Proximate composition and fatty acid profile of the sea cucumber isostichopus badionotus and holothuria floridana

Abstract

The proximate composition and the fatty acids (FA) profile of the two tropical sea cucumbers, i.e., Isostichopus badionotus and Holothuria floridana were analyzed. We observed higher crude protein in I. badionotus (41.7%) than H. floridana (30.2%) and more calcium content in I. badionotus (10.7 mg/g) than H. floridana (6.0 mg/g). The FAs profile of I. badionotus was 52.9% saturated FA (SFA), 30.8% monounsaturated FA (MUFA), and 16.3% polyunsaturated FA (PUFA), with a high abundance of palmitic acid (28.2%). H. floridana showed 7.4 mg/g of phosphorus, and 43.6% PUFA, which were higher than I. badionotus. H. floridana has 34.9% SFA, and 21.5% MUFA. The most important PUFAs were linoleic, arachidonic (ARA) and eicosapentaenoic (EPA). ARA content in H. floridana was 58% higher (24.9%) than I. badionotus (10.4%). Both species had low docosahexaenoic acid (DHA); however, the ΣEPA, DHA of H. floridana (11.2%) was higher than I. badionotus (1.80%).

Introduction

Sea cucumbers (Echinodermata: Holothuroidea), or their dry form (bêche-de-mer or trepang) have been a luxury dietary food for Asians for many centuries (Hair et al., 2018). Currently, these are traditionally consumed as raw, dried, or boiled in various tropical and subtropical countries (Purcell, 2014). In China, Korea, and Taiwan they are also appreciated for their medicinal properties and there are currently several patented healing tonics (Li et al., 2008; Wu et al., 2012; Wijesinghe et al., 2013). The world market and trade for sea cucumber are mainly satisfied with the food market in China, the Hong Kong SAR, Singapore, and the Chinese province of Taiwan. At least 70 countries in the world have registered sea cucumber fisheries (Toral-Granda et al., 2008); among them, 58 species are being usually exploited (Purcell et al., 2012). In the countries of Central America and the Caribbean up to Colombia and Venezuela, there are two commercially attractive species of sea cucumbers, i.e., Isostichopus badionotus and Holothuria floridana (De la Fuente-Betancourt et al., 2001; Tagliafico et al., 2011). The fishing of these species is restricted for quotas and allowed only in certain months. Therefore, several projects have been undertaken to analyze the feasibility and profitability of farming under aquaculture conditions (Zacarías-Soto et al., 2013; Zacarías-Soto et al., 2018; Sánchez-Tapia et al., 2019).

I. badionotus is a large species that grows to a length of 45 cm. The average weight in the adult phase is 769 ± 229 g (Romero-Hernández et al., 2017). For about 8 years ago, research has focused on evaluating the stock in natural environments (Hernández-Flores et al., 2015; Navarrete et al., 2018; López-Rocha and Velázquez-Abunader, 2019) and conservation strategies (Hernández-Betancourt et al., 2018) especially motivated by the high demand for this species in Asia. Also, several studies have been focused on examining the vulnerability to environmental conditions (Gullian-Klanian, 2013; Gullian-Klanian and Terrats-Preciat, 2017), the reproductive cycle (Guzmán et al., 2003), and their medicinal properties (Olivera-Castillo et al., 2013; Olivera-Castillo et al., 2018; Li et al., 2019).

H. floridana is a shallow sea cucumber (< 2 m). The average weight in the adult phase is 64.0 ± 27.2 g (Romero-Hernández et al., 2017). There is little information about this species till yet, which is focused on aspects related to its fishery process (De la Fuente-Bentancourt et al., 2001; Hernández-Flores et al., 2015; Gamboa-Álvarez et al., 2020). Other researchers have described their reproductive cycle (Ramos-Miranda et al., 2017), pathologies (Pomory and Lares, 1998), and medicinal property (Santafé et al., 2014).

In the last ten years, the research on the biochemical properties of sea cucumber has grown significantly. Differences in nutritional composition may be intrinsic in species to species (Wen et al., 2010; Haide et al., 2015) or associated with external factors, such as diet (Wen et al., 2018), climate change (Hudson et al., 2004; Gao et al., 2011; Vergara and Rodríguez, 2016; Künili and Çolakoğlu, 2019), and the type of processing (Özer et al., 2005; Nishanthan et al., 2018). There are very few studies that have been done on the nutritional characteristics of I. badionotus and H. floridana. Currently, there are two reports which emphasize the specimens extracted from Cispatá Bay (Colombia) that identified the presence of 19 to 20 fatty acids (FAs) with structural diversity in H. floridana and I. badionotus, respectively (Guzmán et al., 2014; Pastrana et al., 2016). Thus, the present work aimed to conduct a comparative analysis of the proximate composition and the fatty acid profile of the body wall of the I. badionotus and H. floridana extracted from the Yucatán peninsula (México).

Materials and Methods

Sample collection    A total of 20 tropical holothurian species were collected from the Dzilam de Bravo, Yuc., México (21°19' N y 88°35′ W) in October 2013 (fishing permit PPF/DGOPA–026/13, CONAPESCA, México). Among them, ten were I. badionotus (330 ± 20 g), and the remaining ten samples were H. floridana (168 ± 35 g). The species were caught in sandy areas within 5–9 m depth with the bottom temperature of 24.5 oC by using the AirLine hookah diving system. The species were further transported to the laboratory in a cooler (25 oC) filled with seawater.

All samples from both the species were desensitized by the immersion in ice for 2 h to further proceed for the research on body composition. The body wall, including the muscular band of each species, was homogenized separately for further analysis. Samples were kept frozen at −80 °C for the analysis of nutritional components.

Proximate composition    The international standard methods (AOAC, 2007) were used for the analysis. The sample was dried at 100 °C for 18 h before performing the proximal analyzes. Crude protein (CP) was determined by the Kjeldahl procedure (AOAC 981.10), while the crude lipids were determined with a Soxhlet extraction method (hexane extraction, AOAC 960.39). The fiber crude was determined by the acid and alkaline digestion (AOAC 962.09) and the ash content by using a muffle furnace (550 oC for 5 h, AOAC 920.15). The carbohydrates/nitrogen-free extract (NFE) was determined by mathematical calculations.

Mineral analysis    The analysis of calcium (Ca) and phosphorus (P) was carried out by using 2.5 g of calcined tissue at 550 °C (Thermo Fisher Scientific, USA). The ash was dissolved in 1 mL of concentrated nitric acid. The permanganate titration method (AOAC 944.03) was used for the analysis of Ca, while the spectrophotometric analysis (HACH, USA) was applied by using molybdenum blue reaction (ISO 13730, 1996) for the determination of P.

Analysis of fatty acid profile A tissue sample was lyophilized in a benchtop freeze dryer with a condenser at 110 °C (Virtis Lyon Centre, Canada). Lipid extraction was done by the Folch method (Folch et al., 1957). FAs were esterified by heating in 10% methanol chlorohydric acid (90 °C for 120 min) and then extracted with heptane (Lora et al., 2018). The heptane fraction was analyzed by FID-gas chromatography (Agilent, USA) with a capillary column (J&W DB® 23 122–2332, 250 °C, 30 m, 0.25 mm, 0.25 µm). The conditions for FID-gas chromatography were set at 55 °C for 1 min, followed by a gradient of 25 °C/min to reach 178 °C for 3 min, then at 1.9 °C/min to reach 220 °C, and ending the reaction at 230 °C for 10 min. The identification of chromatographic peaks was done by comparison with retention times and FAMEs standards (Supelco-CRM47885).

Statistical analysis    The results of the proximate analysis and the lipid profile are expressed as a percentage of the mean ± standard deviation (SD), and those of minerals in mg/g of dry sample. Statistical analysis was performed at a 5% significance level. Comparisons between FAs were performed using the Welch-Satterthwaite t-test (Kutner et al., 2005). Permutational multivariate analysis of variance (PERMANOVA) was used to compare the results of proximal analysis between groups (Anderson et al., 2008). Statistical analyses were performed by using the software PAST 3.19, and InfoStat v2017.

Results and Discussion

Proximate composition    The proximate compositions of both the species are shown in Table 1. The CP of H. floridana 30.17 ± 0.44%) was 11.5% lower than I. badionotus. The CP of I. badionotus (41.68 ± 0.43%) was similar to that of Thelenota anax (40.7 ± 0.33%), Holothuria scarba (43.43 ± 0.2%), and Bohadschia marmorata (43.23 ± 0.1%) (Wen et al., 2010). The protein concentration of the body wall varies with the period of activity, seasonal variations, and diet (Ozer et al., 2005; Gao et al., 2011; Vergara and Rodríguez, 2016; Künili and Çolakoğlu, 2019). Previous authors reported that the PC values of the body wall of I. badionotus vary between 23.7 ± 1.4% and 23.7 ± 3.5% when fed with two commercial diets that contained 37.7% and 20.1% of PC, respectively (Zacarías-Soto and Olvera-Novoa, 2015).

Table 1. Proximate composition and micronutrient of the tropical sea cucumbers, Isostichopus badionotus and Holothuria floridana

Component	I. badionotus	H. floridana	p-value
Crude protein (%)*	41.68 ± 0.43	30.17 ± 0.44	0.0009
Total lipids (%)	0.78 ± 0.56	0.78 ± 0.12	ns
Ash*	38.9 ± 0.32	36.2 ± 0.75	0.0001
Crude fiber	0 ± 0	0 ± 0	ns
Carbohydrate / NFE (%)*	10.72 ± 0.01	15.19 ± 0.07	-
Calcium (mg/g)*	10.7 ± 0.08	6.0 ± 0.41	0.006
Phosphorus (mg/g)*	1.7 ± 0.14	7.4 ± 0.37	0.001

Data are mean ± SD; (*) = significant differences at p ≤ 0.05, PERMANOVA with 9999 permutations, (n = 10); Nitrogen-free extract (NFE)

Both species of sea cucumber had low-fat content (< 1%); but the variation among the organisms were greater in I. badionotus (0.22–1.34%). The value of total lipids was in the range of 0.3 to 1.9%, reported in six of the eight tropical species from the Guangzhou market in China (Wen et al., 2010; Haide et al., 2015). And similarly, in Isostichopus spp. (0.07 −0.35%, Vergara and Rodríguez, 2016), P. regalis (1.27%, Roggatz et al., 2018) and H. scabra (1.02%, Sroyraya et al., 2017). The percentage of lipids varies throughout the year due to physiological processes and environmental conditions (Hudson et al., 2004; Gao et al., 2011; Künili and Çolakoğlu, 2019). The mechanisms of energy conservation, such as estivation or dormancy, are examples of physiologic processes that are known to alter the protein/lipid ratio of the body (Yang et al., 2006; Ji et al., 2008; Gullian-Klanian, 2013).

The ash content of both the species were within the range of 36.2–38.9% similar to T. anax (39.2%), S. hermanni (37.9%), and H. fuscopunctata (39.6%, Wen et al., 2010). The ash content in holothurians is high due to large numbers of calcareous spicules in the tissues of the body wall (Yang et al., 2015).

Calcium and phosphorus    The Ca content in I. badionotus (10.7 ± 0.08 mg/g) was 56.1% more than H. floridana (6.0 ± 0.4 mg/g) (Table 1). Both species contain more Ca in their body wall than species such as Stichopus horrens (1.06 mg/g), and Holothuria arenicola (0.83 mg/g) from Chabahar Bay (Barzkar et al., 2017). Using atomic absorption spectroscopy (AAS), other authors have reported Ca content of 26.1–57 mg/g in H. arenicola and A. mauritiana from the Buleji coast (Pakistan; Haide et al., 2015). Also, using inductively coupled plasma atomic emission spectrophotometry (ICP-AES), values between 15 and 68 mg Ca/g have been reported for 11 species of tropical sea cucumbers from Guangzhou, China (Wen and Hu, 2010). Lee et al. (2014) reported the Ca content by using the same technique, as 10.41 mg/g in Apostichopus japonicus, which is similar to our data for I. badionotus.

Ca and P in the bones combine to form calcium phosphate, managing to support the human body. Together these minerals have important metabolic functions such as muscular contraction, nervous stimulation, enzymatic and hormonal activities (Shaker and Deftos, 2019). The body wall of sea cucumbers consists of abundant microscopic skeletal elements, called ossicles that are part of the endoskeleton, composed of mainly calcium carbonate (Lambert, 1997). The recommended reference value for Ca consumption in humans is 900–1 000 mg per day (World Health Organization, 2004). Thus, the consumption of 100 g of any of the mentioned species might fulfill the 60–100% of the daily intake of Ca requirement.

The P level in H. floridana (7.4 ± 0.37 mg/g) was observed as 22.9% more than I. badionotus (1.7 ± 0.14 mg/g). Lee et al. (2014) investigated the P level in A. japonicus using ICP-MS and reported 2.62–2.82 mg P/g, which is lower than the P level of H. floridana found in this work. The mineral body content in sea cucumber depends on diet and varies according to the climate change (Barzkar et al., 2017). The soluble P is absorbed through the skin of sea cucumbers, and the concentration of P in seawater is low. Consequently, the sea cucumbers fulfill their requirement of P by eating phytoplankton. The minimum recommended amount of P for humans is 560 mg per day (World Health Organization, 2004); therefore, both species do not represent an important source of P.

Fatty acids profile    The results of the FAs profile showed significant differences between the species (p < 0.05; Table 2). H. floridana had the highest proportion of polyunsaturated fatty acids (PUFA) (43.6%), followed by saturated fatty acids (SFA) (34.9%) and monounsaturated fatty acids (MUFA) (21.5%). I. badionotus showed a higher content of SFA (52.9%), followed by MUFA (30.8%) and PUFA (16.3%). The FA profile of H. floridana was similar to that of other reported holothurians, such as H. tubulosa and H. polii (Biandolino et al., 2019). The results differ from those previously reported by Guzmán et al. (2014) for the same species who reported absence of PUFA and high levels of SFA (63%) and MUFA (37%).

Table 2. Saturated fatty acid composition of total lipids from body wall of the tropical sea cucumbers Isostichopus badionotus and Holothuria floridana

Fatty acids	Commun name	I. badionotus	H. floridana
Saturated
C 4:0	Butiric	0.15 ± 0.30	n.d.
6:0	Capronic	0.13 ± 0.10	n.d.
8:0	Caprilic	0.07 ± 0.80	0.16 ± 0.17
10:0	Capric	0.04 ± 0.10	0.09 ± 0.10
12:0	Lauric	0.10 ± 0.04	0.30 ± 0.62
13:0	Tridecanoic	0.01 ± 0.02	0.05 ± 0.06
14:0	Miristic	3.91 ± 0.27	2.33 ± 1.11
15:0	Pentadecanoic	2.14 ± 0.17	1.92 ± 0.59
16:0*	Palmitic	27.16 ± 1.20	7.22 ± 1.69
17:0*	Margaric	2.73 ± 0.11	1.90 ± 0.16
18:0	Stearic	8.45 ± 0.95	8.71 ± 0.72
20:0	Arachidonic	2.76 ± 0.16	3.00 ± 0.46
21:0	Henicosanoic	1.67 ± 0.14	3.05 ± 0.85
22:0	Behenic	2.09 ± 0.11	4.37 ± 0.76
23:0	Tricosanoic	0.78 ± 0.04	0.88 ± 1.00
24:0	Tetracosanoic	0.70 ± 0.08	0.94 ± 0.48
∑SFA*		52.90 ± 6.78	34.92 ± 2.60
Monosaturated
ω5
14:1*	Myristoleic	1.13 ± 0.12	0.04 ± 0.04
15:1*	5-Pentadecenoic	3.23 ± 0.30	0.91 ± 1.00
16:1	11-Hexadecanoic	2.36 ± 0.13	0.86 ± 1.00
ω7
16:1	Palmitoleic	9.64 ± 0.80	5.70 ± 1.80
17:1	Margaroleic	0.71 ± 0.19	0.57 ± 0.29
18:1	Vaccenic-cis	5.82 ± 0.14	4.60 ± 0.50
ω9
16:1	Palmitoleic	0.74 ± 0.07	0.15 ± 0.16
18:1	Oleic-cis	0.22 ± 0.90	0.33 ± 0.22
18:1*	Elaidic-trans	2.48 ± 0.15	1.42 ± 0.46
20:1	Gadoleic	0.85 ± 0.29	0.94 ± 0.35
22:1	Erucic	0.55 ± 0.53	0.21 ± 0.17
24:1	Nervonic	3.04 ± 0.14	5.44 ± 2.10
∑MUFA*		30.78 ± 2.72	21.49 ± 2.10
Polyunsaturated
ω3
18:3	Linolenic	0.08 ± 0.10	0.42 ± 0.15
18:4*	Stearidonic	0.02 ± 0.03	0.33 ± 0.20
20:3	Eicosatrienoic	0.19 ± 0.32	n.d.
20:5*	Eicosapentaenoic	1.14 ± 0.74	10.89 ± 1.37
22:6	Docosahexaenoic	0.67 ± 0.36	0.32 ± 0.36
ω4
16:2	Hexadecadienoic	0.24 ± 0.22	0.21 ± 0.23
16:3*	Hexatrienoic	0.15 ± 0.01	0.63 ± 0.15
ω6
16:2	Hexadienoic	0.76 ± 0.36	1.56 ± 0.22
18:2*	Linoleic - trans	0.20 ± 0.01	0.57 ± 0.05
18:2*	Linoleic	0.79 ± 0.06	1.16 ± 0.15
18:3	γ - Linolenic	1.13 ± 0.81	1.52 ± 1.62
20:2	Dihomo γ-linolenic	0.64 ± 0.04	0.58 ± 0.64
20:4*	Arachidonic	10.37 ± 1.00	24.87 ± 4.78
22:5	Docosapentaenoic	n.d.	0.54 ± 0.27
∑PUFA*		16.34 ± 2.32	43.59 ± 6.28

Data are expressed as % of total fatty acids (mean ± SD; n=2); (*) = significant differences between samples (t-test; p < 0.05).

The percentage of PUFA in I. badionotus (20%–35%) was lower than in other species of sea cucumbers (Carballeira et al., 1996; Fredalina et al., 1999; Drazen et al., 2008), and higher than that reported for other Isostichopus species (9.20%; Pastrana et al. 2016). The organisms showed high SFA content (45.04%) and a lower content of MUFA (26.97%). The holothurian diet is mainly based on the consumption of algae and phytoplankton, both of which are important sources of PUFA (Taipale et al., 2020). Previous studies have shown that the FA profile of I. badionotus reared in aquaculture facilities and fed with 42.8% PUFA in the diet reduced the PUFA content in its body wall by 4.6% (Zacarías-Soto and Olvera-Novoa, 2015). A diet with 10.6% PUFA and 30.1% MUFA preserved the original PUFA content in the body tissues, with a similar FA profile.

Polyunsaturated fatty acids    The amount of PUFA was significantly higher in H. floridana (43.89 ± 6.28%) than in I. badionotus (16.34 ± 2.32%) (Table 2). The main differences were in the percentage of linoleic (18:2–ω6), arachidonic (ARA, 20:4–ω6), stearidonic (18:4–ω3), and eicosapentaenoic (EPA, 20:5–ω3). EPA and ARA were significantly higher in H. floridana than in I. badionotus. The predominance of ARA and EPA is a common finding in holothurians, and their presence has been associated mainly with the feeding of macroalgae (Wen et al., 2018; Zacarías-Soto et al., 2018).

The ARA content was 58% higher (24.87 ± 4.78%) in H. floridana than in I. badionotus (10.37 ± 1.0%). However, the ARA content of I. badionotus was higher than that reported for sea cucumber species from temperate and tropical climates (Drazen et al., 2008; Wen et al., 2010; Careaga et al., 2013; Haide et al., 2015).

Both species presented a low amount of docosahexaenoic acid (DHA 22:6–ω3; 0.32 to 0.67%). DHA has been reported in the range of 1% to 8% for other tropical holothurians, such as A. abyssorum, O. mutabilis, P. vitreous, P. brychia, H. arenicola, and even for I. badionotus (Drazen et al., 2008; Haide et al., 2015; Zacarías-Soto and Olvera-Novoa, 2015).

Monounsaturated fatty acids    The MUFA profile was significantly different in both species of sea cucumber (Table 2). The FAs-ω5 (14:1 and 15:1) and the elaidic (18:1–ω9t) showed the main differences. Even so, the total content of ω9 was similar in both species (8.49 ± 2.03%–7.89 ± 0.17%). The predominant MUFAs were nervonic acid (24:1–ω9), elaidic (18:1ω9), and vaccenic (18:1–ω7). Previous studies have shown an abundance of 18:1–ω9 and 18:1–ω7 in H. tubulosa and A. japonicus, respectively (Kasai, 2003; Bilgin et al., 2018). The FA-23:1–ω9 was not detected in the present study, which disagrees with the previous reports done by Guzmán et al. (2014) which reported a high abundance of 24:1–ω9 and 23:1–ω9 in H. floridana. I. badionotus showed high amount of 16:1–ω7 (9.64%) instead of 18:1–ω9, as reported by other researchers (Zacarías-Soto and Olvera-Novoa, 2015).

MUFAs and PUFAs are considered good fats. The replacement of SFA in the diet lowers total cholesterol, low-density lipoproteins (LDL), high-density lipoproteins (HDL), and the ratio of total cholesterol and HDL, thus reducing the incidence of coronary heart disease (Mensink and Katan, 1992). These FAs have the function of maintaining the membrane's fluidity at low temperatures with high pressures (Drazen et al., 2008).

Saturated fatty acids    The results demonstrated a similar pattern of 14 SFA in both species (Table 2). The most abundant SFA were stearic (18:0), palmitic (16:0), and myristic (14:0). This finding is similar to the data reported by Biandolino et al. (2019) for H. tubulosa, and H. polii collected in Taranto (Italy).

The percentage of stearic and myristic was similar in both species (p > 0.05). Palmitic was significantly lower in I. badionotus (27.16 ± 1.20%) than in H. floridana (7.22 ± 1.69%), and similar to the other tropical holothurians, such as T. ananas (22.08 ± 0.41%), T. anax (31.60 ± 0.91%), H. fuscogilva (31.86 ± 0.82%) and H. fuscopunctata (24.80 ± 0.51%) (Wen et al., 2010).

In both species, stearic acid was in the range of 8.45–8.71%, which is lower than previously reported for both species (Guzmán et al., 2014; Zacarías-Soto and Olvera-Novoa, 2015). The FA 14:0 varied between 2.33 ± 1.11%–3.91 ± 0.27% being similar to the previous data reported for both species (Guzmán et al., 2014; Zacarías-Soto and Olvera-Novoa, 2015; Pastrana et al., 2016).

Nutritional quality indexes of lipids    The indices of nutritional quality show the relationship between the percentage of FAs (Table 3). The Σω3 (11.96%) and Σω6 (30.80%) were significantly higher in H. floridana than in I. badionotus, while the Σω9 did not show any significant difference. PUFAs, including EPA and DHA, are healthy nutritional components found in shellfish (Giogios et al., 2009). The EPA/DHA ratio 1:1 is recommended to obtain a protective effect against cardiovascular disease risk (Lluís et al., 2013). The ΣEPA DHA were higher in H. floridana (11.2%) than in I. badionotus (1.80%). However, due to the low content of DHA in both species, the ΣEPA DHA was lower than that reported for other holothurians, such as H. tubulosa (43.21%) and H. polii (56.50%) (Biandolino et al., 2019).

Table 3. Nutritional quality indices from body wall of the tropical sea cucumbers Isostichopus badionotus and Holothuria floridana

Indices	I. badionotus	H. floridana
∑ ω3*	2.08 ± 0.33	11.96 ± 4.75
∑ ω6*	13.88 ± 3.23	30.80 ± 8.06
∑ ω9	7.89 ± 0.17	8.49 ± 2.03
ω3/ω6*	0.15 ± 0.01	0.41 ± 0.15
ω6/ω3*	6.73 ± 0.59	2.65 ± 0.99
PUFA /SFA*	0.31 ± 0.04	1.27 ± 0.22
MUFA/SFA	0.58 ± 0.01	0.62 ± 0.04
EPA + DHA*	1.80 ± 0.35	11.20 ± 2.04

Data are expressed as% of total fatty acids (mean ± SD; n=2); (*) = significant differences between samples (t-test; p<0.05).

The ratio of ω3/ω6 in H. floridana was found in the range of 0.25–0.61%, which is similar to other species of tropical sea cucumbers (Wen et al., 2010). The ratio of ω3/ω6 is commonly used to compare the nutritional value. According to Wood et al. (2004), the ratio of ω3/ω6 between 0.25 to 1.0 is favorable to reduce the risk of cardiovascular diseases. In marine organisms, the amount of ω6 is expected to be higher than ω3 (Tokur et al., 2006).

The MUFA/SFA ratio was the same in both sea cucumbers (0.58–0.62) and lower than the values previously reported for other species of sea cucumbers, such as H. tubulosa (2.10) and H. pili (1.85) (Biandolino et al., 2019).

The PUFA/SFA ratio was significantly lower in I. badionotus (0.31) than in H. floridana (1.27), being also below the optimal intake (PUFA /SFA = 0.4–1) recommended for a healthy diet (Jiménez-Colmenaro, 2007). The PUFA/SFA imbalance affects the cholesterol concentration in the different plasma lipoprotein fractions, increasing LDL (Lee et al., 2015).

Conclusions

The nutritional composition of both species is different, but both are characterized by their high protein content and the presence of essential FAs. I. badionotus showed high levels of PC (41.68%) and 56.1% more Ca than H. floridana (6.0 ± 0.4 mg/g). H. floridana showed high content in Σω3 (11.96%) and Σω6 (30.80%) and the ω3/ω6 ratio coincided with the recommended value for good health. Both species showed a low content of DHA (0.32 to 0.67%); however, the ΣEPA DHA of H. floridana was higher (11.2%), due to its high content of ARA (58%) and EPA (89.5%).

Acknowledgements    The authors wish to acknowledge the contributions of Roberto Hernández Herrera and Gabriela Mendoza Carrion from Northwest Biological Research Center (CIBNOR, México) for their assistance in laboratory analysis. This work was supported by the National Science and Technology Council (Ref M026-16996, CONACYT, MX).

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