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An approach to unraveling the coexistence of snappers (Lutjanidae) using otolith morphology Zahra Sadighzadeh¹, Jose Luís Otero-Ferrer², Antoni Lombarte³, Mohammad R. Fatemi¹, Víctor Manuel Tuset³ ¹Marine Biology Department, Graduate school of Marine Science and Technology, Science and Research Branch, Islamic Azad University, Tehran, Iran. E-mail: zahrasadighzadeh@yahoo.com²Universidade de Vigo, Departamento de Ecología y Biología Animal, Vigo, Galicia, Spain.³Institut de Ciéncies del Mar (CSIC), Passeig Marítim 37-49, 08003, Barcelona, Catalonia, Spain. Summary: The sagittae otolith morphology of marine fishes has been used in many ecomorphological studies to explain certain ecological adaptations of species to habitat. Our study compares the sagittal otolith shapes of ten species of snappers (Family Lutjanidae) inhabiting the Persian Gulf. We used a morphometric analysis of the otolith measurements (length, height, perimeter, area and weight) and of the ratio between the area of the sulcus acusticus and the area of the otolith (S:O). The otolith contour was also analysed using wavelets as a mathematical descriptor. Morphological variations in the otoliths were associated with the morphology and external colouration of snappers as well as ecological traits. An analysis of the interspecific S:O ratio suggested that the highest ratios occurred in snappers inhabiting shallower waters. A categorical multivariate analysis, including morphological, ecological and otolith size factors, showed that the species adapted to dim light conditions had a greater otolith perimeter. An analysis of variance of the otolith contour revealed zones with a higher interspecific variability, although only the antero-dorsal zone showed differing patterns. Although the otolith patterns appear to have a phylogenetic component, they might also be related to diel activity rhythms or to the light conditions in the habitat. The results of the study showed that variation in otolith morphology can be used to explain the coexistence of sympatric species. Keywords: otolith; morphology; biodiversity; functional ecology; snappers; Lutjanidae. Una aproximación a la comprensión de la coexistencia de pargos (Lutjanidae) a partir de la morfología del otolito Resumen: La morfología del otolito sagitta de peces marinos se ha empleado en estudios de ecomorfología al objeto de explicar las adaptaciones ecológicas de las especies al hábitat. Nuestro estudio compara la forma del otolito de diez especies de pargos (familia Lutjanidae) del Golfo Pérsico. El análisis morfológico se realizó a partir de medidas del otolito (longitud, anchura, perímetro, área y peso) y la proporción entre el área del sulcus acusticus y del otolito (S:O). También se analizaron los contornos de los otolitos mediante descriptores matemáticos denominados wavelets. Las variaciones morfológicas en los otolitos se asociaron a la morfología y la coloración externa de los pargos, así como a diversos caracteres ecológicos. Las especies con valores más elevados en la proporción S:O habitan en aguas someras. El análisis multivariante categórico de factores, ecológicos y morfológicos del otolito (forma y tamaño), puso de manifiesto que las especies adaptadas a condiciones tenues de luz presentan el perímetro del otolito más grande. El análisis de varianza del contorno del otolito reveló la presencia de zonas con gran variabilidad inter-específica, si bien solo la parte antero-dorsal permitió distinguir patrones claros de variación. Aunque dichos patrones parecen tener un componente filogenético, también estarían relacionados con el ritmo de actividad diaria o las condiciones de luminosidad en las que viven las especies. Los resultados del este estudio demuestran que la variación morfológica del otolito puede ser usada para explicar la coexistencia de especies simpátricas. Palabras clave: otolito; morfología; biodiversidad; ecología funcional; pargos; Lutjanidae. Citation/Como citar este artículo: Sadighzadeh Z., Otero-Ferrer J.L., Lombarte A., Fatemi M.R., Tuset V.M. 2014. An approach to unraveling the coexistence of snappers (Lutjanidae) using otolith morphology. Sci. Mar. 78(3): 000-000. doi: http://dx.doi.org/10.3989/scimar.03982.16C Editor: E. Massutí. Received: November 6, 2013. Accepted: April 29, 2014. Published: July 16, 2014. Copyright: © 2014 CSIC. This is an open-access article distributed under the Creative Commons Attribution-Non Commercial Lisence (by-nc) Spain 3.0. Contents

Summary Resumen Introduction Materials and methods Results Discussion Acknowledgements References

INTRODUCTIONTop Sensory ecology acts as the interface between processes occurring within organisms and those occurring between organisms and their environment (). Fishes have a variety of sensory receptors that enable them to glean information from their surroundings (). Among these receptors, the inner ear is associated with balance and sound detection (, ). Usually, fishes are classified as hearing generalists if they can detect sound frequencies no greater than 1 to 1.5 kHz; they are classified as hearing specialists if they can detect sound frequencies greater than 1.5 kHz (). Morphologically, the inner ear of teleostean fishes is essentially formed by three semicircular canals and otolithic organs (sacculus, utriculus and lagena), within which are located the otoliths (sagitta, lapillus and asteriscus, respectively) (, , ). The otoliths are acellular concretions of calcium carbonate and other inorganic salts developing over a protein matrix (, , ) and in close association with the sensorial macula (, , ). The otoliths, especially the sagittae, play an important role in inner ear functions (, , ). Previous studies have indicated that the size of the sagittae is an adaptive factor associated with sensitivity to sound (, , , ). Fishes with large otoliths produce sounds and show highly developed intraspecific acoustic communication (, ). These characteristics enable them to live in coastal and deep environments where visual and light communications are less important (, ). Moreover, it has been reported that females can use the auditory sense to detect and locate vocalizing males during the breeding season and can change their hearing sensitivity depending on their reproductive status (e.g. , ). Many fishes vary morphologically among habitats. The variations depend on hydrostatic conditions, visibility, intraspecific competition, buoyancy and predation (, ). Ecomorphology tries to understand how the ecology and evolutionary processes of an organism are related to its morphology (, ). Most ecomorphological studies are focused on feeding mechanisms (, ) and locomotion patterns (, ) because these factors may play a role in shaping the patterns of abundance and habitat distribution in fishes (, ). However, this scientific discipline has also been applied in otolithology because certain characteristics of otoliths (e.g. sulcus area, depth of the sulcus, sulcus area:otolith area ratio or shape) vary according to environmental, ontogenetic, phylogenetic and ecological factors (e.g. , , , , , , , , , , ). However, it is not known how otolith shape variability affects hearing ability (, ). The snappers (Lutjanidae) are a group of circumtropical fishes comprising 23 genera and 123 species (). Twelve species of snappers have been identified along the Iranian coasts of the Persian Gulf and the Oman Sea (, ). Ecologically, snappers play an important role in near-shore systems, including mangroves, seagrass beds and freshwater streams, and in open-water habitats, inside or around reefs (, , , , ). These habitats play different roles in development and life history by serving as daytime refuges, feeding nurseries and/or nesting areas for many species, including snappers. They also offer pre-recruits and juveniles abundant food resources, less competition with adults and less predation (, , , ). Recently, demonstrated that otolith shape descriptors and morphometrics are useful for discriminating among Lutjanus species in the Persian Gulf. In this study, a novel methodology for analysing otoliths based on outline sections is developed. MATERIALS AND METHODSTop Sampling Juvenile (close to the size of first maturity, according to the literature) and adult fishes were collected with bottom traps from January 2010 to December 2011 in the Persian Gulf commercial fishery (Fig. 1). A total of ten species of snappers Lutjanus spp. were collected and measured (total length, TL in cm). The sagittal otoliths were removed, washed, dried and stored in labeled plastic vials. Otoliths from the left side of the fish were oriented with the inner side (sulcus acusticus) up and digitized using a microscope attached to an image analyser. Large otoliths were directly digitized using a digital camera (Canon 450D with 24-105 mm lens). All images included an embedded millimeter scale (Fig. 2).

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Fig. 1. – Map of the Persian Gulf (NE Indian Ocean) showing the study area where snappers were collected.

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Fig. 2. – Sagittal otoliths of each species of snapper. Scale bars: 1 mm.

Otolith morphometry The area (OA in mm²), height (OH in mm), length (OL in mm), perimeter (OP in mm) and sulcus acusticus area (related to sensory macula area) (SA in mm²) were measured using Image-Pro Plus version 4.1.0 software (Media Cybernetics, Inc.). The otolith weight (OW in mg) was also obtained and included in the analysis (Table 1). Kolmogorov–Smirnov and Levene tests were used to check normality of the data distributions and variance homogeneity, respectively. The relationships between the fish length (X) and otolith variables (Y) were estimated using the power equation Y=aX^b, which was log transformed to estimate a and b with a simple linear regression. A one-way analysis of variance (ANOVA) was applied to compare the slopes (b) among species using a post hoc Tukey test. A one-way ANOVA was used to compare the ratio between the sulcus acusticus area and otolith area (S:O) among species (, ). In all cases, variances were unequal at the 95% confidence level. Because the assumption of equal variances was rejected, Tamhane’s T2 was used as a post hoc test. The statistical analyses were performed with the SPSS statistical package (SPSS Inc. 2010).

Table 1. – Summary of descriptive statistics of fish length and otolith size of snappers from the Persian Gulf. L. argentimaculatus, Larg; L. ehrenbergii, Lehr; L. erythropterus, Lery; L. fulviflamma, Lflu; L. johnii, Ljoh; L. lemniscatus, Llem; L. lutjanus, Llut; L. malabaricus, Lmal; L. rivulatus, Lriv; L. russellii, Lrus.

Variables		Larg	Lehr	Lery	Lflu	Ljoh
Total length	min-max	423-802	146-260	316-523	176-260	167-754
Total length	mean±sd	648.2±99.5	203.1±22.5	370.7±61.7	206.27±27.9	364.0±115.9
Otolith area	min-max	67.8-174.7	18.12- 40.1	61.6-113.1	22.1-36.7	30.3-313.1
Otolith area	mean±sd	123.7±31.6	29.6±5.2	74.5±15.6	27.67±5.21	98.1±47.6
Otolith height	min-max	7.4-12.5	3.8-5.7	7.7-10.0	4.3-5.5	5.1-15.5
Otolith height	mean±sd	10.5±1.62	4.8±0.4	8.4±0.7	4.7±0.5	8.7±1.9
Otolith length	min-max	12.7-20.5	6.5-10.4	11.7-16.3	7.3-9.8	8.4-28.8
Otolith length	mean±sd	17.0±2.4	8.6±0.8	12.9±1.4	8.2±0.8	15.1±3.8
Otolith perimeter	min-max	37.5-61.6	18.9-29.2	34.1-46.5	20.5-26.5	24.1-92.7
Otolith perimeter	mean±sd	52.3±7.5	24.7±2.3	37.2±3.8	23.4±2.4	43.3±11.4
Otolith weight	min-max	0.16-0.83	0.03-0.11	0.15-0.38	0.04-0.11	0.05-2.20
Otolith weight	mean±sd	0.47±0.22	0.06±0.02	0.21±0.07	0.07±0.03	0.34±0.29
Aspect ratio	min-max	0.55-0.69	0.51-0.61	0.61-0.68	0.53-0.64	0.53-0.66
Aspect ratio	mean±sd	0.62±0.05	0.55±0.02	0.65±0.02	0.58±0.03	0.58±0.03
Number		13	61	9	11	93
Variables		Llem	Llut	Lmal	Lriv	Lrus
Total length	min-max	298-514	153-232	235-732	405-667	150-372
Total length	mean±sd	379.8±61.7	195.7±19.7	317.6±86.0	484.9±84.0	250.8±54.4
Otolith area	min-max	44.5-92.4	19.5-37.4	39.4-359.5	98.8-175.7	15.5-58.7
Otolith area	mean±sd	63.4±14.7	29.4±5.3	86.3±51.0	119.6±23.4	34.6±11.2
Otolith height	min-max	5.9-8.7	3.9-5.5	5.9-17.3	9.3-12.5	3.5-7.0
Otolith height	mean±sd	7.1±0.9	4.8±0.4	8.9±1.9	10.4±1.0	5.1±0.9
Otolith length	min-max	10.2-15.6	6.8-9.8	9.2-30.2	14.6-19.5	6.5-12.5
Otolith length	mean±sd	12.8±1.5	8.5±0.9	13.3±3.3	16.0±1.5	9.6±1.7
Otolith perimeter	min-max	29.2-46.7	19.4-28.5	25.9-86.2	42.9-58.3	18.9-33.6
Otolith perimeter	mean±sd	35.6±4.7	24.5±2.6	39.8±10.1	48.5±4.4	26.7±4.2
Otolith weight	min-max	0.10-0.40	0.04-0.11	0.10-2.45	0.33-0.86	0.02-0.16
Otolith weight	mean±sd	0.18±0.08	0.07±0.02	0.29±0.36	0.45±0.17	0.07±0.03
Aspect ratio	min-max	0.51-0.62	0.54-0.60	0.57-0.72	0.63-0.68	0.47-0.58
Aspect ratio	mean±sd	0.55±0.03	0.57±0.02	0.67±0.03	0.65±0.02	0.54±0.02
Number		23	23	47	12	32

Interaction between otolith size and environment To test the relevance of otolith size to the ecological role of snappers in the ecosystem, a multivariate analysis was performed with a categorical principal component analysis (CatPCA) (SPSS Inc. 2010). This procedure simultaneously quantified categorical variables and reduced the dimensionality of the data. A two-dimensional plot was then created to represent the morphological similarity of the categorical variables among snappers. The similarity between the variables was assessed on a nominal and numerical scale using the categories created at data collection () (Table 2).

Table 2. – Summary of ecological, functional, morphological and feeding characteristics of snappers in the Persian Gulf according to , .

Species	Environ-ment	Stage ontogenic	Habitat	Depth	Visual field	Life pattern	Feeding habits	Colouration and visual contrasting marks
L. argentimaculatus	Euryhaline	Juvenile	Mangroves, freshwater streams, tidal creeks	Coastal	Dim light	Groups	Fishes and crustaceans	Greenish brown on back, grading to reddish on sides and ventral parts. No spots
L. argentimaculatus	Euryhaline	Adult	Reef and mangroves	Deep	Dim light	Groups	Fishes and crustaceans
L. ehrenbergii	Euryhaline	All	Coast and freshwater stream	Coastal	Light	Groups	Fishes and invertebrates	Often with a series of four or five narrow yellow stripes on the sides below the lateral line. Spots
L. erythropterus	Marine	Juvenile	Muddy substrates	Coastal	Dim light	Groups	Fishes, crustaceans and cephalopods	No spots
L. erythropterus	Marine	Adult	Trawling grounds and reefs	Deep	Dim light	Groups	Fishes, crustaceans and cephalopods	No spots
L. fulviflamma	Euryhaline	Juvenile	Mangroves, freshwater streams, tidal creeks	Coastal	Light	Groups	Fishes, shrimps, crabs and other crustaceans	A series of six or seven horizontal yellow stripes runs on the side, mainly below the lateral line. Spots
L. fulviflamma	Euryhaline	Adult	Reef	Coastal	Light	Groups	Fishes, shrimps, crabs and other crustaceans
L. johnii	Euryhaline	Juvenile	Mangroves	Coastal	Light	Groups	Fishes, shrimps, crabs and cephalopods	Generally yellow with a bronze to silvery sheen. A large black spot
L. johnii	Euryhaline	Adult	Reef	Deep	Light	Groups	Fishes, shrimps, crabs and cephalopods
L. lemniscatus	Marine	Adult	Offshore reef and muddy habits	Deep	Dim light	Solitary	Fishes and invertebrates	Gray-brown or olive. No spots
L. lutjanus	Marine	Adult	Offshore reef and trawling grounds	Deep	Light	Groups	Fishes and crustaceans	Generally silvery white, with a broad yellow stripe running along the side from the eye to the caudal fin base. No spots
L. malabaricus	Marine	Juvenile	shallow inshores	Coastal	Dim light	Groups	Fishes, crustaceans and cephalopods	No spots
L. malabaricus	Marine	Adult	Offshore reef	Deep	Dim light	Groups	Fishes, crustaceans and cephalopods	No spots
L. rivulatus	Marine	Adult	Reefs, shallow flats, coastal slopes	Coastal and deep	Light	Groups	Fishes, crustaceans and cephalopods	Large adults brownish to grey. No spots
L. russellii	Euryhaline	Juvenile	Mangroves, freshwater streams	Coastal	Light	Groups	Fishes and invertebrates	Whitish or pink with silvery sheen. Spots
L. russellii	Euryhaline	Adult	Offshore and inshore reefs	Deep	Light	Groups	Fishes and invertebrates	Whitish or pink with silvery sheen. Spots

A principal component analysis (PCA) was conducted with the morphometric measurements (OA, OH, OL, OP and SA) of the otoliths from all specimens to avoid multicollinearity. First, the effect of fish size on the otolith variables was removed according to . The mean value of the variables for each species was then used in the PCA. Thus, the factors obtained were rescaled by dividing each observed value by the minimum value observed for that feature, yielding categorical values between 1 and 10. In addition, the following variables were also included in the CatPCA: visual field (adapted to light or dim light; species with nocturnal activity and species inhabiting turbid or deep habitats are considered species adapted to dim light conditions), environment (marine or euryhaline), depth distribution (coastal, deep or both), life history pattern (groups or primarily solitary) and visually contrasting markings (with spots on the body or lacking spots). The depth distribution was split into three categories; the remaining variables were each split into two categories. The ecological characteristics of each species are given in Table 2. Otolith contour The analysis of otolith shape was based on a mathematical descriptor, a wavelet (WT), related to the one-dimensional decomposition of the contour (Fig. 3). This procedure is based on expanding the contour into a family of functions obtained as the dilations and translations of a unique function known as a mother wavelet ():

ψ_{s} (x) = \frac{1}{s} ψ (\frac{φ}{s})

where Ψ_s is a function with a support occupying a limited range of the abscissa; choosing its shape adequately and setting a scaling parameter (s) allows the wavelet transform to detect singularities of different sizes in the function analysed. These functions describe the most prominent features of the curve (sharp transitions) in both space and wave number (Fig. 3) (Parisi-Baradad et al. 2005Parisi-Baradad V., Lombarte A., Garcia-Ladona E., et al. 2005. Otolith shape contour analysis using affine transformation invariant wavelet transforms and curvature scale space representation. Mar. Freshw. Res. 56: 795-804., 2010Parisi-Baradad V., Manjabacas A., Lombarte A., et al. 2010. Automated Taxon Identification of Teleost fishes using an otolith online database. Fish. Res. 105: 13-20.). To obtain the wavelets, a total of 512 Cartesian coordinates on each of the orthogonal projections of the otolith were extracted using Age & Shape software (Infaimon SL, Spain). Wavelet functions from 1 to 3 gave details of small variations of the otolith contour, whereas wavelet functions between 7 and 9 showed few contour features. Wavelet number 5 was selected as an intermediate function (Fig. 3). It was also used in a previous study to discriminate Lutjanus species (Sadighzadeh et al. 2012Sadighzadeh S., Tuset V.M., Valinassab T., et al. 2012. Comparison of different otolith shape descriptors and morphometrics in the identification of closely related species of Lutjanus spp. from the Persian Gulf. Mar. Biol. Res. 8: 802-814.).

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Fig. 3. – Scheme showing the procedure for obtaining wavelets.

A graphical feature, the wavelet variance, was used for all species to find zones with higher variability that could indicate different patterns in the shape of the otolith. To determine whether this variability could group the species, a cluster analysis was performed based on quadratic Euclidean distance using Ward’s method. To detect significant differences between the mean functions of groups, an ANOVA test was applied based on the analysis of randomly chosen one-dimensional projections (Cuesta-Albertos and Febrero-Bande 2010Cuesta-Albertos J.A., Febrero-Bande M. 2010. A simple multiway ANOVA for functional data. Test 19: 537-557.). This test is implemented in the function anova.RPm in the R library fda.usc (Febrero-Bande and Oviedo de la Fuente 2011Febrero-Bande M., Oviedo de la Fuente M. 2011. fda.usc: Functional Data Analysis and Utilities for Statistical Computing (fda.usc). R package version 0.9.5. ). The p-values were obtained using 1000 bootstrap replicates.

RESULTSTop

Otolith morphometric analysis

All morphometric variables of the sagittal otoliths showed a good relationship with fish length for each species, with more than 75% of the variance explained, independently of sample size. Otolith area was the variable with the strongest relationship to fish length (r²>0.870), whereas the variation in otolith height was more diverse among species (Table 3). The comparison of slopes showed no specific differences among species for any variables except in the case of L. rivulatus (Table 4). However, the comparisons based on the S:O ratio (Tamhane’s T2 test, p>0.05) clustered the species into six groups in decreasing order of relative size (major to minor): 1) L. lutjanus, 2) L. ehrenbergii and L. fulviflamma, 3) L. fulviflamma and L. russellii, 4) L. malabaricus, L. lemniscatus and L. johnii, 5) L. erythropterus and L. rivulatus, and 6) L. argentimaculatus (Fig. 4).

Table 3. – Power relationships between fish length and otolith variables for snappers from the Persian Gulf. OA, otolith area; OH, otolith height; OL, otolith length; OP, otolith perimeter; OW, otolith weight; TL, total length.

L. argentimaculatus (n= 13)		L. ehrenbergii (n= 61)		L. erythropterus (n= 9)		L. fulviflamma (n= 11)		L. johnii (n= 93)
Equation	r²	Equation	r²	Equation	r²	Equation	r²	Equation	r²
OA=0.004 TL^1.616	0.898	OA=0.011 TL^1.485	0.870	OA=0.067 TL^1.186	0.930	OA=0.023 TL^1.333	0.908	OA=0.0164 TL^1.469	0.979
OH=0.027 TL^0.918	0.878	OH=0.097 TL^0.733	0.814	OH=0.424 TL^0.505	0.865	OH=0.107 TL^0.712	0.803	OH=0.141 TL^0.7005	0.968
OL=0.102 TL^0.790	0.808	OL=0.119 TL^0.807	0.867	OL=0.261 TL^0.660	0.959	OL=0.164 TL^0.734	0.907	OL=0.156 TL^0.7772	0.978
OP=0.218 TL0.852	0.869	OP=0.403 TL^0.774	0.810	OP=0.904 TL^0.629	0.958	OP=0.511 TL^0.717	0.868	OP= 0.484 TL^0.7632	0.953
OW=2 10^–9 TL^2.962	0.866	OW=2 10^–7 TL^2.428	0.851	OW=4 10^–6 TL^1.818	0.972	OW=8 10^–8 TL^2.546	0.792	OW=7 10^–7TL^2.1904	0.970
L. lemniscatus (n= 23)		L. lutjanus (n= 23)		L. malabaricus (n= 47)		L. rivulatus (n= 12)		L. russelli (n= 32)
Equation	r²	Equation	r²	Equation	r²	Equation	r²	Equation	r²
OA=0.015 TL^1.409	0.969	OA=0.003 TL^1.743	0.902	OA=0.007 TL^1.65	0.885	OA=0.187 TL^1.044	0.891	OA=0.006 TL^1.559	0.978
OH=0.081 TL^0.754	0.931	OH=0.064 TL^0.818	0.858	OH=0.105 TL^0.771	0.829	OH=0.332 TL^0.557	0.910	OH=0.078 TL^0.759	0.951
OL=0.206 TL^0.695	0.901	OL=0.062 TL^0.933	0.887	OL=0.0823 TL^0.883	0.912	OL=0.658 TL^0.516	0.860	OL=0.132 TL^0.777	0.969
OP=0.38 TL^0.765	0.913	OP=0.135 TL^0.985	0.891	OP=0.256 TL^0.876	0.811	OP=3.426 TL^0.429	0.584	OP=0.543 TL^0.706	0.951
OW= 8 10^–8 TL^2.455	0.924	OW=2 10^–7 TL^2.469	0.745	OW=2 10^–7 TL^2.475	0.894	OW=4 10^–6 TL^1.893	0.950	OW=3 10^–7 TL^2.229	0.979

Table 4. – Otolith variables presenting significant differences (Tukey’s test) in the slope of relationships between fish length and otolith variables among snappers from the Persian Gulf. ns, not significant; OA, otolith area; OH, otolith height; OL, otolith length; OP, otolith perimeter; OW, otolith weight. Differences are significant (p<0.05) when otolith variables appear.

	L.arg	Lehr	Lery	Lflu	Ljoh	Llem	Llut	Lmal	Lriv	Lrus
L. argentimaculatus (Larg)	-
L. ehrenbergii (Lehr)	OH	-
L. erythropterus (Lery)	OW	ns	-
L. fulviflamma (Lflu)	ns	ns	ns	-
L. johnii (Ljoh)	ns	ns	ns	ns	-
L. lemniscatus (Llem)	ns	ns	ns	ns	ns	-
L. lutjanus (Llut)	ns	ns	OA	ns	ns	OL	-
L. malabaricus (Lmal)	ns	ns	ns	ns	ns	ns	ns	-
L. rivulatus (Lriv)	OH, OP	OP	OL	ns	OL, OP	ns	OA, OL, OP	OA, OL, OP	-
L. russellii (Lrus)	ns	ns	ns	ns	ns	ns	ns	ns	OL	-

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Fig. 4. – Box plots (maximum, minimum, upper and lower quartiles) for the sulcus acusticus area: otolith area ratio (S:O) for snappers from the Persian Gulf. Numbers indicate the corresponding group.

The PCA reduced the otolith dimensions to two sets, OTO1 and OTO2, which were related to the otolith perimeter. The two-dimensional plot of the CatPCA analysis indicated that the first dimension was primarily influenced by environment, visually contrasting markings, the depth distribution and the otolith perimeter. The second dimension was influenced by the otolith morphometry (OTO1) and the visual field (Fig. 5). The total variance explained by the model was 65.8%, including 45.9% along the first dimension and 19.9% along the second. The increase in the depth distribution of the species was positively related to the absence of a spot (visually contrasting markings) on the body of the fish. The species adapted to dim light conditions and deeper distribution had a greater otolith perimeter.

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Fig. 5. – Scatterplot of the CatPCA analysis of ecological, functional and morphological factors influencing the ecomorphological distribution of snappers from the Persian Gulf.

Otolith contour

The graphical illustration of wavelet number 5 showed specific variations associated with prominent features of the otolith contour (Fig. 6). An ANOVA indicated three zones with a high variability (Fig. 7A, B): posterior, antero-dorsal and excisura ostii. The posterior and excisura ostii zones were associated with development of the rostrum, anti-rostrum and post-rostrum. However, only the antero-dorsal zone of the wavelet (Fig. 7C) showed well-defined patterns. A cluster analysis grouped the species into three significant patterns (ANOVA, p<0.05) (Fig. 8A, B): 1) otoliths with a flattened antero-dorsal zone, e.g. L. ehrenbergii, L. fulviflamma, L. lutjanus and L. rivulatus; 2) otoliths with a slight development of the antero-dorsal zone, e.g. L. russellii and L. johnii; and 3) otoliths with an extensive development of the antero-dorsal zone, e.g. L. argentimaculatus, L. erythropterus, L. malabaricus and L. lemniscatus.

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Fig. 6. – Signals of wavelet 5 from the otoliths of snappers from the Persian Gulf. Colours show the similarities between signals.

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Fig. 7. – Graphics indicating zones with higher variability in wavelet 5. (A) variance for all species, (B) otolith contour, (C) wavelet 5 for each species.

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Fig. 8. – A, hierarchical clustering of snappers from the Persian Gulf using antero-dorsal zone; B, mean signal of wavelet 5 for each group showing the morphology of the antero-dorsal zone of the otolith. Numbers indicate the otolith patterns obtained.

DISCUSSIONTop

The S:O ratio and otolith size are related to the hearing capabilities of marine fishes (Gauldie 1988Gauldie R.W. 1988. Function, form and time-keeping properties of fish otoliths. Comp. Biochem. Physiol. Part A 91: 395-402., Montgomery and Pankhurst 1997Montgomery J.C., Pankhurst N.W. 1997. Sensory physiology. In: Randall D.J., Farrell A.P. (eds), Deep-sea Fishes. Academic Press, pp. 325-349.) and ecological factors such as depth distribution, fish mobility and differences in food and spatial niches (Lombarte 1992Lombarte A. 1992 Changes in otolith area:sensory area ratio with body size and depth. Environ. Biol. Fish. 33: 405-410., Aguirre and Lombarte 1999Aguirre H., Lombarte A. 1999. Ecomorphological comparisons of sagittae in Mullus barbatus and M. surmuletus. J. Fish. Biol. 55: 105-114., Tuset et al. 2010Tuset V.M., Piretti S., Lombarte A., et al. 2010. Using sagittal otoliths and eye diameter for ecological characterization of deep-sea fish: Aphanopus carbo and A. intermedius from NE Atlantic waters. Sci. Mar. 74: 807-814.). Our results stressed the relevance of the sagittal otolith characteristics to the ecomorphological characteristics, showing otolith shape patterns associated with functional and ecological factors.

Several species groups of snappers are recognized on the basis of morphology and external colouration, e.g. ‘blue-lined’, ‘black spot’ complex, ‘yellow-lined’ or ‘red-lined’. These groups are congruent with phylogenetic evolution (Miller and Cribb 2007Miller T.L., Cribb T.H. 2007. Phylogenetic relationships of some common Indo-Pacific snappers (Perciformes: Lutjanidae) based on mitochondrial DNA sequences with comments on the taxonomic position of the Caesioninae. Mol. Phyl. Evol. 44: 450-460.). The fishes living in shallower water have acquired a tendency to be yellowish with stripes and form aggregations to avoid large predators. They also have larger eyes and bright colour patterns favouring visual communication. The otoliths are small, most likely to avoid the background noise produced by rough seas (Paxton 2000Paxton J.R. 2000. Fish otoliths: do sizes correlate with taxonomic group, habitat and/or luminescence? Phil. Trans. Roy. Soc. London Ser. B 355: 1299-1303., Volpedo and Echeverria 2003Volpedo A.V., Echeverría D.D. 2003. Ecomorphological patterns of the sagitta in fish on the continental shelf off Argentine. Fish. Res. 60: 551-560., Cruz and Lombarte 2004Cruz A., Lombarte A. 2004. Otolith size and its relationship with colour patterns and sound production. J. Fish Biol. 65: 1512-1525.). In contrast, species inhabiting deeper or dimly illuminated waters have a darker colouration. Many are solitary, exhibit territorial behaviour, and possess larger otoliths (Volpedo and Echeverria 2003Volpedo A.V., Echeverría D.D. 2003. Ecomorphological patterns of the sagitta in fish on the continental shelf off Argentine. Fish. Res. 60: 551-560., Cruz and Lombarte 2004Cruz A., Lombarte A. 2004. Otolith size and its relationship with colour patterns and sound production. J. Fish Biol. 65: 1512-1525., Lombarte et al. 2010Lombarte A., Palmer M., Matallanas J., et al. 2010. Ecomorphological trends and phylogenetic inertia of otolith sagittae in Nototheniidae. Environ. Biol. Fish. 89: 607-618.). This ecological pattern was clearly noted in the species studied, illustrating the relationship of morphology and external colouration vs. otolith size. Thus, the snappers of the ‘black spot’ complex and the ‘yellow-lined’ group (L. ehrenbergii, L. fulviflamma, L. lutjanus and L. russellii), which inhabit shallow waters (Druzhinin 1970Druzhinin A.D. 1970. The range and biology of snappers (Family Lutjanidae). J. Ichthyol. 10: 717-736. , Kuiter and Tonozuka 2001Kuiter R.H., Tonozuka T. 2001. Pictorial guide to Indonesian reef fishes. Part 1 eels-snappers, Muraenidae-Lutjanidae. Zoonetics, Australia, 302 pp. ), showed the highest S:O ratio and the smallest otolith size. The clade containing the ‘red-lined’ and ‘blue-lined’ snappers (L. argentimaculatus, L. erythropterus, L. malabaricus, L. lemniscatus, and L. rivulatus), which live in deeper or dimly illuminated waters and have a dark colouration (Allen 1985Allen G.R. 1985. FAO Species Catalogue. Snappers of the world. An annotated and illustrated catalogue of lutjanid species known to date. FAO Fish. Syn. 125: 1-208. ), showed the lowest S:O ratio and highest otolith size. L. johnii has characteristics common to both groups. Although it should have been closer to the ‘black spot’ species complex, it is genetically closer to L. erythropterus (Miller and Cribb 2007Miller T.L., Cribb T.H. 2007. Phylogenetic relationships of some common Indo-Pacific snappers (Perciformes: Lutjanidae) based on mitochondrial DNA sequences with comments on the taxonomic position of the Caesioninae. Mol. Phyl. Evol. 44: 450-460.).

Species inhabiting environments with a limited visual field can increase their hearing capabilities (Lombarte and Fortuño 1992Lombarte A., Fortuño J.M. 1992. Differences in morphological features of the sacculus of the inner ear of two hakes (Merluccius capensis and M. paradoxus, Gadiformes) inhabits from different depth of sea. J. Morphol. 214: 97-107., Deng et al. 2013Deng X., Wagner H.J. Popper A.N. 2013. Interspecific variations of inner ear structure in the deep-sea fish family Melamphaidae. Anat. Rec. 296: 1064-1082. ). The development of the ostial area of the sulcus acusticus region of the sagittal otolith is correlated with an increase in the proportion of horizontally oriented sensory hair cells (Popper and Coombs 1982Popper A.N., Coombs S. 1982. The morphology and evolution of the ear in actinopterygian fishes. Amer. Zool. 22: 311-328. , Ramcharitar et al. 2006Ramcharitar J., Gannon D.P., Popper A.N. 2006. Bioacoustics of the family Sciaenidae (croakers and drumfishes). Trans. Amer. Fish. Soc. 135: 1409-1431.), which may help to detect directional acoustic stimuli and to locate prey (Popper and Fay 1993Popper A.N., Fay R.R. 1993. Sound detection and processing by fish: critical review and major research questions. Brain Beh. Evol. 41: 14-38.). Moreover, the species that use environments with dim illumination tend to show increases in otolith size and adopt non-visual communication (acoustic or chemical) (Paxton 2000Paxton J.R. 2000. Fish otoliths: do sizes correlate with taxonomic group, habitat and/or luminescence? Phil. Trans. Roy. Soc. London Ser. B 355: 1299-1303., Cruz and Lombarte 2004Cruz A., Lombarte A. 2004. Otolith size and its relationship with colour patterns and sound production. J. Fish Biol. 65: 1512-1525.). Our study showed a relationship between the variations in the antero-dorsal area of the sagittal otolith of snappers and fish behaviour. A flattened shape was observed in L. rivulatus, which forages during the day, whereas extensive development of the antero-dorsal area was found in L. argentimaculatus, a species that is active at night (Martínez-Andrade 2003Martinez-Andrade F. 2003. A comparison of life histories and ecological aspects among snappers (Pisces: Lutjanidae). PhD thesis, Lousiana State University, 194 pp. ). Accordingly, we infer that L. argentimaculatus, L. erythropterus, L. malabaricus and L. lemniscatus (all ‘red-lined’) should be adapted to dim light conditions or nocturnal activity; L. ehrenbergii, L. fulviflamma (‘black spot’ complex), L. lutjanus (‘yellow-lined’) and L. rivulatus (‘blue-lined’) should be more active during the day; whereas L. russellii and L. johnii (‘black spot’ complex) should show a nocturnal-diurnal dichotomy. Thus, the diel activity rhythm facilitates coexistence between competitors extending beyond the effects of adaptation to different behavioral strategies and feeding habitats (Colmenero et al. 2010Colmenero A.I., Aguzzi J., Lombarte A., et al. 2010. Sensory constraints in temporal segregation in two species of anglerfish, Lophius budegassa and L. piscatorius. Mar. Ecol. Prog. Ser. 416: 255-265., Fox and Bellwood 2011Fox R.J., Bellwood D.R. 2011. Unconstrained by the clock? Plasticity if diel activity rhythm in a tropical reef fish, Siganus lineatus. Funct. Ecol. 25: 1096-1105., Azzurro et al. 2013Azzurro E., Aguzzi J., Maynou F., et al. 2013. Diel rhythms in shallow Mediterranean rocky-reef fishes: a chronobiological approach with the help of trained volunteers. J. Mar. Biol. Assoc. U.K. 93: 461-470.).

The results presented here demonstrate that wavelet analysis is a very useful mathematical procedure for ecomorphological studies in addition to its use in species discrimination (Parisi-Baradad et al. 2005Parisi-Baradad V., Lombarte A., Garcia-Ladona E., et al. 2005. Otolith shape contour analysis using affine transformation invariant wavelet transforms and curvature scale space representation. Mar. Freshw. Res. 56: 795-804., 2010Parisi-Baradad V., Manjabacas A., Lombarte A., et al. 2010. Automated Taxon Identification of Teleost fishes using an otolith online database. Fish. Res. 105: 13-20., Sadighzadeh et al. 2012Sadighzadeh S., Tuset V.M., Valinassab T., et al. 2012. Comparison of different otolith shape descriptors and morphometrics in the identification of closely related species of Lutjanus spp. from the Persian Gulf. Mar. Biol. Res. 8: 802-814.). The identification of otolith zones with high morphological variability implies that information on shape of the whole otolith may not be necessary for the identification of stocks or species or for ontogenetic or ecomorphological studies. These findings constitute a novel approach to species discrimination. Finally, discrimination of the activity of fishes will be essential for a better understanding of ecosystem functioning and the ecological roles played by fish species (Pulcini et al. 2008Pulcini D., Costa C., Aguzzi J., et al. 2008. Light and shape: A contribution to demonstrate morphological differences in diurnal and nocturnal Teleosts. J. Morph. 269:375-385., Colmenero et al. 2010Colmenero A.I., Aguzzi J., Lombarte A., et al. 2010. Sensory constraints in temporal segregation in two species of anglerfish, Lophius budegassa and L. piscatorius. Mar. Ecol. Prog. Ser. 416: 255-265., Meakin and Qin 2011Meakin C., Qin J. 2011. Growth, behaviour and colour changes of juvenile King George whiting (Silaginodes punctata) mediated by light intensities. New Zealand J. Mar. Freshw. Res. 46: 111-123., Aguzzi et al. 2013Aguzzi J., Sbragaglia V., Santamaría G., et al. 2013. Daily activity rhythms in temperate coastal fishes: insights from cabled observatory video monitoring. Mar. Ecol. Prog. Ser. 486: 223-236.).

ACKNOWLEDGEMENTSTop

We would like to thank our colleagues at the Persian Gulf and Oman Sea Ecological Research Institute for their kind collaboration. This study was co-funded by the research project AFORO3D (MICIN CTM2010-1970) of the Spanish Government. We would like to thank the reviewers for their comments and suggestions.

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