Comparison of Different Otolith Shape Descriptors and Morphometrics00

ORIGINAL ARTICLE

Comparison of different otolith shape descriptors and morphometricsfor the identification of closely related species of Lutjanus spp. from thePersian Gulf

ZAHRA SADIGHZADEH1*, VICTOR M. TUSET2, TOORAJ VALINASSAB3,

MOHAMMAD R. DADPOUR4 & ANTONI LOMBARTE2

1Marine Biology Department, Faculty of Marine Science & Technology, Islamic Azad University, Tehran, Iran; 2Institut de

Ciencies del Mar (CSIC), Barcelona, Catalonia, Spain; 3Department of Resource Management, Iranian Fisheries Research

Organization (IFRO), Tehran, Iran; and 4Department of Horticultural Sciences, Faculty of Agriculture, University of Tabriz,

Tabriz, Iran

AbstractThe anatomical and morphometric (shape indices, contour descriptors and otolith weight) characterizations of sagittalotoliths were investigated in 11 species of Lutjanus spp. inhabiting the Persian Gulf. This is the first study that compares theefficiency of three different image analysis techniques for discriminating species based on the shape of the outer otolithcontour, including elliptical Fourier descriptors (EFD), fast Fourier transform (FFT) and wavelet transform (WT). Sagittalotoliths of snappers are morphologically similar with some small specific variations. The use of otolith contour based onwavelets (WT) provided the best results in comparison with the two other methods based on Fourier descriptors, but onlythe combination of the all three methods (EFD, FFT and WT) was useful to obtain a robust classification of species. Thespecies prediction improved when otolith weight was included. In relation to the shape indices, only the aspect ratioprovided a clear grouping of species.

Key words: Otolith, morphology, Fourier, wavelets, Lutjanidae, Persian Gulf

Introduction

The Persian Gulf is a semi-enclosed water body

connected to the Oman Sea through the strait of

Hormuz, which is 56 km wide at its narrowest point

and has an average depth of 35 m (Reynolds 1993).

The Oman Sea has an average depth of 700 m and is

connected to the Indian Ocean through the Arabian

Sea (Valinassab et al. 2006). Both are subtropical

water masses located chiefly between 24�308N and

49�628E. The dominant large-scale current is a

counter-clockwise movement, whereby less saline

and less dense water enters at the strait of Hormuz

at the surface and more saline and denser water leaves

the area at the bottom (Hunter 1983; Reynolds

1993). After oil, fisheries represent the second most

important natural resource, and the most important

renewable natural resource in the region (Carpenter

et al. 1997). A total of 12 species of snappers have

been identified along the Iranian coast of the Persian

Gulf and the Oman Sea, including Lutjanus johnii

(Bloch, 1792) and Lutjanus malabaricus (Bloch &

Schneider, 1801), the most abundant species (Vali-

nassab et al. 2006, 2010). They play an important role

in the ecology system of the reefs, mangrove swamps

and seagrass beds (Aiken 1993; Appeldoorn &

Meyers 1993; Baisre 1993; Claro et al. 2001).

However, the biological and ecological knowledge of

snappers of the area is scarce and is mainly focused on

Lutjanus johnii (Valinassab 2006, 2010).

Sharks and other large fishes are probably their

main predators, but due to the lack of adequate

morphological knowledge of their sagittal otoliths it

was not possible to identify them in the stomach

content where they represent the main remnants of

*Correspondence: Zahra Sadighzadeh, Marine Biology Department, Faculty of Marine Science & Technology, Islamic Azad University,

Tehran, 1477893855, Iran. E-mail: [email protected]

Published in collaboration with the University of Bergen and the Institute of Marine Research, Norway, and the Marine Biological Laboratory,

University of Copenhagen, Denmark

Marine Biology Research, 2012; 8: 802�814

(Accepted 5 April 2012; Published online 14 August 2012; Printed 24 August 2012)

ISSN 1745-1000 print/ISSN 1745-1019 online # 2012 Taylor & Francis

http://dx.doi.org/10.1080/17451000.2012.692163

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http://dx.doi.org/10.1080/17451000.2012.692163

the fish prey (Harkonen 1986; Smale et al. 1995;

Volpedo & Echeverrıa 2000; Assis 2003; Campana

2004; Tuset et al. 2008).

The otolith is an acellular concretion compound,

mainly of calcium carbonate, crystallized in aragonite

and other inorganic salts, which develop over a

protein matrix (Carlstrom 1963; Blacker 1969; De-

gens et al. 1969; Cermeno et al. 2006). They are

located in the inner ear of vertebrates in close

association with the sensitive maculae of the labyr-

inthine compartments (Cordier & Dalcq 1954;

Weichert & Prech 1981; Hildebrand 1988; Jobling

1995). The otolith shape has a high degree of inter-

specific variation, which can be used to identify the

species (Nolf 1985; Harkonen 1986; Smale et al.

1995; Volpedo & Echeverrıa 2000; Assis 2003;

Campana 2004; Tuset et al. 2008). Several methods

such as Fourier analysis, wavelets and curvature scale

space analysis have been used for automatic identifi-

cation of species (Parisi-Baradad et al. 2005; Piera

et al. 2005; Martı-Puig et al. 2010; Capoccioni et al.

2011; Tuset et al. in press). Our study intends to

represent a useful method to recognize snapper species

in the stomach content of their predators using

otoliths. Therefore, the aims of this article are (i) to

characterize morphologically and morphometrically

the sagittal otoliths of snappers of Lutjanus spp. of the

Persian Gulf and (ii) to test and compare three

different methods (elliptic fourier descriptors, fast

Fourier transform and wavelet transform) to discrimi-

nate species using otolith contour and otolith weight.

Materials and methods

Sampling

Eleven species of snappers of the genus Lutjanus were

collected from the Strait of Hormuz (Figure 1)

with the help of local fisheries. These included

Lutjanus argentimaculatus (Forsskal, 1775) (n�13),

Lutjanus ehrenbergii (Peters, 1869) (n�61), Lutjanus

Figure 1. Map of the Persian Gulf (NE Indian Ocean) showing the area from where Lutjanus spp. were collected.

Identification of snappers using otoliths 803

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erythropterus Bloch, 1790 (n�9), Lutjanus

fulviflamma (Forsskal, 1775) (n�11), Lutjanus johnii

(n�93), Lutjanus lemniscatus (Valenciennes, 1828)

(n�23), Lutjanus lutjanus Bloch, 1790 (n�23),

Lutjanus malabaricus (n�47), Lutjanus rivulatus

(Cuvier, 1828) (n�12) and Lutjanus russellii

(Bleeker, 1849) (n �32). Total fish length (TL in

cm) was measured for all individuals. Their otoliths

were removed, washed, dried and stored in plastic

vials. They were also weighed (OW) to the nearest 0.01

g. Due to lack of sufficient specimens of Lutjanus

bengalensis (Bloch, 1790), this species was omitted

from the mathematical analysis.

Morphometry and morphology of otolith sagittae

Otoliths from the left side of the fish were orientated

with the inner side (sulcus acusticus) upwards and

rostrum to the right for digitizing using a microscope

attached to an image analyser with a magnification

depending on the size of the otolith. All images were

captured with an embedded 1-mm scale which was

used to avoid magnification effects in the morpho-

metric calculations. Otolith length (OL in mm),

height (OH in mm), area (OA in mm2) and perimeter

(OP in mm) (Figure 2) were measured using Image-

Pro Plus version 4.1.0 software (Media Cybernetics

Inc.). Shape indices were obtained by combining size

parameters (Russ 1990; Tuset et al. 2003): aspect

ratio (OH/OL), compactness (OP2/OA) and rectan-

gularity (OA/(OL*OH)), applying an ANOVA fol-

lowed by Student Newman�Keuls test for multiple

comparisons of means at a 5% significance level

(PB0.05). Descriptive statistics of fish and otolith

variables by species are given in Table I. The otolith

descriptions follow Tuset et al. (2008).

Elliptical Fourier descriptors (EFD)

The otolith outline was extracted by using the

Shape program (Iwata & Ukai 2002). The software

generates 20 harmonics, using elliptical Fourier

descriptors (EFD), whose combinations allow

reconstructing of the otolith contour (Kuhl &

Giardina 1982; Tracey et al. 2006; Farias et al.

2009). Each harmonic was composed of four coeffi-

cients and therefore 80 coefficients were obtained for

each individual. The Shape package automatically

normalizes the contour in relation to the first

harmonic and consequently they become invariant

to size, rotation and starting point, which causes the

degeneration of the three first coefficients to fixed

values: a1�1, b1�c1�0 (Kuhl & Giardina 1982;

Iwata & Ukai 2002). For this reason, each otolith

contour was drawn by only 77 coefficients. The first

nine harmonics (FDs 4�12) were used to rebuild the

outline attaining more than 90% of the shape

variation. The minimum number of harmonics is

assembled by plotting the percentage of accumulated

variance explained by the nth harmonic vs. the

harmonic number, n (Stransky et al. 2008).

Fast Fourier transform (FFT)

The otolith silhouette was traced in a counter

clockwise direction and digitized into 512 x�y

equidistant coordinates by using the tip of the otolith

rostrum as a common starting point for the coordi-

nates (Age & Shape Software, Infaimon SL, Spain)

of the software Image Pro Plus. A fast Fourier

transform (FFT) was calculated as a Cartesian

FFT. The Cartesian FFT uses the x�y coordinates

as complex numbers (a� ib), where a is the real

component and ib the imaginary component, repre-

senting the amplitudes of the cosine and sine waves,

Figure 2. Mesial surface of sagittal otoliths of Lutjanus spp. illustrating features considered.

804 Z. Sagighzadeh et al.

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respectiv

ely(P

ieraet

al.

2005).

The

resulta

nt

512

set

of

com

plex

nu

mbers

or

descrip

tors

were

subse-

qu

ently

norm

alized

for

differen

cesin

oto

lithpositio

n

by

setting

the

0th

descrip

tor

to0,

an

dfo

rsize

an

d

rota

tion

of

the

oto

lithby

div

idin

gall

the

descrip

tors

with

the

firstd

escripto

r(S

mith

1992;

Berg

eniu

s

etal.

2005).

The

norm

alized

descrip

tors

(a?�ib?)

were

used

toca

lcula

teth

eabso

lute

valu

e(h

arm

on

ic)

of

each

descrip

tor

(Christo

pher

&W

aters

1974):

Horm

onic¼

ffiffiffiffiffia0n

p2þ

ib0

ðÞ

2n

The

nu

mber

of

Fou

rierd

escripto

rsreq

uired

was

determ

ined

when

accu

mu

lated

varia

nce

expla

ined

at

least

90%

.T

herefo

re,it

was

necessa

ryto

captu

reth

e

first133

descrip

tors.

Beca

use

the

Cartesia

nd

escrip-

tors

are

asy

mm

etrical

aro

un

dth

em

idd

lefreq

uen

cy,

both

end

softh

earra

yare

requ

iredin

the

recon

struc-

tion

.C

on

sequ

ently,

oto

lithou

tline

shape

was

recon

-

structed

by

usin

gth

efirst

two

an

dla

sttw

o

descrip

tors,

the

firstth

reean

dla

stth

reed

escripto

rs,

an

dso

on

un

tilth

efirst

an

dla

st133

descrip

tors

were

used

(Berg

eniu

set

al.

2005).

Wavelet

transform

(WT

)

The

WT

isbased

on

expan

din

gth

eco

nto

ur

into

a

fam

ilyof

fun

ction

sobta

ined

as

the

dila

tion

san

d

tran

slatio

ns

of

au

niq

ue

fun

ction

kn

ow

nas

am

oth

er

wav

elet(M

alla

t1991).

These

fun

ction

sd

escribe

both

insp

ace

an

dw

ave

nu

mber,

the

most

pro

min

ent

featu

resof

the

curv

e.T

he

sign

als

of

wav

eletshave

differen

tam

plitu

des,

hen

cesm

all

(low

)w

aven

um

-

bers

(frequ

encies)

are

asso

ciated

with

asm

ooth

ly

vary

ing

con

tou

r,w

hile

larg

ew

aven

um

bers

are

asso

-

ciated

with

varia

tion

on

asm

all

spatia

lsca

le(P

arisi-

Bara

dad

etal.

2005,

2010).

To

obta

inth

eoto

lith

con

tou

r,a

tota

lof

512

Cartesia

nco

ord

inates

on

each

of

the

orth

ogon

al

pro

jection

s,w

hich

isa

perp

end

icula

rim

age

of

an

object

(Sch

warzh

an

s

1980;N

olf

1985),

were

extra

ctedu

sing

Age

&S

hape

pro

gra

m(In

faim

on

SL

,S

pain

)so

ftware

Image

Pro

Plu

s.T

he

wav

eletsfo

ur,

five

an

dsix

were

selectedas

the

represen

tativ

esof

the

oto

lithco

nto

ur.

Sta

tistical

analy

ses

Norm

ality

of

varia

bles

an

dhom

ogen

eityof

varia

nces

for

each

EF

Dco

efficient,

FF

Tharm

on

icor

WT

poin

t,w

ereex

am

ined

by

usin

gK

olm

ogoro

v�S

mirn

ov’s

and

Leven

e’stests,

respectively.

Data

were

transfo

rmed

usin

g1/x

or

log

10 ,

when

the

variables

did

not

meet

the

assum

ptio

ns.

Inth

ecase

of

the

WT

,

the

num

ber

ofvariab

lesw

asso

hig

hth

atth

ose

who

did

not

meet

the

assum

ptio

ns

were

elimin

ated.A

nalysis

of

covarian

ce(A

NC

OV

A)

test(P

B0.0

5)

was

perfo

rmed

Table I. Descriptive statistics of fish and otolith variables for Lutjanids from Persian Gulf. Larg, Lutjanus argentimaculatus; Lehr, L. ehrenbergii; Lery, L. erythropterus; Lful, L. fulviflamma; Ljoh, L.

johnii; Llem, L. lemniscatus; Llut, L. lutjanus; Lmal, L. malabaricus; Lriv, L. rivulatus; Lrus, L. russellii; letters indicate groups from SNK test.

Larg Lehr Lery Lful Ljoh Llem Llutj Lmal Lriv Lrus(n�13) (n�61) (n�9) (n�11) (n�93) (n�23) (n�23) (n�47) (n�12) (n�32)

Fish length min�max 423�802 146�260 316�523 176�260 167�754 298�514 153�232 235�732 405�667 150�372mean9sd 648.2999.5 203.1922.5 370.7961.7 206.3927.9 364.09116.0 379.89 61.7 195.7919.7 317.6985.9 484.9984.0 250.8954.4

Area min �max 67.83�174.66 18.15�40.12 61.57�113.06 22.11�36.70 30.27�313.09 44.49�92.36 19.5�37.35 39.39�359.45 98.77�175.65 15.54�58.73mean9sd 123.66931.62 29.5695.16 74.52915.59 27.6795.21 98.13947.59 63.44914.68 29.4495.31 86.33951.00 119.64923.44 34.60911.18

Height min �max 7.40�12.53 3.79�5.68 7.67�10.02 4.27�5.51 5.10�15.46 5.87�8.73 3.93�5.54 5.94�17.31 9.34�12.51 3.46�6.99mean9sd 10.4591.62 4.7790.44 8.3990.71 4.7390.50 8.6991.99 7.0690.88 4.8390.44 8.8691.88 10.4191.01 5.1490.88

Length min �max 12.74�20.49 6.54�10.42 11.68�16.32 7.27�9.82 8.36�28.83 10.24�15.55 6.83�9.82 9.23�30.16 14.55�19.48 6.50�12.50mean9sd 16.9892.42 8.6390.83 12.8791.40 8.1990.84 15.1193.84 12.7891.50 8.5290.86 13.3293.34 15.9891.49 9.6191.66

Perimeter min �max 37.50�61.62 18.89�29.24 34.10�46.53 20.52�26.52 24.10�92.74 29.15�46.67 19.37�28.45 25.95�86.19 42.86�58.28 18.93�33.60mean9sd 52.2697.51 24.6692.34 37.2293.82 23.3592.35 43.27911.37 35.6294.68 24.4792.62 39.82910.07 48.4794.43 26.7194.24

Weight min �max 0.16�0.83 0.03�0.11 0.15�0.38 0.04�0.11 0.05�2.20 0.10�0.40 0.04� 0.11 0.10�2.45 0.33�0.86 0.02�0.16mean9sd 0.4790.22 0.0690.02 0.2190.07 0.0790.03 0.3490.29 0.1890.08 0.0790.02 0.2990.36 0.4590.17 0.0790.03

Aspect ratio min �max 0.55�0.69 0.51�0.61 0.61�0.68 0.53�0.64 0.53�0.66 0.51�0.62 0.54�0.60 0.57�0.72 0.63�0.68 0.47�0.58mean9sd 0.6290.05a 0.5590.02b 0.6590.02d 0.5890.03c 0.5890.03c 0.5590.03b 0.5790.02bc 0.6790.03d 0.6590.02d 0.5490.02e

Compactness min �max 20.10�25.10 18.66�25.74 17.96�19.17 18.68�21.70 17.10�27.47 18.42�24.7 18.01�22.89 16.67�26.87 18.17�23.23 19.22�24.42mean9sd 22.4591.59a 20.7591.39bc 18.7490.46e 19.8490.83cde 20.0791.75bcde 20.2291.40bcd 20.4991.17bcd 19.2391.92de 19.8591.57cde 21.3491.20b

Rectangularity min �max 0.64�0.72 0.68�0.74 0.66�0.70 0.68�0.73 0.68�0.73 0.67�0.73 0.69�0.73 0.67�0.73 0.68�0.73 0.66�0.71mean9sd 0.6990.02ab 0.7190.01c 0.6890.01a 0.7190.02c 0.7190.01c 0.7090.02b 0.7190.01c 0.7090.01b 0.7190.01c 0.6890.01a

Iden

tification

ofsn

appers

usin

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to determine the effect of species (the independent

variable) and fish length (the covariate) on EFD

descriptors. ‘Species’ was considered as the main

factor and ‘fish length’ as the covariate. When a

significant regression coefficient was detected and

homogeneity was observed among groups, then the

effect of fish length (TL) could be removed from

each measurement using this relationship:

Oij; adj ¼ Oij þ b � TLij � MTLj

� �;

where Oij, adj�otolith morphological measurement

of ith fish adjusted to mean fish length of group j;

Oij�original otolith morphological measurement for

ith fish from group j; b �slope of the relationship Oij;

TLij, common to all groups; TLij�fish length of ith

fish in group j; and MTLj�average fish length within

group j. If slopes differed among groups, the correc-

tion for TL was made separately for each group using

the above equation by replacing the common slope

(b) with the group-specific slope (bj). These correc-

tions were effective for scaling all morphological

variables of all otoliths to their predicted TL group

mean (Campana & Casselman 1993; Bolles & Begg

2000; Begg et al. 2001; DeVries et al. 2002;

Bergenius et al. 2005).

Otolith length was normalized to avoid allometric

effects of this parameter in the otolith weight, taking

into account the allometric relationship. A standar-

dized fish length of 22.0 cm was used as the

reference for all species (Lombarte & Lleonart

1993; Lleonart et al. 2000; Tuset et al. 2006).

Multivariate analysis of variance (MANOVA) was

used to test the hypothesis of no difference in otolith

shape between species. A canonical discriminant

function analysis (DFA) was also carried out to verify

the differences between species using the above-

mentioned variables. In the first stage a single-factor

ANOVA was carried out to determine which variables

discriminate among species to rank the potential

predictors. For the second stage, multicollinearity

was avoided in the DFA analysis by obtaining a

matrix correlation and then, eliminating the variables

with a high correlation (r�0.5) and small F-score

from ANOVA. The hypothesis that the between-

group covariances are equal was tested for all models.

The matrices were not homogeneous and the indivi-

dual within-group matrices were used, thus a quad-

ratic discriminant function was computed (Friedland

et al. 1994; Tuset et al. 2006). The classification

accuracy of each DFA was evaluated by leave-one-out

cross-validation (Nishimoto et al. 2010).

Results

Anatomical description

Morphologically, the sagittal otoliths of Lutjanus

spp. are similar with small specific variations

(Figures 3�5). For example, the otolith shape could

be pentagonal (L. argentimaculatus, L. erythropterus,

L. fulviflamma and L. russellii), elliptical

(L. bengalensis, L. ehrenbergii, L. lemniscatus) or could

change from pentagonal to elliptical (L. erythropterus,

L. johnii, L. malabaricus and L. rivulatus) or vice

versa (L. lutjanus).

In all species, the sulcus acusticus is heterosulcoid,

ostial with median position. The ostium is typically

funnel-like, except for L. bengalensis (rectangular),

L. johniiandL. malabaricus (funnel-like to rectangular).

It can be shorter than the cauda (L. argentimaculatus,

L. bengalensis, L. ehrenbergii, L. erythropterus,

L. fulviflamma and L. lutjanus), or approximately as

long as the cauda (L. johnii, L. lemniscatus,

L. malabaricus, L. rivulatus and L. russellii). The cauda

is tubular ending close to the posterior ventral margin.

The species L. malabaricus, L. johnii and

L. lutjanus show a cauda that is slightly curved, while

in the remaining species it is strongly or markedly

flexed.

The anterior margin noticeably varies and can

change with ageing: round in L. rivulatus, round-

angled in L. malabaricus, blunt to peaked in L.

ehrenbergii, peaked in L. lutjanus and L. lemniscatus,

peaked to angled in L. argentimaculatus, peaked to

round in L. erythropterus, L. russellii and angled in L.

bengalensis, L. fulviflamma and L. johnii.

The rostrum is short and broad in all species,

although the tip differs between and within species:

blunt (L. bengalensis, L. ehrenbergii, L. malabaricus and

L. russellii), pointed (L. ehrenbergii, L. erythropterus,

L. johnii, L. lemniscatus and L. lutjanus) round

(L. argentimaculatus, L. erythropterus, L. rivulatus and

L. russellii), oblique (L. fulviflamma) or angled

(L. johnii); with an antirostrum poorly defined or small,

broad and pointed; while the excisura can be wide

without or with a deep and acute notch. Finally, the

posterior region is oblique in most of species but

angled in L. johnii, L. lutjanus and L. malabaricus.

Shape indices

The three shape indices (aspect ratio, compactness and

rectangularity) showed significant differences among

groups of species. The aspect ratio was the index most

variable showing higher mean values in Lutjanus

argentimaculatus, L. erythropterus, L. malabaricus and

L. rivulatus and lowest in L. russellii. By contrast, the

compactness and rectangularity was less apparent for

the groups (Table I, Figure 6).


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Figure 3. Sagittal otoliths of Lutjanus spp. from the Persian Gulf. A, L. argentimaculatus (42.3�63.2�80.2 cm TL); B, L. bengalensis

(21 cm TL); C, L. ehrenbergii (14.6�20.3�26 cm TL); D, L. erythropterus (31.6�38.7�52.3 cm TL). Scale bars �1 mm.


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Figure 4. Sagittal otoliths of Lutjanus spp. from the Persian Gulf. A, L. fulviflamma (17.6�21.4�26 cm TL); B, L. johnii (16.7�46�75.4 cm

TL); C, L. lemniscatus (29.8�40.5�51.4 cm TL); D, L. lutjanus (15.3�19.1�23.2 cm TL). Scale bars �1 mm.


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Figure 5. Sagittal otoliths of Lutjanus spp. from the Persian Gulf. A, L. malabaricus (23.5�45.9�73.2 cm TL); B, L. rivulatus (40.5�53.7�66.7 cm TL); C, L. russellii (15�25.9�37.2 cm TL). Scale bars �1 mm.


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Otolith weight and contour

For the three methods applied (EFD, FFT and WT)

to characterize the otolith contour, the number of

coefficients implied in the mathematical analyses were

very low. In the case of EFD, the shape variability was

fulfilled only with the first 9 coefficients, while a total

of 53 of 1024 FFT harmonics meet the criteria

adequately. Finally, only 8 of 1536 wavelets were

used, of which most corresponded to the wavelet

number four because wavelets five and six were

characterized by a high variability among species

and fish length. However, the otolith weight was the

most important factor for species discrimination

(ANOVA F �113.21, P B0.001).

The FFT was the weakest method for species

discrimination, with a classification success of 47.8%

of cases (Table II). Only the otoliths of Lutjanus

argentimaculatus and L. lemniscatus were identified

above 70%, while L. fluviflamma, L. johnii, L. lutjanus,

L. malabaricus and L. rivulatus were assigned below

40%. The EFD and WT noticeably improved the

identification of the most species increasing the total

percentage to 57.5% and 65.5%, respectively

(Table II); however, it was not the same in L.

lemniscatus, L. erythropterus and L. ehrenbergii. Finally,

the joint application of the three methods allowed a

classification success of 77.6% to be reached. In this

case, the percentage of classification was above 70%,

except for L. fulviflammawhere it was 36.4% (Table II).

Discussion

Several different methods were tested in the statis-

tical DFA cross-validation procedures to determine

otolith shape identification of species. The results of

the morphological study indicate that otoliths of

snappers from the Persian Gulf are very similar in

morphological terms (shape, type of sulcus acusti-

cus, ostium and cauda), but do show differences in

the anterior and posterior rims of the otolith. Up to

now, only Rivaton & Bourret (1999) had provided

images of otoliths of some species of snappers

(Lutjanus argentimaculatus, L. fulviflamma, L. lutjanus

and L. russellii) from the Indian Ocean. Finally,

although the analysis of the otolith outline revealed a

high variability in the most species, only the combi-

nation of all methods provided strong results. The

ability to distinguish between otoliths of these

species is an important finding since species identi-

fication has proven difficult when these species co-

occur in the stomach contents of predators.

The advantage of this multiscale analysis (WT) is

that it enables us to identify single morphological

points (landmarks) located on the x-axis along the

contour where the rostrum is the origin of the

contour (Parisi-Baradad et al. 2005; Piera et al.

2005; Lombarte et al. 2006). The differences

observed in the ventral margin between rostrum

and post-rostrum and did not depend on the fish

length. On the contrary, EFD and FFT only give a

global approximation of outline variability (Reig-

Bolanos et al. 2010). However, EFD does not

require equal intervals along the outline and there-

fore can accommodate significantly more complex

shapes than polar Fourier functions, which describe

and characterize outlines better (e.g. Kuhl &

Giardina 1982; Lestrel 1997; Stransky & MacLellan

2005; Tracey et al. 2006; Stransky et al. 2008).

Notwithstanding, Marti-Puig et al. (2010) asserted

that although EFD can represent any contour when

Figure 6. Box plots for the shape indices (aspect ratio, compact-

ness and rectangularity) by Lutjanus spp. from the Persian Gulf.

(see Table 1 for abbreviation explanations).


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a large number of coefficients are used, but in

practice the application of the number of descriptors

is limited to a certain low value (e.g. Parisi-Bardad

et al. 2005; Tracey et al. 2006; Burke et al. 2008;

present study) representing an approximation to the

original silhouette to a lesser degree than other

analyses. This becomes obvious in the presence of

a close similarity between species. Our results

support the hypothesis that Fourier transcription

methods are more efficient when discriminating

between groups or stocks of fish, but are not when

the aim is to identify and classify closer species.

However, the statistical results of the study showed

that combinations of these methods could be very

useful to discriminate species.

Otolith shape is affected by ecological, ontogenetic,

environmental and genetic factors (Morales-Nin

1987; Castonguay et al. 1991; Gago 1993; Friedland

& Reddin 1994; Lombarte et al. 2003; Cadrin &

Friedland 2005). In this framework, juvenile and

subadult fishes of many snappers of the Persian Gulf

and the Oman Sea exhibit a high grade of adaptability

Table II. Results of cross-validation using leave-one-out method for classifying Lutjanus spp. from the Persian Gulf. EFD, elliptical Fourier

descriptors; FFT, fast Fourier transform; WT, wavelets.

Predicted group membership (percentage)

Actual group Larg Lehr Lery Lful Ljoh Llem Llut Lmal Lriv Lrus

EFD�otolith weight

L. argentimaculatus (Larg) 92.3 7.7

L. ehrenbergii (Lehr) 55.7 6.6 24.6 1.6 3.3 1.6 6.6

L. erythropterus (Lery) 44.4 22.2 22.2 11.1

L. fulviflamma (Lful) 18.2 45.5 9.1 27.3

L. johnii (Ljoh) 9.8 55.4 10.9 19.6 2.2 2.2

L. lemniscatus (Llem) 8.7 4.3 56.5 4.3 26.1

L. lutjanus (Llut) 21.7 4.3 56.5 13.0 4.3

L. malabaricus (Lmal) 8.5 2.1 25.5 6.4 46.8 6.4 4.3

L. rivulatus (Lriv) 8.3 16.7 8.3 66.7

L. russellii (Lrus) 3.2 22.6 74.2

FFT�otolith weight


L. ehrenbergii (Lehr) 60.7 3.3 16.4 1.6 8.2 1.6 4.9 3.3

L. erythropterus (Lery) 11.1 66.7 11.1 11.1

L. fulviflamma (Lful) 36.4 9.1 36.4 9.1 9.1

L. johnii (Ljoh) 1.1 5.4 6.5 37.0 8.7 28.3 12.0 1.1

L. lemniscatus (Llem) 4.3 73.9 4.3 17.4

L. lutjanus (Llut) 26.1 26.1 17.4 30.4

L. malabaricus (Lmal) 2.1 4.3 4.3 27.7 2.1 34.0 23.4 2.1

L. rivulatus (Lriv) 8.3 16.7 41.7 25.0 8.3


WT�otolith weight

L. argentimaculatus (Larg) 100.0

L. ehrenbergii (Lehr) 47.5 3.3 26.2 8.2 3.3 3.3 3.3 3.3 1.6

L. erythropterus (Lery) 55.6 11.1 11.1 11.1 11.1

L. fulviflamma (Lful) 18.2 9.1 45.5 9.1 18.2

L. johnii (Ljoh) 2.2 4.3 81.5 2.2 5.4 3.3 1.1

L. lemniscatus (Llem) 8.7 4.3 4.3 65.2 17.4

L. lutjanus (Llut) 13.0 4.3 4.3 4.3 47.8 13.0 13.0

L. malabaricus (Lmal) 6.4 10.6 10.6 59.6 8.5 4.3

L. rivulatus (Lriv) 8.3 8.3 16.7 66.7

L. russellii (Lrus) 3.2 3.2 3.2 19.4 71.0

EFD�FFT�WT�otolith weight


L. ehrenbergii (Lehr) 75.4 11.5 1.6 9.8 1.6

L. erythropterus (Lery) 77.8 11.1 11.1

L. fulviflamma (Lful) 36.4 36.4 18.2 9.1

L. johnii (Ljoh) 2.2 1.1 81.5 2.2 10.9 2.2

L. lemniscatus (Llem) 4.3 82.6 13.0

L. lutjanus (Llut) 13.0 4.3 78.3 4.3

L. malabaricus (Lmal) 4.3 12.8 6.4 70.2 2.1 4.3

L. rivulatus (Lriv) 8.3 8.3 83.3



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to different environments such as mangroves, sea-

grass beds, freshwater streams or brackish water.

They migrate to rocky environments or coral reefs

when they are adults and then take up permanent

residence there (Druzhinin 1970; Cervigon 1993;

Cocheret et al. 2003). These species differ in beha-

viour (nocturnal or diurnal), coloration patterns on

body, habitat and sociality (solitary or groups)

influencing their behavior and intra- and inter-

specific communications (Lewis & Pring 1986;

Sainsbury 1987; Williams & Russ 1992; Sommer

et al. 1996; Kailola et al. 1993; Lieske & Myers 1994;

Kuiter & Tonozuka 2001). In fact, the anatomical

affinity � narrower otoliths and deeper notch of

excisura ostti between rostrum and antirostrum of

the otolith of Lutjanus ehrenbergii, L. fulviflamma and

L. lutjanus � is reasonable taking into account that

these species inhabit coastal environments and have a

similar coloration and body shape, which may be

interpreted as a common phylogenetic origin where

L. fulviflamma might be the ancestral species.

Our study is the first investigation that compares

actual data with related mathematical protocols by

several methods and provides results of a high degree

of reliability. At this point, we would like to comment

on the phenomenon of multicollinearity among

variables. Elimination of these variables did not

significantly increase the percentage of classification.

It is true that the number of wavelets used in the

discriminant analysis was low, but that was due to the

phenomenon of multicollinearity among the closer

wavelets. Moreover, our study demonstrates that the

variance homogeneity among species is smaller in

wavelets with a low frequency, which show more

details of the otolith profile, which we consider a

relevant result for future studies using wavelets.

Finally, several studies have shown that otolith

weight is a more powerful discriminator and has less

variation than Fourier descriptors (Forsberg & Neal

1993; Tuset et al. 2006). Our results support these

findings and reinforce the fact that future research

should be focused on developing three-dimensional

techniques to help researchers in the proper identi-

fication of species.

Acknowledgements

This work has been supported by the MICIN

CTM2010-19701 (AFORO3D project). The anon-

ymous reviewers provided many helpful comments

on both the structure and analysis of an earlier

version of the report. Their comments resulted in a

much improved manuscript and their assistance is

appreciated. Dr Victor Tuset is worker of CSIC

within the modality ‘JAE-Postdoc’ of Programme

‘Junta para la Ampliacion de Estudios’ co-funded by

the European Social Foundation.

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Comparison of Different Otolith Shape Descriptors and Morphometrics00

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