Abstract
Oxidative stress has been implicated in the ageing process and in several chronic diseases such as diabetes, cancer, and cardiovascular diseases. Endogenous antioxidant defenses, including enzymes and nonenzymatic compounds, try to combat the oxidative stress created by the disequilibrium between the production of reactive oxygen and nitrogen species and the antioxidant defense system. Natural matrices such as food plants could help the exogenous defense antioxidant system in the mentioned process. Within this perspective, Mediterranean regions contribute significantly owing to their richness in species and habitats. This chapter details and compares the antioxidant activities of different edible parts of selected wild species in the Mediterranean regions, which were traditionally gathered and consumed as food and snacks. Thirty-three species from 16 families of flowering plants were studied. Asteraceae (daisy family), Polygonaceae (sorrel family), Rosaceae (dog-rose family), and Lamiaceae (mint family) are the most representative, as 70 % of the reviewed species are taxonomically included in such botanical families. Experimental research on these species is mainly focused on aerial plant pieces, for instance basal and other leaves, midribs, young stems, shoots, and inflorescences, as these plant parts are the most used and available. Given the complexity of antioxidant measurement assays, the following methods have been selected to give an idea of the antioxidant properties of different wild plant foods from the Mediterranean area: reducing power (Folin–Ciocalteu and ferricyanide/Prussian blue assays), 2,2-diphenyl-1-picrylhydrazyl free radical scavenging activity, and lipid peroxidation inhibition (β-carotene/linoleate assay and thiobarbituric acid reactive species assay).
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Keywords
- Antioxidant properties
- Reducing power
- Free radical scavenging activity
- Lipid peroxidation inhibition
- Wild food plants
- Edible plant parts
- Mediterranean foods
1 Oxidative Stress and Antioxidant Defenses
1.1 Reactive Species and the Condition of Oxidative Stress
A free radical is defined as any species containing one or more unpaired electrons (electrons singly occupying an atomic or molecular orbital), whereas reactive species is the collective term for radicals and some other non-radical derivatives of oxygen, nitrogen, or sulfur that can easily generate free radicals and/or cause oxidative damage (Halliwell 2012).
As shown in Table 10.1, reactive oxygen species (ROS) include free radicals such as hydroperoxyl radical (HO2 ●), superoxide anion radical (O2 −●), hydroxyl radical (HO●) and peroxyl radical (ROO●; e.g., lipid derived), and other species such as hydrogen peroxide (H2O2), singlet oxygen (1O2), hypochlorous acid (HOCl), and peroxide (ROOR; Lü et al. 2010; Carocho and Ferreira 2013).
The “primary” ROS O2 −● is formed by the addition of one electron to molecular oxygen; this addition occurs in or outside mitochondria and involves different endogenous enzymatic systems such as NADPH oxidases or xanthine oxidases (Ferreira et al. 2009). At pH 7, HO2 ●, also formed from molecular oxygen, dissociates to O2 −●. This radical is not very active, but it can interact with other molecules generating “secondary” ROS, such as H2O2 (by superoxide dismutase, SOD in Haber–Weiss reaction) and then HO● (by Fenton reaction—electron transfer from transition metals to H2O2), with the latter considered the most toxic ROS (Valko et al. 2007; Ferreira et al. 2009; Flora 2009; Carocho and Ferreira 2013). In the presence of H2O2 and the chloride ion (Cl−), the enzyme myeloperoxidase produces OCl− and then HOCl; the latter species can generate HO● by reacting with O2 −● or Fe2+. OCl− can also react with H2O2 to make singlet O2 (1O2) (Halliwell 2006). Lipid peroxidation promotes the production of different types of ROS such as R● that can react with O2 to form ROO●; if not neutralized, these radicals react with other adjacent lipids producing hydroperoxide lipids (ROOH) that can easily be decomposed to form new R●, initiating a process that is known as chain propagation reaction (Ferreira et al. 2009).
Table 10.1 also lists the reactive nitrogen species (RNS), including nitric oxide radical (NO●), generated in biological tissues by specific nitric oxide synthases (NOS) that transform arginine to citrulline. NO● reacts with O2 ●− to yield peroxynitrite (ONOO−), a non-radical RNS (Ghafourifar and Cadenas 2005; Ferreira et al. 2009).
As shown in Fig. 10.1, reactive species are produced in mitochondria or peroxisomes within metabolic processes or by xanthine oxidase activity, inflammation processes, phagocytosis, arachidonate pathway, ischemia, and physical exercise. Smoking, environmental pollutants, radiation, drugs, pesticides, industrial solvents, and ozone are examples of external factors that promote the production of free radicals (Halliwell 2011; Carocho and Ferreira 2013).
The main targets of reactive species are lipids, proteins, sugars, and nucleic acids (Lü et al. 2010). Lipid peroxidation (attack on membrane lipids) occurs mainly as a result of the action of HO● or 1O2, but also of ONOO−. Proteins can be oxidatively modified in specific amino acids (e.g., nitrosylation with NO●) by free radical-mediated peptide cleavage or by formation of protein cross-linkages due to reaction with lipid peroxidation products (Ferreira et al. 2009; Carocho and Ferreira 2013). In particular, S-nitrosation of glutathione (GSH) produces S-nitrosoglutathione (GSNO), which itself is capable of S-nitrosating cysteine residues in proteins to make cysteine-S-nitrosothiol (Table 10.1). Protein glutathionylation is a prominent consequence of RSS exposure and consists in the redox reaction of protein cysteinyl residues with the tripeptide glutathione, resulting in a protein–glutathione mixed disulfide (Giles et al. 2001; Gruhlke and Slusarenko 2012). The formation of ROS could also contribute to glycoxidative damage; during the initial stages of nonenzymatic glycosylation, sugar fragmentation produces short-chain species such as glycolaldehyde, whose chain is too short to cyclize and is therefore prone to autoxidation (Benov and Beema 2003; Carocho and Ferreira 2013). The damage in nucleic acids induced by reactive species includes production of base-free sites, deletions, modification of all bases, frame shifts, strand breaks, DNA–protein cross-links, and chromosomal arrangements. HO● is known to react with all the components of the DNA molecule, intervening also in DNA oxidation, whereas ONOO− is related to DNA fragmentation (Ferreira et al. 2009; Carocho and Ferreira 2013).
The damage to cells and tissues caused by reactive species, mostly ROS, is called oxidative damage and is a consequence of oxidative stress, a serious imbalance between the generation of ROS and antioxidant protection in favor of the former (Halliwell 2012). Recently, the mentioned author answered the question “does the oxidative stress that is likely to occur as a result of the tissue damage play any role at all in the disease pathology?”, with a firm yes for cancer and neurodegenerative diseases, with a probably yes for inflammatory bowel disease, rheumatic arthritis, chronic granulomatous disease, and with a maybe for atherosclerosis and diabetes.
1.2 Endogenous Antioxidant Defenses
As shown in Fig. 10.2, humans produce many endogenous antioxidant systems (enzymes such as SOD (superoxide dismutases), CAT (catalases), Prx (peroxiredoxins), GPx (glutathione peroxidase), GRed (glutathione reductase) and GST (glutathione-S-transferases), or nonenzymatic antioxidant defenses, namely GSH (reduced glutathione), Q10, and uric acid) but also obtain some other antioxidants from the diet, such as vitamin E, vitamin C, polyphenols, and carotenoids (Halliwell 2011; Carocho and Ferreira 2013).
SOD converts O2 ●− into H2O2 through a dismutation reaction, which is then detoxified to water either by CAT in the peroxisomes or by GPx in the mitochondria, cytosol, or nucleus. Other enzymes that reduce H2O2 are peroxiredoxins (with cysteine in the active site). GRed regenerates GSH that is used as a hydrogen donor by GPx; the latter can also transform hydroperoxide lipids into alcohols (ROH). GSH effectively scavenges ROS (HO●, H2O2, LOO● and ONOO−) either directly or indirectly as a cofactor of several detoxifying enzymes, for example, GPx and GST. In the neutralization process of ROS, GSH is oxidized to glutathione disulphide (GS-SG), which can be further reduced to two GSH molecules by the enzyme GRed. GSH is also able to regenerate other antioxidant molecules such as vitamins C and E and react with a variety of electrophilic xenobiotics in reactions catalyzed by GST, generating products with higher solubility (thus easier to eliminate). Finally, GSH can also neutralize NO●, resulting in the formation of S-nitrosoglutathione (GSNO; Valko et al. 2007; Ferreira et al. 2009).
Coenzyme Q10 acts by preventing the formation of or by neutralizing lipid peroxyl radicals, but its ability to regenerate vitamin E has also been reported. Uric acid prevents the overproduction of oxo-heme oxidants that result from the reaction of hemoglobin with peroxides. It also prevents the lysis of erythrocytes by peroxidation, and it is a potent scavenger of HO● or 1O2 (Carocho and Ferreira 2013).
1.3 Contribution of Plants as Exogenous Antioxidant Defenses
Plants, used since ancient times due to their medicinal properties, may be considered as a source of bioactive compounds with antioxidant potential. These properties have been studied in the past few years, proving their potential to act as functional foods (Krishnaiah et al. 2011).
As shown in Fig. 10.2, different compounds, such as vitamin E, vitamin C, polyphenols, and carotenoids, have been reported to help the endogenous antioxidant defense system as exogenous sources. Vitamin E, a liposoluble vitamin present in the membranes, plays an important role in the prevention of lipid peroxidation. ROS (e.g., HO● and LOO●) react with vitamin E, generating vitamin E●. Then, vitamin C reacts with vitamin E● (Fig. 10.3) producing vitamin C● (that could be eliminated by semidehydroascorbate reductase), regenerating vitamin E. Both radicals (vitamin E● and vitamin C●) are poorly reactive species (Ferreira et al. 2009).
The antioxidant properties of polyphenols, mostly flavonoids and phenolic acids, are conferred by the phenolic hydroxyl groups attached to the ring structures. They can act as reducing agents; hydrogen donators; singlet oxygen quenchers; peroxynitrites, superoxide, hydroxyl, and peroxyl radical scavengers; and even as metal chelators. They also activate antioxidant enzymes, reduce vitamin E radicals, inhibit oxidases, mitigate nitrosative stress, and increase levels of uric acid and low-molecular-weight molecules (Procházková et al. 2011; Carocho and Ferreira 2013).
The main antioxidant potential of carotenoids is due to singlet oxygen quenching. The only free radicals that completely destroy these pigments are peroxyl radicals. Carotenoids are relatively unreactive but may also decay and form nonradical compounds that may terminate free radical attacks by binding to these radicals (Paiva and Russel 1999; Carocho and Ferreira 2013).
According to Halliwell (2012), our endogenous antioxidant defenses are inadequate to prevent oxidative damage completely; hence, dietary sources of antioxidants are especially important to avoid diseases related to oxidative stress. Nevertheless, the contribution of some of them (e.g., polyphenols and carotenoids) to the beneficial dietary effect of plants is uncertain, as suggested by the limited and confusing literature on their in vivo effects, except possibly in the stomach, small intestine, and colon (Halliwell 2011, 2012).
The extracts obtained from plant materials (whole herb or roots, young stems, leaves, basal leaves, shoots, aerial parts, flower buds, flowers, inflorescences, fruits, seeds, and wood) might be used as antioxidants due to the chemical diversity of their phytochemicals and synergistic effects. In fact, the beneficial effects of diet-derived antioxidants may be maximally exerted when they are consumed at currently recommended dietary intakes, rather than in large amounts. Plants are a rich source of antioxidants, nonetheless the protective effect may not be the same by pulling up one or two individual antioxidant molecules into a high-dose pill (Halliwell 2012).
In this perspective, the antioxidant potential of several plants from Portugal and Spain has been extensively reviewed (Barros et al. 2009, 2010a, b, 2011a, b, c; Martins et al. 2011; Morales et al. 2012, 2013a, b; Pereira et al. 2011), revealing very promising results.
1.4 Measurement of Antioxidant Activity in Plants
Regarding the study of antioxidant activity in plants, there is not one method that can provide unequivocal and defining results, which necessitates the use of various methods instead of a one-dimension approach; each method has its specific target within the matrix and its advantages and disadvantages. Some of these procedures use synthetic antioxidants or free radicals; some are specific for lipid peroxidation and require animal or plant cells (Carocho and Ferreira 2013).
One of the methods most frequently used to evaluate the antioxidant properties of different wild edible plants is the Folin–Ciocalteu assay. This method has been often used to evaluate total phenolic content in natural products. However, as it is based on the measurement of the reducing capacity of a sample, nowadays it is being used for antioxidant capacity determination (Huang et al. 2005). It follows the reaction below:
Molybdotungstate (Mo) reagent oxidizes phenols and yields a colored product with an absorption maximum at 745–750 nm. The reagent contains heteropolyphosphotungstates-molybdates that, under basic conditions, react with phenolic compounds to form a phenolate anion, possibly (phenol-MoW11O40)4−, by dissociation of a phenolic proton. This sequence of reversible one- or two-electron reduction reactions leads to blue-colored products (Huang et al. 2005; Prior et al. 2005).
The screening of antioxidant properties can also be measured using chemical assays (i and ii) or assays related to lipid peroxidation (iii and iv):
-
i.
DPPH-scavenging activity:
where X● represents a DPPH radical and AH represents antioxidants present in the sample (plant tissue). Antioxidants donate a hydrogen atom to the DPPH radical, decreasing its absorbance at 517 nm (Antolovich et al. 2002).
-
ii.
Reducing power:
where Fe(CN)6 3− is the compound with the ferric form, and Fe(CN)6 4− is the compound with the ferrous form. Antioxidants present in the wild plants transfer an electron to ferricyanide complex, reducing Fe3+ to Fe2+. The second reaction allows the measurement of the absorbance at 700 nm; higher absorbance corresponds to higher reducing power (Huang et al. 2005; Prior et al. 2005).
-
iii.
β-carotene bleaching inhibition:
where LOO● represents the linoleate free radical. Antioxidants present in the plants donate a hydrogen atom neutralizing the linoleate free radical formed in the system avoiding its attack on the highly unsaturated β-carotene and therefore inhibiting β-carotene bleaching (Prior et al. 2005).
-
iv.
TBARS formation inhibition:
where MDA represents malondialdehyde and TBA, thiobarbituric acid. The antioxidants present in the sample (plant tissue) will inhibit the formation of the MDA-TBA2 complex. The TBARS assay measures the MDA formed as the split product of an endoperoxide of unsaturated fatty acids resulting from oxidation of a lipid substrate. The MDA reacts with TBA to form a pink pigment that is measured spectrophotometrically at 532 nm (Fernández et al. 1997).
As different methods measure the antioxidant activity through different mechanisms, the combined analysis of samples through different assays is often needed to have an overall idea of the properties of a given sample. Therefore, the interpretation of the data of antioxidant activity of foods is complex, because of the variety of assays available, and the different units used for expression of the results make comparison of the data difficult.
In this chapter, data about antioxidant properties of 32 different wild species widespread in the Mediterranean area have been reviewed and compared and information is gathered in Tables 10.2, 10.3, 10.4, and it will be carefully reviewed in the followed sections. For that purpose, they have been grouped according to the different plant parts traditionally used.
2 Overview of the Wild Food Plants with Antioxidant Potential
Since prehistoric times, when our ancestors used hunting and gathering to provide sustenance, wild food plants have played a central role in human diet and nutrition.
All over the world, wild edibles have been used as dietary supplements and are particularly important in times of famine and food shortage. Other plants were used to preserve food and for seasoning regional and traditional recipes. Natural flavors of some species have lent flavor to very poor, insufficient, and monotonous daily meals for decades. Therefore, these plants and the knowledge and practices associated with them are part of an interesting biocultural heritage (Carvalho 2010; Carvalho and Morales 2010; Barros et al. 2010a, 2011a, d).
Demand for natural products and ingredients of high quality has drawn people’s attention to wild edibles, and in many different regions, their use and consumption are becoming more widespread (Łuczaj et al. 2012).
In recent years, experimental research based largely on ethnobotanical surveys and empirical traditional knowledge has shown that wild plants are interesting sources of nutrients and phytochemicals (see also Chap. 9), with significant antioxidant properties (e.g. Barros et al. and Morales et al. cited works) that prevent various illnesses, especially age-related diseases (The Local Food-Nutraceuticals Consortium 2005; Guarrera and Savo 2013).
2.1 Wild Species Providing Vegetables
The Mediterranean flora is a combination of taxa of various biogeographical origins and evolutionary histories effected over time by climatic events and anthropogenic actions with increasing impact (Cowling et al. 1996). Besides floristic diversity, the richness of habitats, different cultures and mores, and landscape management and historic development around the Mediterranean Basin resulted in the common use of many different plants that met basic dietary needs and are interesting food resources, well adapted to local diets and folk traditions (Rivera et al. 2005; Hadjichambiset al. 2008).
Although it is reported that some tree organs (leaves, young shoots, and flowers) are also used (e.g. Tardío et al. 2006), vegetables are mainly the edible product of herbaceous plants and can be roots or underground stems (tubers, bulbs, or rhizomes), whole immature plants (sprouts), stems, whorled basal leaves, expanded leaves, leaf sheaths, midribs and veins, flower heads, and unripe fruits and seeds. Green, vibrant colored or yellowish white, vivid flavored or having very little taste, these edibles are traditionally used raw or cooked for preparing soups, broths, stews, stir-fries, accompaniments, salads, and sometimes desserts.
Several botanical families provide leafy vegetables that play a significant role in different local Mediterranean cuisines and have interesting phytochemical profiles and promising bioactive properties (Guarrera and Savo 2013). Therefore, species of the Asteraceae, Polygonaceae, Brassicaceae, and Amaryllidaceae families are some of the most gathered and consumed edible greens at least in the three large southern European peninsulas (e.g. Pieroni et al. 2005; Tardío et al. 2006; Hadjichambis et al. 2008; Łuczaj et al. 2012). Some examples are basal leaves, midribs, and soft leafy stems of genera such as Chondrilla L., Cichorium L., Hypochaeris L., Scolymus L., Scorzonera L. and Sonchus L. and species from Carduoideae and Asteroideae subfamilies; leaves of docks and sorrels (genus Rumex L.); tender leaves, stems and small flowers from annuals such as Eruca vesicaria (L.) Cav., Raphanus raphanistrum L., Capsella bursa-pastoris (L.) Medik., mustards and wild cabbage; the bulbs, bulbils and linear, channelled or flat leaf blades of Allium species (see Chaps. 4 and 13).
Sweet immature pods and seeds from wild species of the Fabaceae family (e.g. genera Vicia L., Lathyrus L., Astragalus L.) are frequently considered as organoleptically interesting wild food (Carvalho and Telo 2012; Tardío et al 2006) with perceived health benefits.
Other noteworthy leafy vegetables are the vernal leaves of some species of Amaranthaceae (genera Atriplex L. and Chenopodium L.), Boraginaceae (e.g. Borago officinalis L. and Anchusa sp. pl.), and Apiaceae (such as Foeniculum vulgare Mill. and Apium nodiflorum (L.) Lag.).
Small amounts of many of these edibles can safely be eaten raw. Different cooking processes such as soaking or boiling are, sometimes, able to remove most traces of different toxins and alkaloids, for instance. However, some plants have both edible and toxic parts (e.g. bryonies); other botanical families such as Apiaceae have species that can be very poisonous. Many leafy greens have high oxalic acid content (e.g. sorrels), and some accumulate chemicals from several contaminants. Thus, consumers must avoid potential hazards, act with extreme caution, and be informed about the risks and learn how to distinguish between edible and poisonous species, organs, or parts of plants.
Data of antioxidant activity in basal leaves as well as leaves accompanied by other aerial parts of 17 different edible species are shown in Table 10.2.
Anchusa azurea Mill. (bugloss) is a Boraginaceae, commonly consumed after cooking as well as for medicinal purposes against gastralgia, cold, kidney stones, pain, and skin problems (Benítez et al. 2008; Carvalho and Morales 2010; Carvalho 2010; Tardío 2010), and samples of this species gathered from Spain presented the lowest EC50 values (highest antioxidant activity) for DPPH scavenging activity and reducing power (0.02 and 0.01 mg/mL, respectively) (Morales et al. 2013) when compared with all the plant species shown in Table 10.2. Leaves of Borago officinalis L. (borage, also a consumed wild Boraginaceae) from Italy registered the best results in β-carotene bleaching inhibition assays (0.004 mg/mL), according to Conforti et al. (2008).
For the TBARS assay, the leaves of Cichorium intybus L. (chicory), Papaver rhoeas L. (poppy), Rumex pulcher L. (fiddle dock), and Silybum marianum (L.) Gaertn. (milk thistle), also gathered from Spain, presented the lowest EC50 values (0.02 mg/mL; Morales et al. 2013). Traditionally, most of them are eaten cooked; however, they are sometimes boiled and fried in olive oil with garlic, as the fleshy midribs of Silybum marianum. Cichorium intybus and Papaver rhoeas are eaten raw in salads as well. Chicory and poppy are also used in traditional medicine due to their effectiveness in digestive disorders, nervousness, insomnia, respiratory disorders, among others (Benítez et al. 2008; Carvalho and Morales 2010; Carvalho 2010; Tardío 2010). Furthermore, Glechoma hederacea L. from Portugal revealed the highest phenolic content (196.61 mg GAE/g).
Borago officinalis samples obtained from Italy had lower phenolic content (97 mg chlorogenic acid equivalents/g extract) but slightly higher DPPH scavenging activity and β-carotene bleaching inhibition capacity (Conforti et al. 2008) when compared with the samples of the same species obtained from Portugal (Pereira et al. 2011).
Cichorium intybus samples obtained from Italy presented higher phenolic content, expressed in gallic acid equivalents (GAE), DPPH scavenging activity, and β-carotene bleaching inhibition (190 mg GAE/g; 0.026 and 0.10 mg/mL, respectively) (Conforti et al. 2009) than those gathered from Spain and Greece. Moreover, chicory obtained from Spain had the highest reducing power and TBARS formation inhibition (0.57 and 0.02 mg/mL, respectively). Foeniculum vulgare Mill. (fennel), Papaver rhoeas L. and Sonchus oleraceus L. (smooth sow thistle) from Italy presented the highest DPPH scavenging activity (0.148, 0.049 and 0.164 mg/mL, respectively) and β-carotene bleaching inhibition capacity (0.046, 0.007 and 0.065 mg/mL, in that order) when compared with the same species from other countries (Table 10.2). Fennel and poppy leaves also presented the highest activity for TBARS assay (0.24 and 0.283 mg/mL, respectively), according to Conforti et al. (2009), and Papaver rhoeas from Italy presented the highest levels of phenolics (72 mg GAE/g). Rorippa nasturtium-aquaticum (L.) Hayek (watercress) from Portugal showed higher phenolics (50.42 mg GAE/g extract) and DPPH scavenging activity (0.13 mg/mL) but lower reducing power (0.20 mg/mL) than the sample from Turkey (Özen 2009).
It is remarkable that the edible leaves of Anchusa azurea, Borago officinalis, Cichorium intybus, Papaver rhoeas, Rumex pulcher, and Silybum marianum exhibit higher antioxidant activity measured by one or more different assays than the other species. Special attention should be paid to Anchusa azurea leaves gathered in Spain (Morales et al. 2013), which revealed the highest antioxidant activity in all the assays reviewed.
2.2 Wild Species Providing Wild Asparaguses
Sprouts and young shoots (asparaguses) of different plants are also considered edible in southern countries. Asparagus acutifolius L. (Asparagaceae), Bryonia dioica Jacq (Cucurbitaceae), Humulus lupulus L. (Cannabaceae), Tamus communis L. (Dioscoreaceae), and Rubus species (Rosaceae) are some examples of these type of wild edibles usually gathered in early spring while tender and still lacking flower buds (Tardío et al. 2006; Carvalho 2010).
Data on antioxidant activity in young shoots of four wild Mediterranean species are also shown in Table 10.2. The highest phenolic content was found in Tamus communis L. (black bryony) from Portugal (758.99 mg GAE/g).
Asparagus acutifolius L. (wild asparagus), Bryonia dioica Jacq. (white bryony), and Tamus communis from Portugal (Martins et al. 2011) had higher antioxidant activity, with the exception of the TBARS assay, when compared with samples from Spain (Morales et al. 2012).
Edible parts of Tamus communis should be remarked for the coincident results found through the different antioxidant assays performed, revealing a high antioxidant potential.
2.3 Plants Used for Seasoning and Flavoring
Seasoning and preserving food are still common procedures that have an influence on the traditional cuisine and are fundamental to many regional recipes, particularly in rural areas. Many species with natural flavors are used as additives for enhancing the taste and smell of food but their bioactive properties are also important as food preserves (Dias and Dias 2006; Pardo-de-Santayana et al. 2007).
In former times, such species were related to nutritional needs, especially during those famine periods when wild edible plants were the main source of nourishment for rural families. Moreover, different sauces and pastes were prepared with herbs and stored in glass bottles to use all through the year (Póvoa et al. 2009; Carvalho and Morales 2010). An interesting example is the traditional piso from southern Portugal, a paste made of Mentha pulegium L. or M. cervina L (Lamiaceae), crushed with garlic and salt and then covered with olive oil. Experimental assays proved that after a 6-month storage period, food sauces retained their physicochemical properties and could be used for seasoning (Póvoa et al. 2009).
At least in the Iberian Peninsula, Lamiaceae and Apiaceae are undoubtedly the botanical families providing a great number of species used as seasoning and flavoring agents although many others are also used, such as some Fabaceae like Pterospartum tridentatum (L.) Willk. and Cytisus sp. pl., Alliaria petiolata (M. Bieb.) Cavara & Grande (Brassicaceae) and Allium ampeloprasum L., A. schoenoprasum L. and A. triquetum L. (Amaryllidaceae) (Pardo-de-Santayana et al. 2007; Carvalho 2010). Many of these species are also included in the preparation of different fresh beverages, liqueurs, and herbal teas drunk daily or after meals (Carvalho 2010; Sõukand et al 2013)
Data regarding flowers and inflorescences of Foeniculum vulgare, Mentha pulegium L. (pennyroyal), Origanum vulgare L. (oregano), Rosa canina L. (dog rose), Sambucus nigra L. (elder), and Thymus mastichina L. (mastic thyme), widespread Mediterranean perennial herbs traditionally used for medicinal purposes and seasoning, are also listed in Table 10.3.
Of all the species mentioned in Table 10.3, Mentha pulegium and Origanum vulgare are two of the most studied species. Mentha pulegium from Portugal presented the highest reducing power and β-carotene bleaching inhibition capacity (0.12 and 0.01 mg/mL, respectively, Fernandes et al. 2010); Origanum vulgare from Portugal had the highest amount of total phenolics (368 mg GAE/g) and the lowest EC50 values (highest antioxidant activity) for the TBARS assay (0.01 mg/mL, Barros et al. 2010a), whereas the same species from Turkey presented the highest DPPH scavenging activity (0.01 mg/mL, Şahin et al. 2004). The flowers of these two species should be highlighted for their high antioxidant capacity measured by different assays, with coincidences among studies performed with samples from different origins, showing their higher antioxidant potential compared with flowers of other species.
2.4 Wild Edible Fruits
Regarding wild Mediterranean fruits, five wild species were reviewed: Arbutus unedo L. (strawberry-tree), Crataegus monogyna Jacq. (common hawthorn), Prunus spinosa L. (blackthorn), Rosa canina L., and Rubus ulmifolius Schott (blackberry), and the results are summarized in Table 10.4.
Arbutus unedo from Algeria presented the highest antioxidant potential for radical scavenging activity and reducing power (0.006 and 0.001 mg/mL, Boulanouar et al. 2013), but Crataegus monogyna from Spain showed the lowest EC50 values for lipid peroxidation assays, such as β-carotene bleaching inhibition and TBARS assay (0.02 mg/mL, Morales et al. 2013a). The sample from Portugal revealed the highest phenolic content, expressed in mg per g of extract (247 mg GAE/g, Barros et al 2011c). The different units used for expression of the results of antioxidant activity of plant material make the comparison of data difficult (Table 10.4). However, Arbutus unedo and Crataegus monogyna are two of the fruits which reported the highest values in the Folin–Ciocalteu assay.
2.5 Underutilized and Underexploited Species
Many plant resources, growing as wild plants or that have been naturalized growing on their own, are well adapted to different ecological situations and have great potential to be exploited. This is the case of many leafy vegetables from the Fabaceae, Brassicaceae, and Amaryllidaceae families that have a surprising number of edible species and varieties. A number of them are naturalized from old crops and long-time introduced specimens. Lentils, peas and wormseed (Chenopodium ambrosioides L.) are some examples. Leeks and wild garlic, for instance, also have great potential that sometimes is forgotten and not used (Carvalho 2010).
Wild fruits and aromatic species used to be commonly preserved and stored for consumption during long and hard winters. These are species, such as Rosa sp. pl. and many others from woods, scrubland, riversides, and natural prairies or meadows, that have become underutilized because various staple products from the retail market or cultivated for daily meals are now offered or more accessible (Carvalho and Morales 2010). However, experimental research shows that some of them have great antioxidant potential (Barros et al. 2010b, 2011a, b).
In rural areas from the Iberian Peninsula, people have brought some of the most popular wild plants used as food additives and beverages from the wild to grow in their home gardens, in order to make them easily available (Carvalho and Morales 2010). This behavior shows that some species can be easily adapted to cultivation providing sustainable use without endangering wild populations (see Chap. 5).
3 Concluding Remarks
A widespread traditional use of many wild botanicals (e.g. leafy vegetables, flowers, fruits and seeds) as food was the starting point of experimental research on the antioxidant potential of several plants in Mediterranean regions. The diversity of phytochemicals, present in different edible parts of selected species, provides antioxidant properties with potential health benefits. Whenever possible, data obtained were systematically compared with other studies already published. The antioxidant activity results, using the same methodology, can be expressed differently (e.g. EC50 or as trolox equivalents); therefore, in some cases it is very difficult to compare results.
Overall, leaves of Anchusa azurea, Apium nodiflorum, Borago officinalis, Cichorium intybus, Papaver rhoeas, Rumex pulcher, and Silybum marianum; young shoots of Tamus communis; flowers and inflorescences of Mentha pulegium and Origanum vulgare; and fruits of Arbutus unedo and Crataegus monogyna stand out among others for their antioxidant potential. Moreover, it can be highlighted that, in general, fruits were the most active plant part (EC50 values of all the assays ranged between 0.001 and 5.4 mg/mL), whereas in most cases, leaves reported lower antioxidant activity (EC50 values between 0.01 and 13 mg/mL).
There are also numerous publications of the antioxidant potential and bioactive compounds present in the same parts of the reviewed 32 species from other countries that do not belong to the Mediterranean. Asparagus acutifolius from Brazil (Tiveron et al. 2012), China (Shou et al. 2007), USA (Sun et al. 2007a and b), and Poland (Vinson et al. 1998); Borago officinalis from Lithuania (Bandoniene and Murkovic 2002; Bandoniene et al. 2005); Crataegus monogyna fruits from France (Froehlicher et al. 2009); Foeniculum vulgare from Iran (Motamed and Naghibi 2010); Rorippa nasturtium-aquaticum from Iran (Bahramikia and Yazdanparast 2010), Denmark (Justesen and Knuthsen 2001), Brazil (Hassimotto et al. 2009), and Australia (Lako et al. 2007); Rosa canina from Austria (Wenzig et al. 2008) and Denmark (Kirkeskov et al. 2011); Sambucus nigra from Austria (Rieger et al. 2008) and USA (Wu et al. 2004) are some examples of wild species studied out of the Mediterranean area.
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Barros, L., Morales, P., Carvalho, A., Ferreira, I. (2016). Antioxidant Potential of Wild Plant Foods. In: Sánchez-Mata, M., Tardío, J. (eds) Mediterranean Wild Edible Plants. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-3329-7_10
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