Services on Demand
Journal
Article
text in 
English (pdf)
Article in xml format
Article references
Automatic translation
Send this article by e-mailIndicators
-
Cited by SciELO -
Access statistics
Related links
-
Similars in
SciELO
Share
Permalink
Ciencias marinas
Print version ISSN 0185-3880
Cienc. mar vol.41 n.3 Ensenada Sep. 2015
https://doi.org/10.7773/cm.v41i3.2464
Articles
Otolith Sr:Ca ratio and morphometry as indicators of habitat of a euryhaline species: The case of the silverside Odontesthes bonariensis
1 Instituto de Investigaciones en Producción Animal-Concejo Nacional de Investigaciones Científicas y Técnicas-Universidad de Buenos Aires (INPA-CONICET-UBA), Av. Chorroarín 280 (C1427CWO), Buenos Aires, Argentina
2 Centro Austral de Investigaciones Científicas-Concejo Nacional de Investigaciones Científicas y Técnicas (CADIC-CONICET), Bernardo Houssay 200 (V9410CAB), Ushuaia, Argentina
The silverside Odontesthes bonariensis is a euryhaline species native of South America and represents a very important fishing resource for the Plata Basin (Argentina and Uruguay). This study compares the Sr:Ca ratio of water as well as the Sr:Ca ratio and morphometry of the sagittal otolith of the silverside present in different environments (one salt lake, two freshwater dams, one lagoon, and one estuary) in order to evaluate the use of these variables as markers of habitat. The pattern of the Sr:Ca ratio in the water agrees with the one found in the otoliths, showing a positive relationship with the conductivity of the water. Univariate and multivariate analyses of variance indicated significant differences (P < 0.05) among the localities studied for the morphometric indices. The discriminant function analysis provided a high percentage of correctly classified individuals for the saltwater environment (100%) and the lentic water bodies and estuary (60-80%), circularity and form factor being the most relevant morphometric variables. These results indicate that the Sr:Ca ratio and otolith morphometry are good markers of habitat for this important resource.
Key words: morphometry; Sr:Ca; otolith; Odontesthes bonariensis; Argentina
El pejerrey Odontesthes bonariensis es una especie eurihalina nativa de Sudamérica y representa un importante recurso pesquero para la cuenca del Plata (Argentina y Uruguay). En este estudio se comparó la relación Sr:Ca del agua y la relación Sr.:Ca y morfometría de los otolitos sagittae de pejerreyes presentes en diferentes ambientes (un lago de agua salada, dos embalses de agua dulce, una laguna y un estuario) con el objetivo de evaluar el uso de estas variables como marcadores de hábitat. El patrón de la relación Sr:Ca del agua concuerda con la hallada en los otolitos, mostrando una relación positiva con la conductividad del agua. Los análisis univariados y multivariados indicaron diferencias (P < 0.05) entre las localidades estudiadas para los índices morfométricos. El análisis discriminante mostró un elevado porcentaje de individuos correctamente clasificados para el ambiente de agua salada (100%), los cuerpos de agua lenticos y el estuario (60-80%), siendo la circularidad y el factor de forma los índices morfométricos de mayor relevancia para esta clasificación. Estos resultados indican que la relación Sr:Ca y la morfometría del otolito son buenos marcadores de hábitat para este importante recurso.
Palabras clave: morfometría; Sr:Ca; otolito; Odontesthes bonariensis; Argentina
Introduction
The Argentinian silverside, Odontesthes bonariensis (Valenciennes 1833), is one of the most important fishery resources in estuaries and rivers of southwestern South America. This species inhabits diverse habitats such as dams, lakes, rivers, lagoons, and estuaries in Argentina, Uruguay, Brazil, and Chile, and has been introduced into other South American countries (e.g., Bolivia and Peru) and other continents (e.g., Europe and Asia) (Chiba et al. 1989, Gandolfi et al. 1991, Brian and Dyer 2006, Avigliano and Volpedo 2013a). In Argentina, Brazil, and Uruguay it is found in the Plata Basin and in lentic water bodies such as dams, lakes, and lagoons, both artificial and natural (Brian and Dyer 2006, Tombari and Volpedo 2008, Avigliano and Volpedo 2013a). In general, during the larval and juvenile stages, this species feeds primarily on plankton, whereas during the adult stage, it also ingests other organisms such as gastropod molluscs and crustaceans (Escalante and Grosman 2001); however, in lotic water bodies where plankton is relatively scarce, such as the Plata River estuary, the silverside's diet is mainly based on molluscs and fish (Escalante and Grosman 2001). This species presents temperature-dependent sex determination. Spawning generally occurs twice a year, from March to April and from August to November (Barco 1986). Sexual maturity is attained between the first and second year of life (total length of ~140 mm), depending on the region (Barco 1986).
The silverside is the second most important freshwater fishery resource in Argentina and Uruguay, and a large part of the production is exported to Europe (the Netherlands, Italy, and Ukraine), Russia, and the United States (MINAGRI 2014). The volume of exported silverside derives exclusively from the lower section of the Plata Basin (Plata River, Uruguay River, and Paraná River) and has increased in recent years, from 641 in 2007 to 551 t in 2012, with an export peak (724 t) in 2008 (MINAGRI 2014).
Avigliano et al. (2014) suggested the possible existence of two fish stocks with a high degree of connectivity in the lower section of the Plata Basin, one corresponding to the Uruguay River and Paraná Delta and the other to the Plata estuary; however, historical catch data and data on the status of these stocks are lacking. Information is also lacking on the connectivity between these populations and those from other basins in the region, such as the Negro River (Uruguay) or the Salado River (Argentina), among others. In particular, the Salado River basin is connected to several lentic water bodies of the Pampean Plain (e.g., the lagoons Chascomús, Barranca, Adela, Chis Chis, El Burro) where the species is caught for subsistence, recreational, and, to a lesser extent, commercial purposes. Despite the importance of this resource, specific management measures have not been devised for the silverside in the Plata Basin. Identifying the fish stocks is therefore important to be able to generate stock-specific tools for the sustainable management of the silver-side populations.
Among the most commonly used approaches for identifying stocks are capture-recapture procedures, size structure analysis, genetic identification, and otolith morphometry and microchemistry analysis (e.g., Park and Moran 1994). The otoliths of teleost fish, located in the vestibular system, are complex polycrystalline structures composed mainly of calcium carbonate and small amounts of other minerals (trace elements) immersed in an organic matrix (Campana 1999). In certain species, the concentration of some of these elements, like strontium, barium, zinc, and magnesium, among others, is related to the their concentration in water (Campana 1999, Sturrock et al. 2012, Avigliano 2014). These characteristics, coupled with the fact that they are inert and acellular metabolic structures that constantly incorporate chemical elements from water, make otoliths a useful tool for fish stock assessments and life history studies (Campana 1999; Avigliano and Volpedo 2013b; Avigliano et al. 2014, 2015a, 2015b, 2015c).
In view of the positive relationship that exists between salinity and the strontium:calcium (Sr:Ca) ratio in water and some fish otoliths (Secor et al. 1995, Zlokovitz et al. 2003, Kraus and Secor 2004, Schuchert et al. 2010, Tabouret et al. 2010, Avigliano et al. 2014), studies relating water parameters (Sr:Ca and salinity) and the otolith Sr:Ca ratio have been able to identify fish stocks and migratory routes (e.g., Secor et al. 1995; Zlokovitz et al. 2003; Tabouret et al. 2010; Avigliano et al. 2015b, 2015c). Otolith morphometrics are also used to identify fish stocks (e.g., Longmore et al. 2010, Cañás et al. 2012, Avigliano et al. 2014, Keating et al. 2014, Vieira et al. 2014). The morphometric analysis of otoliths permits a quantitative description of the shape and contour that can be statistically compared (Lestrel 1997). Some of the most commonly used shape indices are circularity, rectangu-larity, ellipticity, form factor, and sulcus area/otolith area (e.g., Volpedo et al. 2008, Longmore et al. 2010, Cañás et al. 2012, Tuset et al. 2013, Avigliano et al. 2014). In recent studies, both methods have been used (e.g., Longmore et al. 2010, Avigliano et al. 2014).
The objective of this study was to compare the Sr:Ca ratio and morphometry of the sagittal otolith of a euryhaline species, the silverside O. bonariensis, from different environments in Argentina (dam, lake, lagoon, and estuary) in order to evaluate the use of these variables as markers of habitat. This information is important for fish stock identification and interconnectivity studies and the development of management policies.
Materials and methods
Study area
Water bodies located in three different regions of Argentina were studied (fig. 1). In the northwest, samples were collected from two artificial dams: Los Alisos (24°11'S-65°18'W) and Cabra Corral (25°27'S-65°27'W). Los Alisos Dam, located 1260 m above sea level, has an electrical conductivity of <250 μScm-1 and maximum depth of 22 m. Cabra Corral Dam, located 1100 m above sea level, along the Juramento River, has a mean electrical conductivity of 421 μScm-1 and maximum depth of 90 m (Muñoz et al. 2005). The dams are not interconnected and the region has a subtropical semi-arid climate.
Figure 1: Study area. The numbered circles indicate the water and silverside (Odontesthes bonariensis) collection sites.
In the Pampean Plain (humid pampa), samples were collected from the Plata River (35°3'5.09"S, 57°2'47.79"W) and Chascomús Lagoon (35°34'00"S, 58°01'00"W). The Plata River is a wide estuary that receives the waters from the Plata Basin and flows into the Atlantic Ocean. It has a mean depth of between 5 and 25 m (Guerrero et al. 2010) and the electrical conductivity ranges from 67 to 30,300 μScm-1 (Avigliano and Volpedo 2013b). Chascomús Lagoon is located 10 m above sea level and forms part of the lower basin of the Salado River. It has a maximum depth of 3.4 m and mean conductivity is 2200 μScm-1 (Llames et al. 2009). The region has a warm temperate climate and the hydrologi-cal regime alternates between flood and dry periods (Vervoorst 1967). Flooding produces channels that connect Chascomús Lagoon with the Plata estuary via the Salado River.
Chasicó Lake (38°36'39.41"S, 63°4'48.68"W), located -20 m above sea level in a transition area between the Pampean and Patagonian regions, is independent from the other systems studied. It has a maximum depth of 16 m and the electrical conductivity is high (38.800 μScm-1) (Avigliano et al. 2012).
Sample collection
Water and fish samples were collected simultaneously between August and September 2011 from the two dams (Los Alisos and Cabra Corral), Plata estuary, Chascomús Lagoon, and Chasicó Lake. Triplicate water samples were collected manually at 0.5 m depth using polyethylene bottles previously washed three times with distilled water and water from the sampling site. The samples were acidified to 0.2% (v/v) (pH < 2) using nitric acid and transported in darkness at 4°C to the laboratory. They were then vacuum-filtered through 0.45 μm Whatman GF/F filters. The samples were kept at 4°C until analysis. Sample collection, preservation, preparation, and analysis were conducted according to standardized methods (APHA 1995).
Specimens of O. bonariensis were caught using multifilament three-layer nets (inner mesh, 3 × 3 cm; external meshes, 10 × 10 cm) and with hooks. They were transported to the laboratory at 4 °C where the size was measured and the sagittal otoliths were extracted. In all cases, the specimens were sexually mature adults (size at sexual maturity = ~140 mm, Barco 1986). Mean size, size range, and number of individuals used per site is shown in table 1.
Determination of water and otolith Sr and Ca
The concentration of Ca in water was determined (in triplicate) by volumetic titrations with ethylenediaminetetra-acetic acid (EDTA) (APHA 1995). The concentration of Sr in water was determined (in triplicate) using an inductively coupled plasma optical emission spectrometer (ICP-OES, PerkinElmer Optima 2000 DV, Überlingen, Germany), equipped with a cross-flow nebulizer, Scott chamber, and quartz torch (method 200.7, EPA 1994). We used an attenuated radial view axis (detection limit = 12 μgL-1). The samples were introduced into the equipment with a PerkinElmer AS-90 Plus autosampler. External calibrations were performed in all cases using PerkinElmer Pure Quality Control Standard 21 (QCS 21, USA). Every 10 samples, a blank and a sample of known concentration prepared from the QCS 21 standard were analyzed to determine whether interference or cross-contamination had occurred. The water used throughout the study was obtained from a Milli-Q water purification system (Millipore, Sao Paulo, Brazil) with a resistivity of 18.2 MOhm cm.
The results were examined and assessed in relation to the known concentration. The reported results were corrected based on a control blank. The Sr:Ca ratios were then calculated.
Only the right sagittal otoliths were used for this study (Los Alisos, N = 15; Cabra Corral, N = 15; Plata River, N = 154; Chascomús, N = 17; Chasicó, N = 48). They were rinsed in Milli-Q water and dried. Each one was weighed on an analytical balance (error <0.001 g) and digested with 50% nitric acid on a sand bed heated to 400-450 °C for 1 h (Avigliano et al. 2014). Otolith Sr was determined by ICP-OES and Ca was determined by the titration method using EDTA (APHA 1995). The equipment, procedure, and quality control were the same as used to determine water Sr and Ca.
The efficiency of the otolith digestion process was verified using certified reference materials (FEBS-1, National Research Council, Canada) and an acceptable recovery percentage was obtained (93% for Sr and 110% for Ca). All otolith determinations were made in triplicate.
Otolith morphometry
The right sagittal otoliths of all the fish specimens captured were photographed under a stereoscopic microscope (Leica EZ4 HD). The following morphometric variables were recorded on the images using an image processor (Image-ProPlus 4.5): otolith length (OL), otolith width (OW), and otolith perimeter (OP), in millimeters; and otolith area (OA) and sulcus area (SA), in square millimeters. The following shape indices were then calculated: circularity (OP2/OW), rectangularity (OA/[OL × OW]), ellipticity (OL-OW/OL + OW), form factor ([4π × OA/OP2]), and SA/OA. The nomenclature of the indices used was taken from Tuset et al. (2013) and Volpedo et al. (2008). Circularity provides information on the complexity of the otolith contour (Tuset et al. 2003). Rectangularity gives information on the approximation to a rectangular or square shape, a value of 1 indicating a perfect rectangle or square. Ellipticity reflects the similarity to an ellipse, values close to 0 indicating a tendency towards circularity. The form factor is a dimensionless value that indicates the similarity of the otolith contour to a circle; its values range from 0 to 1, a value of 1 corresponding to a perfect circle (Tuset et al. 2003). The SA/OA index indicates the percentage of the otolith area occupied by the sulcus. The sulcus is the contact area of the otolith with the saccular macula that transmits information to the brain about the relative position of the fish in the water column and auditory information (Volpedo et al. 2008).
Statistical analysis
The Sr:Ca ratio of the water from the different sampling sites was compared by a Kruskal-Wallis nonparametric analysis of variance. The Sr:Ca ratio in the otoliths was transformed with the function log(x + 1) because the assumptions of normality and homogeneity of variance were not met (Shapiro-Wilk and Levene tests, respectively). After verifying these assumptions, an analysis of covariance (ANCOVA) was applied to determine if otolith weight affected the Sr:Ca ratio. The Sr:Ca ratio correlated positively with otolith weight and was corrected by subtracting the common slope in ANCOVA (P < 0.01, b = 0.033) (Longmore et al. 2010, Kerr and Campana 2014, Avigliano et al. 2015b). This fit eliminated the effect of otolith weight on the transformed Sr:Ca variable (ANCOVA, P > 0.05). Finally, the Sr:Ca ratio in the otoliths was compared among study sites by a univariate analysis of variance (ANOVA) and Tukey's multiple comparison test. The mean water and otolith Sr:Ca ratios were represented in box plots.
The morphometric variables did not fit the normal distribution and homogeneity of variance (Shapiro-Wilk, P < 0.01; Levene, P > 0.05) and were therefore transformed with the function log(x + 1). ANCOVA (P < 0.01) was then used to correct the effect of otolith length on the studied variables. The following constants were used for the correction: circularity, b = -0.03; rectangularity, b = -0.01; ellipticity, b = -0.01; form factor, b = 0.17; and SA/OA, b = -0.003. The morphometric variables were analyzed by ANOVA and Tukey's test was used to evaluate the differences among sampling sites. Moreover, a multivariate analysis of variance (MANOVA) was applied to determine whether differences existed among sites considering all the morphometric variables simultaneously. Hotelling's T2 test was then applied to evaluate the differences among sites.
A canonical discriminant analysis (CDA) was performed using the morphometric variables in order to obtain the cross-classification matrix and determine the capacity of these variables to identify the site of origin of the fish (e.g., Longmore et al. 2010, Kerr and Campana 2014). The standardized canonical discriminant function coefficients were used to determine the contribution of each variable to the discrimination of the groups. All statistical analyses were performed using InfoStat.
Results
Sr:Ca ratio in water and otoliths
The Chasicó Lake water samples had high Sr:Ca values (Kruskal-Wallis, P < 0.001). Low values were recorded for the Plata estuary and Los Alisos Dam waters, and there were no differences between these two sites (Kruskal-Wallis, P > 0.05) (fig. 2a). Intermediate values were obtained for the water samples from Cabra Corral Dam and Chascomús Lagoon (P > 0.05) (fig. 2a).
Figure 2: Mean Sr:Ca ratio of water (a) and otoliths (b) per sampling site. The bars indicate the standard deviation.
There were no significant differences between the Sr:Ca ratios of the silverside otoliths from the Cabra Corral Dam and Plata estuary (ANOVA, P < 0.05). Differences were found, however, between the Sr:Ca ratios of the otoliths from the other sampling sites (P < 0.05). They were significantly lower in the otoliths from Los Alisos Dam and higher in those from Chasicó Lake (fig. 2b).
Otolith morphometry
A representative image of the otoliths from each site is shown in figure 3.
Figure 3: Right sagittal otoliths of Odontesthes bonariensis from each sampling site. The sulcus was painted with graphite under a magnifying glass (20×) for better visualization. A, anterior; D, dorsal; S, sulcus; V, ventral; P, posterior. Bar = 1 mm.
Significantly high circularity and ellipticity values were obtained for the Chasicó Lake otoliths (table 2), indicating high edge complexity and an elliptical morphology. The Chascomús Lagoon otoliths had significantly low rectangu-larity and circularity values (P < 0.05), whereas the form factor was significantly high (P < 0.05). This indicates a morphology tending towards circularity with low edge complexity. On the other hand, the SA/OA value was higher for this body of water (table 2).
Table 2: Mean ± standard deviation of the otolith morphometric variables transformed with function log(x + 1) per sampling site. Different letters in the columns indicate significant statistical differences (ANOVA, P < 0.05).
The otoliths from the Plata estuary specimens tended to be elliptic-square in shape related to high ellipticity and rectangularity (table 2), and the otolith edge showed low complexity. The lowest form-factor value was recorded for the Cabra Corral otoliths, indicating a tendency towards a square shape (table 2). The otoliths from Los Alisos specimens showed high rectangularity and low edge complexity (table 2).
The MANOVA showed significant differences for the morphometric variables among the study sites (P < 0.05). Hotelling's T2 test did not reveal significant differences between Los Alisos and Chascomús (P > 0.05); however, Cabra Corral, Plata estuary, and Chasicó differed significantly among themselves and from Los Alisos and Chascomús (P < 0.001).
The CDA plot (fig. 4) shows a clear separation between O. bonariensis from Chasicó Lake and from the other four sites. The data corresponding to the Chascomús Lagoon fish tended to separate from that corresponding to the Plata estuary fish. The Cabra Corral and Los Alisos values overlap. The first canonical axis explained 99.8% of the variance among groups. According to the standardized canonical discriminant function coefficients (SC) obtained, the indices that contributed most to the discrimination along this axis were circularity (SC = 2.27) and form factor (SC = 2.05), followed by rectangularity (SC = -0.51), SA/OA (SC = -0.42), and ellipticity (SC = -0.04). The CDA cross-classification table (table 3) revealed a high percentage of correctly classified individuals for Chasicó Lake (100%) and Los Alisos Dam (80%), and a moderate percentage of correctly classified individuals for Chascomús Lagoon, Cabra Corral Dam, and Plata estuary (60-64.7%).
Discussion
The concentration of elements deposited in otoliths can to a large extent be affected by the chemical composition of the water and to a lesser extent by the temperature and diet (Campana 1999, Wells et al. 2003, Ranaldi and Gagnon 2008, Brown and Severin 2009, Sturrock et al. 2012). In general, the Sr concentration in otoliths of freshwater, estuarine, and anadromous fish species correlates positively with the salinity (e.g., Kraus and Secor 2004, Sturrock et al. 2012); however, this relationship depends on the species and should be analyzed before being used in fish stock identification, connectivity, and migration studies. Particularly in marine species, the relationship between otolith Sr and salinity tends to be weak (Brown and Severin 2009, Sturrock et al. 2012). Brown and Severin (2009) indicated that the water Sr:Ca ratio is more homogenous in marine environments than in freshwater or brackish environments. Hence, the variation in otolith Sr:Ca ratios of marine species is strongly influenced by physiological factors rather than by exposure to heteroge-nous environments (Campana 1999, Brown and Severin 2009).
Odontesthes bonariensis, a highly plastic species, tolerates a wide range of salinities and inhabits both freshwater and saltwater environments, including rivers, lagoons, lakes, and estuaries (Brian and Dyer 2006, Avigliano and Volpedo 2013a). In this study, the water and otolith Sr:Ca ratios showed similar tendencies. Even though the Plata River presents a wide range of conductivity, these tendencies are consistent with the salinity and conductivity reported for the studied water bodies (Muñoz et al. 2005, Llames et al. 2009, Avigliano et al. 2012, Avigliano and Volpedo 2013b). This suggests that salinity at the sampling sites is positively related to the water and otolith Sr:Ca ratios, as has been reported by other authors for different estuarine and freshwater species in diverse aquatic systems (Brown and Severin 2009, Sturrock et al. 2012). The fact that Sr incorporation into otoliths is affected by the environment makes this element a potential tool for future fish displacement and stock identification studies. In this sense, the otolith Sr:Ca ratio proved to be a good marker of habitat for O. bonariensis. It has also been reported to be a good indicator of habitat for two other South American euryhaline species, Lycengraulis grossidens (Mai et al. 2014) and Micropogonias furnieri (Albuquerque et al. 2012). Ibáñez et al. (2012) used Sr:Ca ratios to study displacement patterns of mugilid species in the Caribbean Sea, while Hedger et al. (2008) applied this methodology to other salinity-tolerant species of the Northern Hemisphere, including Anguilla rostrata.
Other approaches such as the analysis of otolith morphology and morphometry have been widely used to differentiate fish stocks (Longmore 2010, Cañás et al. 2012, Keating et al. 2014, Vieira et al. 2014), and even to identify existing species (Tuset et al. 2013, Zhuang et al. 2014) or fossilized fish (Reichenbacher et al. 2009, Reichenbacher and Reichard 2014); however, only a few studies relate morphometric variables to different environments or ecomorphological patterns (Nelson et al. 1994; Volpedo and Fuchs 2010; Avigliano et al. 2012, 2014).
Previous studies have reported a positive relationship between salinity or conductivity and the tendency towards ellipticity of O. bonariensis otoliths from Chasicó Lake (Avigliano et al. 2012) and the Plata estuary (Avigliano et al. 2014); these studies used the otolith width:length index as an indicator of ellipticity. In agreement with these authors, in the present study we found that the otoliths tended to be elliptic or elliptic-square in shape in more saline systems, such as Chasicó Lake and the Plata estuary, and observed relatively low ellipticity in less saline systems, such as Chascomús Lagoon and the Cabra Corral and Los Alisos dams (table 2).
The size of the sulcus has also been associated with mobility (Lombarte and Popper 1994, Arellano et al. 1995, Tuset et al. 2003, Avigliano et al. 2014). For example, in some species of the genus Merluccius, this index was associated with water column use; however, in some species of the genus Mullus, it was associated with differences in feeding behavior (Aguirre and Lombarte 1999). Avigliano et al. (2014) reported that the SA/OA ratio tends to be greater in populations of O. bonariensis from the Plata estuary that undertake long migrations. In the present study, the relationship between displacements and relative size of the sulcus was not evident since the SA/OA index for the Plata River, where most migratory propulations are found, was similar or significantly lower than that obtained for the lentic water bodies (table 2). This could be due to different reasons. First, the sulcus area was analyzed in a two-dimensional plane without considering sulcus depth, which may differ depending on the different environments studied and habits of the populations (see Tuset et al. 2003). Second, the presence of a less migratory population, which tends to remain for a longer time in saline waters of the Plata estuary (Avigliano et al. 2014), may have a negative effect on the SA/OA index; however, this option seems less likely because the two known stocks migrate (to a lesser or greater extent) during the breeding period and overlap considerably in the study area (Avigliano et al. 2014).
Excluding ellipticity, the indices calculated for the otoliths of O. bonariensis from the Plata estuary fell within the range obtained for the other study sites (table 2). This could be attributed to the migratory behavior of the species in the estuary, since one of the stocks distributed in Samborombón Bay during summer (November-May), migrates for the purpose of breeding to the large rivers of the Paraná Delta (freshwater) during the cold months of the year (June-October) (Avigliano and Volpedo 2013b). Hence, the estuarine fish are exposed to different habitats and important changes in temperature and salinity, which would be reflected in the otolith morphometry.
The differences found using multiparametric tests indicate a high dissimilarity in otolith shapes, particularly in the circularity, form factor, and rectangularity indices. The CDA classification percentages are similar to those reported by other authors (see for example Tuset et al. 2003), who have indicated that the otolith shape indices can be used as natural markers, not only to separate the species, but also to identify populations. The morphometric variables analyzed herein should therefore be useful indicators of habitat.
In summary, our findings indicate that the Sr:Ca ratio and otolith morphometry are good markers of habitat for the silverside O. bonariensis. The data reported here serve as reference for studies on the biology and population dynamics (life history, stock identification, etc.) of this and other euryhaline species. The studied variables can be used to identify stocks in other South American basins where the species is found (e.g., Plata Basin, Lagoa dos Patos) and evaluate the degree of connectivity among them. This information is important for the proper management of fishery resources.
Acknowledgments
Funding was received from the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET, Argentina, PIP 112-20120100543CO), Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT, Argentina, PIP 2010-1372), and University of Buenos Aires (UBACYT 20620110100007). We thank the editor and reviewers for their valuable comments.
REFERENCES
Aguirre H, Lombarte A. 1999. Ecomorphological comparisons of sagittae in Mullus barbatus and M. surmuletusJ. Fish Biol. 55: 105-114. [ Links ]
Albuquerque CQ, Miekeley N, Muelbert JH, Walther BD, Jaureguizar AJ. 2012. Estuarine dependency in a marine fish evaluated with otolith chemistry. Mar. Biol. 159: 2229-2239. [ Links ]
[APHA] American Public Health Association. 1995. Standard Methods for the Examination of Water and Wastewater. 19th ed. APHA, Washington, DC. 541 pp. [ Links ]
Arellano RV, Hamerlynck O, Vinex M, Mees J, Hostens K, Gijselinck W. 1995. Changes in the ratio of the sulcus acusticus area to the sagitta area of Pomatoschistus minutus and P. lozanoi (Pisces, Gobiidae). Mar. Biol. 122: 355-360. [ Links ]
Avigliano E. 2014. Otolith and its application to determine commercial fish stocks from de la Plata River and the South Atlantic coast. PhD thesis, Universidad de Buenos Aires, Argentina. 127 pp. [ Links ]
Avigliano E , Volpedo AV. 2013a. Actinopterygii, Atheriniformes, Atherinopsidae, Odontesthes bonariensis Valenciennes 1835: New records for the Plata Basin, Argentina. Check List 9: 640-641. [ Links ]
Avigliano E , Volpedo AV . 2013b. Use of otolith strontium:calcium ratio as indicator of seasonal displacements of the silverside (Odontesthes bonariensis) in a freshwater-marine environment. Mar. Freshwat. Res. 64(8):746-751 [ Links ]
Avigliano E , Tombari A, Volpedo AV . 2012. ¿Los otolitos reflejan el estrés ambiental? Biol. Acuat. 27: 9-5. [ Links ]
Avigliano E , Riaños Martinez CF, Volpedo AV . 2014. Combined use of otolith microchemistry and morphometry as indicators of the habitat of the silverside (Odontesthes bonariensis) in a freshwater-estuarine environment. Fish. Res. 149: 55-60. [ Links ]
Avigliano E , Saez MB, Rico R, Volpedo AV . 2015a. Use of otolith strontium:calcium and zinc:calcium ratios as an indicator of the habitat of Percophis brasiliensis Quoy & Gaimard, 1825 in the southwestern Atlantic Ocean. Neotrop. Ichthyol. http://dx.doi.org/10.1590/1982-0224-20130235 [ Links ]
Avigliano E , Velasco G, Volpedo AV . 2015b. Use of lapillus otolith microchemistry as an indicator of the habitat of Genidens barbus from different estuarine environments in the southwestern Atlantic Ocean. Environ. Biol. Fish. http://dx.doi.org/10.1007/s10641-015-0387-3 [ Links ]
Avigliano E , Velasco G , Volpedo AV . 2015c. Assessing the use of two southwestern Atlantic estuaries by different life cycle stages of the anadromous catfish Genidens bar bus (Lacépéde 1803) as revealed by Sr:Ca and Ba:Ca ratios in otoliths. J. Appl. Ichthyol. http://dx.doi.org/10.1111/jai.12766 [ Links ]
Barco V. 1986. Análisis de la situación actual y perspectivas de desarrollo pesquero en embalses de Colombia. Trabajos presentados al Taller internacional sobre ecología y manejo de peces en lagos y embalses. Santiago, Chile, 5-10 de noviembre de 1984. COPESCAL Documento Técnico (FAO), (4): 237pp. [ Links ]
Brian S, Dyer H. 2006. Systematic revision of the South American silversides (Teleostei, Atheriniformes). Biocell 30: 69-88. [ Links ]
Brown RJ, Severin KP. 2009. Otolith chemistry analyses indicate that water Sr:Ca is the primary factor influencing otolith Sr:Ca for freshwater and diadromous fish but not for marine fish. Can. J. Fish. Aquat. Sci. 66: 1790-1808. [ Links ]
Campana SE. 1999. Chemistry and composition of fish otoliths: Pathways, mechanisms and applications. Mar. Ecol. Prog. Ser. 188: 263-297. [ Links ]
Cañás L, Stransky C, Schlickeisen J, Sampedro MP, Fariña AC. 2012. Use of the otolith shape analysis in stock identification of anglerfish (Lophius piscatorius) in the Northeast Atlantic. ICES J. Mar. Sci. 69: 250-256. http://dx.doi.org/10.1093/icesjms/fss006 [ Links ]
Chiba K, Taki Y, Sakai K, Oozeki Y. 1989. Present status of aquatic organisms introduced into Japan. In: De Silva SS (ed.), Exotic Aquatic Organisms in Asia. Proceedings of the Workshop on Introduction of Exotic Aquatic Organisms in Asia. Spec. Publ. Asian Fish. Soc., pp. 63-70. [ Links ]
[EPA] Environmental Protection Agency. 1994. Methods for the Determination of Metals in Environmental Samples. Supplement 1. EPA.Cincinnati, Ohio, 58 pp. [ Links ]
Escalante A, Grosman F. 2001. Alimentación natural del pejerrey. In: Grosman F (ed.), Fundamentos Biológicos, Económicos y Sociales para una Correcta Gestión del Recurso Pejerrey. Editorial Astyanax, Azul, Buenos Aires, pp. 67-75. [ Links ]
Gandolfi G, Zerunian S, Torricelli P, Marconato AI. 1991. Pesci delle acque interne italiane. Ministero dell'Ambiente e Unione Zoologica Italiana. Instituto Poligrafico e Zecca dello Stato, Roma. 618 pp. [ Links ]
Guerrero RA, Piola AR, Molinari G, Osiroff AP. 2010. Climatología de temperatura y salinidad en el Río de la Plata y su Frente Marítimo, Argentina-Uruguay. 1st ed. Mar del Plata, Argentina. Instituto Nacional de Investigación y Desarrollo Pesquero. 95 pp. [ Links ]
Hedger RD, Atkinson PM, Thibault I, Dodson JJ. 2008. A quantitative approach for classifying fish otolith strontium: calcium sequences into environmental histories. Ecol. Inform. 3: 207-217. [ Links ]
Ibáñez AL, Chang CW, Hsu CC, Wang CH, Iizuka Y, Tzeng WN. 2012. Diversity of migratory environmental history of the mullets Mugil cephalus and M. curema in Mexican coastal waters as indicated by otolith Sr:Ca ratios. Cienc. Mar. 38: 73-87. [ Links ]
Keating JP, Brophy D, Officer RA, Mullins E. 2014. Otolith shape analysis of blue whiting suggests a complex stock structure at their spawning grounds in the Northeast Atlantic. Fish. Res. 157: 1-6. [ Links ]
Kerr LA, Campana SE . 2014. Chemical composition of fish hard parts as a natural marker of fish stocks. In: Cadrin SX, Kerr LA , Mariani S (eds.), Stock Identification Methods: Applications in Fishery Science. Academic Press, pp. 205-234. [ Links ]
Kraus RT, Secor ER. 2004. Incorporation of strontium into otoliths of an estuarine fish. J. Exp. Mar. Biol. Ecol. 302: 85-106. [ Links ]
Lestrel PE. 1997. Fourier Descriptors and their Applications in Biology. Cambridge University Press, Cambridge, UK, 466 pp. [ Links ]
Llames ME, Lagomarsino L, Diovisalvi N, Fermani P, Torremorell AM, Perez G, Unrein F, Bustingorry J, Escaray R, Ferraro M, Zagarese HE. 2009. The effects of light availability in shallow, turbid waters: A mesocosm study. J. Plankton Res. 31: 1517-1529. http://dx.doi.org/10.1093/plankt/fbp086 [ Links ]
Lombarte A , Popper AN. 1994. Quantitative analysis of postembryonic hair cell addition in the otolithic endorgans of the inner ear of the European hake, Merluccius merluccius (Gadiformes, Teleostei). J. Comp. Neurol. 345: 419-428. [ Links ]
Longmore C, Fogarty K, Neat F, Brophy D , Trueman C, Milton A, Mariani S . 2010. A comparison of otolith microchemistry and otolith shape analysis for the study of spatial variation in a deep-sea teleost, Coryphaenoides rupestrisEnviron. Biol. Fish. 89: 591-605. [ Links ]
Mai AC, Condini MV, Albuquerque CQ , Loebmann D, Saint'Pierre TD, Miekeley N , Vieira JP. 2014. High plasticity in habitat use of Lycengraulis grossidens (Clupeiformes, Engraulididae). Estuar. Coast. Shelf. Sci. 141: 17-25. [ Links ]
[MINAGRI] Ministerio de Agricultura, Ganadería y Pesca de la Nación. 2014. Estadísticas: Productos de río por origen y destino. Argentina [cited 15 August 2014]. Available from: http://www.minagri.gob.ar/site/pesca/index.php. [ Links ]
Muñoz LM, Barros SE, Chihan SE, Franqui FR, Barrientos DJ. 2005. Rendimiento de la pesca deportiva del pejerrey (Odontesthes bonariensis) en el embalse Cabra corral, Salta, Noroeste de Argentina. In: Memorias del VI Congreso Internacional sobre Manejo de Fauna Silvestre en la Amazonia y Latinoamérica, Iquitos, Perú, pp. 86-91. [ Links ]
Nelson K, Hutchinson ES, Li G, Sly FL, Hedgecock D. 1994. Variation in life history and morphology in northern anchovies (Engraulis mordax)CalCOFI Rep. 35: 108-120. [ Links ]
Park L, Moran P. 1994. Developments in molecular genetic techniques in fisheries. Rev. Fish Biol. Fish. 4: 272-299. [ Links ]
Ranaldi MM, Gagnon MM. 2008. Zinc incorporation in the otoliths of juvenile pink snapper (Pagrus auratus Forster): The influence of dietary versus waterborne sources. J. Exp. Mar. Biol. Ecol. 360: 56-62. [ Links ]
Reichenbacher B, Reichard M. 2014. Otoliths of five extant species of the annual killifish Nothobranchius from the East African savannah. PloS ONE 9: e112459. [ Links ]
Reichenbacher B , Kamrani E, Esmaeili HR, Teimori A. 2009. The endangered cyprinodont Aphanius ginaonis (Holly, 1929) from southern Iran is a valid species: Evidence from otolith morphology. Environ. Biol. Fish. 86: 507-521. [ Links ]
Schuchert PC, Alexander I, Arkhipkin E, Koenig AE. 2010. Traveling around Cape Horn: Otolith chemistry reveals a mixed stock of Patagonian hoki with separate Atlantic and Pacific spawning grounds. Fish. Res. 102: 80-86. [ Links ]
Secor DH, Henderson-Arzapalob A, Piccoli PM. 1995. Can otolith microchemistry chart patterns of migration and habitat utilization in anadromous fishes? J. Exp. Mar. Biol. Ecol. 192: 15-33. [ Links ]
Sturrock AM, Trueman C M, Darnaude AM, Hunter E. 2012. Can otolith elemental chemistry retrospectively track migrations in fully marine fishes? J. Fish Biol. 81: 766-795. http://dx.doi.org/10.1111/j.1095-8649.2012.03372.x [ Links ]
Tabouret H, Bareille G, Clverie F, Pecheyran C, Prouzet P, Donard OF. 2010. Simultaneous use of strontium:calcium and barium:calcium ratios in otoliths as markers of habitat: Application to the European eel (Anguilla anguilla) in Adour Basin, South West France. Mar. Environ. Res.70: 35-45. [ Links ]
Tombari A , Volpedo VA. 2008. Modificaciones en la distribución original de especies por impacto antrópico: El caso de Odontesthes bonariensis (Pisces: Atherinopsidae). In: Volpedo AV , Fernández Reyes L (eds.), Efecto de los Cambios Globales sobre la Biodiversidad. Buenos Aires, Argentina, pp. 155-165. [ Links ]
Tuset VM, Lombarte A , Gonzalez JA, Pertusa JF, Lorente MJ. 2003. Comparative morphology of the sagittal otolith in Serranus spp. J. Fish Biol. 63: 1491-1504. [ Links ]
Tuset VM , Parisi-Baradad V, Lombarte A . 2013. Application of otolith mass and shape for discriminating scabbardfishes Aphanopus spp. in the north-eastern Atlantic Ocean. J. Fish. Biol. 82: 1746-1752. [ Links ]
Vervoorst FB. 1967. Las comunidades vegetales de la Depresión del Salado. La Vegetación de la República Argentina, Serie Fitogeográica No. 7, Buenos Aires INTA, 259 pp. [ Links ]
Vieira AR, Neves A, Sequeira V, Paiva RB, Gordo LS. 2014. Otolith shape analysis as a tool for stock discrimination of forkbeard (Phycis phycis) in the Northeast Atlantic. Hydrobiologia 728: 103-110. [ Links ]
Volpedo AV , Fuchs DV. 2010. Ecomorphological patterns of the lapilli of Paranoplatense Siluriforms (South America). Fish. Res. 102(1): 160-165. [ Links ]
Volpedo AV , Tombari AD, Echeverría DD. 2008. Eco-morphological patterns of the sagitta of Antarctic fish. Polar Biol. 31: 635-640. [ Links ]
Wells BK, Rieman BE, Clayton JL, Horan DL, Jones CM. 2003. Relationships between water, otoliths, and scale chemistries of Westslope cutthroat trout from the Coeur d'Alene River, Idaho: The potential application of hard-part chemistry to describe movements in freshwater. Trans. Am. Fish. Soc. 132: 409-424. [ Links ]
Zhuang L, Ye Z, Zhang C. 2014. Application of otolith shape analysis to species separation in Sebastes spp. from the Bohai Sea and the Yellow Sea, northwest Pacific. Environ. Biol. Fish. 98: 547-558. http://dx.doi.org/10.1007/s10641-014-0286-z [ Links ]
Zlokovitz ER, Secor DH , Piccoli PM . 2003. Patterns of migration in Hudson River striped bass as determined by otolith microchemistry. Fish. Res. 63: 245-259. [ Links ]
Received: September 2014; Accepted: January 2015
Este es un artículo publicado en acceso abierto bajo una licencia Creative Commons
