346 1·09 45 0·092 1·17 0·57 <0·001
425 1·10 24 1·32 0·57 0·86 <0·001
n, Number of images.
© 2017 The Fisheries Society of the British Isles, Journal of Fish Biology 2017, 91, 1032–1047
Males showed a distinct increase in P1 tooth breadth with length and a change in angle
of the P3 tooth, both of which were far less pronounced in females. Measurements
taken from photos were accurate and repeatable, suggesting that use of photos of live
sharks could be a valuable source of data for future studies.
The results conrm that male C. carcharias undergo an ontogenetic shift in tooth
shape. Upper rst teeth of male sharks become signicantly more broad with increas-
ing shark length, showing negative allometry, and male sharks clustered into cuspidate
and broad-toothed groups that signicantly differed in shark length, with the more
cuspidate group containing smaller sharks than the broad group. These two clusters
probably represent pre and post-ontogenetic shift individuals. This ontogenetic change
in C. carcharias is commonly believed to facilitate the inclusion of marine mammals
into their diet (Tricas & McCosker, 1984; Klimley, 1985; Frazzetta, 1988; Cliff et al.,
1989; Hubbell, 1996; Estrada et al., 2006; Hussey et al., 2012). The medial angle of
the P3 tooth was also found to scale signicantly with male LT, in an isometric rela-
tionship. This tooth has been hypothesized to be a specialized tool for inicting large,
disabling wounds on pinniped prey due to its shape and location on the strongest part
of the jaw (Martin et al., 2005). An increase in the distal inclination of the tooth tip,
as seen in males, could be a further adaptation for handling and despatching marine
mammals. Alternatively, this change in angle could assist in the handling of females
during copulation, during which male sharks bite females in the gill, head and pectoral
regions (Kajiura & Tricas, 1996; Pratt & Carrier, 2001).
Although C. carcharias LTin the cuspidate and broad clusters of males were signi-
cantly different, providing further evidence of a distinct change in tooth shape through
ontogeny, there was signicant variation and overlap in size. This indicates that there
may be individual variation in the length at which male sharks undergo the ontogenetic
shift. Males reach sexual maturity at a similar size to that at which they undergo
the ontogenetic shift in tooth morphology (Cliff et al., 1989). This suggests that the
ontogenetic shifts in diet and tooth shape are intrinsically linked to sexual maturity.
In animals, individual variation in life-history traits such as the onset of maturity,
coupled with behavioural changes such as changes in habitat use and diet, can be com-
ponents of a pace-of-life syndrome, in which life-history trade-offs produce consistent
behavioural differences in areas such as activity level, movement patterns, boldness and
aggressiveness (Ricklefs & Wikelski, 2002; Stamps, 2007; Wolf et al., 2007; Biro &
Stamps, 2008; Réale et al., 2010). For example, in the house mouse Mus musculus,
size and age at maturity are linked to activity level, growth rate, fecundity, adult
body size and longevity, with fast-paced mice being more active, faster growing and
reaching maturity at a smaller size and younger age than slow-paced individuals
(Wirth-Dzieçiołowska et al., 1996, 2005; Wirth-Dzieçiołowska & Czumi´
nska, 2000).
The higher energetic needs of individuals that mature more quickly require mor-
phological and physiological adaptations that enable them to consume the necessary
volume or type of sustenance (Biro & Stamps, 2008). In the case of C. carcharias,
this could pertain to broader teeth facilitating the incorporation of energy-rich marine
mammals into their diet. C. carcharias exhibit sexual and individual differences in
migratory behaviour (Weng et al., 2007; Block et al., 2011; Domeier & Nasby-Lucas,
2012; Kock et al., 2013), that will inuence the water temperatures individuals inhabit.
Because C. carcharias are endothermic (Carey et al., 1982) this will therefore affect
the energetic demands of thermoregulation, producing individual variation in ener-
getic demands that may inuence pace-of-life strategies. Elevated hunger and activity
© 2017 The Fisheries Society of the British Isles, Journal of Fish Biology 2017, 91, 1032–1047
1042 G. C. A. FRENCH ET AL.
levels increase risk of shing mortality and can lead to rapid depletion of fast paced
genotypes (Young et al., 2006; Biro & Post, 2008; Härkönen et al., 2014; Mittelbach
et al., 2014).
Female C. carcharias teeth were found to scale isometrically in relation to LTand
the observed level of variation made any overall relationship very weak. Additionally,
the facts that the angle of the intermediate tooth did not scale with LTand that the
cluster analysis suggested three tooth groups as opposed to the two groups in males,
demonstrate that ontogenetic shifts in tooth shape differ between males and females.
That these tooth types were independent of LTsuggests that female C. carcharias may
exhibit phenotypic polymorphism. Stable-isotope analyses suggest that some females
do not undergo an ontogenetic dietary shift and can show consistent dietary specializa-
tion instead (Estrada et al., 2006; Hussey et al., 2012; Kim et al., 2012; Pethybridge
et al., 2014; Christiansen et al., 2015). The mechanism behind such specialization,
however, has not been elucidated. Tooth polymorphism facilitates niche polymorphism
in sympatric populations of some sh species (Meyer, 1990) and has been linked to
dietary specialization in other shark species (Litvinov, 1983; Litvinov & Laptikhovsky,
2005). As tooth shape is generally accepted to relate to the exploitation of different prey
types in C. carcharias (Tricas & McCosker, 1984; Frazzetta, 1988; Hubbell, 1996), it is
reasonable to suggest that sharks with cuspidate, intermediate or broad teeth feed pref-
erentially on different prey, constituting trophic polymorphism in females. Potential
consequences of specialization in C. carcharias diets include altered food-web struc-
ture if changes in resource availability affect tooth morphs differently (Christiansen
et al., 2015) and differing levels of bioaccumulation of toxins (Young et al., 2006; Biro
& Post, 2008; Härkönen et al., 2014; Mittelbach et al., 2014), an issue already known
to pose a signicant threat to C. carcharias generally (Schlenk et al., 2005; Mull et al.,
2012; Lyons et al., 2013; Marsilli et al., 2016). While geographic variation in female
shark tooth shape cannot be ruled out, it seems less likely as no such variation was
evident in male teeth.
One of the major limitations in establishing the ontogenetic relationships between
morphology, diet and maturity, especially in threatened species, is sample size. For
sharks, the majority of tooth data currently available is from a limited number of jaw
collections, harvested from dead specimens. The current study shows that the novel
photographic method produces accurate and repeatable tooth-shape data of live C. car-
charias in the eld, providing that image quality is controlled, and these data can be
used to study the ontogenetic dietary shift. The increase in accuracy when comparing
digital and manual measurements of P1 teeth and pooled P1 and P2 teeth is probably
due to parallax error, induced by P2 teeth not being exactly front on to the camera due
to their position in the jaw. This highlights the importance of ensuring that the position
of the tooth relative to the camera is directly parallel.
This non-lethal research method can be used to provide sample sizes that better elu-
cidate the onset and occurrence of ontogenetic shifts within and between populations,
in addition to individual variation, sexual dimorphism and polymorphism in C. car-
charias and potentially other sharks as well. Ontogenetic shift dynamics are a major
component of elasmobranch life history. Consideration of sexual and individual varia-
tion in ontogenetic shift dynamics will therefore be important both for understanding
the ecology of a species, and for the development of effective management strategies.
We thank W. Chivell, H. Otto, K. Baker, O. Keller, the Dyer Island Conservation Trust and
Marine Dynamics for facilities and eldwork support in Gansbaai, South Africa. We are also
© 2017 The Fisheries Society of the British Isles, Journal of Fish Biology 2017, 91, 1032–1047
grateful to members of the Hughes Lab for comments on the manuscript and the University of
Sussex, National Geographic Society and Royal Society for funding. The authors conrm that
there is no conict of interest to declare.
Supporting Information
Supporting Information may be found in the online version of this paper:
A SI. Additional data.
Abramoff, M. D., Magalhaes, P. J. & Ram, S. J. (2004). Image processing with ImageJ. Biopho-
tonics International 11, 36–42.
Applegate, S. P. & Espinosa-Arrubarrena, L. (1996). The fossil history of Carcharodon and its
possible ancestor, Cretolamna – a study in tooth identication. In Great White Sharks:
The Biology of Carcharodon carcharias (Klimley, A. P. & Ainley, D. G., eds), pp. 19–36.
San Diego, CA: Academic Press.
Bemis, W. E., Moyer, J. K. & Riccio, M. L. (2015). Homology of lateral cusplets in the teeth of
lamnid sharks (Lamniformes: Lamnidae). Copeia 103, 961972.
Biro, P. A. & Post, J. R. (2008). Rapid depletion of genotypes with fast growth and bold per-
sonality traits from harvested sh populations. Proceedings of the National Academy of
Sciences 105, 2919–2922.
Biro, P. A. & Stamps, J. A. (2008). Are animal personality traits linked to life-history produc-
tivity? Trends in Ecology & Evolution 23, 361– 368.
Block, B. A., Jonsen, I. D., Jorgensen, S. J., Winship, A. J., Shaffer, S. A., Bograd, S. J., Hazen,
E. L., Foley, D. G., Breed, G. A., Harrison, A.-L., Ganong, J. E., Swithenbank, A., Castle-
ton, M., Dewar, H., Mate, B. R., Shillinger, G. L., Schaefer, K. M., Benson, S. R., Weise,
M. J., Henry, R. W. & Costa, D.P. (2011). Tracking apex marine predator movements in
a dynamic ocean. Nature 475, 86– 90.
Bruce, B. D. (1992). Preliminary observations on the biology of the white shark, Carcharodon
carcharias, in South Australian waters. Australian Journal of Marine and Freshwater
Research 43, 1– 11.
Bruce, B. D. (2006). The biology and ecology of the white shark, Carcharodon carcharias.In
Sharks of the Open Ocean (Camhi, M. D., Pikitch, E. K. & Babcock, E. A., eds), pp.
69–81. Oxford: Blackwell Publishing Ltd.
Bruce, B. D. & Bradford, R. W. (2012). Habitat use and spatial dynamics of juvenile white
sharks, Carcharodon carcharias, in eastern Australia. In Global Perspectives on the Biol-
ogy and Life History of the White Shark (Domeier, M. L., ed), pp. 225253. Boca Raton,
FL: CRC Press.
Carey, F. G., Kanwisher, J. W., Brazier, O., Gabrielson, G., Casey, J. G. & Pratt, H. L. (1982).
Temperature and activities of a white shark, Carcharodon carcharias.Copeia 1982, 254.
Carlisle, A. B., Kim, S. L., Semmens, B. X., Madigan, D. J., Jorgensen, S. J., Perle, C. R.,
Anderson, S. D., Chapple, T. K., Kanive, P. E. & Block, B. A. (2012). Using stable isotope
analysis to understand the migration and trophic ecology of Northeastern Pacic white
sharks (Carcharodon carcharias). PLoS One 7, e30492.
Castro, J. I. (2012). A summary of observations on the maximum size attained by the white
shark, Carcharodon carcharias.InGlobal Perspectives on the Biology and Life History
of the White Shark (Domeier, M. L., ed), pp. 8590. Boca Raton, FL: CRC Press.
Christiansen, H. M., Fisk, A. T. & Hussey, N. E. (2015). Incorporating stable isotopes into a
multidisciplinary framework to improve data inference and their conservation and man-
agement application. African Journal of Marine Science 37, 189– 197.
Cliff, G., Dudley, S. F. J. & Davis, B. (1989). Sharks caught in the protective gill nets off Natal,
South Africa. 2. The great white shark Carcharodon carcharias (Linnaeus). African Jour-
nal of Marine Science 8, 131–144.
© 2017 The Fisheries Society of the British Isles, Journal of Fish Biology 2017, 91, 1032–1047
1044 G. C. A. FRENCH ET AL.
Compagno, L. J. V. (1990). Relationships of the megamouth shark, Megachasma pelagios (Lam-
niformes: Megachasmidae), with comments on its feeding habits. In Elasmobranchs as
Living Resources: Advances in the Biology, Ecology, Systematics, and the Status of the
Fisher ies (Pratt, H. L. Jr, Gruber, S. H. & Taniuchi, T., eds), pp. 357– 379. National
Oceanic and Atmospheric Administration Technical Report, National Marine Fisheries
Service 90.
Compagno, L. J. V. (2001). Sharks of the world: an illustrated and annotated catalogue of shark
species known to date, Vol. 2. Bullhead, mackerel and carpet sharks (Heterodontiformes,
Lamniformes and Orectolobiformes). FAO Species Catalogue for Fishery Purposes 1.
Rome: FAO.
Domeier, M. L. & Nasby-Lucas, N. (2012). Sex-specic migration patterns and sexual segrega-
tion of adult white sharks Carchardon carcharias in the Northeastern Pacic. In Global
Perspectives on the Biology and Life History of the White Shark (Domeier, M. L., ed),
pp. 133–146. Boca Raton, FL: CRC Press.
Estrada, J. A., Rice, A. N., Natanson, L. J. & Skomal, G. B. (2006). Use of isotopic analysis
of vertebrae in reconstructing ontogenetic feeding ecology in white sharks. Ecology 87,
Francis, M. P. (1996). Observations on a pregnant white shark with a review of reproductive
biology. In Great White Sharks: The Biology of Carcharodon carcharias (Klimley, A. P.
& Ainley, D. G., eds), pp. 158– 172. London: Academic Press.
Frazzetta, T. H. (1988). The mechanics of cutting and the form of shark teeth (Chondrichthyes,
Elasmobranchii). Zoomorphology 108, 93–107.
Fu, A. L., Hammerschlag, N., Lauder, G. V., Wilga, C. D., Kuo, C. -Y. & Irschick, D. J. (2016).
Ontogeny of head and caudal n shape of an apex marine predator: the tiger shark (Gale-
ocerdo cuvier). Journal of Morphology 277, 556– 564.
Habegger, M. L., Motta, P. J., Huber, D. R. & Dean, M. N. (2012). Feeding biomechanics
and theoretical calculations of bite force in bull sharks (Carcharhinus leucas) during
ontogeny. Zoology 115, 354– 364.
Hamady, L. L., Natanson, L. J., Skomal, G. B. & Thorrold, S. R. (2014). Vertebral bomb radio-
carbon suggests extreme longevity in white sharks. PLoS One 9, e84006.
Härkönen, L., Hyvärinen, P., Paappanen, J., Vainikka, A. & Tierney, K. (2014). Explorative
behavior increases vulnerability to angling in hatchery-reared brown trout (Salmo trutta).
Canadian Journal of Fisheries and Aquatic Sciences 71, 1900–1909.
Heithaus, M., Dill, L. M., Marshall, G. & Buhleier, B. (2002). Habitat use and foraging behav-
ior of tiger sharks (Galeocerdo cuvier) in a seagrass ecosystem. Marine Biology 140,
Hubbell, G. (1996). Using tooth structure to determine the evolutionary history of the white
shark. In Great White Sharks: The Biology of Carcharodon carcharias (Klimley, A. P. &
Ainley, D. G., eds), pp. 9– 18. San Diego, CA: Academic Press.
Huber, D. R., Weggelaar, C. L. & Motta, P. J. (2006). Scaling of bite force in the blacktip shark
Carcharhinus limbatus.Zoology 109, 109– 119.
Hussey, N. E., McCann, H. M., Cliff, G., Dudley, S. F., Wintner, S. P. & Fisk, A. T. (2012).
Size-based analysis of diet and trophic position of the white shark Carcharodon car-
charias in South African waters. In Global Perspectives on the Biology and Life History
of the White Shark (Domeier, M. L., ed), pp. 2749. Boca Raton, FL: CRC Press.
Hutchinson, G. E. (1957). Concluding remarks. Cold Spring Harbour Symposia on Quantitative
Biology 22, 415–442.
Huveneers, C., Holman, D., Robbins, R., Fox, A., Endler, J. A. & Taylor, A. H. (2015). White
sharks exploit the sun during predatory approaches. American Naturalist 185, 562–570.
Irschick, D. J. & Hammerschlag, N. (2014). Morphological scaling of body form in four shark
species differing in ecology and life history. Biological Journal of the Linnean Society
114, 126–135.
Jeffreys, G. L., Rowat, D., Marshall, H. & Brooks, K. (2013). The development of robust mor-
phometric indices from accurate and precise measurements of free-swimming whale
sharks using laser photogrammetry. Journal of the Marine Biological Association of the
United Kingdom 93, 309–320.
Kajiura, S. & Tricas, T. (1996). Seasonal dynamics of dental sexual dimorphism in the Atlantic
stingray Dasyatis sabina.Journal of Experimental Biology 199, 2297– 2306.
© 2017 The Fisheries Society of the British Isles, Journal of Fish Biology 2017, 91, 1032–1047
Kim, S. L., Tinker, M. T., Estes, J. A. & Koch, P. L. (2012). Ontogenetic and among-individual
variation in foraging strategies of Northeast Pacic white sharks based on stable isotope
analysis. PLoS One 7, e45068.
Kiszka, J. J., Aubail, A., Hussey, N. E., Heithaus, M. R., Caurant, F. & Bustamante, P. (2015).
Plasticity of trophic interactions among sharks from the oceanic south-western Indian
Ocean revealed by stable isotope and mercury analyses. Deep Sea Research Part I:
Oceanographic Research Papers 96, 49 58.
Klimley, A. P. (1985). The areal distribution and autoecology of the white shark, Carcharodon
carcharias, off the west coast of North America. Memoirs of the Southern California
Academy of Sciences 9, 15–40.
Klimley, A. P. (1987). The determinants of sexual segregation in the scalloped hammerhead
shark, Sphyrna lewini.Environmental Biology of Fishes 18, 27–40.
Kock, A., O’Riain, M. J., Mauff, K., Me¨
yer, M., Kotze, D. & Grifths, C. (2013). Residency,
habitat use and sexual segregation of white sharks, Carcharodon carcharias in False Bay,
South Africa. PLoS One 8, e55048.
Kolmann, M. A. & Huber, D. R. (2009). Scaling of feeding biomechanics in the horn shark
Heterodontus francisci: ontogenetic constraints on durophagy. Zoology 112, 351– 361.
Lessells, C. M. & Boag, P. T. (1987). Unrepeatable repeatabilities: a common mistake. Auk 104,
Lingham-Soliar, T. (2005). Caudal n allometry in the white shark Carcharodon carcharias:
implications for locomotory performance and ecology. Naturwissenschaften 92,
Litvinov, F. F. (1983). Two forms of teeth in the blue shark Prionace glauca.Journal of Ichthy-
ology 22, 154–156.
Lucifora, L. O., Cione, A. L., Menni, R. C. & Escalante, A. H. (2003). Tooth row counts,
vicariance and the distribution of the sand tiger shark Carcharias taurus.Ecography 26,
Lyons, K., Carlisle, A., Preti, A., Mull, C., Blasius, M., O’Sullivan, J., Winkler, C. & Lowe, C.
G. (2013). Effects of trophic ecology and habitat use on maternal transfer of contaminants
in four species of young of the year lamniform sharks. Marine Environmental Research
90, 27–38.
Marsilli, L., Coppola, D., Giannetti, M., Casini, S., Fossi, M. C., van Wyk, J. H., Sperone, E.,
Tripepi, S., Micarelli, P. & Rizzuto, S. (2016). Skin biopsies as a sensitive non-lethal
technique for the ecotoxicological studies of great white shark (Carcharodon carcharias)
sampledinSouthAfrica.Expert Opinion on Environmental Biology 5, 1.
Martin, R. A., Hammerschlag, N., Collier, R. S. & Fallows, C. (2005). Predatory behaviour
of white sharks (Carcharodon carcharias) at Seal Island, South Africa. Journal of the
Marine Biological Association of the United Kingdom 85, 1121– 1135.
Matich, P. & Heithaus, M. R. (2015). Individual variation in ontogenetic niche shifts in habitat
use and movement patterns of a large estuarine predator (Carcharhinus leucas). Oecolo-
gia 178, 347–359.
Matich, P., Heithaus, M. R. & Layman, C. A. (2011). Contrasting patterns of individual special-
ization and trophic coupling in two marine apex predators: specialization in top marine
predators. Journal of Animal Ecology 80, 294– 305.
Meyer, A. (1989). Cost of morphological specialization: feeding performance of the two
morphs in the trophically polymorphic cichlid sh, Cichlasoma citrinellum.Oecologia
80, 431–436.
Meyer, A. (1990). Morphometrics and allometry in the trophically polymorphic cichlid sh,
Cichlasoma citrinellum: alternative adaptations and ontogenetic changes in shape. Jour-
nal of Zoology 221, 237–260.
Mittelbach, G. G., Ballew, N. G., Kjelvik, M. K. & Fraser, D. (2014). Fish behavioral types and
their ecological consequences. Canadian Journal of Fisheries and Aquatic Sciences 71,
Mochizuki, K. & Fumio, O. (1990). Trigonognathus kabeyai a new genus and species of squalid
shark in Japan. Japanese Journal of Ichthyology 36, 385–390.
Mollet, H. F., Cailliet, G. M., Klimley, A. P., Ebert, D. A., Testi, A. D. & Compagno, L. J.
V. (1996). A review of length validation methods and protocols to measure large white
© 2017 The Fisheries Society of the British Isles, Journal of Fish Biology 2017, 91, 1032–1047
1046 G. C. A. FRENCH ET AL.
sharks. In Great White Sharks: The Biology of Carcharodon carcharias (Klimley, A. P.
& Ainley, D. G., eds), pp. 91– 108. London: Academic Press.
Moyer, J. K., Riccio, M. L. & Bemis, W. E. (2015). Development and microstructure of tooth
histotypes in the blue shark, Prionace glauca (Carcharhiniformes: Carcharhinidae) and
the great white shark, Carcharodon carcharias (Lamniformes: Lamnidae). Journal of
Morphology 276, 797–817.
Mull, C. G., Blasius, M. E., O’Sullivan, J. B. & Lowe, C. G. (2012). Heavy metals, trace elements
and organochlorine contaminants in muscle and liver tissue of juvenile white sharks,
Carcharodon carcharias, from the Southern California Bight. In Global Perspectives on
the Biology and Life History of the White Shark (Domeier, M. L., ed), pp. 5975. Boca
Raton, FL: CRC Press.
Pethybridge, H. R., Parrish, C. C., Bruce, B. D., Young, J. W. & Nichols, P. D. (2014). Lipid,
fatty acid and energy density proles of white sharks: insights into the feeding ecology
and ecophysiology of a complex top predator. PLoS One 9, e97877.
Pratt, H. L. (1996). Reproduction in the male white shark. In Great White Sharks: The Biology
of Carcharodon carcharias (Klimley, A. P. & Ainley, D. G., eds), pp. 131 138. London:
Academic Press.
Pratt, H. L. & Carrier, J. C. (2001). A review of elasmobranch reproductive behavior with a case
study on the nurse shark, Ginglymostoma cirratum.InThe Behavior and Sensory Biology
of Elasmobranch Fishes: An Anthology in Memory of Donald Richard Nelson (Tricas, T.
C. & Gruber, S. H., eds), pp. 157–188. Dordrecht: Springer.
Randall, J. E. (1973). Size of the great white shark (Carcharodon). Science 181, 169– 170.
Randall, J. E. (1987). Refutation of lengths of 11.3 m, 9.0 m and 6.4 m attributed to the white
shark, Carcharodon carcharias.California Fish & Game 73, 163– 168.
Réale, D., Garant, D., Humphries, M. M., Bergeron, P., Careau, V. & Montiglio, P. -O. (2010).
Personality and the emergence of the pace-of-life syndrome concept at the population
level. Philosophical Transactions of the Royal Society B 365, 4051– 4063.
Ricklefs, R. E. & Wikelski, M. (2002). The physiology/life-history nexus. Trends in Ecology &
Evolution 17, 462–468.
Schlenk, D., Sapozhnikova, Y. & Cliff, G. (2005). Incidence of organochlorine pesticides in
muscle and liver tissues of South African great white sharks Carcharodon carcharias.
Marine Pollution Bulletin 50, 208–211.
Shimada, K. (2002a). Teeth of embryos in lamniform sharks (Chondrichthyes: Elasmobranchii).
Environmental Biology of Fishes 63, 309– 319.
Shimada, K. (2002b). The relationship between tooth size and body length in the white shark
Carcharodon carcharias Lamniformes: Lamnidae. Journal of Fossil Research 35, 28–33.
Sokal, R. R. & Rohlf, F. J. (1995). Biometry. New York, NY: W. H. Freeman.
Stamps, J. A. (2007). Growth-mortality tradeoffs and personality traits in animals. Ecology Let-
ters 10, 355–363.
Towner, A. V., Underhill, L. G., Jewell, O. J. D. & Smale, M. J. (2013a). Environmental inu-
ences on the abundance and sexual composition of white sharks Carcharodon carcharias
in Gansbaai, South Africa. PLoS One 8, e71197.
Towner, A. V., Wcisel, M. A., Reisinger, R. R., Edwards, D. & Jewell, O. J. D. (2013b). Gaug-
ing the threat: the rst population estimate for white sharks in South Africa using photo
identication and automated software. PLoS One 8, e66035.
Towner, A. V., Leos-Barajas, V., Langrock, R., Schick, R. S., Smale, M. J., Kaschke, T., Jew-
ell, O. J. D. & Papastamatiou, Y. P. (2016). Sex-specic and individual preferences for
hunting strategies in white sharks. Functional Ecology 30, 1397– 1407.
Tricas, T. C. & McCosker, J. E. (1984). Predatory behaviour of the white shark (Carcharodon
carcharias) with notes on its biology. Proceedings of the California Academy of Sciences
43, 221–238.
Van Valen, L. (1965). Morphological variation and width of ecological niche. American Natu-
ralist 99, 377– 390.
Weng, K. C., Boustany, A. M., Pyle, P., Anderson, S. D., Brown, A. & Block, B. A. (2007).
Migration and habitat of white sharks (Carcharodon carcharias) in the eastern Pacic
Ocean. Marine Biology 152, 877–894.
Werner, E. E. & Gilliam, J. F. (1984). The ontogenetic niche and species interactions in
size-structured populations. Annual Review of Ecology and Systematics 15, 393– 425.
© 2017 The Fisheries Society of the British Isles, Journal of Fish Biology 2017, 91, 1032–1047
Whitenack, L. B. & Motta, P. J. (2010). Performance of shark teeth during puncture and draw:
implications for the mechanics of cutting. Biological Journal of the Linnean Society 100,
Wilson, D. S. (1975). The adequacy of body size as a niche difference. American Naturalist 109,
Wirth-Dzieçiołowska, E. & Czumi´
nska, K. (2000). Longevity and aging of mice from lines
divergently selected for body weight for over 90 generations. Biogerontology 1, 171–178.
Wirth-Dzieçiołowska, E., Czuminska, K., Reklewska, B. & Katkiewicz, M. (1996). Life time
reproductive performance and functional changes in reproductive organs of mice selected
divergently for body weight over 90 generations. Animal Science Papers and Reports 14,
Wirth-Dzieçiołowska, E., Lipska, A. & W
esierska, M. (2005). Selection for body weight induces
differences in exploratory behavior and learning in mice. Acta Neurobiologiae Experi-
mentalis 65, 243–253.
Wolf, M., van Doorn, G. S., Leimar, O. & Weissing, F. J. (2007). Life-history trade-offs favour
the evolution of animal personalities. Nature 447, 581–584.
Yano, K., Mochizuki, K., Tsukada, O. & Suzuki, K. (2003). Further description and notes of nat-
ural history of the viper dogsh, Trigonognathus kabeyai from the Kumano-nada Sea and
the Ogasawara Islands, Japan (Chondrichthyes: Etmopteridae). Ichthyological Research
50, 251–258.
Young, J. L., Bornik, Z. B., Marcotte, M. L., Charlie, K. N., Wagner, G. N., Hinch, S. G. &
Cooke, S. J. (2006). Integrating physiology and life history to improve sheries manage-
ment and conservation. Fish and Fisheri es 7, 262 283.
Electronic References
Fergusson, I., Compagno, L. J. V. & Marks, M. (2009). Carcharodon carcharias:TheIUCN
Red List of Threatened Species 2009. Available at
Litvinov, F. F. & Laptikhovsky, V. V. (2005). Methods of investigations of shark heterodonty and
dental formulae’s variability with the blue shark, Prionace glauca takenasanexample.
International Council for the Exploration of the Sea CM 2005/N:27. Available at www
Malcolm, H., Bruce, B. D. & Stevens, J. D. (2001). A Review of the Biology and Status of
White Sharks in Australian Waters. Canberra: Department of Environment and Energy.
Available at
Stanley, R. (1995). DARWIN: Identifying Dolphins from Dorsal Fin Images. St Petersburgh, FL:
Eckerd College. Available atcation.html/
© 2017 The Fisheries Society of the British Isles, Journal of Fish Biology 2017, 91, 1032–1047
... From embryogenic formation through to maturity, many species undergo distinct developmental changes in anatomy, behaviour and physiology (French et al., 2017;Habegger et al., 2011;Olson, 1996). ...
... Distinct developmental events that occur through the course of an organism's life are called ontogenetic shifts and are not uniform across populations or species, as they are derived from individual rates of development (French et al., 2017;Matich & Heithaus, 2015;Turner Tomaszewicz et al., 2017). One example of an ontogenetic shift related to the overall growth and foraging ability of individual organisms is the bite force of sharks, which may be responsible for correlations between animal size and niche divergence (French et al., 2017;Grubbs, 2010;Matich & Heithaus, 2015). ...
... Distinct developmental events that occur through the course of an organism's life are called ontogenetic shifts and are not uniform across populations or species, as they are derived from individual rates of development (French et al., 2017;Matich & Heithaus, 2015;Turner Tomaszewicz et al., 2017). One example of an ontogenetic shift related to the overall growth and foraging ability of individual organisms is the bite force of sharks, which may be responsible for correlations between animal size and niche divergence (French et al., 2017;Grubbs, 2010;Matich & Heithaus, 2015). For many marine predators, including sharks, prey capture and subsequent consumption are explicitly related to the mouth and its associated structures. ...
Full-text available
Teeth are an integral component of feeding ecology with a clear link between tooth morphology and diet, as without suitable dentition prey cannot be captured nor broken down for consumption. Bull sharks Carcharhinus leucas undergo an ontogenetic niche shift from freshwater to marine habitats, which raises the question: does tooth morphology change with ontogeny? Tooth shape, surface area and thickness were measured using both morphometrics and an Elliptic Fourier Analysis, to determine if morphology varied with position in the jaw and if there was an ontogenetic change concordant with this niche shift. Significant ontogenetic differences in tooth morphology as a function of position in the jaw and shark total length were found, with upper and lower jaws of bull sharks presenting two different tooth morphologies. Tooth shape and thickness fell into two groupings, anterior and posterior, in both the upper and lower jaws. Tooth surface area, however, indicated three groupings, mesial, intermediate and distal, in both the upper and lower jaws. While tooth morphology changed significantly with size, showing an inflexion at sharks of 135 cm total length, each morphological aspect retained the same tooth groupings throughout. These ontogenetic differences in tooth morphologies reflect tooth strength, prey handling and heterodonty. This article is protected by copyright. All rights reserved.
... It is also curious that ontogenetic changes of tooth morphologies can affect certain teeth or tooth families at specific locations of the jaw. The most extreme case concerns the upper first and third teeth of C. carcharias, which width and angle are respectively and significantly modified after sexual maturation in males, contrary to females [French et al., 2017]. ...
... Meckelian (lower) teeth (dignathic heterodonty). The continuous and lifelong replacement of teeth in elasmobranchs makes this variation dynamic in time (ontogenetic heterodonty), their tooth types being replaced, linked to dietary shifts (Luer et al., 1990;Powter et al., 2010) and reproductive status (Reif, 1976;Springer, 1979;Gottfried and Francis, 1996;Motta and Wilga, 2001;Purdy and Francis, 2007;Powter et al., 2010;French et al., 2017). ...
... In elasmobranchs, tooth replacement occurs at various rates and following different patterns, depending, for instance, on tooth imbrication and water temperature, and may also differ between jaws (Strasburg, 1963;Luer et al., 1990;Correia, 1999;Moyer and Bemis, 2016;Meredith Smith et al., 2018). Gynandric heterodonty (sexual dimorphism in teeth) is very common in elasmobranchs (Feduccia and Slaughter, 1974;Taniuchi and Shimizu, 1993;Kajiura and Tricas, 1996;Geniz et al., 2007;Gutteridge and Bennett, 2014;Underwood et al., 2015;French et al., 2017) and affects specific tooth files (reported in Dasyatidae, Carcharhinidae, and Leptochariidae) to the whole dental set at various degrees during the sexually mature stage (Cappetta, 1986). The higher and sharper mature male teeth are indeed assumed to function in grasping females and consequently to facilitate clasper introduction during copulation (Springer, 1966;McEachran, 1977;McCourt and Kerstitch, 1980;Cappetta, 1986;Ellis and Shackley, 1995;Kajiura and Tricas, 1996;Pratt Jr. and Carrier, 2001;Litvinov and Laptikhovsky, 2005;Gutteridge and Bennett, 2014). ...
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Teeth are serial structures whose evolutionary and developmental history is intricately linked with the emergence of mineralised tissues in vertebrates. Teeth display a broad range of forms and differ in developmental patterns in extant vertebrates, making them remarkable elements to study species diversification. Selachian teeth renew permanently and display morphologies that are correlated with mating and trophic behaviours.This work first assesses the variation of tooth forms in two scyliorhinids by using 3D geometric morphometrics and machine learning. The emergence of gynandric heterodonty is detailed for the first time along the ontogeny of sharks and it is demonstrated that this natural variation should be first assessed before performing species discrimination.This work also questions the role of specific proteins on the acquisition of a shark tooth form over development. Functional tests suggest an impact of Shh and Fgf3 in the cusp morphogenesis and in the mineralisation process. These proteins are promising explanatory variables to the inter- and intraspecific tooth differences observed, leading to hypotheses on their role in the evolution of structures with speciation and trophic and mating behaviours.Histological data on extant chondrichthyan vertebrae finally highlight the unsuspected proportion of extant elasmobranchs exhibiting fibrous mineralisation in the neural arches, a bone-like tissue which occurrence had long been refuted in this group. Evolutionary considerations are discussed in the light of the evolution of jawed vertebrates and question on the ecological factors that led particular tissues to be restricted to specific shark and batoid groups.
... These ecological functions may, however, be undermined in the future if ocean acidification disrupts biomineralization and adversely affects the mechanical (e.g. hardness and stiffness) and morphological properties of teeth needed to maintain foraging performance (Frazzetta, 1988;French et al., 2017;Motta & Wilga, 2001;Whitenack & Motta, 2010). For example, teeth of lower mechanical resilience (i.e. more brittle) are more vulnerable to physical damage and blunting, thereby compromising puncture performance (Corn et al., 2016). ...
... Teeth are the key structure for predation, and their mechanical and morphological properties can determine the foraging efficiency of sharks (Frazzetta, 1988;French et al., 2017). For example, broader triangular teeth have lower puncture performance than narrowcusped teeth (Whitenack & Motta, 2010), implying that abrasion resistance of teeth is important to maintain foraging efficiency (Corn et al., 2016). ...
Ocean acidification can cause dissolution of calcium carbonate minerals in biologi- cal structures of many marine organisms, which can be exacerbated by warming. However, it is still unclear whether this also affects organisms that have body parts made of calcium phosphate minerals (e.g. shark teeth), which may also be impacted by the ‘corrosive’ effect of acidified seawater. Thus, we examined the effect of ocean acidification and warming on the mechanical properties of shark teeth (Port Jackson shark, Heterodontus portusjacksoni), and assessed whether their mineralogical proper- ties can be modified in response to predicted near-future seawater pH (–0.3 units) and temperature (+3°C) changes. We found that warming resulted in the production of more brittle teeth (higher elastic modulus and lower mechanical resilience) that were more vulnerable to physical damage. Yet, when combined with ocean acidifica- tion, the durability of teeth increased (i.e. less prone to physical damage due to the production of more elastic teeth) so that they did not differ from those raised under ambient conditions. The teeth were chiefly made of fluorapatite (Ca5(PO4)3F), with in- creased fluoride content under ocean acidification that was associated with increased crystallinity. The increased precipitation of this highly insoluble mineral under ocean acidification suggests that the sharks could modulate and enhance biomineralization to produce teeth which are more resistant to corrosion. This adaptive mineralogical adjustment could allow some shark species to maintain durability and functionality of their teeth, which underpins a fundamental component of predation and sustenance of the trophic dynamics of future oceans.
... White sharks are one of the largest predatory fishes, reaching 602 cm total length (TL) and weighing ~2 530 kg (Christiansen et al. 2014). They feed on a wide variety of prey, including marine mammals, elasmobranchs, teleosts and invertebrates (Klimley and Anderson 1996;Hussey et al. 2012;de Vos et al. 2015;French et al. 2017). White sharks have been shown to induce risk effects in other species, such as Cape fur seals Arctocephalus pusillus pusillus, whereby they impact the spatial and temporal behaviour of seals at colonies, while also inducing physiological stress (Pyle et al. 1996;de Vos et al. 2015;Hammerschlag et al. 2022). ...
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Risk-induced fear effects exerted by top predators are pervasive in terrestrial and marine systems, with lasting impacts on ecosystem structure and function. The loss of top predators can disrupt ecosystems and trigger trophic cascades, but the introduction of novel apex predators into ecosystems is not well understood. We documented the emigration of white sharks Carcharodon carcharias in response to the presence of a pair of killer whales, Orcinus orca, at a large white shark aggregation site in South Africa. Between February and June in 2017, five white shark carcasses washed up on beaches in Gansbaai, Western Cape Province, four of which had their livers removed. Sightings per unit effort (sea days) and telemetry data demonstrated that white sharks emigrated from Gansbaai following these predation events, and in response to further sightings of this pair and other killer whale pods in the vicinity. Tagging data demonstrated the immediate departure of white sharks from Gansbaai, and some sharks were subsequently moving east. Contrary to expected and well-documented patterns of white shark occurrence at this site, their sightings dropped throughout the following 2.5 years; change-point analysis on both datasets confirmed these departures coincided with killer whale presence and shark carcasses washing out. These findings suggest that white sharks respond rapidly to risk from a novel predator, and that their absence triggered the emergence of another predator, the bronze whaler Carcharhinus brachyurus. Predator–prey interactions between white sharks, other coastal sharks, and killer whales are increasing in South Africa and are expected to have pronounced impacts on the ecosystem.
... In Atlantic stingrays Hypanus sabinus (Lesueur, 1824), for example males develop more cuspidate teeth during the mating season, supposedly to get a better grip on the female during mating (Kajiura & Tricas, 1996). Temporal tooth variations are facilitated by the polyphyodont tooth replacement and are not restricted to gynandric heterodonty, but can also occur throughout ontogeny dependent or independent of sex (Berio et al., 2020;French et al., 2017;Herman et al., 1993;Hubbell, 1996;Purdy & Francis, 2007). Such ontogenetic shifts in tooth morphologies are often linked to dietary shifts, for example in large predatory species such as the white shark: juvenile white sharks are predominantly piscivorous as they have not yet reached the body size to hunt and feed on large prey, while older specimens mainly feed on marine mammals (Cliff et al., 1989;Estrada et al., 2006;Hussey et al., 2012;Tricas & McCosker, 1984). ...
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The lifelong tooth replacement in elasmobranch fishes (sharks, rays and skates) has led to the assemblage of a great number of teeth from fossil and extant species, rendering tooth morphology an important character for taxonomic descriptions, analysing phylogenetic interrelationships and deciphering their evolutionary history (e.g. origination, divergence, extinction). Heterodonty (exhibition of different tooth morphologies) occurs in most elasmobranch species and has proven to be one of the main challenges for these analyses. Although numerous shark species are discovered and described every year, detailed descriptions of tooth morphologies and heterodonty patterns are lacking or are only insufficiently known for most species. Here, we use landmark-based 2D geometric morphometrics on teeth of the tiger shark Galeocerdo cuvier to analyse and describe dental heterodonties among four different ontogenetic stages ranging from embryo to adult. Our results reveal rather gradual and subtle ontogenetic shape changes, mostly characterized by increasing size and complexity of the teeth. We furthermore provide the first comprehensive description of embryonic dental morphologies in tiger sharks. Also, tooth shapes of tiger sharks in different ontogenetic stages are reassessed and depicted in detail. Finally, multiple cases of tooth file reversal are described. This study, therefore, contributes to our knowledge of dental traits across ontogeny in the extant tiger shark G. cuvier and provides a base-line for further morphological and genetic studies on the dental variation in sharks. Therefore, it has the potential to assist elucidating the underlying developmental and evolutionary processes behind the vast dental diversity observed in elasmobranch fishes today and in deep time. K E Y W O R D S elasmobranch, embryonic dentition, geometric morphometrics, ontogenetic trajectory, teeth, tooth pattern reversal
... Como sucede con la mayoría de las especies pelágicas, los Tiburones Blancos son difíciles de estudiar debido a su gran tamaño, su gran movilidad, la complejidad de mantenerlos en cautiverio y a las limitantes logísticas de conducir investigación en el mar. (French et al., 2017;Santana-Morales et al., 2020b). Presenta largas hendiduras branquiales, y en el dorso tiene una aleta dorsal alta y ancha de forma triangular cuyo borde posterior presenta una punta inferior libre y de color oscuro, mientras que la segunda aleta dorsal es muy pequeña, de tamaño similar al de la aleta anal. ...
... Como sucede con la mayoría de las especies pelágicas, los Tiburones Blancos son difíciles de estudiar debido a su gran tamaño, su gran movilidad, la complejidad de mantenerlos en cautiverio y a las limitantes logísticas de conducir investigación en el mar. (French et al., 2017;Santana-Morales et al., 2020b). Presenta largas hendiduras branquiales, y en el dorso tiene una aleta dorsal alta y ancha de forma triangular cuyo borde posterior presenta una punta inferior libre y de color oscuro, mientras que la segunda aleta dorsal es muy pequeña, de tamaño similar al de la aleta anal. ...
El objetivo general del Programa de Acción para la Conservación de la Especie Tiburón Blanco (PACE) consiste en establecer una estrategia integral de investigación, protección y conservación del Tiburón Blanco en aguas mexicanas, que permita incrementar el conocimiento de la especie, robustecer las medidas de manejo para su aprovechamiento no extractivo sustentable y prevenir y mitigar las posibles amenazas para la especie y su hábitat.
... White sharks around strandings were on average 0.21 m larger than white sharks observed away from whale carcasses. White sharks are known to undergo an ontogenetic shift as they mature, moving from a diet consisting mostly of fish to primarily mammalian prey (Estrada French, 2017). Only two individuals observed in the vicinity of whale carcass strandings could be considered adult white sharks based on their total length (Bruce, 2008). ...
White sharks (Carcharodon carcharias) are attracted to and scavenge on floating whale carcasses. However, little is known about how stranded whale carcasses may affect their behaviour. With increasing whale populations and beach stranding events, sharks may be attracted to nearshore waters at carcass sites, increasing the potential conflict with human use. Here, we used aerial drones to assess whether white shark behaviour around stranded whale carcasses differs from their behaviour away from carcasses. We quantified white shark behaviour by measuring swim speed, net velocity, straightness and sinuosity of shark tracks, as well as the total length of each shark. White sharks in the vicinity of whale carcasses travelled at 0.46 m s⁻¹ (±0.06 SD) faster, were 0.26 m (±0.15 SD) longer, swam tracks that were 0.15 (±0.11 SD) lower on the straightness index, and showed more sinuous tracks by 0.07 (±0.02 SD), compared to sharks away from a carcass. The presence of a stranded whale carcass may, therefore, significantly altered the behaviour and size of white sharks close to shore. As white shark activity increases in a relatively small nearshore area, which was indicated by decreased straightness and increased sinuosity, there may be an elevated risk of shark interactions with water users in the vicinity of stranded whale carcasses.
... Ellis and Shackley 1995;Moyer and Bemis 2016;Purdy and Francis 2007;Sadowsky 1970;Straube et al. 2008;Taniuchi 1970), however, it is unknown for most, especially in deep-sea sharks (Cullen and Marshall 2019;Martins et al. 2015;Pinchuk and Permitin 1970). The known cases comprise ontogenetic differences (Mello and Brito 2013), which may be due to differences in diet (French et al. 2017;Powter et al. 2010;Raschi et al. 1982;Reif 1976;Schwartz and Hurst 1996;Tomita et al. 2017) as well as seasonal changes due to sexual or population-level differences (Lucifora et al. 2003). Therefore, it is possible that the presence of intraspecific variation in tooth morphologies in extant species is more common than documented. ...
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An important character on several taxonomic levels for shark identification is the tooth morphology. Sharks show a variety of highly specialized dentitions reflecting adaptations to their feeding habits. Intraspecific variation of tooth morphology such as sexual or ontogenetic dimorphism is poorly known in many species, even though tooth morphology plays a decisive role in the characterization of the fossil record of sharks, which comprises mostly fossil teeth. Here we analyzed the dentition of 40 jaws of the Velvet Belly Lantern Shark Etmopterus spinax and identified ontogenetic and sexual dimorphic characters such as total number of teeth, number of upper teeth, cusplet numbers in upper jaw teeth and width of lower jaw teeth. Dimorphic characters may reduce intraspecific competition for food, as E. spinax segregates by sex and size and may allow for identifying the male sex. The lower jaw tooth height, a sexually non-dimorphic character, was used to recalculate the total length of specimens, which represents the first such approach for a squaliform shark. Results derived from the extant E. spinax are subsequently applied to fossil Etmopterus sp. teeth (Miocene) to gain individual information such as sex or size, but also characterize the extinct population from the excavation site by a size distribution profile in comparison to data from extant populations. This approach indicates the presence of multiple ontogenetic stages in the extinct population.
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Assessing progress for the endangered white shark (Carcharodon carcharias) relative to Canadian conservation objectives requires understanding distribution patterns. From the largest tagging dataset in the Northwest Atlantic (2010-2020; 272 deployments), we determined the proportion of the population detected in Canadian waters, characterized patterns in occupancy, and explored the behavioural characteristics of animals while in Canadian waters vs elsewhere in their range. The component of the population detected in Canadian waters annually was highly variable, yet proportionately small. Juveniles and sub-adults were 4.7 and 3.4 times more likely, respectively, to move northward than adults. From June to November, all PSAT-tagged white sharks remained primarily in coastal locations within the 200 m bathymetric contour and exhibited shallow diving behaviour within the top 100 m of the water column. However, individuals in Canadian waters experienced a more restricted temperature range and used proportionately less of the water column. Accounting for behavioural effects on distribution when predicting habitat use from environmental associations will become critical to evaluate the population-level impact of recovery actions implemented under Canadian legislation.
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Top-predators may be extremely vulnerable to environmental contaminants, such as organochlorines (OCs) and polycyclic aromatic hydrocarbons (PAHs), mostly because of their position in the trophic web. In this study, the use of skin biopsy is proposed as a sensitive non-lethal technique for the toxicological assessment of white shark (Carcharodon carcharias) living off the South African coasts. In 2012, 15 specimens of great white shark were sampled in the waters off Dyer Island and Geyser Rock. Then OCs and PAHs were extracted from muscle and biomarkers techniques for the evaluation of the cytochrome P4501A (CYP1A), Vitellogenin (Vtg) and Zona Radiata Proteins (Zrp) in the skin have been developed for the first time. The results showed levels of OCs higher than those found in the literature, ranging in ng/g dry weight (d.w.) from 6.80 to 21.26 for hexachlorobenzene (HCB), from 86.72 to 1416.97 for DDTs and from 379.76 to 11284.31 for polychlorinated biphenyls (PCBs). Furthermore, the values of both pp’DDE/pp’DDT and pp’DDE/DDTs ratios suggest a recent DDT introduction in the environment, probably related to its use against malaria during the period 2000-2005 in KwaZulu-Natal. However, PAHs showed the highest levels, almost double compared to OCs, almost certainly due to the big oil traffic present in South Africa. Regarding biomarkers results, important responses for CYP1A have been highlighted, possibly due to a contamination by planar compounds such as PAHs. Finally, the preliminary results of Vtg and Zrp, biomarkers of estrogenic effects, showed the presence of these proteins in sexually immature females and males.
How morphology changes with size can have profound effects on the life history and ecology of an animal. For apex predators that can impact higher level ecosystem processes, such changes may have consequences for other species. Tiger sharks (Galeocerdo cuvier) are an apex predator in tropical seas, and, as adults, are highly migratory. However, little is known about ontogenetic changes in their body form, especially in relation to two aspects of shape that influence locomotion (caudal fin) and feeding (head shape). We captured digital images of the heads and caudal fins of live tiger sharks from Southern Florida and the Bahamas ranging in body size (hence age), and quantified shape of each using elliptical Fourier analysis. This revealed changes in the shape of the head and caudal fin of tiger sharks across ontogeny. Smaller juvenile tiger sharks show an asymmetrical tail with the dorsal (upper) lobe being substantially larger than the ventral (lower) lobe, and transition to more symmetrical tail in larger adults, although the upper lobe remains relatively larger in adults. The heads of juvenile tiger sharks are more conical, which transition to relatively broader heads over ontogeny. We interpret these changes as a result of two ecological transitions. First, adult tiger sharks can undertake extensive migrations and a more symmetrical tail could be more efficient for swimming longer distances, although we did not test this possibility. Second, adult tiger sharks expand their diet to consume larger and more diverse prey with age (turtles, mammals, and elasmobranchs), which requires substantially greater bite area and force to process. In contrast, juvenile tiger sharks consume smaller prey, such as fishes, crustaceans, and invertebrates. Our data reveal significant morphological shifts in an apex predator, which could have effects for other species that tiger sharks consume and interact with. J. Morphol., 2016. © 2016 Wiley Periodicals, Inc.
Fine-scale predator movements may be driven by many factors including sex, habitat and distribution of resources. There may also be individual preferences for certain movement strategies within a population which can be hard to quantify. Within top predators, movements are also going to be directly related to the mode of hunting, for example sit-and-wait or actively searching for prey. Although there is mounting evidence that different hunting modes can cause opposing trophic cascades, there has been little focus on the modes used by top predators, especially those in the marine environment. Adult white sharks (Carcharhodon carcharias) are well known to forage on marine mammal prey, particularly pinnipeds. Sharks primarily ambush pinnipeds on the surface, but there has been less focus on the strategies they use to encounter prey. We applied mixed hidden Markov models to acoustic tracking data of white sharks in a coastal aggregation area in order to quantify changing movement states (area-restricted searching (ARS) vs. patrolling) and the factors that influenced them. Individuals were re-tracked over multiple days throughout a month to see whether state-switching dynamics varied or if individuals preferred certain movement strategies. Sharks were more likely to use ARS movements in the morning and during periods of chumming by ecotourism operators. Furthermore, the proportion of time individuals spent in the two different states and the state-switching frequency, differed between the sexes and between individuals. Predation attempts/success on pinnipeds were observed for sharks in both ARS and patrolling movement states and within all random effects groupings. Therefore, white sharks can use both a 'sit-and-wait' (ARS) and 'active searching' (patrolling) movements to ambush pinniped prey on the surface. White sharks demonstrate individual preferences for fine-scale movement patterns, which may be related to their use of different hunting modes. Marine top predators are generally assumed to use only one type of hunting mode, but we show that there may be a mix within populations. As such, individual variability should be considered when modelling behavioural effects of predators on prey species.