Seasonal variations in gross biochemical composition, percent edibility, and condition index of the clam Ruditapes decussatus cultivated in the Ria Formosa (South Portugal).
KEY WORDS: biochemical composition, condition index, percent edibility, Ria Formosa, Ruditapes decussatus, seasonal variations, grooved carpet clam
The grooved carpet shell clam Ruditapes decussatus (L. 1758) is one of the most popular and profitable molluscs of lagoon and coastal sites in the Mediterranean, having been used as a food source for centuries. Between 1996 and 2008, official statistics suggested an average pooled catch of 4 mt in Portugal, Spain, France, Ireland, and Tunisia (FAO 2010). In Portugal, the harvesting of bivalves--in particular, R. decussates--is central to aquaculture revenue. In 2007, the national annual production reported for this species reached 2 mt, representing 27% of total seafood cultured in Portugal, of which approximately 90% originated in the Ria Formosa (INE 2007). Here, clams are grown ("farmed") in plots exploited by clam farmers, locally known as "mariscadores," usually organized in professional associations. Clam farming involves seeding juveniles collected from natural beds into plots maintained in tidal flats and harvesting commercial-size animals (i.e., >20 mm). The culture of R. decussatus in the Ria Formosa is central to the local socioeconomic framework involving, directly or indirectly, more than 4,500 people (INE 2007). In 1996, there were 1,587 licensed clam farming plots in the intertidal area of the Ria Formosa, covering a total of 0.47 x[10.sup.6] [m.sup.2] (Cachola 1996), approximately 1% of the total intertidal area of the lagoon. More recently, the ICNB (2004) confirmed the existence of 1,290 plots in the Ria Formosa, a decrease in numbers but a 10-fold increase in the occupied intertidal area (about 4.76 x[10.sup.6] [m.sup.2]). In addition to the official catch figures, widespread illegal and largely opportunistic fishing and harvesting by elements foreign to the local associative system most likely doubles the official production estimates (Ant6nio Laboratory6ia, VIVMAR, pers. comm.).
Percent edibility (i.e., meat content/yield), physiological condition, and biochemical composition of bivalves vary seasonally with latitude and are strongly related to water temperature, food availability, and the gametogenic cycle (Beninger & Lucas 1984, Karakoltsidis et al. 1995, Okumus & Stirling 1998, Orban et al. 2002, Delgado et al. 2004, Ojea et al. 2004, Orban et al. 2006). Proteins, lipids, carbohydrates and minerals are major contributors to the nutritional value and organoleptic properties of clams (Orban et al. 2006), and justify the very high demand for this product in national and international markets. In R. decussatus, both stored and recently assimilated nutrients are used for gametogenesis (Perez-Camacho et al. 2003), characteristic of an intermediate strategy between opportunistic and conservative lifestyles (Rodriguez-Moscoso & Arnaiz 1998). During the reproductive cycle of this species, gametogenesis extends from the end of winter and spring; spawning occurs throughout the summer months, and a resting period occurs in autumn and early winter (Rodriguez-Moscoso & Arnaiz 1998).
Percent edibility or the condition index (CI) have long been used for biological and commercial purposes (Venkataraman & Chari 1951, Baird 1958). These are closely related to the gametogenic and nutrient reserve storage-consumption cycles, and thus to meat quality (Gabbott 1975). In industrial settings, CI has been adopted in international trade as a standard criterion to select the best product. It is also recognized as a useful biomarker reflecting the ability of bivalves to withstand adverse natural and/or anthropogenic stress (Mann 1978, Bressan & Marin 1985, Fernandez-Castro & de Vido de Mattio 1987). Hence, the CI may be considered a measure of "fatness" and "marketability" of a commercially exploited species and, together with proximate biochemical composition, is probably the most practical and simple method of monitoring gametogenic activity (Okumus & Stifling 1998).
To understand the seasonality of R. decussatus nutritional value, thus providing an improved basis for its economic valuation, this study aimed to investigate the changes in grooved carpet shell clam gross biochemical composition in the Ria Formosa (southern Portugal). Moisture, ash, protein, total and nonprotein nitrogen, carbohydrates, and lipid contents, as well as percent edibility and CI were assessed with monthly periodicity for 1 y.
MATERIALS AND METHODS
Environmental Data, Sampling, and Processing
The study was carried out between January and December 2006. Monthly average air temperature and precipitation recorded at a meteorological station (Faro International Airport) in the Ria Formosa were used to assess seasonality in climatic conditions. Samples of R. decussatus clams (~1 kg, about 140 individuals) were obtained directly from a farmer's plot belonging to VIVMAR Association on a monthly basis. This ensured that all tested biological material was of commercial value and was harvested from the same area of the Ria Formosa. Immediately after harvest, the samples were transported to the laboratory in a refrigerated box, washed, and placed in prefiltered (GF/C, Whatman Int. Ltd., UK) seawater for 3-4 h to purge pseudo feces and stomach content. Thirty individuals were then randomly selected for biometric measurements and for the determination of the percent edibility and CI. The remaining clams were stored at -20[degrees]C for later biochemical composition analysis.
Biometric Parameters, Percentage Edibility, and CI
Individual clams were weighed ([+ or -] 0.1 mg) and their maximum length measured using a precision caliper (to 0.05 mm). Clams were manually shucked by cutting the adductor muscle with a knife, and the meat was pressed with blotting paper to remove excess moisture before weighting. The meat and shells were subsequently dried at 105[degrees]C for 24 h and weighed again.
Percent edibility was calculated as
PE = (MWW/TW) x 100,
where PE is percent edibility, MWW is meat wet weight (measured in grams), and TW is the total clam weight including the shell (measured in grams) (Venkataraman & Chari 1951, Mohite et al. 2009). CI was calculated as
CI - (MDW/SDW) x 1,000,
where MDW is meat dry weight (measured in grams) and SDW is the shell dry weight (measured in grams), following Lucas and Beninger (1985) and Orban et al. (2006).
Moisture and ash content of clams was determined for 30 individuals using the AOAC (2005) methods (Refs. 950.46 and 938.08, respectively). Total nitrogen (bulk protein content) was determined using the Kjeldahl method (Ref. 955.04 (AOAC 2005)). This was also used to determine nonprotein nitrogen content after precipitation of proteins with 10% (w/v) trichloroacetic acid. Net protein content was calculated as the difference between total nitrogen and nonprotein nitrogen multiplied by 6.25, the conversion factor used for meat and meat products (Pearson 1973). Carbohydrate and total lipids were determined according to Dubois et al. (1956) and Bligh and Dyer (1959), respectively. Biochemical analyses were carried out individually on 9 randomly selected clams.
Initially, l-way analysis ofcovariance was used to test whether putative seasonal variations (month) in the biological traits (response variables) covaried with individual size (length). Because no significant effects of length on biochemical composition were found (Table 1), 1-way analysis of variance and the Tukey honestly significant difference test were carried out to uncover any significant seasonal changes in biochemical composition, condition, or edibility. The lipid content values were log-transformed to correct for (severe) non-normality. In addition, relationships between monthly data on biochemical composition, CI, and edibility were investigated using Spearman's rank correlation coefficient. All statistical procedures were carried out at the 0.05 level of significance using R (R Development Core Team 2007).
Monthly average air temperature and precipitation for the Ria Formosa are illustrated in Figure 1. Higher temperatures were observed in summer (25[degrees]C in July and August) and the lowest in winter (<9[degrees]C). Monthly precipitation records showed an extreme value in November with 252 mm, which was much higher than the range observed throughout the rest of the year (15-40 mm).
[FIGURE 1 OMITTED]
Biochemical composition (Fig. 2), percent edibility, and CI (Fig. 3) varied with the season (Table 2). Average monthly moisture contents were significantly higher (P < 0.05) during autumn and winter (85.9% in March and 86.9% in November) than in June (82.6%). On the other hand, ash (which indicates the inorganic compounds content) was significantly higher (P < 0.05) during January and February (3.4% and 3.6%) compared with the rest of the year. Between March and August, a second period of intermediate values (~3.1%) was observed. From August to November, the clams had the lowest values of ash content (about 2.8%).
The carbohydrate content varied widely from 0.4% in January and July to 2.6% in September. Average log-transformed lipid content showed no significant seasonal variation despite the large variability on a monthly basis. The lowest lipid content was measured in April (0.07%) and the lowest total nitrogen content was measured between October and November (~1.2%). In contrast, total nitrogen content was significantly higher in June, August, and September (~1.5%). Despite null values of nonprotein nitrogen found in May and July, the total and nonprotein nitrogen contents evidenced complementary seasonal trends. The resulting protein content was significantly higher (P < 0.05) during early summer, averaging 8.5% from May to July, in contrast to winter values, which ranged from 5.9% in December to 6.7% in January.
Percent edibility of clams was significantly lower (P < 0.05) in January and February (-24%) compared with the April/June or October/December trimesters (30 32%). On the other hand, the CI of the clams was significantly higher (P < 0.05) from April to June (98.6-107.2) than from July to December, when intermediate values of 83.4-88.2 were recorded. Clams showed the lowest CIs (<77.2) in January and March.
[FIGURE 2 OMITTED]
Few pairwise correlation coefficients (Table 3) were judged to be significant (P < 0.05). Temperature and/or precipitation were associated with ash, total nitrogen and/or protein content, and CI. Moreover, CI and percent edibility were intercorrelated and associated with protein content and nonprotein nitrogen content.
[FIGURE 3 OMITTED]
Temperature and food availability have been considered the main factors conditioning the growth and hence production in bivalves. The effect of these variables is complex and depends on species-specific acquisition and expenditure of energy in the natural environment (Bayne & Newell 1983). In temperate tidal lagoons with considerable open-sea water exchanges and high primary production (e.g., Sufa Lagoon in Turkey or the Ria Formosa in Portugal), the food supply is not considered a limiting factor for growth and reproduction of bivalves (Serdar & Lok 2009), which feed mainly on microalgae (Delgado & Perez-Camacho 2005). Consequently, temperature is the key factor controlling the reproductive cycle of R. decussatus (Urrutia et al. 1999, Delgado & Parez-Camacho 2007, Matias et al. 2009), influencing seasonal biochemical composition and nutritional conditions (Gozler & Tarkan 2000, Perez-Camacho et al. 2003, Fernandez-Reiriz et al. 2007).
Seasonal biochemical composition followed the changes in percent edibility and CI, which indirectly reflect R. decussatus reproductive phases (Gozler & Tarkan 2000, Mohite et al. 2009). From January until June, the increasing temperatures induce gametogenesis (Delgado & Perez-Camacho 2007), resulting in an increase in percent edibility and CI. During this period, R. decussatus accumulated and used carbohydrates, lipids, proteins, and minerals, presumably for gonad development. The sudden decrease in all these parameters, which occurred between June and July, most likely coincided with spawning, and the phase may have lasted until September, when the species entered the resting phase.
Our results compare well with studies on the seasonality of clam physiology at other latitudes, including the Galician Rias in northwest Spain (Ojea et al. 2004), the Lagoon of Venice in Italy (Matin et al. 2003), Sufa and Cordak lagoons in Turkey (Gozler & Tarkan 2000, Serdar & L6k 2009), and Atlantic coast of Morocco (Shafee & Daoudi 1991), despite the differences in methodology. Overall, carbohydrates and lipids show complementary trends, with carbohydrates (and moisture levels) reaching minima during the summer, when lipid and protein content peaked. In addition, all previously mentioned study sites sustain similar seasonal trends of CIs, with small latitudinal changes. The more southern the location, the sooner gametogenesis, ripping, and spawning occur (Meneghetti et al. 2004), with spawning starting in August in northwest Spain (Perez-Camacho et al. 2003), in June/July in south Portugal, and in May in Morocco (Shafee & Daoudi 1991).
In the Ria Formosa, total nitrogen, nonprotein nitrogen, and thus protein contents show that the nitrogen metabolism in R. decussatus varies on a monthly basis. However, the lower nonprotein nitrogen registered during the summer, suggests that the majority of the clam nitrogen metabolism is being channeled to the spawning process during that period (Marin et al. 2003). Although the glycogen content is the parameter most often linked to seasonal variation in clam carbohydrate levels, direct determination of total carbohydrates not only allows the evaluation of the same type of seasonal changes, but also adds all the other types of mono- and polysaccharides involved in the clam's life cycle, thus becoming a more integrative parameter. In fact, the seasonal variation of glycogen and carbohydrates is strongly correlated, with the former being responsible for approximately 50% of the variance of the latter (Robert et al. 1993, Serdar & Lok 2009). In autumn and early winter, R. decussatus accumulates glycogen prior to gametogenesis, before it is used as an energy source for gonad development, in anticipation of the spawning period taking place during the summer (Ojea et al. 2004).
Lipids are the biomolecules that are more influenced by the clams" annual reproductive cycle because of their relationship with gonad maturation. The large variability of lipid content, evidenced by the SDs, may be related to the differential gender-related sexual dynamics of this species (Perez-Camacho et al. 2003). The link between the lipid and carbohydrate contents may thus be rooted in the assumption that many lipids accumulated by clams are sourced from glycogen reserves (Marinet al. 2003). This metabolic relationship underpins the opposite trends observed between the seasonal variations of these 2 parameters observed in the current study. This was particularly evident in July and August. During the remainder of the year, the clams attempt to accumulate lipid reserves through food ingestion in preparation for the next reproductive cycle (Marin et al. 2003).
Seasonal variations in the nutritional value can also be accessed, in a more global approach, using meat yield-related indices. In the Ria Formosa, the physiological condition of R. decussatus is higher between April and June, and lower during the rest of the year. Taking into account the physiological condition of the species and its nutritional value, in terms of protein content, the best period of the year to consume R. decussatus would be summer. However, this same period is understood to be the worst to do so from a toxicological point of view, because of the increased risk of poisoning by shellfish toxins (Vale & Sampayo 2002). In summer, consumers should exercise particular care when buying these bivalves, and always make sure to acquire depurated and certified products (Vale et al. 2008). On the other hand, the demand for R. decussatus and, consequently, its market value are also very high during the Christmas season. The product's "health threat" is not an issue at this time of the year (Vale & Sampayo 2003), but its physiological condition is at its worst, leading to a discrepancy between the nutritional value and the demand for this product, similarly to the case of R. philippinarum in the Lagoon of Venice in Italy (Marin et al. 2003).
The clam R. decussatus is an important natural resource and food product in the Ria Formosa, and its exploitation sustains an significant part of the local economy. Analysis of R. decussatus percent edibility and CIs allowed inference of its reproductive cycle: Gametogenesis started in January, spawning took place from June to September, and the resting stage occurred between October and December. The high seasonal variability observed in the biochemical composition of this species was most likely a result of the reproductive cycle, and it showed typical features of the life history of bivalve molluscs at temperate latitudes. Similarly to mariculture populations in Galicia (Spain), Lagoon of Venice (Italy), Turkey, and Morocco, the peak in nutritional value is observed during the summer, whereas the slump occurs during winter. Curiously, these two periods coincide with the peak of major commercial demand.
We thank Vera Francisco, Ana Sofia Viegas, and Andreia Geraldes for their contribution in laboratory processing of samples. We dedicate this work to the memory of Antonio Laboia, President of VIVMAR, a regional clam farmers association, who recently passed away. Work was funded in part by the project O-DOIS--Oxygen Dynamics coupled with Organic Carbon Mineralization in Intertidal Sandflats: Role of Porewater Advection (POCTI/CTA/47078/2002).
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* Corresponding author. E-mail: email@example.com
JAIME ANIBAL, (1) *. EDUARDO ESTEVES (2) AND CARLOS ROCHA (3)
(1) CIMA-Centro de Investigacao Marinha e Ambiental, Universidade do Algarve, Instituto Superior de Engenharia, Campus da Penha, 8005-139 Faro, Portugal, (2) Centro de Ciencias do Mar CCMar AlgarveCIMAR Laborat6rio Associado and Universidade do Algarve, Instituto Superior de Engenharia, Campus da Penha, 8005-139 Faro, Portugal; 3School of Natural Sciences, Trinity College Dublin, College Green, Dublin 2, Ireland
TABLE 1. Results of analyses of covariance per parameter studied in R. decussates from the Ria Formosa (South Portugal). Parameter Factor df SS MS Moisture Month 11 558.61 50.78 Length 1 0.18 0.18 Month X length 11 16.74 1.52 Residuals 335 396.44 1.18 Ash Month 11 19.70 1.79 Length 1 0.07 0.07 Month x length 11 1.05 0.10 Residuals 336 39.82 0.12 Carbohydrates Month 11 45.98 4.18 Length 1 0.25 0.25 Month X length 11 0.93 0.09 Residuals 83 11.51 0.14 Logio(lipids) Month 11 10.88 0.99 Length 1 0.47 0.47 Month X length 10 2.33 0.23 Residuals 27 6.20 0.23 Total nitrogen Month 11 1.18 0.11 Length 1 0.00 0.00 Month x length 11 0.34 0.03 Residuals 81 1.67 0.02 Nonprotein nitrogen Month 11 0.77 0.07 Length 1 0.00 0.00 Month x length 11 0.15 0.01 Residuals 82 0.72 0.01 Proteins Month 11 76.64 6.97 Length 1 0.30 0.30 Month X length 11 16.44 1.49 Residuals 80 96.73 1.21 Condition index Month 11 35,064 3,188 Length 1 19 19 Month X length 11 1,562 142 Residuals 335 53,717 160 Percent edibility Month 11 2,451.8 222.9 Length 1 24.7 24.7 Month x length 11 102.9 9.4 Residuals 335 3,563.1 10.6 Parameter Factor F Value P Value Moisture Month 42.91 [<10.sup.-6] Length 0.15 0.6945 Month X length 1.29 0.2308 Residuals Ash Month 15.11 [<10.sup.-6] Length 0.57 0.4526 Month x length 0.81 0.6317 Residuals Carbohydrates Month 30.14 [<10.sup.-6] Length 1.78 0.1857 Month X length 0.61 0.8153 Residuals Logio(lipids) Month 4.31 0.0010 Length 2.06 0.1625 Month X length 1.01 0.4569 Residuals Total nitrogen Month 5.20 [<10.sup.-5] Length 0.15 0.7021 Month x length 1.51 0.1435 Residuals Nonprotein nitrogen Month 8.04 [<10.sup.-6] Length 0.03 0.8742 Month x length 1.57 0.1234 Residuals Proteins Month 5.76 [<10.sup.-6] Length 0.25 0.6211 Month X length 1.24 0.2777 Residuals Condition index Month 19.88 [<10.sup.-6] Length 0.12 0.7284 Month X length 0.89 0.5549 Residuals Percent edibility Month 20.96 [<10.sup.-6] Length 2.32 0.1285 Month x length 0.88 0.5605 Residuals MS, mean squares; SS, sum of squares. TABLE 2. Biochemical composition, condition index, and percent edibility of R. decussatus from Ria Formosa: seasonal variation (mean [+ or -] SD) for monthly samples of n individuals. Month (2006) Parameter n January Moisture 30 85.96 [+ or -] 0.25 (de) Ash 30 3.42 [+ or -] 0.58 (ef) Carbohydrates 9 0.38 [+ or -] 0.13 (ab) Lipids * 3 2.25 [+ or -] 3.57 (b) Total nitrogen 9 1.31 [+ or -] 0.11 (a-d) Nonprotein 9 0.25 [+ or -] 0.03 (b) nitrogen Proteins 9 6.67 [+ or -] 0.77 (ab) Condition 30 72.80 [+ or -] 17.24 (de) index Percent 30 24.4 [+ or -] 3.69 edibility Month (2006) Parameter February March Moisture 83.84 [+ or -] 2.10 (bc) 85.87 [+ or -] 1.05 (d) Ash 3.59 [+ or -] 0.51 (f) 2.99 [+ or -] 0.28 (a-d) Carbohydrates 1.44 [+ or -] 0.81 (de) 0.84 [+ or -] 0.26 (ab) Lipids * 1.71 [+ or -] 1.84 (b) 0.20 [+ or -] 2.38 (a) Total nitrogen 1.37 [+ or -] 0.12 (a-d) 1.28 [+ or -] 0.07 (abc) Nonprotein 0.23 [+ or -] 0.05 (b) 0.15 [+ or -] 0.12 (ab) nitrogen Proteins 7.13 [+ or -] 0.64 (abc) 7.11 [+ or -] 0.83 (abc) Condition 73.37 [+ or -] 8.98 (bc) 77.17 [+ or -] 16.13 (d) index Percent 24.0 [+ or -] 5.5 (fg) 27.0 [+ or -] 3.9 (abc) edibility Month (2006) Parameter April May Moisture 83.96 [+ or -] 0.84 (bc) 83.59 [+ or -] 0.85 (b) Ash 3.11 [+ or -] 0.42 (cd) 3.10 [+ or -] 0.28 (bcd) Carbohydrates 0.69 0.13 (ab) 0.79 [+ or -] 0.18 (ab) Lipids * 0.07 [+ or -] 5.71 (a) 1.22 [+ or -] 10.13 (ab) Total nitrogen 1.39 [+ or -] 0.17 (a-c) 1.35 [+ or -] 0.20 (a-d) Nonprotein 0.17 [+ or -] 0.17 (b) 0.00 [+ or -] 0.00 (a) nitrogen Proteins 7.63 [+ or -] 1.41 (abc) 8.48 [+ or -] 1.24 (bc) Condition 98.34 [+ or -] 13.52 (bc) 98.56 [+ or -] 12.83 (b) index Percent 30.6 [+ or -] 2.7 (ab) 31.9 [+ or -] 2.3 (b-e) edibility Month (2006) Parameter June July Moisture 82.55 [+ or -] 1.54 (a) 84.51 [+ or -] 1.26 b, Ash 3.21 [+ or -] 0.25 (de) 3.05 [+ or -] 0.356[degrees]d Carbohydrates 1.91 [+ or -] 0.24 (e) 0.38 [+ or -] 0.21' Lipids * 0.53 [+ or -] 1.53 (ab) 0.87 [+ or -] 2.25,b Total nitrogen 1.52 [+ or -] 0.22 (d) 1.37 [+ or -] 0.14'-'' Nonprotein 0.13 [+ or -] 0.15 (ab) 0.00 [+ or -] 0.00, nitrogen Proteins 8.66 [+ or -] 1.56 (c) 8.52 [+ or -] 0.87 b' Condition 107.21 [+ or -] 16.89 (a) 86.40 [+ or -] 9.92 b, index Percent 32.1 [+ or -] 4.0 (c-f) 28.3 [+ or -] 3.69 edibility Month (2006) Parameter August September Moisture 84.61 [+ or -] 1.2l (bc) 84.43 [+ or -] 0.83 (bc) Ash 2.83 [+ or -] 0.08 (ab) 2.89 [+ or -] 0.09 (abc) Carbohydrates 1.47 [+ or -] 0.42 (de) 2.62 [+ or -] 0.28 (f) Lipids * 0.72 [+ or -] 1.09 (ab) 1.23 [+ or -] 4.36 (ab) Total nitrogen 1.47 [+ or -] 0.11 (cd) 1.44 [+ or -] 0.18 (bcd) Nonprotein 0.27 [+ or -] 0.1l (b) 0.22 [+ or -] 0.09 (b) nitrogen Proteins 7.47 [+ or -] 1.17 (abc) 7.60 [+ or -] 1.44 (abc) Condition 85.43 [+ or -] 7.70 (c) 88.19 [+ or -] 9.98 (bc) index Percent 26.5 [+ or -] 2.l (a) 27.2 [+ or -] 2.5 (efg) edibility Month (2006) Parameter October November Moisture 86.37 [+ or -] 0.64 (de) 86.85 [+ or -] 0.57 Ash 2.88 [+ or -] 0.13 (abc) 2.74 [+ or -] 0.45 (a) Carbohydrates 1.35 [+ or -] 0.25 (cde) 0.96 [+ or -] 0.38 (bc) Lipids * 0.26 ([dagger] ab) 0.48 [+ or -] .30 (ab) Total nitrogen 1.19 [+ or -] 0.15 (a) 1.21 [+ or -] 0.14 (ab) Nonprotein 0.19 [+ or -] 0.08 (b) 0.14 [+ or -] 0.11 (ab) nitrogen Proteins 6.25 [+ or -] 1.25 (a) 6.69 [+ or -] 1.00 (ab) Condition 85.08 [+ or -] 9.30 (de) 83.37 [+ or -] 14.31 (e) index Percent 30.2 [+ or -] 2.2 (d-g) 29.6 [+ or -] 2.7[pounds sterling] edibility Month (2006) Parameter December Moisture 86.33 [+ or -] 0.81 (de) Ash 3.13 [+ or -] 0.25 (cde) Carbohydrates 1.88 [+ or -] 0.50 (e) Lipids * 0.36 [+ or -] 2.85 (ab) Total nitrogen 1.17 [+ or -] 0.08 (a) Nonprotein 0.23 [+ or -] 0.03 (b) nitrogen Proteins 5.90 [+ or -] 0.48 (c) Condition 84.84 [+ or -] 9.36 (de) index Percent 30.0 [+ or -] 2.5 (bcd) edibility Parameters are in percent except for condition index. * These values are back-calculated from the log-transformed values used in the analysis. The body mass of at least 3 individuals had to be pooled to obtain each replicate. ([dagger]) Only one replicate available. Within a row, values not sharing the same superscripts are significantly different (P < 0.05). TABLE 3. Matrix of Spearman correlation coefficients (R) and respective P values for pairwise correlation analysis (n = 12) of monthly mean air temperature, precipitation, biochemical composition, condition index, and percent edibility of R. decussatus from Ria Formosa. Parameter Temperature Precipitation Moisture Ash Precipitation -0.57 0.0543 Moisture -0.19 0.55 0.5486 0.0625 Ash -0.59 -0.01 -0.50 0.0441 0.9828 0.1006 Carbohydrates 0.21 -0.06 -0.11 -0.09 0.5121 0.8629 0.7292 0.7787 Log(lipids) -0.03 -0.26 -0.29 0.35 0.9225 0.4168 0.3541 0.2652 Total nitrogen 0.48 -0.45 -0.76 0.14 0.1114 0.1446 0.0040 0.6646 Nonprotein -0.32 0.32 0.28 0.13 nitrogen 0.3033 0.3126 0.3777 0.6881 Protein 0.57 -0.65 -0.83 0.11 0.0543 0.0220 0.0008 0.7292 Condition index 0.66 -0.64 -0.62 -0.10 0.0190 0.0261 0.0332 0.7456 Percent 0.28 -0.21 -0.24 -0.06 edibility 0.3839 0.5128 0.4433 0.8629 Log Total Nonprotein Parameter Carbohydrates (Lipids) Nitrogen Nitrogen Precipitation Moisture Ash Carbohydrates Log(lipids) 0.01 0.9656 Total nitrogen 0.27 0.29 0.4038 0.3541 Nonprotein 0.32 0.25 0.03 nitrogen 0.3126 0.4357 0.9225 Protein -0.08 0.16 0.78 -0.56 0.8122 0.6175 0.0026 0.0562 Condition index 0.19 -0.17 0.55 -0.54 0.5567 0.5868 0.0666 0.0682 Percent 0.06 -0.49 -0.01 -0.66 edibility 0.8459 0.1063 0.9828 0.0190 Condition Parameter Protein Index Precipitation Moisture Ash Carbohydrates Log(lipids) Total nitrogen Nonprotein nitrogen Protein Condition index 0.76 0.0040 Percent 0.35 0.77 edibility 0.2652 0.0034 Significant (P < 0.005) coefficients are printed in bold type.
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|Author:||Anibal, Jaime; Esteves, Eduardo; Rocha, Carlos|
|Publication:||Journal of Shellfish Research|
|Date:||Apr 1, 2011|
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