Fatty acid profile of Cystoseira C. Agardh (Phaeophyceae, Fucales) species from the Tunisian coast: Taxonomic and nutritional assessments

Bouafif, Cyrine; Messaoud, Chokri; Boussaid, Mohamed; Langar, Habib; Bouafif, Cyrine; Messaoud, Chokri; Boussaid, Mohamed; Langar, Habib

doi:10.7773/cm.v44i3.2798

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Ciencias marinas

Print version ISSN 0185-3880

Cienc. mar vol.44 n.3 Ensenada Sep. 2018 Epub July 30, 2021

https://doi.org/10.7773/cm.v44i3.2798

Articles

Fatty acid profile of Cystoseira C. Agardh (Phaeophyceae, Fucales) species from the Tunisian coast: Taxonomic and nutritional assessments

Perfil de ácidos grasos de especies de Cystoseira C. Agardh (Phaeophyceae, Fucales) de la costa tunecina: Evaluaciones taxonómicas y nutricionales

Cyrine Bouafif¹^*

Chokri Messaoud²

Mohamed Boussaid²

Habib Langar¹

^¹Université de Tunis El Manar, Faculté des Sciences de Tunis, Département de Biologie, 2092, Tunis, Tunisia.

^²University of Carthage, National Institute of Applied Science and Technology, Department of Biology, Centre Urbain Nord, BP 676, 1080, Tunis, Tunisia.

Abstract

A screening of the total lipids and fatty acids (FAs) of 11 brown algae species of the genus Cystoseira (Phaeophyceae, Fucales) from the Tunisian coast is presented and discussed. Cystoseira species showed low total lipid content, ranging from 19.8 to 68.2 mg·g^-1 dry weight. Fourteen major FAs were detected in the lipid extract of Cystoseira. The FA profile of lipid extracts was characterized by high amounts of saturated FAs (SFAs) ranging from 40.51% to 57.91% of total FAs, with predominance of the lipid fraction of palmitic acid (>30% of total FAs). The arachidonic acid (C20:4n-6) levels were found to be significantly high, ranging from 8% to 16% of total FAs. Multivariate analyses of FA composition showed low geographic differentiation, providing further evidence of intraspecific diversity. Cystoseira crinita, Cystoseira schiffneri, Cystoseira amentacea var. stricta, and Cystoseira sedoides stood out for their low polyunsaturated fatty acid (PUFA)/SFA ratios, low n-6/n-3 PUFA ratios, high unsaturation, and low atherogenicity and thrombogenicity indices, suggesting high nutritional value.

Key words: marine algae; Cystoseira; fatty acids; polyunsaturated fatty acids; Tunisia

Resumen

Aquí se presenta y discute un análisis de los lípidos totales y ácidos grasos (AG) de 11 especies de algas pardas del género Cystoseira (Phaeophyceae, Fucales) de la costa de Túnez. Las especies de Cystoseira mostraron un contenido lipídico total bajo que osciló entre 19.8 y 68.2 mg·g^-1 de peso seco. Se detectaron 14 AG mayoritarios en el extracto lipídico de Cystoseira. El perfil de AG de los extractos de lípidos estuvo caracterizado por altas cantidades de AG saturados (AGS) que variaron de 40.51% a 57.91% del total de AG, con predominio de la fracción lipídica del ácido palmítico (>30% del total de AG). Los niveles de ácido araquidónico (20:4n-6) fueron significativamente altos, y variaron entre el 8% y el 16% del total de los AG. Los análisis multivariados de la composición de AG mostraron baja diferenciación geográfica, lo que aporta más evidencia de diversidad intraespecífica. Cystoseira crinita, Cystoseira schiffneri, Cystoseira amentacea var. stricta y Cystoseira sedoides destacaron por presentar bajas relaciones de ácidos grasos polinsaturados (PUFA)/AGS y PUFA n-6/n-3, alta insaturación y bajos índices de aterogenicidad y trombogenicidad, lo que sugiere un alto valor nutricional.

Palabras clave: algas marinas; Cystoseira; ácidos grasos; ácidos grasos polinsaturados; Túnez

Introduction

In brown algae, fatty acids (FA) are known to have important properties. They constitute a source for pheromone biosynthesis and have antimicrobial (^{Rosell and Srivastava 1987}), anti-inflammatory (^{Calder 2006}, ^{Kumari et al. 2010}), and antioxidant (^{Kumar et al. 2011}) properties. These metabolites are also known for their ability to prevent heart disease and inhibit tumor progression (^{Pereira et al. 2012}). In situ, brown algae use FA-derived compounds as a chemical defense (^{Pohnert and Boland 2002}, ^{Barre
et al. 2004}), i.e., to deter herbivores (^{Schnitzler et al. 2001}). Fatty acids (FAs) and lipid components have scarcely been studied for their chemotaxonomic implications in macroalgae (^{Khotimchenko et al. 2002}, ^{Galloway et al. 2012}, ^{Kumari et
al. 2013}).

Among brown algae, Cystoseira (Ochrophyta, Phaeophyceae) is one of the most widely distributed genera of the Fucales order in the Mediterranean (^{Amico 1995}, ^{Pellegrini et al. 1997}). In the Mediterranean Sea, the Cystoseira are canopy-forming algae that dominate the rocky infralittoral zone. This genus comprises 42 species distributed mainly in the Mediterranean Sea and the adjacent Atlantic Ocean (^{Guiry and Guiry 2016}).

A great diversity of Cystoseira is present along the Tunisian coast. According to ^{Bouafif et al. (2014}, ²⁰¹⁶⁾, 31 species are present on the Tunisian littoral, but little information about the chemical composition of the algae from this region has been published (^{Frikha et al.
2011}). Moreover, it is hard to distinguish species and varieties of the genus Cystoseira due mainly to the high morphological plasticity of the taxa and to the active process of speciation of the genus (^{Ercegovič 1952}, ^{Amico
1995}). Classification of this genus based on chemical compounds, such as sterols and terpenes, started in the 1990s (^{Piattelli 1990}, ^{Amico 1995}). Metabolites isolated from the Cystoseira species have been used as chemotaxonomic markers (^{Amico 1995}, ^{Pellegrini et al. 1997}). Total lipid and FA profiles vary significantly among Cystoseira species (^{Vizetto-Duarte et al. 2015}) and might be useful for taxonomic purposes (^{Galloway et al.
2012}). Moreover, the nutritional value of Cystoseira FAs has never been studied in Tunisia. However, some works have been done on the nutritional quality of FAs of some Cystoseira species in the Mediterranean (^{Ragonese et al. 2014}), the Atlantic (^{Vizetto-Duarte et al. 2015}), and the Indian Ocean (^{Kumari et al. 2010}, ^{Kumari et al. 2013}).

The aim of this paper is to assess the composition of FAs extracted from 11 Cystoseira species (Fig. 1) growing along the Tunisian coast (i) to evaluate the efficiency of Cystoseira FAs as chemotaxonomic markers associated with criteria performed on the morphological diversity of Tunisian Cystoseira taxa (^{Bouafif et al.
2014}, ²⁰¹⁶) and (ii) to estimate the nutritional characteristics of one of the most abundantly available brown macroalgae in the Mediterranean. To the best of our knowledge, this is the first report on the FA profile of some endemic Mediterranean species of Cystoseira.

Figure 1 Location of sampling sites and list of species collected at each site: 1, Cap Zebib (37º16ʹ9.15ʺN, 10º3ʹ59.18ʺE); 2, Kelibia (36º50ʹ26.66ʺN; 11º7ʹ18.31ʺE); and 3, Kerkennah Archipelago (34º39ʹ25.94ʺN, 10º58ʹ20.87ʺE).

Materials and methods

Fieldwork and algal samples

Eleven species and infraspecific taxa of the genus Cystoseira were collected in the upper intertidal zone between 0.5 and 2.0 m depth in October 2014: Cystoseira amentacea var. stricta, Cystoseira barbata, Cystoseira compressa, Cystoseira crinita, Cystoseira elegans, Cystoseira foeniculacea, Cystoseira foeniculacea f. latiramosa, Cystoseira foeniculacea f. tenuiramosa (from 2 localities), Cystoseira schiffneri, Cystoseira sauvageauana, and Cystoseira sedoides (Figs. 1, 2). Specimens were transported to the laboratory in an icebox. Species were identified by morphological examination according to specialized literature on the genus Cystoseira (^{Hamel 1931-1939}, ^{Ercegovič 1952}, ^{Gómez-Garreta et al. 2001}) after careful cleaning that removed epiphytes and sand. A representative specimen of each species was deposited in the Herbarium of the Faculty of Sciences of Tunis (Tunisia) in the Department of Biology. Samples of each freshly collected and identified species were rinsed with distilled water, dried in an oven at 30 ºC for 72 h, then stored in darkness and kept in the dry at room temperature until further use. Each sample consisted of a mixture of 2 to 4 infertile adult thalli. The same stage of development of thalli was considered to pass up unpredictability linked to the physiological state of individuals, and entire algal thalli were considered when determining total lipids and FAs to avoid any intra-thallus variation among the species (^{Connan et al. 2007}, ^{Abdala-Díaz et al. 2014}).

Figure 2 Cystoseira species collected along the Tunisian coast (scale bar = 1 cm). 1, Cystoseira amentacea var. stricta; 2, Cystoseira barbata; 3, Cystoseira compressa; 4, Cystoseira crinita; 5, Cystoseira elegans; 6, Cystoseira foeniculacea; 7, Cystoseira foeniculacea f. latiramosa; 8, Cystoseira foeniculacea f. tenuiramosa (North); 9, Cystoseira foeniculacea f. tenuiramosa (South); 10, Cystoseira schiffneri; 11, Cystoseira sauvageauana; 12, Cystoseira sedoides.

Extraction and estimation of total lipids

Five grams of each sample were pulverized in liquid nitrogen with a mortar and pestle. Extraction was done by the chloroform-methanol method according to ^{Nomura et al. (2013)}. The obtained organic phase was subjected to total lipid and FA methyl esters (FAME) analysis. Total lipid content was determined gravimetrically and expressed as milligrams per gram of dry weight (DW) after evaporation of the solvent on a rotary vacuum evaporator at 30 ºC. All analyses were performed in triplicate.

Preparation of fatty acid methyl esters

FAs were transformed to their FAME by transmethylation in accordance with ^{Prevot and Mordret (1976)}, with slight modifications. Briefly, 1.0 mL of hexane was added to 10 ± 1 mg of total lipid aliquot and 0.2 mL 2 N NaOH in MeOH, vortexed for 10 s, then heated at 55 ºC for 30 s. Then 0.2 mL 2 N HCl in MeOH was added and vortexed for 60 s. The mixture was centrifuged (Sorvall RC5C instruments, Fiberlite F21-8x50y rotor, Thermofisher, USA) at 1,000 × g for 5 min. The upper hexane layer containing FAME was subjected to gas chromatography coupled with mass spectrometry analysis.

Gas chromatography coupled with mass spectrometry analysis

Gas-chromatography coupled with mass spectrometry (GC-MS) was used to establish the FA profile of the lipid fraction. GC-MS analysis was done on an Agilent 7890A chromatograph equipped with an Agilent 5975C inert Mass Selective Detector and a HP-5 MS fused-silica capillary column (30.0 m × 0.25 mm, 0.25 μm film thickness). The column temperature regime was 150 ºC for 2 min, followed by 230 ºC at 4 ºC·min_-1 and 230 ºC for 5 min. Helium was used as a carrier gas at a rate flow of 0.8 mL·min^-1. Mass scan range was 50-550 amu at 70 eV and scan velocity was 2.86 scans per second. One microliter of each sample was injected. Identification of FAME was carried out by comparing their retention times with those of FAME standards and by comparing their mass spectra with those recorded in the NIST08 and W8N08 mass spectral libraries.

Determining lipid quality indices

For the unsaturation index (UI), the molar proportion (percentage) of each FA was multiplied by the number of double bonds after addition:

UI = Sum % unsaturated acids × number of double bonds (1)

To assess the nutritional and lipid quality of Cystoseira species, health lipid indices (indices of atherogenicity [IA] and thrombogenicity [IT]) were estimated in accordance with the ^{Ulbricht and Southgate (1991)} method based on FA composition: where MUFA indicates monounsaturated FA and PUFA indicates polyunsaturated FA.

IA= C12:0+4 X C14:0+C16:0∑MUFA+ ∑n-6 PUFA+ ∑(n-3 PUFA) . (2)

IT=C14:0+C16:0+C18:00.5 X ΣMUFA +0.5 X Σn-6 PUFA+3 X Σn-3 PUFA + Σn-3 PUFAΣ(n-6 PUFA) , (3)

Statistical analysis

The results were expressed as mean values ± standard deviation of the 3 replicates. Mean total lipid and FA values were assessed using one-way analysis of variance (ANOVA) at P < 0.05, using the Statgraphics Centurion 16.1.11 software for Windows. Multivariate analyses (^{Sokal and Michener 1958}) were carried out to evaluate the grouping of the studied species according to their total lipid and FA composition: (i) the cluster analysis was performed using the unweighted pair group method with arithmetic mean (UPGMA) and the Euclidean distance (D_E), the UPGMA being authentic for ecological classification tools especially in species composition (^{Legendre and Legendre 1998}); (ii) the principal component analysis (PCA) was carried out to differentiate between species and forms. Multivariate analyses were done using the MultiVariate Statistical Package (MVSP) software for Windows v3.1, following ^{Kovach (2007)}.

Results

Total lipid content

The total lipid content of the 11 Cystoseira species showed wide fluctuations (Table 1). The yield for the total lipid fraction extracted varied in the range between 1.98% (C. schiffneri) and 6.82% DW (C. sauvageauana) (Table 1).

Table 1 Lipid extracts of Cystoseira species collected along the Tunisian coast. DW, dry weight; FW, fresh weight; N, northern coast of Tunisia; and S, southeastern coast of Tunisia.

Species	Total lipids
	(mg·g^-1 DW)*	Yield* (FW% w/w)
Cystoseira amentacea var. stricta (N)	39.60 ± 3.60^cd	5.28 ± 2.31^cd
Cystoseira barbata (S)	30.80 ± 2.80^ef	4.11 ± 1.80^ef
Cystoseira compressa (N)	46.20 ± 4.20^bc	6.16 ± 2.70^bc
Cystoseira crinita (N)	66.00 ± 6.00^a	8.80 ± 3.86^a
Cystoseira elegans (S)	47.50 ± 4.50^b	6.33 ± 2.78^b
Cystoseira foeniculacea (N)	52.80 ± 4.80^b	7.04 ± 3.09^b
Cystoseira foeniculacea f. latiramosa (N)	24.20 ± 2.20^fg	3.23 ± 1.41^fg
Cystoseira foeniculacea f. tenuiramosa (N)	31.20 ± 2.40^e	4.16 ± 1.82^e
Cystoseira foeniculacea f. tenuiramosa (S)	33.00 ± 3.00^de	4.40 ± 1.93^de
Cystoseira sauvageauana (N)	68.20 ± 6.20^a	9.09 ± 3.99^a
Cystoseira schiffneri (S)	19.80 ± 1.80^g	2.64 ± 1.16^g
Cystoseira sedoides (N)	33.00 ± 3.00^de	4.40 ± 1.93^de

*Data are expressed as mean ± SD, where n = 3; values in a column without a common superscript are significantly different (P < 0.05).

Fatty acid profile of lipid extract

Fourteen major FAs were identified in the lipid fraction of the 11 Cystoseira species (Table 2). The FA content of Cystoseira lipids varied widely between species. The FA profile of lipid extracts was characterized by high amounts of saturated FAs (SFAs) ranging from 40.51% (C. amentacea var. stricta) to 57.91% (C. compressa) of total FAs. Palmitic acid (C16:0) was the predominant lipid fraction, with the highest rate being found in C. foeniculacea f. tenuiramosa (44.70%). Cystoseira barbata was found to be rich in myristic acid (C14:0, 7.45%), while stearic acid (C18:0) characterized C. compressa (15.27%) (Table 2).

Table 2 Fatty acid composition and nutritional indices (expressed as percent of total fatty acids) for Cystoseira species collected along the Tunisian coast. N, north; S, south; ∑SFAs, sum of saturated fatty acids; ∑MUFAs, sum of monounsaturated fatty acids; ∑PUFAs, sum of polyunsaturated fatty acids; AA, arachidonic acid; EPA, eicosapentanoic acid; Tr., trace fatty acids that were present at <0.1%; n.d., fatty acid not detected; UI, unsaturation index; IA, index of atherogenicity; IT, index of thrombogenicity.

Common name

Cystoseira amentacea var. stricta

Cystoseira barbata

Cystoseiracom presa

Cystoseira crinita

Cystoseira elegans

Cystoseira foeniculacea

Cystoseira foeniculacea f. latiramosa

Cystoseira foeniculacea f. tenuiramosa (N)

Cystoseira foeniculacea f. tenuiramosa (S)

Cystoseira sauvageauan α

Cystoseira schiffneri

Cystoseira sedoides

C14:0

5.82 ± 0.13^abcd

7.45 ± 0.69^a

4.39 ± 0.44^def

6.91 ± 0.13^ab

5.60 ± 2.33^bcd

5.17 ± 0.39^cdef

3.87 ± 0.02^ef

5.24 ± 1.39^bcde

5.10 ± 0.22^cdef

6.38 ± 1.82^abc

5.08 ± 0.37^cdef

3.54 ± 0.65^f

C15:0

n.d.

0.20 ± 0.17^bc

0.13 ± 0.22^c

0.23 ± 0.23^bc

n.d.

0.75 ± 0.37^a

n.d.

Tr.

0.48 ± 0.04^c

0.44 ± 0.09^b

C16:0

32.96 ± 1.76^de

32.05 ± 0.20^de

38.05 ± 1.83^bc

30.13 ± 0.33^e

36.18 ± 1.77^bcd

38.78 ± 1.18^bc

39.11 ± 0.64^bc

44.70 ± 6.44^a

39.88 ± 3.54^b

35.37 ± 0.25^cd

32.89 ± 3.09^de

35.19 ± 0.23^cd

C18:0

1.73 ± 0.33^e

6.19 ± 2.21^bcd

15.27 ± 3.37^a

3.47 ± 1.76^de

4.29 ± 0.61^cde

4.14 ± 0.24c^de

7.82 ± 0.15^b

3.20 ± 0.67^de

2.50 ± 1.93^e

6.95 ± 3.39^bc

3.01 ± 3.07^e

1.60 ± 0.13^e

∑SFA

40.51 ± 1.33^f

45.69 ± 1.33^def

57.91 ± 3.87^a

40.64 ± 1.72^f

47.38 ± 4.62^cde

48.09 ± 1.62^bcd

51.56 ± 0.14^bc

53.14 ± 8.41^b

54.91 ± 2.96^cde

49.33 ± 2.51^bcd

42.11 ± 0.13^f

41.90 ± 0.81^ef

C16:1n-7

3.00 ± 0.28^ef

2.93 ± 0.38^efg

3.13 ± 0.26^ef

1.92 ± 0.05^g

3.81 ± 0.82^e

7.82 ± 0.63^b

5.46 ± 0.02^d

6.36 ± 0.63^cd

7.47 ± 0.30^b

2.20 ± 1.47^fg

7.26 ± 0.60^bc

9.91 ± 0.57^a

C18:1n-9

26.88 ± 1.31^a

26.56 ± 2.05^ab

20.60 ± 0.67^ef

24.55 ± 1.60^bc

21.56 ± 0.32d^ef

17.67 ± 1.06^g

19.71 ± 0.55^fg

20.42 ± 0.93^ef

20.79 ± 2.16^def

22.05 ± 1.50^de

25.19 ± 0.42^ab

22.84 ± 0.86^cd

Trans-18:1

2.35 ± 0.39^bc

1.78 ± 0.06^bc

1.57 ± 0.41^c

1.24 ± 0.05^c

4.58 ± 3.25^a

2.72 ± 0.23^bc

1.12 ± 0.05^c

2.62 ± 0.17^bc

1.28 ± 0.26^c

2.27 ± 0.12^bc

4.64 ± 0.30^a

3.49 ± 1.27^ab

∑MUFAs

32.23 ± 1.80^b

31.27 ± 1.33^bc

25.30 ± 0.36^f

27.71± 1.58^def

29.93 ± 4.22^bcd

28.21 ± 0.91^cdef

26.30 ± 0.57^f

29.40 ± 0.80^bcde

29.51 ± 2.38^bcde

26.51 ± 1.83^ef

37.09 ± 1.18^a

36.17 ± 0.96^a

C18:2n-6

4.81 ± 0.08^bc

5.69 ± 0.77^ab

3.86 ± 1.94b^cd

5.32 ± 0.29^bc

7.59 ± 2.13^a

5.87 ± 0.45^ab

5.94 ± 0.23^ab

3.40 ± 2.95^cd

5.73 ± 0.36^ab

5.56 ± 1.56^abc

4.15 ± 0.22^bcd

2.42 ± 0.31^d

C18:3n-6

1.12 ± 0.34^ab

0.87 ± 0.75^abc

Tr.

0.99 ± 0.05^ab

1.67 ± 0.90^a

1.76 ± 0.54^a

0.38 ± 0.04^bc

0.68 ± 1.18^bc

0.23 ± 0.10^bc

0.61 ± 0.45^bc

0.77 ± 0.04^bc

0.40 ± 0.15b^c

C18:4n-3

3.10 ± 0.23^a

1.46 ± 0.21^bcd

1.07 ± 0.82^cd

2.36 ± 2.06^abc

0.62 ± 0.11^d

2.20 ± 0.21^abc

2.71 ± 0.01^ab

2.06 ± 1.90^abc

1.27 ± 0.03^bcd

1.37 ± 0.24^bcd

1.62 ± 0.17^bcd

0.92 ± 0.10^cd

C20:2n-6

n.d.

0.31 ± 0.55^b

0.33 ± 0.25^b

n.d.

0.71 ± 0.32^b

0.34 ± 0.25^b

0.27 ± 0.19^b

0.20 ± 0.24^b

n.d.

0.37 ± 0.15^b

1.08 ± 0.21^a

C20:3n-6

0.96 ± 0.03^bcd

0.51 ± 0.36^cd

0.87 ± 0.69^cd

2.07 ± 1.46^a

0.74 ± 0.05^cd

1.32 ± 0.12^abc

1.08 ± 0.05^bc

1.01 ± 0.93^bc

0.40 ± 0.39^cd

Tr.

0.60 ± 0.06^cd

1.92 ± 0.38^ab

C20:4n-6 (AA)

14.45 ± 0.41^ab

12.70 ± 0.56^bc

7.35 ± 2.46^f

15.98 ± 1.54^a

10.97 ± 0.67^cd

9.94 ± 0.79^de

7.91 ± 0.25^ef

8.20 ± 0.75^ef

12.74 ± 1.07^bc

14.56 ± 1.51^ab

10.47 ± 1.41^d

11.97 ± 1.19^cd

C20:5n-3

1.74 ± 0.43^cde

1.43 ± 0.09^def

1.59 ± 0.31^de

3.31 ± 0.62^a

0.86 ± 0.05^f

2.01 ± 0.17^cd

3.01 ± 0.39^ab

1.58 ± 0.84^de

1.20 ± 0.12^ef

2.01 ± 0.72^cd

1.63 ± 0.24^de

2.42 ± 0.20^bc

∑PUFAs

26.17 ± 0.62^ab

24.12 ± 0.81^bc

15.05 ± 4.14^e

30.35 ± 2.38^a

22.45 ± 0.50^bc

23.80 ± 2.08^bc

22.10 ± 0.36^cd

17.21 ± 7.62^de

21.77 ± 0.82^bcd

24.12 ± 0.77^bc

19.60 ± 1.26c^de

21.15 ± 0.90^cd

PUFA/SFA

0.65 ± 0.03^a

0.50 ± 0.02^b

0.26 ± 0.09^d

0.75 ± 0.09^a

0.49 ± 0.06^b

0.48 ± 0.06^b

0.41 ± 0.01^bc

0.34 ± 0.18^cd

0.45 ± 0.03^bc

0.50 ± 0.04^b

0.48 ± 0.03^b

0.52 ± 0.03^b

Σn-3

4.83 ± 0.56^ab

2.89 ± 0.28^cde

2.66 ± 1.02^cde

5.67 ± 1.75^a

1.48 ± 0.06^e

4.20 ± 0.37^abc

5.69 ± 0.39^a

3.65 ± 2.68^bcd

2.47 ± 0.13^de

3.38 ± 0.13^bcd

3.24 ± 0.07^bcd

3.34 ± 0.147^bcd

Σn-6

21.33 ± 0.66^b

19.76 ± 0.56^bc

12.39 ± 3.43^g

24.68 ± 0.79^a

20.97 ± 0.56^bc

19.09 ± 1.70^bcd

15.66 ± 0.32^efg

13.29 ± 5.13^fg

19.11 ± 0.50^bcd

20.73 ± 0.51^bc

16.35 ± 1.19^def

17.80 ± 0.76^cde

Σn-6/Σn-3

4.41 ± 0.64^cd

5.75 ± 0.44^bc

4.66 ± 1.95^bcd

4.69 ± 1.63^cd

10.95 ± 3.57^a

4.67 ± 0.12^cd

2.76 ± 0.13^d

6.16 ± 5.63^bc

7.83 ± 0.19^b

6.26 ± 1.16^bc

5.04 ± 0.25^bcd

5.33 ± 0.08^bcd

AA/EPA

8.77 ± 2.74^bc

8.88 ± 0.17^bc

4.62 ± 1.37^ef

5.93 ± 1.52^def

12.85 ± 1.53^a

4.97 ± 0.30^def

2.66 ± 0.26^f

6.75 ± 4.46^cde

10.66 ± 0.96^ab

7.76 ± 2.28^bcd

6.47 ± 0.55^cde

4.94 ± 0.09^def

126.95 ± 2.32^ab

110.56 ± 2.43^c

77.23 ± 12.90^e

137.41 ± 8.38^a

103.02 ± 2.92^cd

107.74 ± 5.57^c

100.0 ± 3.11^cd

90.26 ± 25.23^de

104.91 ± 2.90^cd

113.25 ± 5.96^bc

105.97 ± 4.92^c

111.68 ± 4.31^bc

0.96 ± 0.05^c

1.15 ± 0.02^abc

1.40 ± 0.13^ab

0.99 ± 0.03^c

1.13 ± 0.31^bc

1.15 ± 0.08^abc

1.14 ± 0.02^abc

1.48 ± 0.59^a

1.18 ± 0.10^abc

1.20 ± 0.14^abc

0.94 ± 0.07^c

0.86 ± 0.07^c

0.98 ± 0.04^c

1.33 ± 0.09^bc

2.23 ± 0.47^a

0.94 ± 0.16^c

1.55 ± 0.27^bc

1.32 ± 0.10^bc

1.32 ± 0.05^bc

1.88 ± 1.10^ab

1.49 ± 0.16b^c

1.44 ± 0.17^bc

1.12 ± 0.01^c

1.08 ± 0.05^c

Values are expressed as mean ± SD of 3 replicates at 95% confidence interval. Different superscript letters in the same row are significantly different (P < 0.05); values were rounded off to 2 decimal places and may not total 100%.

MUFAs ranged from 25.30% of total FAs in C. compressa to 37.1% in C. schiffneri. The major MUFA (>20% of total FAs) for most of the studied Cystoseira species was oleic acid (C18:1).

Total PUFAs varied between 15.05% (C. compressa) and 30.35% (C. crinita). Among the PUFAs, arachidonic acid (C20:4n-6) was the most abundant in the analyzed species, with a particular high level of 15.98% in C. crinita. The highest percentage of linoleic acid (C18:2n-6) was observed in C. elegans (7.59%), while the highest percentages of the eicosapentaenoic acid (C20:5n 3) and stearidonic acid (C18:4n-3) were observed in C. crinita (3.31%) and C. amentacea var. stricta (3.10%), respectively. Omega 3 PUFAs were detected in all studied species. Total omega 3 (∑n-3) ranged between 1.48% (C. elegans) and 5.69% (C. foeniculacea f. latiramosa). Cystoseira foeniculacea f. latiramosa and C. crinita were the richest species in n-3 PUFA (5.69% and 5.67% of total FAs, respectively). This richness is associated with the high rates of n-3 marine triglyceride (C20:5n-3), an important n-3 PUFA, that they contain. Stearidonic acid (C18:4n-3) was also detected in all studied species in rates varying between 0.62% (C. elegans) and 3.10% (C. amentacea var. stricta). Linoleic acid (C18:2n-6) was found in all studied species at rates ranging between 2.42% (C. sedoides) and 7.59% (C. elegans). Cystoseira crinita was the richest in the dihomo-γ-linolenic acid (C20:3n-6, 2.07%), an uncommon FA.

Discrimination of Cystoseira

The results of FA composition were evaluated using multivariate analyses to investigate whether the various lipid and FA patterns correlated with the taxonomic position of the brown Cystoseira algae and lead to distinguish between species and forms. Differentiating species according to their chemical composition could be valuable when examining any possible relationship between them. In this regard, a PCA was performed to consider the FA composition of each sample investigated. The 3 axes accounted for 86.89% of total variance. The first 2 dimensions explained 78.07% of the variability. Principal component (PC) 1 was defined by palmitic acid (C16:0), oleic acid (C18:1n-9), and arachidonic acid (C20:4n-6), while the most discriminant variable along the PC2 axis was stearic acid (C18:0) and explained 27.89% of total variation. PC3 was defined by elaidic acid (Trans C18:1), myristic acid (C14:0), palmitoleic acid (C16:1n-7), and linoleic acid (C18:2n-6). Plotting on axes 1 and 2 divided species into 3 major groups (Fig. 3). The first group included only C. compressa, the second comprised the C. foeniculacea group (C. foeniculacea and its forms tenuiramosa and latiramosa), and the third, the most heterogeneous one, comprised the other Cystoseira samples (Fig. 3).

Figure 3 Principal component analysis using fatty acid composition of Cystoseira taxa. The Cystoseira foeniculacea forms are denoted by squares. S, south; and N, north.

With the hierarchical clustering analysis, the dendrogram of FAs for the Cystoseira samples showed the presence of 4 clusters that were connected at D_E = 14.7 (Fig. 4). Species were grouped independently of their geographic distribution. The greatest similarity was observed between C. amentacea var. stricta and C. crinita at D_E = 5.2. As in the PCA model, the C. foeniculacea forms were closely linked and grouped in a single cluster at D_E = 11.4 (Fig. 4).

Figure 4 Dendrogram showing hierarchical clustering (UPGMA method) of Cystoseira samples by fatty acid content. S, south; N, north.

Nutritional quality assessment

The PUFA/SFA ratio is commonly used to evaluate the nutritional quality of the lipid fraction of foods. Except for C. compressa and C. foeniculacea f. tenuiramosa, the Cystoseira species analyzed in the present study exhibited PUFA/SFA ratios exceeding 0.4 (Table 2). The n-3 and n-6 PUFAs represent a significant part of the Cystoseira lipids. The n-3 PUFA ranged between 1.48% (C. elegans) and 5.69% (C. foeniculacea f. latiramosa), while the n-6 PUFA varied between 12.39% (C. compressa) and 24.68% (C. crinita) of total FA. The 11 Cystoseira species exhibited high unsaturation indices, varying from 77.23 (C. compressa) to 137.41 (C. crinita). The highest IA and IT values were, respectively, 1.48 (C. foeniculacea f. tenuiramosa) and 2.23 (C. compressa) (Table 2).

Discussion

Total lipid content in the 11 Cystoseira species analyzed in this study was close to that reported for C. brachycarpa (^{Ragonese et al. 2014}) off Italy and C. osmundacea (^{Khotimchenko et al.
2002}) in the Sea of Japan. However, total lipid rates for Tunisian Cystoseira were higher than those for Moroccan Cystoseira from the Atlantic (between 1.3 and 16 mg·g^-1 DW, ^{Valls et al. 1993}) and those for Indian Cystoseira (between 6.1 and 6.7 mg·g^-1 fresh weight [FW], ^{Kumari et
al. 2013}). The species investigated here are poorly studied in the world as regards their total lipid content. This study shows that Tunisian C. barbata (4.11 g·100 g^-1 FW) and C. crinita (8.8 g·100 g^-1 FW) are richer in total lipids than species from the Black Sea harvested during the same season (0.84 g·100 g^-1 FW for C. barbata [^{Ivanova et al. 2012}] and 0.72 g·100 g^-1 FW for C. crinita [Ivanova et al. 2013]), and these differences are related to environmental conditions. In fact, it is proven that in algae, total lipid content depends on temperature, light, and salinity (^{Kim et al. 1996}), factors that are very different between Tunisian and Black Sea waters. Intraspecific variability in total lipid content could also be dependent on the physiological state of the species, as suggested by the higher rate observed in this study for C. barbata (3.08%), compared to that reported by ^{Frikha et al. (2011)} for the same species in almost the same environmental conditions (2.51%, Gulf of Gabès, Tunisian southern coast).

In General, C. compressa was the richest in SFA, whereas C. amentacea var. stricta and C. schiffneri stood out for their high content of PUFA and MUFA. Palmitic acid (C16:0) was the main FA of the Cystoseira lipids, followed by oleic acid. These results confirm data previously reported in the literature for the profile commonly seen in brown algae, especially in Cystoseira species (^{Khotimchenko et al. 2002}; ^{Ivanova et al. 2012}, ²⁰¹³; ^{Kumari et al.
2013}; ^{Ragonese et al. 2014}; ^{Vizetto-Duarte et al. 2015}). For a given taxon, the differences between the FA profile observed in Tunisia and those reported in the literature for other regions could be related to the different seasons in which the studied samples were harvested and so to the different physiological states of the concerned species and/or to the differences in environmental conditions of habitats in the different regions. Temperature seems to be the factor that most affects the percentage of SFA and PUFA; for instance, ^{Colombo et
al. (2006)} proved that algae from cold water (e.g., Canada) were usually richer in PUFA, with a higher n-3/n-6 FA ratio, than algae from warm water (e.g., China), and studies carried out in cold waters (Atlantic waters) exhibited higher SFA ratios than PUFA ratios in Cystoseira species (^{Vizetto-Duarte et al. 2015}). However, the highest PUFA ratios found in warm-water algae from the Sea of Japan (^{Nomura et al. 2013}) suggest that the environmental factors in the species’ habitat, other than temperature, could influence the FA profiles of algae.

Species from different localities did not show clustering behavior along the 2 axes of the PCA (Fig. 3). Furthermore, the PCA score plot of species highlighted that the FA composition of a species was independent of its origin. This low geographic differentiation could be explained by intraspecific diversity, which might affect the variability in FA composition. Samples of the C. foeniculacea group were distributed mainly along axis 2 and aggregated close to each other (group 2), showing low variation in the pool of variables considered and that species displayed a similar lipid profile (Fig. 3). The C. foeniculacea group was clustered according to its forms. Cystoseira foeniculacea f. tenuiramosa from different regions (north and south) were grouped together.

It is not surprising that C. schiffneri was segregated from the C. foeniculacea group since C. schiffneri (^{sensu Hamel 1939}) (^{Hamel 1931-1939}), considered as a synonym of C. foeniculacea f. schiffneri (Hamel) Gómez-Garreta, Barceló, Ribera and Rull Lluch(^{Gómez-Garreta et al. 2001}), was recently reinstated as a specific rank, a distinct entity of the Cystoseira species (^{Bouafif et
al. 2016}). This discrimination of Cystoseira based on FAs supports the reinstatement of C. schiffneri (Hamel) as a specific rank.

Hierarchical clustering analysis revealed that species were more related to each other by their FA composition than by their geographic distribution, highlighting the intraspecific diversity in the genus Cystoseira (Fig. 4). The clustering of the C. foeniculacea group according to the FA profile supports earlier evidence that lipid composition could be a biochemical marker for each taxonomic group.

The PUFA/SFA ratios obtained in the present study are within the nutritional guidelines recommending a PUFA/SFA ratio higher than 0.4 (^{Wood et al. 2004}). The n-6/n-3 PUFA ratios ranging from 2.76 (C. foeniculacea f. latiramosa) to 10.95 (C. elegans) for the 11 Cystoseira species were comparable to those for Portuguese Cystoseira species (^{Vizetto-Duarte et al. 2015}), and these high ratios are explained by the high levels of n-6 PUFAs in the lipid composition of the species. Seaweed FAs are beneficial for the prevention of cardiovascular diseases and other chronic diseases, such as diabetes, hypertension, and autoimmune disease, in humans (^{Dawczynski et al. 2007}). Some studies suggested a beneficial n-6/n-3 ratio between 1:1 and 5:1 for human nutrition (^{Simopoulos 2002}, ²⁰⁰⁸); the Food and Agriculture Organization of the United Nations/World Health Organization committee recommended, in turn, an n-6/n-3 ratio between 5:1 and 10:1 (^{FAO/WHO 1995}). Regarding our results, all 11 Tunisian Cystoseira species have high nutritional values.

High IA and IT values have adverse effects on human health and are considered potent indicators of and important factors for increased risk of coronary heart disease, where the higher the values the more degraded the nutritional quality (^{Ulbricht and Southgate 1991}). The IT values for the algae analyzed in the present study were comparable to the IT values found by Ulbricht and Southgate (1991) for meat (0.7-1.1) and milk-based products (1.32). Thus, the results obtained in the present study suggest that C. amentacea, C. crinita, and C. sedoides were more antithrombogenic and antiatherogenic than the other analyzed Cystoseira species and could be used in nutraceuticals or food.

In conclusion, all studied species of Cystoseira have the same qualitative major FA composition. Interspecific quantitative variability in FA composition is, however, pointed out. This variability could be linked to environmental, biological, and physiological factors. Clustering of C. foeniculacea and its infrataxa (the latiramosa and tenuiramosa forms) according to the FA profiles suggest a possible use of FA composition for taxonomic purposes for the genus Cystoseira. This study further supports and confirms the recent study by ^{Bouafif et al. (2016)} about the reinstatement of the endemic Mediterranean C. schiffneri, considered before as a form of C. foeniculacea. The PUFA/SFA, n-6/n-3 PUFA, IA, and IT, indicators of nutritional lipid quality in food, suggest that the Cystoseira species studied here can be an interesting source of dietary FAs with beneficial effects on human health.

To our knowledge, this work is one of the rare investigations of lipid composition and nutritional value of Mediterranean Cystoseira species, some of which are rare and endemic.

Acknowledgments

We are grateful to the Regional Activity Center for Specially Protected Areas for its financial support. The authors are grateful to the staff from the Laboratory of Plant Biotechnology (National Institute of Applied Science and Technology, Tunis, Tunisia) for their technical assistance. Many thanks go to the anonymous reviewers for their comments and constructive criticism of the manuscript.

References

Abdala-Díaz RT, Cabello-Pasini A, Márquez-Garrido E, López-Figueroa F. 2014. Intra-thallus variation of phenolic compounds, antioxidant activity, and phenolsulphatase activity in Cystoseira tamariscifolia (Phaeophyceae) from southern Spain = Variación intratalo de compuestos fenólicos, actividad antioxidante y actividad de la fenolsulfatasa en Cystoseira tamariscifolia (Phaeophyceae) del sur de España. Cienc. Mar. 40(1): 1-10. http://dx.doi.org/10.7773/cm.v40i1.2350 [ Links ]

Amico V. 1995. Marine brown algae of family Cystoseiraceae: Chemistry and chemotaxonomy. Phytochemistry 39(6): 1257-1279. https://doi.org/10.1016/0031-9422(95)00199-h [ Links ]

Barre SLL, Weinberger F, Kervarec N, Potin P. 2004. Monitoring defensive responses in macroalgae- limitations and perspectives. Phytochem. Rev. 3(3): 371-379. https://doi.org/10.1007/s11101-005-1459-3 [ Links ]

Bouafif C, Verlaque M, Langar H. 2014. Cystoseira taxa new for the marine flora of Tunisia. Cryptogamie Algol. 35(3): 269-283. http://dx.doi.org/10.7872/crya.v35.iss3.2014.269 [ Links ]

Bouafif C, Verlaque M, Langar H. 2016. New contribution to the knowledge of the genus Cystoseira C. Agardh in the Mediterranean Sea, with the reinstatement of species rank for C. schiffneri Hamel. Cryptogamie Algol. 37(2): 133-154 http://dx.doi.org/10.7872/crya/v37.iss2.2016.133 [ Links ]

Calder PC. 2006. n-3 polyunsaturated fatty acids, inflammation, and inflammatory diseases. Am. J. Clin. Nutr. 83(6): 1505S-1519S. https://doi.org/10.1093/ajcn/83.6.1505S [ Links ]

Colombo ML, Risè P, Giavarini F, De Angelis L, Galli C, Bolis CL. 2006. Marine macroalgae as sources of polyunsaturated fatty acids. Plant Foods Hum. Nutr. 61(2): 64-69. https://doi.org/10.1007/s11130-006-0015-7 [ Links ]

Connan S, Deslandes E, Gall EA. 2007. Influence of day-night and tidal cycles on phenol content and antioxidant capacity in three temperate intertidal brown seaweeds. J. Exp. Mar. Biol. Ecol. 349(2): 359-369. https://doi.org/10.1016/j.jembe.2007.05.028 [ Links ]

Dawczynski C, Schubert R, Jahreis G. 2007. Amino acids, fatty acids, and dietary fibre in edible seaweed products. Food Chem. 103(3): 891-899. https://doi.org/10.1016/j.foodchem.2006.09.041 [ Links ]

Ercegovič A. 1952. Fauna i Flora Jadrana. Jadranske cistozire. Njihova morfologija, ekologija i razvitak/Fauna et Flora Adriatica. Vol. 2- Split, Institut za Oceanografiju i Ribarstvo Split, pp. 1-172 (Croatian), 173-210 (French), 211-212 (references), Map. [ Links ]

[FAO/WHO] Food and Agriculture Organization of the United Nations/World Health Organization. 1995. WHO and FAO joint consultation: Fats and oils in human nutrition. Nutr. Rev. 53(7): 202-205. https://doi.org/10.1111/j.1753-4887.1995.tb01552.x [ Links ]

Frikha F, Kammoun M, Hammami N, Mchirgui RA, Belbahri L, Gargouri Y, Miled N, Ben-Rebah F. 2011. Chemical composition and some biological activities of marine algae collected in Tunisia = Composición química y algunas actividades biológicas de algas marinas recolectadas en Túnez. Cienc. Mar. 37(2): 113-124. https://doi.org/10.7773/cm.v37i2.1712 [ Links ]

Galloway AWE, Britton-Simmons KH, Duggins DO, Gabrielson PW, Brett MT. 2012. Fatty acid signatures differentiate marine macrophytes at ordinal and family ranks. J. Phycol. 48(4): 956-965. https://doi.org/10.1111/j.1529-8817.2012.01173.x [ Links ]

Gómez-Garreta A, Barcelo I-Martí MC, Ribera-Siguán MA, Rull-Lluch J. 2001. Cystoseira C. Agardh. In: Gómez-Garreta A (ed.), Flora Phycologica Iberica. Vol. 1, Fucales. Universidad de Murcia Press, Murcia (Spain), pp. 99-166. [ Links ]

Guiry MD, Guiry GM. 2016. AlgaeBase. [Accessed 05 December 2016] World-wide electronic publication, National University of Ireland, Galway. http://www.algaebase.org [ Links ]

Hamel G. 1931-1939. Phéophycées de France. [Publisher unknown] Paris (France), 432 pp. + 10 Plates. [ Links ]

Ivanova V, Stancheva M, Merdzhanova A. 2012. Fatty acids composition of macroalgae from Bulgarian Black Sea coast. OUAC 23(1): 35-40. https://doi.org/10.2478/v10310-012-0005-6 [ Links ]

Ivanova V, Stancheva M, Petrova D. 2013. Fatty acid composition of Black Sea Ulva rigida and Cystoseira crinita. Bulg. J. Agric. Sci. 19(S1): 42-47. [ Links ]

Khotimchenko SV, Vaskovsky VE, Titlyanova TV. 2002. Fatty acids of marine algae from the Pacific coast of North California. Bot. Mar. 45(1): 17-22. https://doi.org/10.1515/bot.2002.003 [ Links ]

Kim MK, Dubacq JP, Thomas JC, Giraud G. 1996. Seasonal variations of triacylglycerols and fatty acids in Fucus serratus. Phytochemistry 43(1): 49-55. https://doi.org/10.1016/0031-9422(96)00243-9 [ Links ]

Kovach WL. 2007. MVSP-A Multi-Variate Statistical Package for Windows, ver. 3.1. Kovach Computing Services, Pentraeth (Wales, United Kingdom), 137 pp. [ Links ]

Kumar M, Kumari P, Trivedi N, Shukla MK, Gupta V, Reddy CRK, Jha B. 2011. Minerals, PUFAs and antioxidant properties of some tropical seaweeds from Saurashtra coast of India. J. Appl. Phycol. 23(5): 797-810. https://doi.org/10.1007/s10811-010-9578-7 [ Links ]

Kumari P, Bijo AJ, Mantri VA, Reddy CRK, Jha B. 2013. Fatty acid profiling of tropical marine macroalgae: An analysis from chemotaxonomic and nutritional perspectives. Phytochemistry 86: 44-56. https://doi.org/10.1016/j.phytochem.2012.10.015 [ Links ]

Kumari P, Kumar M, Gupta V, Reddy CRK. Jha B. 2010. Tropical marine macroalgae as potential sources of nutritionally important PUFAs. Food Chem. 120(3): 749-757. https://doi.org/10.1016/j.foodchem.2009.11.006 [ Links ]

Legendre P, Legendre L. 1998. Numerical Ecology. 2nd English Ed. Elsevier Science BV, Amsterdam (Netherlands), 853 pp. [ Links ]

Nomura M, Kamogawa H, Susanto E, Kawagoe C, Yasui H, Saga N, Hosokawa M, Miyashita K. 2013. Seasonal variations of total lipids, fatty acid composition, and fucoxanthin contents of Sargassum horneri (Turner) and Cystoseira hakodatensis (Yendo) from the northern seashore of Japan. J. Appl. Phycol. 25(4): 1159-1169. https://doi.org/10.1007/s10811-012-9934-x [ Links ]

Pellegrini M, Valls R, Pellegrini L. 1997. Chimiotaxonomie et marqueurs chimiques dans les algues brunes. Lagascalia 19(1-2): 145-164. [ Links ]

Pereira H, Barreira L, Figueiredo F, Custódio L, Vizetto-Duarte C, Polo C, Rešek E, Engelen A, Varela J. 2012. Polyunsaturated fatty acids of marine macroalgae: Potential for nutritional and pharmaceutical applications. Mar. Drugs 10(9): 1920-1935. https://doi.org/10.3390/md10091920 [ Links ]

Piattelli M. 1990. Chemistry and taxonomy of Sicilian Cystoseira species. New J. Chem. 14: 777-782. [ Links ]

Pohnert G, Boland W. 2002. The oxylipin chemistry of attraction and defense in brown algae and diatoms. Nat. Prod. Rep. 19(1): 108-122. https://doi.org/10.1039/a806888g [ Links ]

Prevot AF, Mordret FX. 1976. Utilisation des colonnes capillaires de verre pour l’analyse des corps gras par chromotographie en phase gazeuse. Rev. Fr. Corps Gras. 23(7/8): 409-423. [ Links ]

Ragonese C, Tedone L, Beccaria M, Torre G, Cichello F, Cacciola F, Dugo P, Mondello L. 2014. Characterisation of lipid fraction of marine macroalgae by means of chromatography techniques coupled to mass spectrometry. Food Chem. 145: 932-940. https://doi.org/10.1016/j.foodchem.2013.08.130 [ Links ]

Rosell KG, Srivastava LM. 1987. Fatty acids as antimicrobial substances in brown algae. In: Ragan MA, Bird CJ (eds.), Twelfth International Seaweed Symposium. Developments in Hydrobiology, vol. 41. Springer, Dordrecht, (Netherlands), pp. 471-475. https://doi.org/10.1007/978-94-009-4057-4_69 [ Links ]

Schnitzler I, Pohnert G, Hay M, Boland W. 2001. Chemical defense of brown algae (Dictyopteris spp.) against the herbivorous amphipod Ampithoe longimana. Oecologia 126(4): 515-521 https://doi.org/10.1007/s004420000546 [ Links ]

Simopoulos AP. 2002. The importance of the ratio of omega-6/omega-3 essential fatty acids. Biomed. Pharmacother. 56(8): 365-379. https://doi.org/10.1016/s0753-3322(02)00253-6 [ Links ]

Simopoulos AP. 2008. The importance of the omega-6/omega-3 fatty acid ratio in cardiovascular disease and other chronic diseases. Exp. Biol. Med. 233(6): 674-688. https://doi.org/10.3181/0711-mr-311 [ Links ]

Sokal RR, Michener CD. 1958. A statistical method for evaluating systematic relationships. Univ. Kansas Sci. Bull. 38: 1409-1438. [ Links ]

Ulbricht TLV, Southgate DAT. 1991. Coronary heart disease: seven dietary factors. Lancet 338(8773): 985-992. https://doi.org/10.1016/0140-6736(91)91846-M [ Links ]

Valls R, Piovetti L, Banaigst B, Praud A. 1993. Secondary metabolites from Morocco brown algae of the genus Cystoseira. Phytochemistry 32(4): 961-966. https://doi.org/10.1016/0031-9422(93)85236-k [ Links ]

Vizetto-Duarte C, Pereira H, Bruno de Sousa C, Pilar-Rauter A, Albericio F, Custódio L, Barreira L, Varela J. 2015. Fatty acid profile of different species of algae of the Cystoseira genus: a nutraceutical perspective. Nat. Prod. Res. 29(13): 1264-1270. https://doi.org/10.1080/14786419.2014.992343 [ Links ]

Wood JD, Richardson RI, Nute GR, Fisher AV, Campo MM, Kasapidou E, Sheard PR, Enser M. 2004. Effects of fatty acids on meat quality: a review. Meat Sci. 66(1): 21-32. https://doi.org/10.1016/S0309-1740(03)00022-6 [ Links ]

Received: May 01, 2017; Accepted: April 01, 2018

^*Corresponding author. E-mail: bouafif.cyrine@gmail.com

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Cienc. mar vol.44 n.3 Ensenada Sep. 2018 Epub July 30, 2021

https://doi.org/10.7773/cm.v44i3.2798