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Seasonal and spatial variation of carbon and nitrogen stable isotopes in mangrove oysters (Crassostrea corteziensis) from the northwest coast of Mexico.

ABSTRACT The aim of this study was to evaluate how Crassostrea corteziensis interacts with its habitat (abiotic factors) and to examine the isotopic variations that may exist over different scales of space and time at a subtropical gradient. This information will contribute to the work required to understand the ecology of this oyster species. We analyzed stable isotopes ([delta][sup.13]C and [delta][sup.15]N) in oyster soft tissue and the concentrations of chlorophyll a, N[H.sub.4.sup.+], and N[O.sub.3.sup.-1] in the waters of 6 lagoons during the dry and rainy seasons of 2008 and 2009. The mean C:N ratios in soft tissue were generally greater than 3.5 in the different lagoons and during both seasons, indicating a relatively high amount of lipids in the soft tissue related to reproductive activity. The isotopic variability between sites in this study (-25.5 to -17.1% [per thousand] for [delta][sup.13]C and 6.5 to 13.7% [per thousand] for [delta][sup.15]N) suggested differences in the composition of suspended organic matter in the diet of this species at different locations, showing an opportunistic behavior that allowed us to detect differences on temporal and spatial scales. On a temporal scale, however, there was no difference in [delta][sup.13]C, which was most likely related to the high food availability and the observation that individuals tend to feed on and share the same overabundant prey. In the case of [delta][sup.15]N, significant temporal differences were evident in only a few lagoons. These differences were related to a differential contribution of N[H.sub.4.sup.+] and NOT as primary sources to the suspended organic matter pool during the 2 seasons. On a spatial scale, some lagoons showed significant differences (P < 0.05) and high [delta][sup.15]N values (>10% [per thousand]) in addition to high concentrations of N[H.sub.4.sup.+]. Enriched [delta][sup.15]N values are often associated with an anthropogenic impact, as human and animal waste nitrate have [delta][sup.15]N values of approximately 10-20% [per thousand].

KEY WORDS: [delta][sup.13]C, [delta][sup.15]N, aquaculture, oyster farms Sinaloa, trophic ecology, Crassostrea corteziensis

INTRODUCTION

The state of Sinaloa in northwest Mexico is characterized by a subtropical climate and a large number of coastal lagoons that are populated by a variety of marine mammals, birds, reptiles, and a wide variety of fish and shellfish (Martinez-Lopez et al. 2007). The relatively extensive coastal plain of this region has favored the development of tourism, mechanized agriculture, important fisheries of lobsters and fish, and, more recently, shrimp and oyster cultures (Peez-Osuna et al. 2003, Osuna-Martinez et al. 2010).

An oyster culture is 1 form of sustainable shellfish farming that can be conducted in the natural environment (Marin-Leal et al. 2008, Rodriguez-Jaramillo et al. 2008) but require sample knowledge of oyster ecology (Dame & Prins 1998). Three species of wild oysters are found along the Pacific coast of Mexico: Crassostrea iridescens Hanley, Crassostrea corteziensis Hertlein, and Crassostrea palmula Carpenter. Of these, the mangrove oyster (Crassostrea corteziensis) is widely exploited for human consumption (Peez-Osuna et al. 1995) and has been proposed as viable option for oyster farming in Mexico (Ramirez & Sevilla 1965, Chavez-Villalba et al. 2005).

The mangrove oyster is most often cultured in coastal lagoons in Sinaloa (Osuna-Martinez et al. 2010). Currently, there is much interest in improving the protocols for cultivating this species in other areas of Mexico, such as the state of Sonora (Mazon-Suestegui et al. 2011). However, despite the importance of marine bivalves to coastal ecosystems, knowledge about fundamental aspects of their ecology, such as their food sources, is still lacking (Marin-Leal et al. 2008). In addition, the influence of abiotic environmental factors, such as temperature and salinity, are not well understood.

These limitations have prompted the need for additional tools to understand more fully the processes affecting the ecology of Crassostrea corteziensis. Isotopic studies ([delta][sup.13]C and [delta][sup.15]N) of marine bivalves have contributed to a greater understanding of their role in marine food webs (Lorrain et al. 2002, Yokoyama et al. 2005) and of changes caused by the variability of environmental parameters (Lefebvre et al. 2009). Knowledge of these 2 features can contribute to the evaluation for a successful culturing of this species in other locations. In addition, the use of oysters as sentinels of marine ecotoxicological studies has been suggested to assess coastal water quality (Peez-Osuna et al. 1995), because oysters are very sensitive to pollutants and provide a rapid response. By measuring their [delta][sup.13]C and [delta][sup.15]N content, these bivalves can be used as monitors of anthropogenic effects on watersheds, and freshwater and coastal ecosystems (Fry 1999, Costanzo et al. 2001, Jennings & Warr 2003).

Evidence of seasonal isotopic differences in consumer tissues and their potential diets has been reported mostly for invertebrates from different estuaries (Fry & Sherr 1984, Michener & Schell 1994, Malet et al. 2007), whereas temporal variations have been demonstrated to be site specific (Fukumori et al. 2008, Marin Leal et al. 2008). Therefore, ecological studies based on stable isotopes of C and N need to be conducted such that the spatial and temporal scales are able to evidence the variability in [delta][sup.13]C and values (Boyce et al. 2001).

The aim of this study was to use stable isotope ratios ([delta][sup.13]C, [delta][sup.15]N) and the C: N ratio in the soft tissue of Crassostrea corteziensis on a biogeographical scale along the coastal lagoons of Sinaloa (Mexico), and compare those ratios with chemical and physicochemical conditions of the water column (nutrient concentrations, temperature, salinity, chlorophyll a [Chi a] and turbidity) to evaluate the response of C. corteziensis to habitat variations on space and timescales across a subtropical gradient. Thus, our work on this sessile primary consumer provides useful information for understanding oyster ecology and the trophic dynamics of coastal lagoons in the southeastern Gulf of California.

MATERIALS AND METHODS

Study Area and Sampling

Oysters were sampled by hand from mangrove roots at 22 sites in 6 coastal lagoons in the state of Sinaloa, northwest Mexico, during the rainy season of October 2008 and the dry season of May 2009. The sampled lagoons were Santa Maria-Ohuira-Topolobampo (25[degrees]35'46" N. 109[degrees]3'22" W), San Ignacio-Navachiste-El Macapule (25[degrees]25'59" N. 108[degrees]44'30" W), Santa Maria-La Reforma (24[degrees]49'46" N, 107[degrees]58'46" W), Altata-Ensenada del Pabellon (24[degrees]32'57" N, 107[degrees]46'12" W), Ceuta (24[degrees]09'20" N, 107[degrees]10'58" W), and Urias (23[degrees]12'14" N, 106[degrees]22'10" W; Fig. 1). Groups of 25 oysters (pools) were removed from each of the 22 sampling sites along the 6 coastal lagoons. To have an equal number of pools per locality (and therefore the interpretation of data is more robust and not biased by unequal numbers), we used a simple random sample without replacement. In total, 1,100 Crassostrea corteziensis were collected (44 pools)-550 individuals for each season. Just after sampling, live oysters were cleaned and transported to the laboratory. Oysters were measured individually (total length in millimeters) and varied from 37.7-54.4 mm in total length, with a mean size of 46.2 [+ or -] 3.22 mm (SD). Total live weight (TLW) was estimated (only the wet tissue weight, in grams) and varied from 1.14-3.02 g, with a mean of 1.82 [+ or -] 0.46 g. Oysters were dissected to separate the soft tissues (visceral mass, muscle, and gills), which were first freeze-dried for 72 h (-49[degrees]C at 0.081 torr) and were then redried (55[degrees]C) to a constant weight for 48 h. The dry soft tissue weight (DSTW) was determined for the soft tissues alone and varied from 0.15-0.54 g, with a mean of 0.27 [+ or -] 0.08 g (Table 1). Last, the samples were stored in a desiccator until isotopic analyses were conducted.

Concurrent with the oyster collection, water column temperature and salinity were measured in situ with a multiprobe system (YSI 556 MPS). Water samples (3 L) were taken at each site to determine the levels of Chi a (Holm-Hansen & Riemann 1978), ammonium (Solorzano 1969), total suspended solids (American Public Health Association 1989), and nitrate/nitrite (Strickland & Parsons 1972).

Analytical Procedure

Soft tissue pool samples (n = 25) collected from each sampling site (22 sites during the rainy season and 22 sites during the dry season) were pulverized and homogenized in an automatic agate mortar. Then, 1 [+ or -] 0.1 mg of each pool sample was weighed using an OHAUS analytical scale balance (precision, [+ or -] 0.0001 g) and stored in tin capsules (8X5 mm). The [delta][sup.13]C and [delta][sup.13]N composition was determined at the Mass Spectrometry Laboratory of the Centro Interdisciplinary de Ciencias Marinas. Mexico. This determination was conducted using an elemental analyzer coupled to an isotope ratio mass spectrometer (FINNIGAN DELTA V Plus, Thermo Scientific) coupled to an elemental analyzer (Elemental Combustion System, Costech model 4010) with a precision of 0.02% [per thousand] for [delta][sup.13]C and 0.1% [per thousand] for 8I SN. The C:N ratio was calculated from the total organic carbon and total nitrogen values obtained from the elemental analyzer. The C:N ratio was used to estimate the lipid content of the tissue according to Post et al. (2007), where a C:N ratio less than 3.5 signifies a low lipid content, and had no significant influence on the [delta][sup.13]C values of the tissue (DeNiro & Epstein 1977, Monson & Hayes 1982).

Statistical Analyses

We compared the [delta][sup.13]C, [delta][sup.15]N, and C:N values of Crassostrea corteziensis within and among coastal lagoons and between seasons. Data were tested for normality (Shapiro-Wilk's test) and homogeneity of variance (Levene's test). Stable isotope and physicochemical parameter data failed these assumptions. Therefore, a nonparametric 1-way ANOVA (Kruskal-Wallis test) was used to detect significant temporal and spatial variations in isotope values and physicochemical parameters. When differences were found among coastal lagoons, we used a post hoc Dunn's test for multiple mean comparisons (Zar 1999).

Total live weight and DSTW were used as indicators of animal health. Spearman's rank correlation analyses for TLW and DSTW versus C:N values. [delta][sup.13]C, and [delta][sup.13]N were performed for each season. Statistical analyses were performed using Statistica v. 8.0 (Hill & Lewicki 2007), with significance set at P < 0.05.

RESULTS

A significant relationship was found in the dry season between DSTW and TLW (r = 0.80; Fig. 2A), but not between DSTW and total length (r = 0.12) or TLW (r = 0.48). For the rainy season, a significant relationship was observed between DSTW and TLW (r = 0.88; Fig. 2B), but not between total length and DSTW (r = 0.29) or TLW (r = 0.50). Significant differences were found only in TLW between seasons in Santa Maria-Ohuira-Topolobampo (H = 5.33), Santa Maria-La Reforma (H = 5.30), and Altata-Ensenada del Pabellon (H = 4.08). Because there were significant differences in TLW between seasons, this parameter was selected for comparison with isotopic values.

The C:N ratios of oyster soft tissues at the 6 sites ranged from 5.3-7.7 (Table 2). Significant differences were found between the dry and rainy season in San Ignacio-Navachiste-El Macapule (H = 5.33), Santa Maria-Ohuira-Topolobampo (H = 5.33), and Ceuta (H = 3.85). The comparison of the soft tissue C:N ratios between lagoons showed no differences in the rainy season (H = 5.20) and significant differences in the dry season (H = 18.99). The post hoc test showed differences between Ceuta and Urias (Dunn's test, P < 0.05).

There was a significant difference in [delta][sup.15]N values but not in [delta][sup.13]C values between seasons for all lagoons. The post hoc test showed differences between the dry and rainy seasons in Urias (H = 3.85) and Altata-Ensenada del Pabellon (H = 5.33). Oysters sampled during the rainy season were depleted in [[delta].sup.N] values compared with those sampled during the dry season (Table 2). Based on these results, 2 categories (dry and rainy) were used in subsequent analyses.

During the dry season, the [delta][sup.15]N values of soft tissue ranged from 10.7 to 13.8% [per thousand], and in [delta][sup.13]C the values ranged from -23.1% [per thousand] to 18.2% [per thousand] (Table 2). A comparison of soft tissue [delta][sup.15]N and [delta][sup.13]C values among lagoons showed significant differences for [delta][sup.15]N (H = 17.49) and [delta][sup.13]C (H = 18.16). The post hoc test showed differences between Ceuta and Santa Maria-La Reforma (Dunn's test, P < 0.05). No relationship was observed between TLW and [delta][sup.13]C (r = -0.02) or [delta][sup.15]N (r = -0.10) or between C:N and [delta][sup.13]C (r = -0.37) or [delta][sup.15]N (r = -0.10). However, a significant relationship was found between the C:N ratio and TLW (r = 0.54; Fig. 3A) and between the C:N ratio and [delta][sup.15]N (r = 0.57; Fig. 3B).

During the rainy season, the [delta][sup.15]N values of soft tissue ranged from 6.5% [per thousand] to 13.7% [per thousand], and the [delta][sup.13]C values ranged from -25.6% [per thousand] to -17.1% [per thousand] (Table 2). No differences were found among lagoons for [delta][sup.13]C (H = 8.70), but significant differences were found for [delta][sup.15]N (H = 11.85). A post hoc test showed that there were differences between Santa Maria-Ohuira-Topolobampo and Santa MarIa-La Reforma (Dunn's test, P < 0.05). A significant relationship was found between TLW and [delta][sup.13]C (r = -0.55; Fig. 3C), but no significant relationship was observed between TLW and [delta][sup.15]N (r = 0.27) or the C:N ratio (r = -0.12). In addition, no significant relationship was observed between the C:N ratio and [delta][sup.13]C (r = -0.32) or S15N (r = 0.08).

Temperature and salinity were greater in Santa Maria-Ohuira-Topolobampo and San Ignacio-Navachiste-El Macapule compared with Santa Maria-La Reforma and Altata-Ensenada del Pabellon in both seasons, but no clear trends were found for Chi a, N[H.sub.4.sup.+], [N.sub.3.sup.-], or total suspended solids (Table 3). Comparisons within each lagoon showed significant differences between seasons (Kruskal-Wallis test; Table 3). Significant differences between lagoons were found for temperature during the rainy season between Ceuta and San Ignacio-Navachiste-El Macapule (H=13.89), for salinity between Ceuta and Santa Maria-Ohuira-Topolobampo (H = 15.77), and for N[H.sub.4.sup.+] between Altata-Ensenada del Pabellon and Santa Maria-Ohuira-Topolobampo (H = 10.68).

DISCUSSION

C:N Ratios and Lipid Content

The mean C:N ratios of the soft tissue of Crassostrea corteziensis were, in general, greater than 3.5 during both seasons for all lagoons (Table 2). A correlation between a high C:N ratio and a high lipid content in the tissue has been established in several studies (e.g., Tieszen et al. 1983, Lorrain et al. 2002, Thompson et al. 2002). In addition, it is commonly accepted that the soft tissues of bivalves have a relatively high lipid content (Watanabe et al. 2005, Bodin et al. 2007), as illustrated by Marin-Leal et al. (2008), who reported C:N ratios of 4-8 in soft tissue of Crassostrea gigas.

Significant differences were found between seasons in San Ignacio-Navachiste-El Macapule, Santa Maria-Ohuira-Topolobampo and Ceuta, which may be related to reproductive activity (Marin-Leal et al. 2008). Although Crassostrea corteziensis maintains reproductive activity throughout most of the year, gonad development has been reported to occur predominately during the dry season (Hurtado et al. 2012). Peez-Osuna et al. (1993) found a variation pattern in soft tissue lipid content of C. corteziensis ranging from 9.4% during rainy season to 19.3% during the dry season. Such changes have been related to the predominance of gametogenesis during the dry season and to spawning during the rainy season, which is reflected in the total soft tissue weight and an increase in the C:N ratio.

Greater C:N ratios were detected in oysters from the Ceuta lagoon than the Urias lagoon during the dry season (Table 2), which could be associated with food availability. Previous studies found different abundances and compositions of phytoplankton among lagoons and among seasons (Guerrero-Galven et al. 1999, Ibarguen-Zamudio 2006). In addition, the same trend was observed for the concentration of Chi a between the Ceuta and Urias lagoons (Table 3). Arellano-Martinez et al. (2004) mention that Chi a is generally used as a proxy of phytoplankton biomass, and therefore the Chi a concentration, in combination with patterns of gonad development and oyster lipid content (energy reserve), provides a useful picture of the endogenous reserve mobilization in relation to food availability. Based on the high weight and C:N ratios of the oysters and the high Chi a concentration in the Ceuta lagoon, it appears that oysters from the Ceuta lagoon have a greater availability of food than those in the Urias lagoon (Table 2).

As for trophic ecology, the isotopic variability found in the oysters in the current study (Table 2) fell into the range reported for particulate organic matter and macroalgae blooms along the Sinaloa coast (PiNon-Gimate et al. 2009). Oysters are known to be able to select among different available food sources (Harris et al. 2010) and are commonly defined as opportunistic suspension feeders because of their physiological characteristics, which use a wide range of particles (including detritus) in their habitats (Hsieh et al. 2000, Dubois et al. 2007). Similar isotopic variability was observed in Crassostrea gigas (-23% [per thousand] to -21% [per thousand] for [delta][sup.13]C and 4% [per thousand] to 12% [per thousand] for [delta][sup.15]N) from Normandy, France (Marin-Leal et al. 2008), and these spatial and seasonal variations of [delta][sup.13]C and [delta][sup.15]N signatures suggest that suspended organic matter contributed to their diets in different ways among locations. Therefore, the high isotopic variability confirms that Crassostrea corteziensis is also an opportunistic filter feeder.

Temporal Variation of [delta][sup.13]C and [delta][sup.15]N in Crassostrea corteziensis

In the current study, the similar [delta][sup.13]C values recorded among the northwest Mexican lagoons during different seasons could be associated with food availability and species physiology. Marin-Leal et al. (2008) highlighted the capability of filter feeders to use internal reserves when the concentration of particles in the water is lower. The lack of significant differences between seasons may result from the high abundance of food and the fact that individuals tend to feed on and share the same overabundant prey, minimizing variations around the average isotopic signature. The northwest Mexican lagoons (especially Altata-Ensenada del Pabellon) reflect an integrated value from the entire lagoon and not from 1 particular site (Pinon-Gimate et al. 2009). Therefore, it is assumed that carbon isotopic composition is a function of the ecosystem's primary productivity (Gu et al. 1996), and the similarity in the isotopic composition between rainy and dry seasons may be the result of high food availability on the area.

In the case of C. corteziensis [delta][sup.15]N soft tissue, the temporal variation between the Urias lagoon and Altata-Ensenada del Pabellon lagoon was related to the influence of abiotic parameters, where a differential contribution of N[H.sub.4.sup.+] and N[O.sub.3.sup.-] was observed during the two seasons (Table 3). Marin-Leal et al. (2008) found a similar behavior for C. gigas, where dissolved nitrogen concentrations were related to greater [delta][sup.15]N values during spring and summer due to the proliferation of benthic microalgae and accumulation of macroalgal detritus on the surface sediments. The high [delta][sup.13]C and especially [delta][sup.15]N values may be caused by an elevated load of nutrients from anthropogenic discharges (Ruiz-Fernandez et al. 2003, Pinon-Gimate et al. 2009, Paez-Osuna et al. 2013), which is discussed below.

Spatial Variation of [delta][sup.13]C and [delta][sup.15] N in Crassostrea corteziensis

Several studies have shown that physical, chemical, and biological processes have a strong influence on the isotopic composition of different ecosystem compartments variation (Hobson & Clark 1992, McCutchan et al. 2003, Vanderklift & Ponsard 2003, Sweeting et al. 2007). The differences found between Santa Maria--La Reforma and Santa Maria-Ohuira-Topolobampo lagoons during the rainy season in the [delta][sup.15]N values may be more linked to processes occurring at the dissolved inorganic nitrogen (DIN) level (Sherwood & Rose 2005). Enrichment in [sup.15]N in the available DIN pool can be a result of (1) recycling of nitrogen, particularly from higher trophic levels, which leads to a pool of ammonia enriched in [sup.15]N, which is then assimilated and reflected in the local food chain, and (2) discharge of anthropogenic waste enriched in [sup.15]N and transported by river runoff, which can generate coastal primary production with a high [delta][sup.15]N signature (Chouvelon et al. 2012).

Last, there were significant differences in [delta][sup.15]N and [delta][sup.13]C between Santa Maria-La Reforma and Ceuta during the dry season. We observed values of [delta][sup.15]N ranging from 10[per thousand] to 12[per thousand] and for [delta][sup.13]C of approximately -20[per thousand] (-22[per thousand], except for the Ceuta lagoon). In the case of [delta][sup.15]N, there is a correlation between this isotope and N[H.sub.4.sup.+] concentrations. Chemically fixed or reactive nitrogen compounds, such as nitrate and ammonium, serve as the principal sources of nitrogen to sustain biological processes and is 1 of the major nutrients required by phytoplankton. In the case of estuarine systems, where ammonium can be abundant, its [delta][sup.15]N level is often high (commonly, >10[per thousand]). [delta][sup.15]N increases as the ammonium concentration decreases along transects from riverine to marine waters as a result of the discrimination associated with ammonium consumption by nitrification and/or ammonium assimilation (Sigman et al. 2009). Thus, these [delta][sup.15]N signatures may be caused by anthropogenic impacts because the values for human and animal waste nitrate are approximately 4[per thousand] to 12[per thousand] (Aravena et al. 1993, Ruiz-Fernandez et al. 2003).

Typical [delta][sup.13]C values of phytoplankton are close to -21[per thousand] (Gearing et al. 1984), which is actively consumed by Crassostrea corteziensis. The exception is the Santa Maria-La Reforma lagoon, where values of -19[per thousand] are associated with other organic matter sources or pollution. The Santa Maria-La Reforma lagoon receives the municipal discharge of the Culiacan River, which, as a result of its load of contaminants, has been reported to affect the estuarine zone (Paez-Osuna et al. 2013). Therefore, although the [delta][sup.15]N level of the DIN was not evaluated in the current study, our results confirm the use of [delta][sup.13]C and [delta][sup.15]N signals in suspension feeders to monitor processes that occur along the estuarine gradient, as has been reported in other regions (Hughes & Sherr 1983, Riera & Richard 1996, Deegan & Garritt 1997).

ACKNOWLEDGMENTS

We thank the following organizations: Programa de Becas Posdoctorales en la UNAM, Instituto de Ciencias del Mar y Limnologia (ICMyL), Universidad Nacional Autonoma de Mexico (UNAM), PAPI1T 1N208813 project. IPN, CONACYT, PIFI, EDI, and COFAA-IPN for the academic and financial support. Partial support was received from the project CONACYT 204818 of INFR-2013-01 del Programa de Apoyo a Proyectos de Investigacion e Innovacion Tecnologica.

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YASSIR EDEN TORRES-ROJAS, (1) * FEDERICO PEEZ OSUNA, (1) MAGDALENA BERGES TIZNADO, (1) JAIME CAMALICH CARPIZO (2) AND SERGIO AGUINIGA GARCIA (2)

(1) Instituto de Ciencias del Mar y Limnologia, Universidad Nacional Autonoma de Mexico, Joel Montes Camarena s/n, Apartado Postal 811, C.P. 82040, Mazatlen, Sin., Mexico; (2) Centro Inter disciplinario de Ciencias Marinas, Instituto Politecnico Nacional, IPN s/n Col, Playa Palo de Santa Rita, La Paz, B.C.S. C.P. 23096, MExico

* Corresponding author. E-mail: yassirtorres@gmail.com

DOI: 10.2983/035.033.0211

TABLE 1.

Crassostrea corteziensis length and weight (mean [+ or -]
SD) along the northwest of Mexico (n = number of pools [each
pool comprised 25 individuals)).

Location           Code   Season   n       Length (mm)

Santa Maria-       SMOT   Rainy    4   43.12 [+ or -] 3.88
  Ohuira-                 Dry      4   48.49 [+ or -] 1.52
  Topolobampo
San Ignacio-       SINM   Rainy    4   45.71 [+ or -] 2.29
  Navachiste-             Dry      4   49.34 [+ or -] 0.58
  El Macapule
Santa Maria-La     SMLR   Rainy    4   45.19 [+ or -] 1.18
  Reforma                 Dry      4   47.73 [+ or -] 6.08
Altata-Ensenada    AEP    Rainy    4   42.45 [+ or -] 3.05
  del Pabellon            Dry      4   46.84 [+ or -] 2.65
Ceuta              C      Rainy    3   45.42 [+ or -] 1.12
                          Dry      3   49.45 [+ or -] 1.54
Urias              U      Rainy    3   46.60 [+ or -] 2.42
                          Dry      3   47.84 [+ or -] 1.19

                   Total soft tissue     Dry soft tissue
Location               weight (g)           weight (g)

Santa Maria-       1.60 [+ or -] 0.28   0.26 [+ or -] 0.04
  Ohuira-          2.72 [+ or -] 0.25   0.43 [+ or -] 0.09
  Topolobampo
San Ignacio-       1.70 [+ or -] 0.37   0.29 [+ or -] 0.07
  Navachiste-      2.11 [+ or -] 0.31   0.29 [+ or -] 0.10
  El Macapule
Santa Maria-La     1.36 [+ or -] 0.15   0.24 [+ or -] 0.03
  Reforma          1.93 [+ or -] 0.11   0.25 [+ or -] 0.02
Altata-Ensenada    1.36 [+ or -] 0.15   0.24 [+ or -] 0.03
  del Pabellon     1.84 [+ or -] 0.23   0.22 [+ or -] 0.05
Ceuta              1.67 [+ or -] 0.25   0.27 [+ or -] 0.05
                   2.13 [+ or -] 0.78   0.34 [+ or -] 0.16
Urias              1.72 [+ or -] 0.16   0.22 [+ or -] 0.01
                   1.86 [+ or -] 0.06   0.21 [+ or -] 0.02

TABLE 2.

Isotopic carbon and nitrogen ratios, and elemental C/N
ratios of soft tissues (mean [+ or -] SD) along the northwest of
Mexico (n = number of pools [each pool comprised 25
individuals]).

                                             [delta]
Location           CODE   Season   n      [sup.15]N (%)

Santa Maria-       SMOT   Rainy    4   12.55 [+ or -] 0.90
  Ohuira-                 Dry      4   12.45 [+ or -] 0.05
  Topolobampo
San Ignacio-       SINM   Rainy    4   11.88 [+ or -] 1.21
  Navachiste-             Dry      4   12.94 [+ or -] 0.04
  El Macapule
Santa Maria-       SMLR   Rainy    4   10.13 [+ or -] 1.72
  La Reforma              Dry      4   10.80 [+ or -] 0.10
Altata-Ensenada    AEP    Rainy    4   11.11 [+ or -] 0.25
  del Pabellon            Dry      4   12.51 [+ or -] 0.85
Ceuta              C      Rainy    3   12.27 [+ or -] 1.11
                          Dry      3   13.16 [+ or -] 0.09
Urias              U      Rainy    3   10.47 [+ or -] 1.42
                          Dry      3   11.73 [+ or -] 0.03

                         [delta]
                        [sup.15]N                CrN/
Location             ([per thousand])          [micro]g

Santa Maria-       -19.79 [+ or -] 2.48   5.84 [+ or -] 0.06
  Ohuira-          -19.50 [+ or -] 0.10   6.79 [+ or -] 0.07
  Topolobampo
San Ignacio-       -20.50 [+ or -] 0.86   5.92 [+ or -] 0.31
  Navachiste-      -20.85 [+ or -] 0.13   6.62 [+ or -] 0.06
  El Macapule
Santa Maria-       -19.47 [+ or -] 2.40   5.73 [+ or -] 0.40
  La Reforma       -19.14 [+ or -] 0.18   6.12 [+ or -] 0.12
Altata-Ensenada    -19.74 [+ or -] 0.71   5.85 [+ or -] 0.42
  del Pabellon     -19.26 [+ or -] 0.72   6.01 [+ or -] 0.38
Ceuta              -22.27 [+ or -] 0.94   5.99 [+ or -] 0.34
                   -21.04 [+ or -] 0.05   7.64 [+ or -] 0.10
Urias              -21.80 [+ or -] 3.64   5.59 [+ or -] 0.25
                   -20.69 [+ or -] 0.13   5.57 [+ or -] 0.03

TABLE 3.

Environmental parameters (mean [+ or -] SD) for each site
along the northwest  of Mexico between October 2008 and May
2009.

                                     Temperature
Location        Code   Season       ([degrees]C)

Santa Maria-    SMOT   Rainy      32.2 [+ or -] 0.7
Ohuira-                Dry             32.7 *
Topolobampo

San Ignacio-    SINM   Rainy      32.4 [+ or -] 0.6
Navachiste-El          Dry             32.8 *
Macapule

Santa Maria-    SMLR   Rainy    30.3 [+ or -] 0.7 (b)
La Reforma             Dry      30.7 [+ or -] 0.8 (a)

Altata-         AEP    Rainy    29.4 [+ or -] 0.5 (b)
Ensenada               Dry      29.7 [+ or -] 1.4 (a)
del Pabellon

Ceuta            C     Rainy    28.1 [+ or -] 0.8 (a)
                       Dry      28.5 [+ or -] 1.4 (a)

Urias            u     Rainy    31.3 [+ or -] 1.5 (a)
                       Dry      30.0 [+ or -] 0.3 (a)

                      Salinity              Chlorophyll
Location                (psu)                a (mg/[m.sup.3])

Santa Maria-    38.9 [+ or -] l.l (b)   1.6 [+ or -] 2.3h
Ohuira-         37.7 [+ or -] 1.6 (a)   1.2 [+ or -] 1.3 (a)
Topolobampo

San Ignacio-    37.2 [+ or -] 1.0       0.2 [+ or -] 0.9
Navachiste-El   36.6 [+ or -] 2.3       0.7 [+ or -] 0.5
Macapule

Santa Maria-    34.7 [+ or -] 0.8       0.4 [+ or -] 0.9 (b)
La Reforma      35.1 [+ or -] 1.8       0.8 [+ or -] 1.2 (a)

Altata-         32.2 [+ or -] 1.9       1.7 [+ or -] 2.0 (b)
Ensenada        32.8 [+ or -] 0.9       4.2 [+ or -] 2.4 (a)
del Pabellon

Ceuta           26.2 [+ or -] 6.8 (b)   1.4 [+ or -] 1.2
                35.6 [+ or -] 8.4 (a)   2.8 [+ or -] 1.9

Urias           32.8 [+ or -] 2.6 (b)   1.1 [+ or -] 1.0
                39.0 [+ or -] 0.5 (a)   1.1 [+ or -] 0.9

                   Total suspended
                        solids             N[H.sub.4.sup.+]/
  Location              (mg/L)                /([micro]M)

Santa Maria-    13.1 [+ or -] 28.6 (b)   22.8 [+ or -] 10.1 (b)
   Ohuira-      12.0 [+ or -] 25.0 (a)    8.6 [+ or -] 5.5 (a)
 Topolobampo

San Ignacio-      29.4 [+ or -] 75.8       9.7 [+ or -] 13.6
Navachiste-El     28.0 [+ or -] 50.8        4.6 [+ or -] 4.9
  Macapule

Santa Maria-    35.5 [+ or -] 27.l (b)    6.6 [+ or -] 2.0 (b)
 La Reforma     19.5 [+ or -] 12.3 (a)   6.8 [+ or -] 11.8 (a)

   Altata-        32.5 [+ or -] 19.7      1.6 [+ or -] 0.3 (b)
  Ensenada        29.4 [+ or -] 20.1     6.2 [+ or -] 10.8 (a)
del Pabellon

    Ceuta       49.2 [+ or -] 42.6 (b)     10.2 [+ or -] 8.4
                8.1 [+ or -] 26.4 (a)       8.1 [+ or -] 7.7

    Urias         23.0 [+ or -] 19.5       10.9 [+ or -] 6.0
                  22.8 [+ or -] 19.2       11.9 [+ or -] 3.2

                 N[H.sub.3.sup.+]/
Location            /([micro]M)

Santa Maria-      1.0 [+ or -] 0.2
Ohuira-           1.0 [+ or -] 0.4
Topolobampo

San Ignacio-      0.9 [+ or -] 1.0
Navachiste-El     0.9 [+ or -] 0.4
Macapule

Santa Maria-      1.4 [+ or -] 0.9
La Reforma        1.5 [+ or -] 0.4

Altata-         0.3 [+ or -] 0.2 (b)
Ensenada        1.3 [+ or -] 0.4 (a)
del Pabellon

Ceuta           7.1 [+ or -] 8.7 (b)
                1.0 [+ or -] 8.1 (a)

Urias             1.0 [+ or -] 0.4
                  2.4 [+ or -] 1.0

Differences among sites were tested for significance using
the Kruskal-Wallis test at P < 0.05. Means within each
column for each lagoon with different superscripts are
significantly different at P < 0.05. * Only one data point.
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Author:Torres-Rojas, Yassir Eden; Osuna, Federico Peez; Tiznado, Magdalena Berges; Carpizo, Jaime Camalich;
Publication:Journal of Shellfish Research
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Geographic Code:1MEX
Date:Aug 1, 2014
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