Zoological Journal of the Linnean Society, 2009, 155, 834–844. With 7 figures
Variation in elasmoid fish scale patterns is informative
with regard to taxon and swimming mode
ANA L. IBAÑEZ1,2*, IAN G. COWX2 and PAUL O’HIGGINS3
1
Departamento de Hidrobiología, Universidad Autónoma Metropolitana-Iztapalapa, Av. San Rafael
Atlixco 186, Col. Vicentina, D.F. 09340 México
2
Hull International Fisheries Institute, Hull HU6 7RX, UK
3
Hull York Medical School. The University of York, Heslington York YO10 5DD, UK
Received 9 March 2007; accepted for publication 10 March 2008
Variations in scales from nine regions on the flank of teleost fish were examined from the point of view of functional
adaptation and with regard to which scales best differentiate species. Three teleost species were selected; two are
from the genus Mugil, M. cephalus and M. curema, which are phylogenetically distant from the third, Dicentrarchus labrax. Scale form was described using seven landmarks, the coordinates of which were subjected to
generalized Procrustes analysis followed by principal components analysis. Principal component scores were
submitted to cross-validated discriminant analysis to assess the utility of each scale in identifying species. The best
discrimination (98%) was obtained with the scale from the central-dorsal area. Scales from the anterior and central
zones are relatively wide dorsoventrally and narrow anteroposteriorly. This appears to be related to the profile of
the lateral body wall and with subcarangiform swimming. Scales from the posterior region are anteroposteriorly
long and dorsoventrally narrow, this shape possibly being related to thrust. Despite the wide phylogenetic
separation between mullets and D. labrax, the pattern of scale variation is similar. This may imply strong
functional convergence, although studies of sister taxa with different swimming modes are required to confirm
this. © 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 155, 834–844.
ADDITIONAL KEYWORDS: Dicentrarchus labrax – geometric morphometrics – landmarks – Mugil cephalus
– Mugil curema – scale morphology.
INTRODUCTION
Scales from the majority of teleost fishes (a group
which includes more than 26 000 species including
sea bass and grey mullet) belong to the elasmoid type.
Elasmoid scales are thought to be derived from the
superficial ‘dental’ tissues that covered the rhombic
scales in ancestral osteichthyan fish (Sire & Huysseune, 2003). Thesleff, Vaahtokari & Partanen (1995)
supported this view because scales develop close to
the epidermal–dermal junction, and show a development sequence similar to that of teeth.
Fish scales have been used for various purposes:
the most frequent uses being in ageing (Bagenal,
1974), to discern life history characteristics, to study
population dynamics; to assess bioaccumulation of
pollutants such as heavy metals (Basu et al., 2006;
*Corresponding author. E-mail: [email protected]
834
Lake et al., 2006); to determine diet based on their
presence in stomach contents or faecal wastes
(Mauchline & Gordon, 1984); to interpret past biodiversity (Shackleton, 1987; McDowall & Lee, 2005);
in comparative and phylogenetic studies (Lippitsch,
1992; Roberts, 1993); to isolate DNA (Yue & Orban,
2001); and to assess developmental and evolutionary
origins (Reif, 1980; Hutchinson, Carvalho & Rogers,
2001; Sire & Akimenko, 2004).
One other application that has received little attention is the use of fish scale shape to identify stock
membership using Fourier analysis (Poulet et al.,
2005) or more recently, geometric morphometrics
(Ibañez, Cowx & O’Higgins, 2007). The latter study
demonstrated the effectiveness of elasmoid scale
shape to discriminate different species and populations of mullet (Family Mugilidae) based on a single
scale taken from the shoulder region of each fish, the
position on the fish’s body from which scales are
© 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 155, 834–844
VARIATIONS IN ELASMOID FISH SCALE FORM
typically taken for ageing studies. No account was
taken of possible changes in scale shape over the body
of the fish and how this could be relevant in group
identification or of how scale variation might relate to
swimming mode and possibly hydrodynamic function.
This latter factor is of interest because several studies
noted the significance of microstructure and hydrodynamic properties of fish scale profiles (Burdak, 1957,
1986; Sudo et al., 2002; Ikoma et al., 2003). Burdak
(1986) studied the ontogeny of cteni (spine-like ornamentations), the squamation pattern of Mugil saliens
(Risso), and the overlapping of scales of different
Cyprinidae species and suggested the degree of scale
overlap (more imbricate pattern) provides protection
against collision in nectonic species.
In the present study we extended the work of
Ibañez et al. (2007) to examine how scales from nine
regions, spanning the craniocaudal and dorsoventral
axes, of the lateral body wall, vary in form. We
assessed patterns of scale variation among three fish
species to determine, by anatomical region, which are
the best scales to differentiate the species. Additionally, we related the observed patterns of among
species variation in the shapes of scales from nine
regions of the body to evolutionary history and swimming mode to assess the potential of this approach in
the wider context of studies of function.
The species chosen for this study were the congeneric Mugilidae Mugil cephalus (Linnaeus, 1758) and
Mugil curema (Valenciennes, 1836) and the European
sea bass Dicentrarchus labrax (Linnaeus, 1758)
(Pisces: Moronidae). Mugil cephalus and M. curema
are useful model species because they are morphologically similar but exhibit remarkable genetic divergence compared with other members of the family
(Caldara et al., 1996). Comparison of the two muglids
with a distantly related taxon (Dicentrarchus) provides an interesting, although of necessity incomplete, view of intra- and intertaxon differences.
Nelson (2006) considered sea bass to belong to the
Serie Percomorpha (fishes with fin spines, protractile
maxilla, and pelvic fin position thoracic or jugular)
while mullets belong to the closely related Atherinomorpha, although this is open to conjecture because
Johnson & Patterson (1993) and Chen, Bonillo &
Lecointre (2003) considered mullets and sea bass
as distantly related members of the Percomorpha.
The three species have ctenoid scales, allowing us to
evaluate the extent to which phylogeny and function
impact on scale form.
MATERIAL AND METHODS
FISH SCALE COLLECTION
Specimens of Mugil cephalus (30) and M. curema
(nine) were collected from Mexico City central fish
835
market and Dicentrarchus labrax (15) from a local
fish market in Hull, UK (possibly sourced from a
fish farm). All were adult specimens with average
furcal lengths of 29.65 ± 1.31, 31.83 ± 2.13 and
31.95 ± 1.18 cm for M. cephalus, M. curema, and
D. labrax, respectively. Specimens were transported
fresh to the laboratory where scales were removed for
examination. This was achieved by dividing the lefthand side of the fish into zones along the longitudinal
and transverse axes of the body. Longitudinally the
zones were: zone A (anterior), zone C (central), and
zone P (posterior). Transversally the fish body was
divided into three zones: zone 2 was limited at the
lateral line level, zones 1 and 3 were above and below
this strip, respectively. Consequently, the flank of the
fish was divided into nine areas (Fig. 1). In this study,
the term ‘area’ refers to the nine sections of the side
of the body while ‘zone’ means longitudinal and transversal sections (A, C, and P; 1, 2, and 3, respectively).
One scale was removed from each area of each specimen for examination and any regenerated scales were
discarded. Therefore, the sample comprised: 270
scales from M. cephalus (30 fish ¥ nine scales), 81 M.
curema scales (nine fish ¥ nine scales) and 135 D.
labrax scales (15 fish ¥ nine scales); 486 scales in
total. The scales were cleaned using soft soap and tap
water, dried with blotting paper and a digital image
was taken of each scale from the flat screen of a
microfiche projector.
Seven landmarks per scale were taken using
TPSdig software (Rohlf, 2006) following the protocol
of Ibañez et al. (2007). The landmarks were located on
key features of the ctenoid scale that are common to
all scales of the species under study. This ensures
that in subsequent interpretation of results, variations in particular landmarks can be related to shared
features of form. The following landmarks were considered appropriate (Fig. 2): landmarks 1 and 3 are
the ventro- and dorsolateral tips of the anterior
portion of the scale; landmark 2 is in the centre of the
anterior edge of the scale, landmarks 4 and 6 are at
the boundary between the anterior portion with
circuli and the posterior area covered by cteni; landmark 5 is the focus of the scale; and landmark 7 is
positioned at the tip of the posterior portion of the
scale.
MORPHOMETRICS
The configurations of landmark coordinates for the
486 sampled scales were scaled, translated and
rotated using generalized Procrustes analysis (GPA).
They were then submitted to tangent projection
(Dryden & Mardia, 1993) and subsequently to principal components analysis (PCA; Dryden & Mardia,
1993; Kent, 1994). The principal component (PC)
© 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 155, 834–844
836
A. L. IBAÑEZ ET AL.
A
C
P
1
A1
C1
2
3
A2
C2
A3
C3
P1
P2
P3
Figure 1. Sampling areas on the flank of fish. Longitudinally the zones were: zone A (anterior) from behind the
operculum to the middle of the first dorsal fin (around the fourth spine for Dicentrarchus labrax and the second in Mugil
species); zone C (central) was from the middle of the first fin and the tip of the second fin; zone P (posterior) was between
the tip of the second dorsal fin and the beginning of the caudal fin, equivalent to the caudal peduncle. Transversely the
fish body was divided into three zones: zone 2 was limited at the lateral line level, zones 1 and 3 were above and below
this strip, respectively. Consequently, the flank of the fish was divided into nine areas: A1, A2, A3, C1, C2, C3, P1, P2,
and P3.
Figure 2. Landmark definitions.
scores were labelled by longitudinal zone (A to P) and
then by transversal zone (1 to 3) to describe the
distribution of the scales along the body and also by
species. The extremes of each PC were then used to
reconstruct the expected shapes of landmark configurations with those particular scores by adding to the
mean tangent coordinates the products of these PC
scores and the eigenvectors for those PCs before projecting back from the tangent to the configuration
space (O’Higgins, Chadfield & Jones, 2001). The differences in shape between the mean and the shapes
represented by the extremes of PCs of interest were
visualized using transformation grids (Bookstein,
1989; Marcus et al., 1996; Dryden & Mardia, 1998)
computed with MORPHOLOGIKA2 (O’Higgins &
Jones, 2006).
To examine the potential for differences in shape in
classifying unknown specimens, the scores of specimens on all nonzero PCs were submitted to discriminant analysis (SPSS ver. 13.0) to compute generalized
Mahalanobis’ distances, discriminant functions, and
to assess the efficacy of the latter in classification. This
was carried out using cross-validation, in which multiple repeated analyses were carried out leaving out
one individual in the construction of the discriminant
function before classifying this individual according
to the function. This reduces the likelihood of overestimating the efficacy of discriminant functions by
using them to classify specimens employed in their
construction. Percentage correct classification rates
were recorded. With regard to form (size plus shape),
ln centroid size (the square root of the sum of squared
distances between each landmark and the centroid of
the landmark configuration) was added as a column of
the data matrix (of registered coordinates) (Mitteroecker, Gunz & Bookstein, 2005) and the GPA/PCA and
discriminant analysis analyses were repeated.
The configurations of landmark coordinates for
each area by species were scaled, translated, and
rotated using GPA to obtain the consensus configuration (a single set of landmarks which represents the
central tendency of an observed sample; i.e. each area
of each species). The nine consensus configurations
for each species were then jointly subjected to GPA/
PCA to examine the pattern of shape variation among
areas within each species. Thereafter, the morphological distance matrix of Procrustes chord distances (the
square root of the sum of squared differences between
the positions of the landmarks in two optimally
superimposed configurations at centroid size) among
consensus configurations by area was computed.
Finally, the correlation among the three matrices (one
© 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 155, 834–844
VARIATIONS IN ELASMOID FISH SCALE FORM
837
RESULTS
per species) was assessed by the Mantel test (using zt
software; Bonnet & Van de Peer, 2002), in which the
null hypothesis is that distances between scales from
different areas in one matrix are independent of the
distances between equivalent scales in the other
matrix.
GPA/PCA resulted in a set of PCs that describe the
patterns of shape variability among scales. In particular, we were concerned to know the extent to
which scale shape variability relates to species and
0.12
A
0.08
0.04
-0.40
-0.32
-0.24
-0.16
-0.08
0.08
0.16
0.24
-0.04
Zone A
Zone C
Zone P
-0.08
-0.12
0.12
B
0.08
0.04
-0.40
-0.32
-0.24
-0.16
-0.08
0.08
0.16
0.24
-0.04
Zone 1
Zone 2
Zone 3
-0.08
-0.12
Figure 3. First two principal components of scale shape. A, labelled by longitudinal zones. B, labelled by transverse
zones.
0.12
0.08
0.04
-0.40
-0.32
-0.24
-0.16
-0.08
0.08
0.16
0.24
-0.04
-0.08
-0.12
M. cephalus
M. curema
D. labrax
Figure 4. First two principal components (PCs) of shape labelled by species. Thin plate spline transformation grids for
the extreme points of each PC are shown; these are superimposed on the shapes predicted when the average landmark
configuration of all specimens is deformed into that of a hypothetical specimen positioned at the extreme of the PC of
interest.
© 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 155, 834–844
838
A. L. IBAÑEZ ET AL.
anatomical location. This was assessed directly by
discriminant analysis (see below) but was explored
initially by examination of PC plots to see if there was
any evidence of clustering by species or area.
The first PC explained 69.6 % of the total variance
while the second accounted for 7.9 % for the GPA/PCA
analysis of the 486 scales examined. Two major
groups are visible in the PCA plot (Fig. 3A). Scales
from zones A and C are similar and grouped towards
the right (more +ve) extreme of PC1, whereas scales
from zone P are more to the left (more -ve). Scales
from zones 1 and 3 are relatively close to each other
and generally have smaller or more negative scores
on the plot of PCs 1 and 2, Figure 3B, whereas zone
2 scales tend to have larger or more positive scores.
The distributions in both plots show a continuum of
shape variation, but with scales from area P, and
especially P3, being most differentiated in shape.
Species are also to some extent distinguished in this
PC 1 vs. 2 plot (Fig. 4) with D. labrax having the most
Table 1. Percentage of scales from each zone correctly classified (cross-validated and using shape principal components
scores alone) with pooled species. Wilk’s lambda values in parentheses, all P < 0.001
Zones
A
C
P
Average ± STD
1
2
3
Average ± SD
92.6 (0.046)
94.4 (0.023)
83.3 (0.078)
90.10 ± 5.96
98.1 (0.035)
92.6 (0.029)
88.9 (0.060)
93.20 ± 4.63
81.5 (0.085)
94.4 (0.031)
92.6 (0.050)
89.50 ± 6.99
90.73 ± 8.46
93.80 ± 1.04
88.27 ± 4.68
Table 2. Classification results†‡ for the discriminant analysis (original) and the cross-validation testing procedure
(cross-validated) for the three species of the scales from area C1
Predicted group membership
Original
Count
%
Cross-validated*
Count
%
Species
M. cephalus
M. curema
D. labrax
Total
M. cephalus
M. curema
D. labrax
M. cephalus
M. curema
D. labrax
30
0
0
100.0
0
0
0
9
0
0
100.0
0
0
0
15
0
0
100.0
30
9
15
100.0
100.0
100.0
M. cephalus
M. curema
D. labrax
M. cephalus
M. curema
D. labrax
30
1
0
100.0
11.1
0
0
8
0
0
88.9
0
0
0
15
0
0
100.0
30
9
15
100.0
100.0
100.0
*In cross validation, each case is classified by the functions derived from all cases other than that case. M., Mugil; D.,
Dicentrarchus.
†100.0% of original grouped cases correctly classified.
‡98.1% of cross-validated grouped cases correctly classified.
Table 3. Percentage of scales from each zone correctly classified (cross-validated and using principal components scores
plus ln centroid size) with pooled species. Wilk’s lambda values in parentheses, all P < 0.001
Zones
A
C
P
Average ± STD
1
2
3
Average ± STD
100 (0.004)
98.1 (0.005)
100 (0.008)
99.37 ± 1.10
100 (0.005)
100 (0.007)
98.1 (0.007)
99.37 ± 1.10
94.4 (0.020)
100 (0.005)
92.6 (0.015)
95.67 ± 3.86
98.13 ± 3.23
99.37 ± 1.10
96.90 ± 3.84
© 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 155, 834–844
VARIATIONS IN ELASMOID FISH SCALE FORM
A)
M. cephalus
P1
A2
1
C1
PC2 (21.39%)
P3
C3
-1
A1
C2
1
2
1
2
P2
-1
A3
PC1 (66.24%)
B)
M. curema
C3
A1
1
PC2 (13.56%)
P2
P1
-1
A2
C1
P3
A3
-1
C2
PC1 (72.95%)
C)
D. labrax
C1
A2
P3
1
PC2 (21.57%)
positive, M. curema intermediate, and M. cephalus
the most negative PC2 scores. The Mugil species, M.
cephalus and M. curema, show more overlap with
each other on PC2 than either does with D. labrax.
The general pattern of morphological differences
described by these first two PCs was explored using
transformation grids (Fig. 4). The left-most grid represents the mean shape warped to a PC1 score of
-0.40 (scales from the caudal peduncle) with the
right-most representing a PC1 score of 0.24 (scales
from central and anterior zones). Caudal peduncle
scales were characterized by a relatively shorter
distance between the focus and landmark 7 with a
concave, anterior edge, whereas this distance for
anterior and central scales was relatively larger with
the focus more central and the anterior edge convex.
The scales from the anterior and central area were
relatively wide and short. The relative elongation of P
zone scales reflects a larger area of insertion into the
epidermis. Multivariate regressions of all PCs onto
zone or area confirmed these general trends.
Variation among species is represented by PC2, on
which D. labrax had more positive scores than Mugil,
was visualized by transformation grids computed
from the mean with PC2 scores of 0.12 (upper grid)
and -0.12 (Fig. 4). PC2 (7.9% total variance) represented a lesser proportion of overall shape variation
than PC1 (69.6% total variance). The key difference
between these grids was in the relative location of
focus, which was relatively more posterior in D.
labrax. Further, the anterior edge was convex in D.
labrax but concave in Mugil species.
The cross-validated discriminant analysis using
shape variables (PC scores) from all 486 scales correctly classified 84.8 % by species, whereas the proportion of scales from each zone correctly classified
(cross-validated and with pooled species) varied
between 81.5 and 98.1% (Table 1). The lowest classification rate, 81.5 %, was obtained using scales from
area P1, whilst area C1 was best with 98.1% crossvalidated correct classification. The highest correct
classification rates, and smallest standard deviations,
were found for zones C and 2, whereas the weakest
discrimination was for scales from the ventral area.
Most misclassifications occurred between the two
Mugil species. All scales from area C1 of the original
grouped cases were correctly classified without
cross-validation (Table 2); but the cross-validated
analysis misclassified one scale from M. curema to M.
cephalus (Wilk’s lambda = 0.035, P < 0.001). Classification results improved when size information was
included in the discriminant analysis, except for
area P3 where the cross-validated classification rate
remained the same (Table 3). Higher classification
values and smaller standard deviations were found
for zones A, C, and 2.
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C2
-1
1
A3
P2
A1
2
P1
-1
C3
PC1 (52.93%)
PC1 (52.93%)
Figure 5. Principal components analysis (PC1 and PC2)
of mean scale shapes in each area: A1, A2, A3, C1, C2, C3,
P1, P2, P3 as defined in Fig. 1. A, Mugil cephalus; B, Mugil
curema; C, Dicentrarchus labrax.
A second set of analyses examined the patterns of
variation of scale shape among anatomical regions
within each species and then compared these patterns
among species. GPA/PCA carried out using species
mean shapes for each area resulted in the plots of PC1
vs. 2 (Fig. 5A–C). The first PC explained 66, 73, and
53%, of the total variance, whereas the second
© 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 155, 834–844
840
A. L. IBAÑEZ ET AL.
Table 4. Procrustes distances between scales from each of the nine areas in each species
A) Mugil cephalus
A1
A2
A3
C1
C2
C3
P1
P2
P3
A1
A2
A3
C1
C2
C3
P1
P2
P3
0
0.065
0.115
0.053
0.065
0.134
0.139
0.073
0.304
0
0.137
0.083
0.026
0.158
0.179
0.118
0.347
0
0.070
0.120
0.028
0.074
0.070
0.219
0
0.068
0.089
0.100
0.044
0.269
0
0.141
0.164
0.105
0.333
0
0.061
0.080
0.199
0
0.080
0.177
0
0.239
0
A1
A2
A3
C1
C2
C3
P1
P2
P3
0
0.090
0.036
0.024
0.093
0.061
0.111
0.091
0.254
0
0.103
0.077
0.049
0.132
0.185
0.154
0.331
0
0.037
0.102
0.047
0.101
0.074
0.240
0
0.078
0.065
0.115
0.089
0.261
0
0.133
0.169
0.135
0.322
0
0.075
0.073
0.203
0
0.064
0.159
0
0.204
0
A1
A2
A3
C1
C2
C3
P1
P2
P3
0
0.088
0.101
0.066
0.074
0.137
0.154
0.140
0.260
0
0.068
0.096
0.030
0.118
0.160
0.120
0.229
0
0.069
0.075
0.094
0.129
0.109
0.196
0
0.089
0.103
0.117
0.121
0.220
0
0.127
0.166
0.123
0.242
0
0.059
0.052
0.128
0
0.091
0.130
0
0.139
0
B) Mugil curema
A1
A2
A3
C1
C2
C3
P1
P2
P3
C) Dicentrarchus labrax
A1
A2
A3
C1
C2
C3
P1
P2
P3
accounted for 21, 14, and 22% for M. cephalus, M.
curema, and D. labrax, respectively. There was a weak
trend apparent in PC1 of each analysis, such that more
posterior scales had higher PC1 scores than anterior.
As plots of pairs of PCs presented a relatively
incomplete picture of the overall patterns of variation,
Procrustes distances were also computed among
scales from each of the nine areas in each species.
These are shown in Table 4. As assessed by matrix
correlations and Mantel tests, the patterns of variation of shape among anatomical regions were highly
significantly correlated among species (Table 5). The
matrices 4A and 4B from the Mugil species were more
similar to each other than either was to D. labrax. In
general, distances between scales from anterior and
Table 5. Matrix correlations between the Procrustes distance matrices of Table 4. Simple Mantel test, P value in
parentheses (precision a = 0.01)
M. curema
D. labrax
M. cephalus
M. curema
0.938 (P = 0.0002)
0.866 (P = 0.0004)
0.868 (P = 0.0004)
M., Mugil; D., Dicentrarchus.
central zones were smaller than those between posterior and other zones. Area C3 was also relatively
distinctive. Therefore, there is strong evidence that
the patterns of scale shape variation are very similar
© 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 155, 834–844
VARIATIONS IN ELASMOID FISH SCALE FORM
among species, with only marginally greater similarity between the species of Mugil than between these
and Dicentrarchus. This is consistent with the observation of clustering of scales by anatomical region,
irrespective of species, in Figure 3.
DISCUSSION
This study examined which anatomical region possesses scales that best discriminate among species,
thus extending an earlier study (Ibañez et al., 2007).
Further, the mean pattern of scale shape variation
over the body was compared among species to assess
potential phylogenetic and functional influences.
DISCRIMINATION
BETWEEN SPECIES
In the present study, species were successfully
identified by discriminant analyses. In part, these
A
Anterior
1
Low
curvature
C
Central
841
differences in scale shape among species might be
linked to functional species-specific habits as well as
to phylogenetic relationships. These sources of variation are discussed later.
Size information was also important in the discriminant analysis results; four areas attained 100%
correct classification and results improved in other
areas, with the exception of P3, when centroid size
was factored into the model. Even when the specimens of the three species were of similar length,
differences in centroid size of the scales were found
amongst them, with the exception of those from area
P3. Thus, when using this approach to discriminate
between species and populations, it is important that
centroid size is factored into the procedure and taking
scales from area P3 (posterior lower ventral) is
avoided. The preference would be to take scales from
areas C1 and C2.
P
Posterior
more curved
extremes
a’
b’
a
b
2
c
d
c’
Angles increase
from center
to extremes
d’
3
Average
scales shape
Figure 6. Scaled body section of slices (in grey) in the different longitudinal (A, C, and P) and transversal zones (1, 2,
and 3). Angles increase from the central areas to the extremes. The lower insets show the transformations between the
overall scale consensus shape (reference) and the shapes represented by the extremes of principal component 1 (PC1)
(targets; leftmost = -ve PC1 scores; rightmost = +ve PC1 scores; see Fig. 4), which broadly reflect anterior–posterior
variation in scale shape.
© 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 155, 834–844
842
A. L. IBAÑEZ ET AL.
A bird’s-eye
view of
subcarangiform gait,
the fish is moving its tail
from side to side
Water drag with
caudal thrust (in black)
Figure 7. Specific swimming modes identified within body/caudal fin propulsion, based on the extended classification
scheme (Lindsey, 1978) proposed by Breder (1926). Reprinted from Lindsey CC. Form, function and locomotory habits in
Fish. Pages. 9 & 10, Figs 1 and 2. In: Hoar D, Randall DJ, eds. Fish Physiology. Vol. VII New York: Academic Press,
Copyright (1978), with permission from Elsevier.
PATTERNS
OF SCALE SHAPE VARIATION OVER
THE BODY
Although scales from all areas of the body performed
well in discriminating the three species, variability in
the shapes of scales was found among them. Scales
from zones A and C are similar shapes but differ from
zone P scales; zones 3 and 1 scales also exhibit some
differences in shape, but these are less pronounced.
Areas with greater shape variability appear to be less
effective in discrimination. Shape variations along the
longitudinal and transversal axes of the body seem to
be related to the curvature of the fish (Fig. 6). In the
posterior region of the fish (zone P), body surface area
decreases substantially and curvature increases. The
scale rows fit into a smaller surface area, this being
accomplished by reducing the size of the scales and
changing their shape. They become compressed along
the dorsoventral axis (equivalent to elongation along
the anterior–posterior axis), thus allowing more space
for adjacent rows of scales.
Fish scales also need to be tailored to aid locomotion and reduce drag during swimming. Figure 7
depicts the specific swimming modes identified within
body/caudal fin propulsion (BCF, after Blake, 2004),
based on the extended classification scheme proposed
by Breder (1926). According to Lindsey (1978), Mugil
species and fish from the Family Serranidae (Serranidae split into: Serranidae and Moronidae; the
latter being where D. labrax actually belongs) show
subcarangiform locomotion, where the lateral flexures
of the body muscles propel fish forwards. The more
undulatory waves a fish can exert against the surrounding water, and the faster and more exaggerated
the waves are, the more power the fish can generate
(Moyle & Cech, 2004).
The pattern of scale shape variation along the body
may also be functionally related to swimming mode.
The anterior and central area scales are relatively
wide in the dorsoventral direction and short in
anterior–posterior, which could facilitate the side-toside undulations of subcarangiform swimming. Conversely, scales from the posterior region are relatively
long anteroposteriorly, with the focus relatively more
central and with a larger area of insertion into the
epidermis to resist vortex, thrust, and water pressure
produced by caudal fin propulsion. In addition, scales
from the anterior, central, and posterior region exhibit
differences in arc angles and, as with different kinds of
architectural arches, may be adapted to different loadings (Leontovich, 1959). The latter differences affect
resistance to drag during swimming mode.
A further factor that may underlie the observed
pattern of scale shape variation over the body relates
to their development, the process of squamation.
According to Sire & Akimenko (2004), the first scales
to appear in most bony fish taxa are those of the
midline row at the level of the caudal peduncle, this
is followed by a rapid extension of squamation anteriorly and posteriorly along this row, while new rows
© 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 155, 834–844
VARIATIONS IN ELASMOID FISH SCALE FORM
are added dorsally and ventrally. To explain this
squamation pattern, Sire & Arnulf (1991) suggested
that the tension transmitted to the skin during swimming could induce scale development in this region as
a means of resisting excessive bending. Fish scale
shape may be adapted to cover the different surfaces
of the body, but also to allow fish undulations in the
anterior and central areas and to resist the strains
and water drag within the peduncle caudally.
The similarity in patterns of scale shape variation
over the body among the Mugil species and D. labrax
is striking considering the marked differences in
their gross morphological body features and phylogenetic relationships. Whatever classification is used
(Johnson & Patterson, 1993; Pickett & Pawson, 1994;
Miya, Kawaguchi & Nishida, 2001; Chen et al., 2003
or Nelson, 2006), all agree on the large evolutionary
distance between the Mugiliformes and Perciformes.
As patterns of scale shape variation do not differ
greatly between the Mugil species and D. labrax,
and given the phylogenetic distance between these
two genera, these patterns may be informative with
respect to swimming mode; alternatively, they may be
plesiomorphic. Studies of additional taxa are required
to resolve this question.
In conclusion, geometric morphometric methods
applied to fish scales can provide a useful tool to
discriminate among closely related species that are
otherwise difficult to distinguish. The method is nondestructive, quick and less costly than genetic analysis, thus allowing many individuals from a population
or community to be screened.
ACKNOWLEDGEMENTS
We thank Héctor Espinosa-Pérez for his help with
taxonomy subjects.
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