The tooth, the whole tooth and nothing but the tooth: tooth shape and ontogenetic shift dynamics in the white shark Carcharodon carcharias

Abstract

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.

Full text

Journal of Fish Biology (2017) 91, 1032–1047
doi:10.1111/jfb.13396, available online at wileyonlinelibrary.com
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.
INTRODUCTION
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-
gia.c.a.french@gmail.com
1032
© 2017 The Fisheries Society of the British Isles

ONTOGENETIC SHIFT DYNAMICS IN CARCHARODON CARCHARIAS 1033
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.
MATERIALS AND METHODS
TOOTH CUSPIDITY
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

ONTOGENETIC SHIFT DYNAMICS IN CARCHARODON CARCHARIAS 1035
(a) (b)
(c) (d)
RP2
RP2
Crown
height
Crown width
Palatoquadrate symphysis
RP1
RP1
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 (34·58∘S; 19·35∘E), using a novel photographic method and ImageJ software
(www.imagej.nih.gov; 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)
Positive
LP2
LP3
Midpoint
Negative
Tooth angle
LP2
LP3
RP3
RP3
RP4
RP4
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

ONTOGENETIC SHIFT DYNAMICS IN CARCHARODON CARCHARIAS 1037
TOOTH ANGLE
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
(1996).
SHARK TOTAL LENGTH
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).
PHOTOGRAPHIC METHOD
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 (www.darwin.eckerd.edu), 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.
STATISTICAL ANALYSES
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
.r-project.org) 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.
(a)
(b)
LP1LP2
LP1
LP2
F. 4. Photographs taken on (a) 15 March 2015 (K. Baker, www.sharkwatch.sa) 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; www.ibm.com); SW,
within group variance and SA, among group variance). Repeatability (R)=SA2(S2)−1+SA2,
where S2=SW,SA2=(SA−SW)n0
−1,wheren0=[1(a−1)][∑ni−∑ni2∑ni)−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

ONTOGENETIC SHIFT DYNAMICS IN CARCHARODON CARCHARIAS 1039
1·0
23456
1·1
1·2
IT
1·3
1·4
1·5
(a)
1·0
23456
1·1
1·2
1·3
1·4
(b)
–3
LT (m)
–2
–1
Tooth angle
0
1
2
(c)
–20
3·5
2·5 4·5 5·5
3·52·5 4·5 5·5
–10
–15
0
–5
10
5
15
(d)
(c)
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.
RESULTS
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=−0·617x−5·1663, 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.
0·9
1·0
1·1
1·2
1·3
IT
1·4
1·5
1·6
(a)
1·10·9 1·3 1·5
IT
(b)
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% .. 0·73–1·27, 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.
DISCUSSION
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)≥3and≥4
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.
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ONTOGENETIC SHIFT DYNAMICS IN CARCHARODON CARCHARIAS 1041
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

ONTOGENETIC SHIFT DYNAMICS IN CARCHARODON CARCHARIAS 1043
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.
References
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, 961–972.
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. 225–253. 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. 85–90. 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,
829–834.
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,
237–248.
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. 27–49. 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

ONTOGENETIC SHIFT DYNAMICS IN CARCHARODON CARCHARIAS 1045
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,
116–121.
Lingham-Soliar, T. (2005). Caudal n allometry in the white shark Carcharodon carcharias:
implications for locomotory performance and ecology. Naturwissenschaften 92,
231–236.
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,
567–572.
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,
927–944.
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. 59–75. 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

ONTOGENETIC SHIFT DYNAMICS IN CARCHARODON CARCHARIAS 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,
271–286.
Wilson, D. S. (1975). The adequacy of body size as a niche difference. American Naturalist 109,
769–784.
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,
187–198.
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 www.iucnredlist.org/details/3855/0
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
.ices.dk/sites/pub/CM%20Doccuments/2005/N/N2705.pdf
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 https://publications.csiro.au/rpr/download?pid=procite:1d0d13e5-7a60-
4e65-be78-636e6f2dd22e&dsid=DS1/
Stanley, R. (1995). DARWIN: Identifying Dolphins from Dorsal Fin Images. St Petersburgh, FL:
Eckerd College. Available at http://darwin.eckerd.edu/?page=photo_identication.html/
© 2017 The Fisheries Society of the British Isles, Journal of Fish Biology 2017, 91, 1032–1047