3.1. Biometric Data and Proximate Chemical Composition
The biometric data of
Chaceon maritae (
Table 1) did not show significant differences between seasons either in terms of carapace length (CL) or in terms of weight. On the contrary, specimens collected in March presented a carapace width (CW) significantly higher than specimens collected in October.
C. maritae CW sizes up to 165 mm were reported for males and up to 120 mm for females, although relatively few female crabs grow larger than 100 mm (CW) [
5,
8]. The differences in CW observed between seasons suggest that crabs caught in March were older than crabs caught in October. However, in both seasons, all crabs analyzed were roe-bearing females.
The analysis of the chemical composition and nutritional value of
C. maritae was carried out on previously water boiled and frozen crabs, since this is the main form as red crabs from Namibe are marketed. When analyzing the effect of boiling on the proximate chemical composition of several crab species, other authors reported controversial results. Thus, when some reported no significant differences between raw and cooked tissues [
41], others reported lower moisture and higher ash and protein content after cooking [
15,
16]. However, even when there were variations in moisture, protein, and ash contents of raw and cooked tissues, these variations occurred within narrow ranges of values [
15,
16].
The proximate chemical composition of the edible tissues of boiled
C. maritae caught during March and October is presented in
Table 2. Although there may have been some change in relation to raw meat, the muscle of boiled
C. maritae collected off the coast of Namibe presented a proximate chemical composition in line with that of other raw or cooked geryonid crab species. Thus,
C. maritae from Namibe presented a protein, ash, and fat content similar to those reported for raw
C. affinis from Madeira (Portugal) (17.8; 2.3 and 0.7 g/100 g, for protein, ash, and fat, respectively) [
11], to steamed
C. quinquedens from Nova Scotia (Canada) (15.1, 1.75, 0.88 g/100g for protein, ash, and fat, respectively) [
42] and a fat content similar to that reported to boiled
C. quinquedens from New Jersey (United States of America) (0.9 g/100 g) [
43]. Moreover, the proximate chemical composition was also similar to adult females from other crab species like swimming crab (
Portunus trituberculatus) (15.73 and 1.20 g/100g of protein and fat, respectively) [
17] or blue swimmer crab (
Portunus pelagicus) (18.4 and 1.08 g/100g of protein and fat, respectively) [
14].
In general, significant differences were observed between the chemical composition of the different tissues (
Table 2). Thus, the muscle has the highest moisture and ash content, the ovaries have the highest protein content, and the hepatopancreas has the highest fat content. It was observed that muscle and ovaries contained more protein than hepatopancreas and that hepatopancreas and ovaries were richer in fat. Due to their higher fat content, ovaries and hepatopancreas presented an energy value higher than the muscle. Other authors reported similar patterns of tissue composition in other species of crabs from other locations, like wild-caught and pond-reared swimming crab
(Portunus trituberculatus) adult females [
17], blue swimmer crab (
Portunus pelagicus) [
14], Atlantic spider crab (
Maja brachydactyla) [
13], or brown crab (
Cancer pagurus) [
12]. However, in some species, lower fat contents in muscle, ovary, and hepatopancreas has been reported [
12,
13]. The differences observed between tissues could be related to their functions. The muscle is a structural tissue mostly composed of proteins and structural lipids, whereas hepatopancreas and ovaries are rich in storage lipids necessary to fulfil crabs’ physiological needs [
15].
When comparing the proximate chemical composition in the two seasons under analysis (March and October), the most pronounced difference observed was in the hepatopancreas moisture and fat contents. Thus, hepatopancreas of animals caught in October presented a moisture content lower and a fat content higher (approximately 16%) than hepatopancreas of animals caught in March. These differences could be related to environmental variations, like changes in temperature or in nutrients availability, as well as differences in animal physiology [
15]. Seasonal fluctuations in fat content were also reported in brown meat (mostly gonads plus hepatopancreas) of
Cancer pagurus from the Scottish coast, whose fat content, either raw or boiled, was higher in crabs caught during the summer than in crabs caught during the spring [
15].
3.2. Fatty Acid Profile and Cholesterol Content
The fatty acid profile of edible tissues of
C. maritae caught in March and in October is presented in
Table 3. Significant differences (
p < 0.05) were observed both among tissues and between seasons. In both seasons, polyunsaturated fatty acids (PUFA) were the main group of fatty acids in muscle, which was followed by monounsaturated fatty acids (MUFA) and, lastly, by saturated fatty acids (SFA). On the other hand, MUFA were the main group in hepatopancreas, which was followed by SFA in October or by PUFA in March. In March, PUFA and MUFA (
p > 0.05) were the main groups of fatty acids in ovaries, but, in October, PUFA content was significantly higher than MUFA content. In ovaries, SFA were the minor group of fatty acids in both seasons.
In all tissues and in both seasons, palmitic acid (C16:0) was the main SFA, accounting for about 50% of the total SFA. The second most important SFA was stearic acid (C18:0) accounting for about 20% in muscle and hepatopancreas and about 15% in ovaries. Within MUFA, the oleic acid (C18:1ω9) was the most abundant. As a matter of fact, oleic acid accounted for more than 50% of the total in all tissues and in both seasons analyzed. In muscle and ovaries, oleic acid was followed by the mixture of palmitoleic acid (C16:1ω7) and its isomer (C16:1ω9), whereas, in the hepatopancreas, it was followed by eicosenoic acids (C20:1ω9 + ω7). Eicosapentaenoic acid (EPA) (C20:5ω3) and docosahexaenoic acid (DHA) (C22:6ω3) were the main PUFA in all tissues and in both seasons analyzed. Despite some variations within the percentage of each fatty acid, the fatty acid profile of cooked muscle from
C. maritae from Namibe was in accordance to those reported for the muscle of other cooked [
16,
43] or raw [
12,
13,
14,
16,
17] crab species. The effect of boiling on the fatty acid profile seems to be controversial. Thus, while Maulvault et al. [
15] showed that boiling strongly decrease SFA, MUFA and PUFA contents both in muscle and brown meat
of Cancer pagurus, Risso and Carelli [
16] showed that boiling leads to an increase of PUFA content of
Lithodes santolla.
Similar to what was observed in red crab from Namibe, MUFA were also the main group of fatty acids in the hepatopancreas of males and females of
Cancer pagurus from English Channel and the Scottish coast [
12]. However, in other species, namely in
Maja brachydactyla [
13] and
Portunus pelagicus [
14], SFA were the main group of fatty acids in hepatopancreas.
The main differences observed among tissues were in the MUFA C20:1(ω11 + ω9 + ω7) and C22:1ω11, which presented higher values in hepatopancreas than in ovaries and muscle, and in DHA and EPA, where concentrations in hepatopancreas, especially in October, were lower than in muscle and in ovaries. The differences observed between tissues must be related to their different physiological functions. The higher percentage of C20:1(ω11 + ω9 + ω7) in hepatopancreas was also reported by others [
12,
13,
14]. The presence of cetoleic acid (C22:1ω11) was also reported in the cooked muscle of
Chaceon quinquedens (1.7 %) and
Cancer irroratus (4.3 %) from Northwest Atlantic [
43].
When comparing the fatty acid profile in both seasons, it was possible to observe that, in October, the percentage of SFA and MUFA in muscle and hepatopancreas increased and the percentage of PUFA decreased, while, in ovaries, the values were constant. As previously mentioned, these differences could be a consequence of changes in temperature, nutrient availability, or animal physiology. According to Cuculescu et al. [
44], fatty acids may play an important role in the adjustments of membrane fluidity to variations in environmental temperature. These authors suggested that the accumulation of long-chain PUFA before the cold season could make crabs more able to adapt to rapid decreases in temperature and the accumulation of saturated fatty acids before the hot season more capable of adapting to rapid increases in temperature [
44]. Thus, the higher percentage of SFA and MUFA in muscle and hepatopancreas observed in October (immediately after the cold season) and the higher percentage of PUFA observed in March (before the cold season) could be related to this temperature adaptation.
Together, DHA and EPA accounted for about 31% to 35% of total fatty acids in muscle, 23% to 25% in ovaries, and 13% to 19% in hepatopancreas. The content of these two important ω3-fatty acids in the edible crab tissues was higher than 200 mg/100 g in the muscle. This intake is adequate for the primary prevention of cardiovascular disease based on European Food Safety Authority (EFSA) recommendation intake for adults (250 mg/day) [
45]. Moreover, the ratio ω3-PUFA/ω6-PUFA ranged from 3.04 (hepatopancreas in October) to 5.70 (muscle in March), the atherogenic index from 0.24 (muscle in March) and 0.45 (hepatopancreas in October), and the thrombogenic index from 0.13 (muscle in March) to 0.30 (hepatopancreas in October). All these indices are important to evaluate the nutritional quality of fat present in food. An imbalanced ω3/ω6 ratio shifts the physiological state to one that is proinflammatory, prothrombotic, and pro-aggregatory, with increases in blood viscosity, vasospasm, vasoconstriction, and cell proliferation. Western diets are characterized by high ω6 and low ω3 intake, which leads to a ω6/ω3 around 20:1, whereas a 1:1 to 2:1 ω6-PUFA to ω3-PUFA should be the target ratio for health [
46]. The atherogenic and thrombogenic indices were created by Ulbricht & Southgate [
31] to evaluate the predisposition of food to influence the incidence of coronary heart disease, which has the potential to promote thrombus formation and increased plasma cholesterol levels.
The high ω3-PUFA/ ω6-PUFA are in accordance with the values reported from other species such as
M. brachydactyla [
13],
P. trituberculatus [
17], or
C. pagurus [
12] and higher than the values reported to
P. pelagicus [
14]. The AI and TI indices are similar to that reported to
C. pagurus [
12] and to the muscle and gonads of
M. brachydactyla [
13], and lower than those reported in other food items like lamb chop (IA 1.00; IT 1.33), raw minced beef (IA 0.72; IT 1.27), or chicken (IA 0.5; IT 0.95) [
30]. According to these three indices, the edible tissues of
C. maritae had high nutritional quality.
Muscle cholesterol levels were similar in both seasons (
Table 3). The values obtained were like that reported among other species, such as cooked
Chaceon quinquedens,
Cancer borealis, and
Cancer irroratus [
43], but higher than values reported among raw or cooked
Lithodes santolla [
16] and raw
C. pagurus [
12] and
M. brachydactyla [
13]. These differences could be related to differences between species and/or environmental conditions or with the culinary processes that the crabs suffered before being analyzed. Risso & Carelli [
16] reported significant differences in cholesterol levels between raw (37.3 mg/100 g) and cooked (51.0 mg/100g)
Lithodes santolla, which could not be explained by only differences in moisture content. The authors suggested that these differences could be related to alterations occurring in protein-cholesterol complexes of tissues after heating. Cholesterol plays a role in the membrane’s fluidity and permeability and is a precursor of vitamin D, adrenal and sex steroid hormones, and bile salts. Most authoritative bodies do not provide a maximum amount for cholesterol consumption, but, when they do, the advice is to not exceed 300 mg/day [
47]. Thus, although having a cholesterol content higher than that found in several other crab species, the cholesterol content of
C. maritae from the Namibe was still significantly lower than this maximum.
3.3. Amino Acid Profile
Proteins are essential elements of a healthy diet, which allow both growth and maintenance of the 25,000 proteins encoded within the human genome, as well as other nitrogenous compounds [
33]. The amino acid profile is one of the factors that influence dietary protein quality. Amino acid could be classified as nonessential amino acids (NEAA), such as those that can be synthesized by the body, or essential amino acids (EAA), which are those that the human body cannot synthesize and, therefore, must be provided through diet. According to the World Health Organization [
33], histidine, isoleucine, leucine, lysine, methionine, phenylalanine, threonine, tryptophan, and valine are EAA, whereas aspartic and glutamic acids, asparagine, alanine, serine, cysteine, tyrosine, glycine, arginine, glutamine, and proline are NEAA. However, some NEAA, such as cysteine, tyrosine, glycine, arginine, glutamine, or proline, are termed conditionally indispensable since they became essential under specific pathological or physiological conditions [
48].
The amino acid profile of
C. maritae muscle is given in
Table 4. Tryptophan, asparagine, and glutamine were destroyed by acid hydrolysis and were not determined. No significant differences were observed between the amino acid profiles of crabs caught in March or in October. Thus, in both seasons, glutamic acid was the main NEAA, which was followed by aspartic acid and arginine. In what concerns EAA, leucine and lysine were the ones that presented higher contents. In general, these results agree with those found in the literature for other crab species [
12,
13,
14,
17]. In both seasons, NEAA dominates the protein content resulting in EAA/NEAA ratios lower than 1. This result is also in agreement with the scientific literature since it is known that crustacean muscle contains more non-essential amino acids, which are synthesized or modified in the body, than essential amino acids [
12].
The essential amino acid score (EAAS) was calculated concerning the reference amino acid pattern for adults (
Table 5). Results showed that muscle protein is well balanced when concerning EAA, presenting EAAS higher than 100 for all EAA except for valine, which reached 84 and 89 in March and October, respectively. The limiting amino acids differ among muscle protein of different crab species. For example, isoleucine was reported as the limiting amino acids in
M. brachydactyla [
13] and methionine in
C. pagurus [
12], while tryptophan was reported as the limiting amino acid in
P. pelagicus [
14].
Results showed that
C. maritae protein from Namibe has high quality and could be considered a good source of EAA. Intakes of EAA higher than those in the reference amino acid pattern could be useful to complement low-quality proteins from other dietary sources. Moreover, high EAA intakes could be important, not only to support growth or N-balance but also to support other functions such as lean body mass retention, cell signaling, bone health, glucose homeostasis, and satiety induction [
48].
3.4. Essential Elements and Contaminants
Minerals are essential for human health, so their quantification is important for assessing the nutritional quality of foods [
17]. Mineral concentration in the edible tissues of boiled
C. maritae caught in March and October are presented in
Table 6. In general, the mineral content of crabs caught in March or in October did not show marked differences. In muscle, Na was the most abundant macro element, which was followed by K, P, and Mg. The same trend has been reported to other crab species [
13,
17]. However, red crab from Namibe presented an Na concentration much higher than those of other species, which should be related to the addition of sodium chloride to the water used for cooking.
Significant differences were generally observed between trace metal content of the different tissues (
Table 6), with these contents being lower in muscle than in ovaries and hepatopancreas. The differences in trace metal concentrations verified among tissues were also reported by other authors, and could be related to their distinct physiological functions [
13]. In agreement with the results found in other crab species [
13,
17], Zn was the most abundant trace metal in all crab tissues. The concentration of this metal was particularly high in ovaries. The selective incorporation of Zn in the ovary tissue suggests that this metal could be important for
C. maritae oogenesis. Other crustaceans also showed an accumulation of Zn in the ovary tissue, which suggests the incorporation of this metal into metalloenzymes and its involvement in the stabilization of storage proteins used during embryogenesis [
52,
53]. The Adequate Intake values of macro and trace metals set by EFSA (
Table 6) indicate that
C. maritae from Namibe is a particularly good source of Se, I, Cu, and Zn. From the nutritional point of view, the high Zn, I, and Se content are particularly important, since deficiencies in these minerals are widespread, including in European countries [
54,
55]. Deficiencies in these minerals can contribute to poor growth, intellectual impairments, perinatal complications, and increased risk of morbidity and mortality [
54].
Arsenic, Hg, Cd, and Pb are the elements of greatest concern for seafood safety [
56], with Cd being the one of greatest concern with regard to crab contamination. Previous studies have shown that considerable levels of Cd could be found in the hepatopancreas of crabs from distinct geographic locations [
13,
15,
57]. For this reason, the European Union published an information note saying that consumption of brown crab meat could lead to unacceptable cadmium exposure and that consumers should be advised to avoid or limit its consumption [
58]. Cadmium concentrations in the edible tissues from
C. maritae from Namibe were very low and below the maximum levels laid down in European regulations (
Table 6), which shows that its consumption presents no risk of exposure to high levels of Cd. Furthermore, results obtained showed that the concentrations of Pb and Hg in the edible tissues of
C. maritae were also below the maximum levels laid down in European regulations (
Table 6). At present, no maximum limit is set by the European Union for As in seafood. However, the values obtained were low when compared to other crab species caught in other locations [
7,
13,
17,
56,
59]. Moreover, it is known that the predominant form of As in seafood is the non-toxic arsenobetaine [
56]. The low concentration of toxic elements in
C. maritae from Namibe could be related not only with species characteristics, but also with other factors that could influence the uptake of metals, like the concentration of exposure, climate, salinity, and possible synergistic and antagonistic effects of other metals and organic compounds that could be present [
7,
57]. Results obtained showed that
C. maritae from Namibe is a safe food in what concerns heavy metal contamination.