Vegetables Future Alternatives for Traditionally Consumed...

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Weeds and Food Diversity: Natural Yield Assessment andFuture Alternatives for Traditionally Consumed WildVegetablesAuthor(s): María Molina , Javier Tardío , Laura Aceituno-Mata , Ramón Morales , Victoria Reyes-García , and Manuel Pardo-de-Santayana Source: Journal of Ethnobiology, 34(1):44-67. 2014.Published By: Society of EthnobiologyDOI: http://dx.doi.org/10.2993/0278-0771-34.1.44URL: http://www.bioone.org/doi/full/10.2993/0278-0771-34.1.44

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WEEDS AND FOOD DIVERSITY: NATURAL YIELDASSESSMENT AND FUTURE ALTERNATIVES FOR

TRADITIONALLY CONSUMED WILD VEGETABLES

Marıa Molina,1 Javier Tardıo,2 Laura Aceituno-Mata,3 Ramon Morales,4

Victoria Reyes-Garcıa,5 and Manuel Pardo-de-Santayana6

Wild edible plants, and particularly weeds, continue to be an important dietary component of many people

around the world. We study the availability and yield of 15 weedy vegetables traditionally consumed in theMediterranean region to assess their potential sustainable exploitation. Fieldwork was conducted in Central

Spain during 2007–2009. Yields ranged between 10–460 g per plant in non-clonal species and between 400–

5,000 g m22 in clonal species. According to local plant density estimates, a total of 1800 kg ha21 forFoeniculum vulgare, 700–1000 kg ha21 for Beta maritima, Rumex pulcher, Papaver rhoeas and Silybummarianum, and 80–400 kg ha21 for the remaining species could be obtained, except for Scolymus hispanicusthat only yielded 30 kg ha21. Exploitation of those species should consider local yields and preferences to achieve

sustainability. We propose: 1) organic cultivation for highly valued species with low production rates in the wild(e.g., Scolymus hispanicus and Silene vulgaris); 2) commercial wild collection for culturally appreciated

species with high yields in the wild (e.g., Allium ampeloprasum and Chondrilla juncea); and 3) maintenance

of traditional practices and rates of harvest for all species for self-consumption.

Keywords: Mediterranean wild edible plants, food production, harvesting, organic farming, appliedethnobotany

Las plantas silvestres comestibles, muchas de ellas malas hierbas, siguen siendo un recurso alimentario

importante en numerosos lugares de todo el mundo. En este trabajo se estudia la disponibilidad y produccion de

15 verduras silvestres consumidas tradicionalmente en el Mediterraneo con el fin de evaluar su posible usosostenible en la alimentacion. El estudio se ha realizado en el Centro de Espana durante 2007–2009. La

produccion oscilo entre 10–460 g por planta en especies no clonales y 400–5,000 g m22 en especies clonales. De

acuerdo con las estimaciones de densidad, podrıan obtenerse 1800 kg ha21 de Foeniculum vulgare, 700–1000 kg ha21 de Beta maritima, Rumex pulcher, Papaver rhoeas y Silybum marianum, y 80–400 kg ha21

del resto de las especies, excepto de Scolymus hispanicus (30 kg ha21). La explotacion sostenible de estas

especies debe tener en cuenta su produccion local y las preferencias culturales. En base a ello proponemos: 1) el

cultivo ecologico de las especies muy valoradas cuyas poblaciones silvestres tienen bajas tasas de produccion(e.g., Scolymus hispanicus y Silene vulgaris); 2) la recoleccion con fines comerciales de las especies muy

productivas y valoradas culturalmente (e.g., Allium ampeloprasum y Chondrilla juncea); 3) la recoleccion

1. Corresponding author. Instituto Madrileno de Investigacion y Desarrollo Rural, Agrario yAlimentario (IMIDRA), Finca El Encın, Apdo. 127, E-28800 Alcala de Henares, Spain ([email protected])

2. Instituto Madrileno de Investigacion y Desarrollo Rural, Agrario y Alimentario (IMIDRA), Spain([email protected])

3. Instituto Madrileno de Investigacion y Desarrollo Rural, Agrario y Alimentario (IMIDRA), Spain;and Dpto. Biologıa (Botanica), Facultad de Ciencias, Universidad Autonoma de Madrid (UAM),C/ Darwin 2, E-28049 Madrid, Spain ([email protected])

4. Real Jardın Botanico de Madrid, CSIC, Plaza de Murillo 2, E-28014 Madrid, Spain ([email protected])5. ICREA and Institut de Ciencia i TecnologiaAmbientals, Universitat Autonoma de Barcelona, E-

08193 Bellaterra, Barcelona, Spain ([email protected])6. Dpto. Biologıa (Botanica), Facultad de Ciencias, Universidad Autonoma de Madrid (UAM), Spain

([email protected])

Journal of Ethnobiology 34(1): 44–67 2014

con fines de autoconsumo de todas las especies respetando las practicas tradicionales y manteniendo unas tasas

sostenibles de recoleccion.

Introduction

Food diversity includes domesticated plant and animal species, but also wildanimal and plant species. Given the profound changes in agricultural practicesand in culinary and nutritional habits, food diversity is globally decreasing.Globalization and modernization have resulted in diet simplification and anincreased dependency on a few staple crops for most nutritional needs (Johnsand Eyzaguirre 2006). Food homogenization relates not only to the consumptionof fewer species, but also to intra-species homogenization. According to FAO(2004), about 75% of the genetic diversity of agricultural crops was lost during thelast century. Many local varieties of crops and animal breeds are threatened byextinction and most wild edible plants are not consumed anymore or onlyseldom (Flyman and Afolayan 2006; Ford-Lloyd et al. 2011).

The decrease of food diversity has led to an increasing concern amongresearchers, consumers, and farmers about its effects in human health, foodsecurity, and food sovereignty (Ayres and Bosia 2011; Dowler and O’Connor2012; Johns and Eyzaguirre 2006). Both scientists and social movements areaware of the need for policies that promote diversified and environmentallyand socially sustainable food production systems (Altieri et al. 2012; La ViaCampesina 2012; Slow Food 2012).

In the context of this work, we define wild edible plants as plant species usedas sources of food that are neither cultivated nor domesticated but availablefrom their wild natural habitats, including weeds growing in agricultural anddisturbed areas. Traditional food systems have typically used a large number ofwild edible plants, including weedy relatives of crops. Weeds probably began tocontribute substantially to the human diet with the beginning of agriculture,which favored the development of their ecological niches. They were a back-upresource in times of shortage, accounting for a significant input of micronutrientsand allelochemicals with a prophylactic effect (Leonti 2012). Nowadays, theconsumption of wild edible plants, although often difficult to assess, is stillsignificant at local and global scales (Bharucha and Pretty 2010; Legwaila et al.2011). Particularly, ethnobotanical surveys in the Mediterranean region reflectthat gathering wild edible plants is at the crossroad of two divergent tendencies:1) a decline in the habit of eating wild edible plants among the generalpopulation; and 2) a renewed interest among some young and middle-agedurban classes interested in the consumption of wild food resources (Ghirardiniet al. 2007; Parada et al. 2011; Łuczaj et al. 2012).

On the one hand, the decline in the consumption of wild edible plants hasbeen attributed to several, non-mutually-exclusive, reasons. First, the decline inthe consumption of wild edibles has been related to the increased accessibility ofmarket food-products, which require less time investment than the gathering ofwild plants (Menendez-Baceta et al. 2012). Second, this decline has also beenrelated to the negative connotations of traditional activities, such as gathering

2014 JOURNAL OF ETHNOBIOLOGY 45

wild edible plants, that are often considered old-fashioned and a symbol ofpoverty (Pieroni et al. 2005). Third, the erosion of traditional knowledge that hasresulted in a lack of skills needed to identify wild edible plants and knowledgeon how to process them is another of the drivers in the decline of wild plantconsumption (Hadjichambis et al. 2008). Finally, some authors have argued thatthere is a rising concern about contamination risks at the harvesting places,which might also discourage some people to harvest wild edibles (Mesa 1996;Wehi and Wehi 2010).

On the other hand, the revival of the consumption of wild foods among certainsocial sectors has been influenced by the increased visibility of wild edibles in themedia (Harford 2011; Łuczaj 2013; Thayer 2006) which has had a boomerang effecton the general perception of wild edible plants. Reasons for this revival arethreefold: 1) the revalorization of typical products in local gastronomies, includinga diversified diet that supplies a wide range of colors, flavors, and textures(Grivetti and Ogle 2000; Pardo-de-Santayana et al. 2010); 2) the use of plantsadapted to local environments as a secure and sustainable source of food, sincemany of the most widely used wild edible plants are weeds that grow inagricultural and disturbed areas near human settlements (Tardıo 2010; Turneret al. 2011); and 3) the growing awareness that wild food intake might providehealth benefits, as they are potentially a source of dietary elements and serve asfunctional foods (Sanchez-Mata et al. 2012). For example, in comparison withconventional crops, wild foods are often richer in bioactive compounds such asessential fatty acids and secondary metabolites with antioxidant activity (Moraleset al. 2012; Schaffer et al. 2005; Trichopoulou and Vasilopoulou 2000).

Those two tendencies of decline and revival of wild food consumption havebeen identified in previous ethnobotanical research in Central Spain, where a fewspecies are still commonly collected while others are not collected anymore, oronly rarely. For instance, recent studies conducted in several villages of CentralSpain reveal that Scolymus hispanicus is still used by 33–38% of the ruralpopulation (Polo et al. 2009) and Silene vulgaris by 14–40% (Andres 2012; Davila2010; Garcıa-Cervigon 2013). In these cases, the recreational motivation forgathering wild plants and appreciation of their flavors mainly explain why thesetwo plants continue to be used in rural communities, which contrasts with thenecessity that drove collection among traditional peasant societies (Aceituno-Mata 2010) and during times of food shortage, like the Spanish postwar period(Tardıo et al. 2006). Other species, like Rumex papillaris, are no longer used insome villages. This is the case in Buitrago de Lozoya, where approximately 30%of the population used this species in the past (Garcıa-Cervigon 2013). Thesestudies also indicate that older people clearly consume and gather more speciesthan the younger generations, but they do not find important differences in thegendered distribution of ethnobotanical knowledge about wild edible plants(Andres 2012; Garcıa-Cervigon 2013; Polo et al. 2009). Nevertheless, we havedetected an increasing interest in wild food collection courses, books, and otheroutreach activities carried out by our research team among urban young peopleconcerned with rural traditional knowledge.

As some researchers have highlighted, weedy vegetables are a potentiallyinteresting source of healthy foods whose sustainable exploitation may be

46 MOLINA et al. Vol. 34, No. 1

encouraged (Hadjichambis et al. 2008). However, to achieve sustainableexploitation, innovative ways of adapting traditional practices into contemporarysocioeconomic contexts are needed (Ladio et al. 1997; Turner and Turner 2008). Inthe framework of sustainable rural development, traditional food revitalizationprojects are being created. Such projects include organic farming and eco-tourismwith guided routes for gathering wild plants and the commercialization ofspecialities made with local products in restaurants and regional markets. Theemerging agroecological movements and the increased demand for organic foodappear as potential niches for traditional food extraction and production systems(Gomez-Baggethun et al. 2010). However, if the demand for wild edible plantsincreases, their sustainable extraction becomes an issue. The sustainableexploitation of wild edible plants requires solid quantitative data on theirpotential yield to assess alternatives for the management of wild food plants(Cunningham 2001). With the exception of a few species (Kerns et al. 2004;Lepofsky et al. 1985; Molina et al. 2011, 2012; Tardıo et al. 2011), there is a generallack of studies on the availability and yield of wild edible plants. Moreover, thepotential yield of weedy wild vegetables has been poorly addressed, particularlyin the Mediterranean region.

Given the interest in weed consumption for food security and foodsovereignty, we study the availability and yield of 15 wild vegetablestraditionally consumed in the Mediterranean region. Based on our results, wepropose three different methods of sustainable exploitation of wild edible plantsand assess which of the studied species are the most suitable for each alternative,according to yield and cultural factors. These results can be used in policiesoriented to promote their sustainable extraction.

Materials and Methods

Wild Edible SpeciesFifteen wild vegetable species were selected based primarily on their

traditional use in Spain (Tardıo et al. 2006) and other Mediterranean and Europeancountries (Hadjichambis et al. 2008; Leonti et al. 2006; Łuczaj et al. 2013) and,secondarily, on their local use and natural occurrence in Central Spain, where field-work was conducted. Species selected belong to eight families and include twelveperennial and three annual herbs (Table 1). With the exception of Rumex papillaris,the selected species are widely distributed in the Mediterranean and Europeancountries (Euro+Med 2012; Tutin et al. 1964–1980). The species Rumex papillaris,also known as R. thyrsiflorus subsp. papillaris (Boiss. & Reut.) Sagredo & Malag., isendemic from continental areas of the Iberian Peninsula (Castroviejo et al. 1986–2012), but can be considered a substitute of other species with a similar taste,more widely distributed and closely related, such as Rumex acetosa L. or evenR. thyrsiflorus Fingerh. All the species selected are non-endangered weedscommonly found in human-disturbed habitats (Carretero 2004). Some of thespecies, such as Apium nodiflorum, occur in aquatic environments and swampy areas.

The aerial parts, including the basal leaf rosette or the leafy young stems, areused in most species. The bulb and the pseudostem formed by the overlapping


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leaf bases are consumed in Allium ampeloprasum (Table 1). In the case of thethistles Scolymus hispanicus and Silybum marianum, the midribs of the basal leaves,known as pencas in Spanish, are eaten. The biotype, the part used, the local modeof preparation and consumption (from Tardıo et al. 2005), and the taste andtexture of the selected plants can be found in Table 1. Six species are mainlyconsumed raw in salads. The remaining nine species are mainly consumedcooked. Some of them are boiled with two or three changes of water to reducetheir bitterness or acidity and improve their palatability.

According to nutritional studies carried out by our research group, several ofthe studied species are rich in bioactive compounds that might have importanthealth benefits because of their antioxidant activity. For instance, Rumex pulcher,Rumex papillaris, and Silene vulgaris are rich sources of vitamin C; Anchusa azureaof folates; Sonchus oleraceus and Chondrilla juncea of a–tocopherol; and Cichoriumintybus, Beta maritima [syn. B. vulgaris subsp. maritima (L.) Arcang.], andTaraxacum obovatum of phenolics and flavonoids (Morales et al. 2011; Morales2011; Sanchez-Mata et al. 2012).

Plant identification and nomenclature follows Flora iberica (Castroviejo et al.1986–2012) and Flora Europaea (Tutin et al. 1964–1980). Since yield variables weremeasured at pre-flowering stages, the species were botanically identified fromleaf morphology and the remaining skeletal stems from the previous season.Voucher specimens at flowering stages were also collected and deposited at theherbarium MA (Real Jardın Botanico, CSIC, Madrid; see voucher number inTable 1).

Study SitesFieldwork was carried out in Central Spain. Mediterranean climate

characterizes the territory. The highest temperatures and the longest summerdrought are reached in the southeastern areas. Mean annual temperature andannual rainfall ranges from 11.0–13.5uC and 600–700 mm in the northern, westernand central sites to 13.0–13.8uC and 400–500 mm in the southeastern locations(SIGA 2012). Because of its proximity to the Madrid Metropolitan Area (,5.3million inhabitants), the landscape of the area has been largely transformed.Croplands mainly devoted to cereals, grapevines, and olive trees, represent24.8% of the total surface of this province, contributing only 0.12% of the grossdomestic product (IE 2011). The economy is mainly based on industry andservices. Agriculture represents an important percentage of land uses only in thesouthern and eastern locations, whereas pastures and forest lands are moreimportant in the northern and western areas. Previous research in the areasuggests that traditionally 5.5% of the local wild flora species were consumed, alarger percentage than expected for a region neighboring an important major city(Aceituno-Mata 2010; Tardıo et al. 2005).

The natural yields and the local availability of each species were estimatedin two different sites of Central Spain. Table 2 lists the study sites, thecharacteristics of the sampling areas (see below), and the month of harvest.Since most species are broadly tolerant to environmental variations, and sincethere is a considerable range of climate, soil types, altitude, and land uses in thisterritory, we selected ecologically different sites. The samplings of Beta maritima


and Rumex papillaris were only conducted in locations with calcareous and non-calcareous soils, respectively, because of their specific soil preferences (Figure 1).

Most of the study sites are located in outlying villages (,10,000 inhabitants)of the province of Madrid, where the study species grow spontaneously(Figure 1). Oligotrophic soils developed on sediments from granite andsandstone are found in mountainous locations from the north (site h; 1140 maltitude), southwest (site b; 780 m), and central plains areas (site c; 690 m). Thelandscape in the southeastern areas is shaped by a bleak plateau with fertileplains along the course of the rivers. Eutrophic soils developed on basic rocks,such as limestone, marl, or gypsum, are found in these locations (sites a, d, e, f, i;450–675 m). Finally, one site is located on calcareous soils in the neighboringprovince of Guadalajara (site g; 876 m).

Sampling Areas and PeriodsOur sampling areas were adjusted to the microdistribution of the species at

the study sites—we adjusted the areas to those places where the species actuallygrow. We differentiated four sampling areas: 1) cultivated lands (olive groves,vineyards, cereal crops, and orchards); 2) uncultivated lands (fallow lands,neglected lands, and pastures); 3) ruderal areas (roadsides, country tracks, andpaths); and 4) aquatic environments (streams and irrigation ditches nearfarmlands).

The microdistribution of the species at the study sites and, consequently, thesampling areas (see Table 2) varied depending on land uses and managementpractices. Figure 2 shows a schematic illustration of the four types of samplingareas and a representative picture of each. In cultivated lands with reducedherbaceous vegetation cover (such as olive groves and vineyards) the samplingarea was restricted to the boundaries of the cultivated plot. In cultivated lands

Table 2. Study sites and harvest conditions of the wild vegetables surveyed.

Site 1 Site 2

Plant species Site1

Samplingareas2 Harvest month Site

Samplingareas

Harvestmonth

Allium ampeloprasum a UL, RA March b CL, RA MarchAnchusa azurea b CL, RA March i CL, UL, RA AprilApium nodiflorum f AE April i AE AprilBeta maritima a CL, UL, RA March–April e CL AprilChondrilla juncea c UL, RA April g UL, RA MayCichorium intybus a CL, UL, RA March c UL, RA April–MayFoeniculum vulgare c UL, RA May f CL, UL, RA MayPapaver rhoeas a CL, UL, RA March–April c UL, RA AprilRumex papillaris b CL, UL, RA March h UL, RA MayRumex pulcher a CL, UL, RA March–April c UL, RA AprilScolymus hispanicus c UL, RA April–May d CL, UL, RA April–MaySilene vulgaris b CL, RA March i CL, RA AprilSilybum marianum a CL, UL, RA March–April c UL, RA April–MaySonchus oleraceus a CL, UL, RA March–April b CL, RA MarchTaraxacum obovatum c UL, RA April i CL, UL April

1 Study sites: a Alcala de Henares; b Cadalso de los Vidrios; c Cantoblanco-Madrid; d Fuentiduena de Tajo; e Morata

de Tajuna; f Perales de Tajuna; g Pioz; h Valdemanco; i Villar del Olmo.2 Sampling areas: CL cultivated lands; UL uncultivated lands; RA ruderal areas; AE aquatic environments.


with an extensive herbaceous cover, however, the entire plot was sampled, aswell as in fallow lands, neglected lands, and pastures. In the case of roadsides orpaths, the plants could only be sampled at the margins. In aquatic environments,the samples were taken only in the water course and damp areas in the margins.All these sampling areas can be considered potential gathering places since theyare similar to those shown by the informants in previous ethnobotanical studies(Aceituno-Mata 2010; Tardıo et al. 2005). They are located in the vicinity of thevillages, generally near agricultural areas where weedy vegetables are abundant.

To obtain a realistic estimate of the species’ edible yields, we only selectedareas where pesticides or herbicides had not been sprayed. However, the streamsand irrigation ditches where Apium nodiflorum naturally occurs at site f wereoccasionally cleaned and herbicides were applied. Production was not quantifiedat this site in 2008 because the scarce plant material remaining after herbicideapplication was not suitable for human consumption.

All the species were sampled in spring, from March to May (see Table 2),and collected in their optimal period of consumption according to previousethnobotanical research (Tardıo et al. 2005). The optimal period was defined asthe time before blooming, when the leaves and stems are still tender but have asize large enough to be gathered. Most plants could be gathered in the middle ofspring (April), whereas the optimal growing stage of some species was reachedin early (e.g., Allium ampeloprasum) or late spring (e.g., Scolymus hispanicus).Harvesting dates also depended on the geographical area and the annualmeteorological conditions. For example, Rumex papillaris was harvested in Marchat site b (780 m altitude) and almost two months later at site h (1140 m).

Figure 1. Localization map of the study sites (for abbreviations see Table 2).


Estimation of Individual Plant YieldsIndividual plant yields of weedy vegetables were estimated during two

(2007–2008) or three (2007–2009) consecutive years. Basic ecological techniqueswere applied following Cunningham (2001). The species were first divided intotwo groups according to their growth forms. The first group, named non-clonalspecies, includes species in which individuals can be easily distinguished. Thisgroup contains perennial and annual species in which the aerial part can beassumed to have developed from a single ‘‘rooted unit.’’ Within this group, aminimum of 25 randomly selected individuals per species were collected at eachsite. The fresh and healthy-appearing edible part was immediately weighed witha field scale. The second group, named clonal species, includes perennial specieswhich grow forming clumps, such as Apium nodiflorum, Silene vulgaris, Rumexpulcher and Rumex papillaris. These herbs usually produce clonal offspring bymeans of vegetative growth. They have stoloniferous stems, branching rhizomesor roots, and dense rosettes or patches that may have originated from one ormore ‘‘rooted units.’’ For clonal species, we collected and weighed the edible

Figure 2. A schematic illustration of the sampling areas (striped area) according to the presence of thespecies (marked with black dots) in cultivated lands (CL), uncultivated lands (UL), ruderal areas (RA),and aquatic environments (AE) and a representative photograph of each area: CL, olive grove withherbaceous cover; UL, neglected land; RA, pathway; AE, a stream nearby farmlands.


plant material from at least 25 quadrats of 20 3 20 cm (0.04 m2) randomly placedinto the clumps formed by these species. Although yield data are not entirelycomparable, we used a quadrat of 20 3 20 cm because this area approximatelycovers the same surface as the single rosette of several species with clearlydifferentiated individuals.

Non-destructive methods of collection were applied to perennial herbs,except for the geophyte Allium ampeloprasum, whose bulb was dug out with ahoe. The basal rosette of leaves and the leafy young stems of the hemicriptophytespecies were harvested with scissors, leaving the root or rhizome intact withoutdamaging its ability to resprout. The leaf blade of the thistles Scolymus hispanicusand Silybum marianum was eliminated before weighing. Leaves were peeled inthe same way they would be prepared for eating, leaving only the edible part, themidrib and petiole. The leafy young stems of Silene vulgaris were collected bypinching and cutting them with the fingers. The aerial parts were harvested inannual species.

Estimation of Plant DensityThe local availability of the species was assessed in terms of plant density

through a minimum of 25 randomly located transects of 25 3 2 m. The UTMcoordinates of transects, from start to finish, were recorded and represented onmaster maps. Fieldwork was limited to the sampling areas previously described(see Figure 2).

Sampling took place between June and August, when we could easilyidentify and count the individuals thanks to the presence of flowers. In somecases, sampling was performed in spring, before crop lands were ploughed toremove weeds. Different procedures were used according to species growth(clonal vs. non-clonal) and biotype (perennials vs. annuals). For non-clonalspecies, we counted the number of individuals in each transect. For clonalspecies, we estimated plant cover by counting the number of 20 3 20 cm quadratsper transect occupied by the plants. For perennial species, plant density wasestimated only in 2008 for the whole period, assuming that it will notsignificantly increase or decrease throughout the study years. For annual specieswe estimated plant density over a two year period (2008 and 2009).

Estimation of the Production per HectareThe individual yield and plant density values herein obtained were

combined to ascertain the approximate production rate per hectare. Productionper hectare was calculated by multiplying the average individual yield data bythe average plant density of the species, assuming that all the plants counted intransects would reach harvestable sizes.

Data AnalysisProduction data are expressed as fresh weight at harvest. Mean value ±

standard error (SE) of the three variables considered (individual plant yield,plant density, and production per hectare) is given for all the samples. Eachsample comprises the dataset (n $ 25) obtained per species, year, and site.Since yield data were not normally distributed (Kolmogorov-Smirnov test)and there was no variance homogeneity among groups (Levene test), we used


non-parametric tests (Kruskal-Wallis and Mann-Whitney U test, applying theBonferroni correction when multiple sets of data were compared). Intra-samplevariability was also assessed with the coefficient of variation (CV).

In order to explore whether yield varied with environmental factors, we usedcorrelation analysis. Monthly and accumulated precipitation and mean temper-ature from January to May were considered, as well as the altitude at the studysites. Data were taken from the meteorological stations nearest to each site(between 0–15 km of distance; 7 km on average) and provided by the SpanishMeteorological State Agency (AEMET). Given the limited number of samples (4–6 samples per species) this analysis was exclusively used in an exploratory way,since long-term research would be necessary for studying the real influence ofsuch factors on yield.

Results and Discussion

Individual Plant YieldYield estimates of the wild greens surveyed are summarized in Table 3. The

mean edible production of non-clonal species ranged from 7.8 g per plant inTaraxacum obovatum (year 2008, site 1) to 458.8 g per plant in Beta maritima (year2007, site 1). Yield estimates of clonal species varied from 15.8 g per quadrat in Silenevulgaris (year 2008, site 2; equivalent to 395 g m22) to 201.8 g in Apium nodiflorum(year 2008, site 2; 5,045 g m22). Overall, the highest yield rates were found in Betamaritima, Foeniculum vulgare and Silybum marianum, and the lowest yield rates werefound in Allium ampeloprasum, Taraxacum obovatum and Silene vulgaris.

Although species yield values were obtained from one collection per season,according to our own cultivation experiments and those of other authors (Casco2000), several species in our sample, such as Cichorium intybus, Rumex pulcher orSilene vulgaris, could tolerate two or even three harvests in a season when theyare cultivated. Thus, for these vegetables, the values presented here clearlyunderestimate potential yields.

There were remarkable differences among samples grown in different sites oryears (Table 3). Four different variation patterns were found: 1) the productionfluctuated between years in a proportional way at both sites (Figure 3A); 2)yield variations were different at each site (Figure 3B); 3) production fluctuatedannually without significant between-site differences (Figure 3C); and 4) between-year and between-site differences did not show a clear pattern (Figure 3D).

In order to explore whether yield varied with environmental factors, weperformed a correlation analysis with monthly and accumulated precipitation,mean temperature, and altitude. When significant, correlation coefficients areshown in Figure 3. In some species, such as Sonchus oleraceus, Alliumampeloprasum and Scolymus hispanicus, yields were positively correlated withmonthly precipitation at harvest time, whereas in others, such as Beta maritima, asignificant correlation was found with accumulated rainfall from January toMarch. Yield fluctuations in other species, such as Cichorium intybus, werecorrelated with mean temperature. In Rumex papillaris, the production wasnegatively correlated with altitude. Additionally, in the first two groups


Tab

le3.

Nat

ura

led

ible

pro

du

ctio

no

fth

esu

rvey

edsp

ecie

sin

des

cen

din

go

rder

of

yie

ld(m

ean

±S

E;

gp

erp

lan

tin

no

n-c

lon

alsp

ecie

san

dg

per

203

20cm

qu

adra

tin

clo

nal

spec

ies)

.

Pla

nt

spec

ies

2007

2008

2009

To

tal

aver

age

Sit

e1

Sit

e2

Sit

e1

Sit

e2

Sit

e1

Sit

e2

No

n-c

lon

alsp

ecie

s

Bet

am

arit

ima

458.

8±

54.8

a32

6.9

±60

.4ab

170.

8±

19.2

b17

5.1

±18

.9b

N/

AN

/A

284.

4±

24.3

Foe

nic

ulu

mv

ulg

are

327.

1±

60.9

a32

8.5

±45

.5a

191.

0±

24.9

a20

0.4

±13

.3a

N/

AN

/A

261.

7±

21.1

Sil

ybu

mm

aria

nu

m30

0.1

±53

.0a

315.

7±

44.2

a19

4.2

±41

.1b

278.

1±

74.6

ab

143.

3±

20.7

bN

/A

246.

1±

22.5

Cic

hor

ium

inty

bus

104.

7±

10.0

a21

0.9

±30

.9b

55.8

±4.

7c15

5.8

±23

.3ab

N/

AN

/A

130.

7±

11.2

An

chu

saaz

ure

aN

/A

139.

1±

19.3

a16

7.2

±29

.0a

59.2

±7.

2b10

7.6

±11

.9a

130.

7±

18.0

a11

7.1

±8.

4P

apav

errh

oeas

30.3

±2.

8a46

.3±

7.0a

b95

.9±

8.0c

83.1

±32

.0ad

52.8

±5.

4bd

37.6

±8.

6a58

.4±

6.1

Sco

lym

us

his

pan

icu

s85

.4±

14.1

a32

.4±

5.8b

41.1

±4.

3b49

.7±

9.9b

N/

AN

/A

52.7

±4.

9C

hon

dri

lla

jun

cea

37.4

±6.

9a20

.3±

2.3a

67.4

±7.

0b11

.8±

0.8c

N/

AN

/A

30.1

±2.

7S

onch

us

oler

aceu

s49

.0±

11.1

aN

/A

18.7

±2.

1a19

.9±

2.1a

37.8

±8.

2a31

.2±

6.1a

28.3

±2.

5A

lliu

mam

pel

opra

sum

16.3

±1.

5ab

14.5

±0.

9ab

8.5

±0.

6c16

.4±

2.5a

9.4

±0.

8c18

.8±

1.1b

13.8

±0.

6T

arax

acu

mob

ovat

um

16.5

±1.

2a20

.7±

2.0a

7.8

±0.

4b8.

1±

0.5b

N/

AN

/A

12.7

±0.

8

Clo

nal

spec

ies

Ap

ium

nod

iflo

rum

101.

0±

8.5a

N/

AN

/A

201.

8±

15.4

bN

/A

N/

A15

2.5

±11

.5R

um

exp

ulc

her

105.

2±

8.3a

b92

.3±

5.4a

b11

5.7

±9.

5a80

.1±

6.6b

N/

AN

/A

98.3

±4.

0R

um

exp

apil

lari

s11

4.8

±11

.5a

60.7

±5.

3b12

1.4

±8.

7a47

.7±

4.8b

N/

AN

/A

86.1

±5.

1S

ilen

ev

ulg

aris

24.9

±1.

4a21

.9±

1.8a

19.6

±1.

5ab

15.8

±1.

1bN

/A

N/

A20

.4±

0.8

N/

A5

No

tA

pp

lica

ble

.

a,b

,c,d

5T

he

sam

esu

per

scri

pt

lett

ers

foll

ow

ing

yie

ldm

easu

rem

ents

inea

chro

win

dic

ate

mea

ns

±S

Eca

nn

ot

be

dis

tin

gu

ish

edst

atis

tica

lly

.D

iffe

ren

tsu

per

scri

pt

lett

ers

ind

icat

eth

e

yie

lds

are

stat

isti

call

yd

iffe

ren

t.P

airs

of

dat

aw

ere

com

par

edu

sin

gM

ann

-Wh

itn

eyU

test

(p,

0.05

);m

ult

iple

sets

of

dat

aw

ere

init

iall

yco

mp

ared

usi

ng

Kru

skal

-Wal

lis

(p,

0.05

).

Pai

rwis

ed

iffe

ren

ces

wer

eth

end

eter

min

edu

sin

ga

Bo

nfe

rro

ni

corr

ecti

on

.


(Figure 3A and B) in which the highest yield rates were recorded at the same siteover the study years, other factors, such as soil characteristics (e.g., pH, texture,nutrients), land uses (e.g., ploughed-unploughed agricultural lands), or even thepresence of local ecotypes of the same species, might have influenced yields.

Regarding intra-sample variability, the species with the highest levels (CVs .

90%) were Papaver rhoeas, Scolymus hispanicus, Silybum marianum and Sonchusoleraceus. Under the same environmental growth conditions, the yield of thesespecies varied widely, possibly because of microhabitat characteristics. Steadyproductions (CVs , 50%) were found in Apium nodiflorum, Rumex papillaris,Rumex pulcher, Silene vulgaris and Taraxacum obovatum, mostly clonal species, inwhich low genetic variability would be expected.

Plant DensityEstimates of plant density are presented in Table 4. Density ranged between

2,000–15,000 plants ha21 and quadrats ha21 in both clonal and non-clonal herbs.Considerably lower values were found in Scolymus hispanicus (500 plants ha21), in

Figure 3. Different patterns of variation on plant yield (A–D; g of edible plant material) between sites(site 1 in black, site 2 in white) and years (2007–2009). The correlation coefficients with environmentalfactors are also shown (P: precipitation, T: temperature, altitude; * p, 0.05, ** p, 0.01).


Tab

le4.

Pla

nt

den

sity

of

per

enn

ial

(200

8)an

dan

nu

al(2

008

and

2009

)sp

ecie

sat

the

sam

pli

ng

area

s(m

ean

±S

E;

ind

ivid

ual

sh

a21

inn

on

-clo

nal

spec

ies,

and

nu

mb

ero

f20

320

cmq

uad

rats

ha2

1o

ccu

pie

db

yth

ep

lan

tin

clo

nal

spec

ies)

.

2008

2009

Pla

nt

spec

ies

Sit

e1

Sit

e2

Sit

e1

Sit

e2

To

tal

aver

age

Clo

nal

spec

ies

Ru

mex

pu

lch

er14

,570

±2,

913a

3,59

3±

812b

--

9,43

5±

1,73

3S

ilen

ev

ulg

aris

7,62

3±

1,11

3a5,

821

±1,

086a

--

6,75

7±

782

Ru

mex

pap

illa

ris

3,85

7±

1,04

6a5,

773

±1,

690a

--

4,72

8±

956

No

n-c

lon

alsp

ecie

s

All

ium

ampel

opra

sum

25,3

50±

7,96

4a11

,552

±2,

966b

--

15,4

94±

3,18

9C

hon

dri

lla

jun

cea

8,77

9±

1,20

6a6,

267

±1,

138a

--

7,68

7±

850

Foe

nic

ulu

mv

ulg

are

2,15

0±

588a

11,4

00±

1,75

7b-

-6,

513

±1,

085

An

chu

saaz

ure

a1,

061

±26

5a5,

907

±83

0b-

-3,

984

±59

1C

ich

oriu

min

tybu

s4,

237

±59

2a2,

914

±63

5a-

-3,

676

±43

9B

eta

mar

itim

a2,

371

±46

9a5,

054

±1,

132b

--

3,41

2±

544

Sco

lym

us

his

pan

icu

s54

2±

82a

537

±16

7a-

-54

0±

84P

apav

errh

oeas

15,6

38±

4,03

9ab

9,91

1±

4,04

7ab

17,1

29±

2,21

4a6,

825

±2,

361b

13,7

04±

1,75

1S

ily

bum

mar

ian

um

1,21

6±

316a

2,18

6±

1,04

1a8,

560

±1,

377b

N/

A4,

500

±77

2S

onch

us

oler

aceu

s3,

386

±66

7a4,

133

±1,

030a

2,00

0±

727a

4,02

1±

768a

3,52

3±

415

N/

A5

No

tA

pp

lica

ble

.

a,b

5T

he

sam

esu

per

scri

pt

lett

ers

foll

ow

ing

den

sity

mea

sure

men

tsin

each

row

ind

icat

em

ean

s±

SE

can

no

tb

ed

isti

ng

uis

hed

stat

isti

call

y.

Dif

fere

nt

sup

ersc

rip

tle

tter

sin

dic

ate

the

den

siti

esar

est

atis

tica

lly

dif

fere

nt.

Pai

rso

fd

ata

wer

eco

mp

ared

usi

ng

Man

n-W

hit

ney

Ute

st(p

,0.

05);

mu

ltip

lese

tso

fd

ata

wer

ein

itia

lly

com

par

edu

sin

gK

rusk

al-W

alli

s(p

,0.

05).

Pai

rwis

ed

iffe

ren

ces

wer

eth

end

eter

min

edu

sin

ga

Bo

nfe

rro

ni

corr

ecti

on

.


agreement with previous studies (Polo et al. 2009). Conversely, Allium ampelopra-sum attained the highest rates (11,000–25,000 plants ha21). Results reveal a widegradient on plant density values, from sparse to high-density distributions; as withplant yields, some species displayed large variation in plant density between sites,especially in Foeniculum vulgare and Rumex pulcher. Intra-species variation in plantdensity was possibly influenced by local differences in soil characteristics and landuse. In Taraxacum obovatum and Apium nodiflorum, plant density was not estimatedbecause the natural microdistribution of these species at the study sites was limitedor it was reduced by herbicide application, as previously mentioned in Apiumnodiflorum at site f. Accordingly, the minimum number of transects required forsampling estimates was not reached (n, 25 transects).

Plant density in annual herbs that were sampled in two different yearsranged from 1,200 plants ha21 in Silybum marianum to 17,000 plants ha21 inPapaver rhoeas (Table 4). Between-site differences were only found in Papaverrhoeas in 2009, whereas the annual yields of Sonchus oleraceus remained steadyover the two years of study. However, the annual availability of Silybummarianum fluctuated considerably and in one instance even dropped below theminimum values required for sampling estimates (n, 25 transects). The totalsurface occupied by this thistle at site c was very small and, consequently, thetotal amount of edible plant material available in this area is also very low. Incontrast to perennials, plant abundance of annual herbs may vary considerablyover time since their seeds can remain in a dormant state for long periods andgerminate only under suitable environmental conditions (Booth et al. 2003).

Plant density of the surveyed wild vegetables was found to be considerablyhigh in most cases, suggesting that the sampling areas can generally provideprolific quantities of wild food resources. As we observed in the course offieldwork, management practices like deep ploughing and herbicide sprayingcaused reversible short-term modifications in plant distribution. The abandon-ment of traditional agricultural activities has also led to the disappearance ofpotential habitats, limiting the availability of these plants, as previously recordedfor Scolymus hispanicus (Polo et al. 2009). In some potential habitats, such asvacant building plots, plants have been definitely removed. Those observationsdovetail with local perception that wild food plants are less abundant now than50 years ago (Tardıo et al. 2005), specifically for the species Scolymus hispanicus,Silene vulgaris, Rumex papillaris and Chondrilla juncea (Aceituno-Mata 2010),although there are no quantitative ecological data for an adequate comparison.The spatial distribution of plants is very important for gatherers, since theharvesting effort depends not only on the density in a certain place but also onthe total abundance of plants available in the area (Polo et al. 2009).

Modern agricultural practices such as tractor ploughing affect not only theplant distribution but also the edible portion of the plants. For example,Chondrilla juncea or Cichorium intybus collectors preferred the blanched shootswhich sprouted in ploughed lands because they found these plants more tenderand less bitter, with a taste that they associate with the modern ‘‘witloof’’ or‘‘Belgian endive’’ (Tardıo et al. 2005; Tardıo 2010). Today, due to modernagricultural practices, these species commonly grow away from farmlands andthey do not develop these blanched shoots.


Production per HectareThe estimated production per hectare of each weedy vegetable is shown in

Figure 4. There was a wide variation in the yields of the plants at the two sitessurveyed, mainly due to differences in plant density figures. At the samplingareas, and in descending order of yield, a total of 1,800 kg ha21 (total averagevalues) of Foeniculum vulgare, 700–1,000 kg ha21 of Beta maritima, Rumex pulcher,Papaver rhoeas and Silybum marianum, and of 80–400 kg ha21 for the remainingspecies could be obtained. The lowest yields (30 kg ha21) were found in Scolymushispanicus. However, according to several ethnobotanical studies, this thistle isone of the most appreciated wild greens and it is still collected nowadays(Aceituno-Mata 2010; Polo et al. 2009; Tardıo et al. 2006).

Alternatives for Traditionally Consumed Wild VegetablesIn this section, we discuss the viability of a sustainable exploitation of wild

vegetables. Sustainable exploitation depends mainly on two factors: 1) naturalavailability; and 2) consumer demand. Because of the different densities andyields in the examined species and because of the different preferences ofgatherers, it is unlikely that one type of management is suitable for all species.Therefore, three likely scenarios for sustainable harvesting have been considered:1) organic farming; 2) harvesting of wild plants for commercial purposes; and3) harvesting of wild plants for domestic consumption. In the light of the resultsobtained in this paper, we discuss how the species studied could fit into thesethree scenarios.

Figure 4. Wild food plants’ production per hectare at the study sites, indirectly calculated fromproduction per plant and plant density (kg ha21; mean ± SE).


Organic Farming

Wild edible plants are a good reservoir of potential new crops for aspecialized market (Turner et al. 2011). Indeed, some examples of ‘‘new’’vegetables are found among wild plants with deep roots in Mediterranean foodtraditions, such as rocket salads (Eruca vesicaria [L.] Cav. and Diplotaxis tenuifolia[L.] DC) and watercress (Rorippa nasturtium-aquaticum Hayek). They are aninteresting case of recent crop domestication in which the favorable combinationof positive experience (sensory component of acceptance) and information (localgastronomy, health promotion) have contributed to successfully spread the useof these species (D’Antuono et al. 2009).

Cultivation under organic conditions might be a viable alternative forthose species that may be more prone to overexploitation, for example becausetheir low natural availability may not satisfy the potentially increasingdemand. This is the case of culturally important species, especially thosewhich showed low production rates, such as Scolymus hispanicus and Silenevulgaris. Both species are currently collected from the wild and sold in localmarkets and restaurants (Barao and Soveral 2010; Tardıo 2010), where atraditional dish using those species can cost 10 J (personal observations in thecity of Madrid, 2012). The agronomic potential of these species has beenpreviously studied (Alarcon et al. 2005; Garcıa et al. 2002). Scolymus hispanicusis considered a neglected crop (Hernandez-Bermejo and Leon 1992) and it iscurrently a minor crop cultivated in southern Spain (Soriano 2010). Moreover,given their low natural density, gathering a considerable amount of thistles is avery time-consuming activity.

Requirements of seeds and seedlings of wild plants, as well as labor costs andproductivity, are not well known. However, cultivation experiments designed toexplore the agronomic feasibility of several of the species studied are currentlybeing conducted by our research group. Additionally, technical information onorganic farming, including processing and organic certification of wild vegetables,is available from previous research, such as the pilot projects conducted in westernand southern Spain (Casco 2000; Fernandez and Lopez 2005). According to theseexperiments and based on their nutritional profiles (Morales et al. 2012; Sanchez-Mata et al. 2012), other candidates for cultivation could be Rumex pulcher, Anchusaazurea, Allium ampeloprasum, Silybum marianum, Cichorium intybus and Chondrillajuncea, although they should be subject to sensory evaluation by panellists in orderto ensure consumer acceptance. In addition, the production of Apium nodiflorum ina similar way to watercress, by hydroponics or aquaculture, may avoid thepollution risk that this aquatic plant is exposed to by the use of pesticides or thepresence of pastoral activity in the area.

Wild Gathering for Commercial Purposes

Sustainable harvesting of wild vegetables might be encouraged as a use ofbiodiversity which potentially offers social benefits to local communities(Menendez-Baceta et al. 2012). Weeds are fast-growing species that reproduceeasily and, even in low-density perennials such as Scolymus hispanicus, anappropriate harvesting procedure allows continued plant growth. Such practicesin harvesting leafy vegetables that were conducted by our informants include


leaving the subterranean organs of perennials intact and collecting fewer butlarger specimens (Aceituno-Mata 2010). Other good practices include allowingthe populations to produce seed, preventing the plants from being exhausted dueto a repeated collection of the same individuals, and not gathering isolatedindividuals (Thayer 2006).

The collection of abundant wild food resources can be turned into acommercial activity to promote rural development. Species with high yields thatare culturally appreciated such as Allium ampeloprasum, Chondrilla juncea, Betamaritima, Rumex papillaris, Foeniculum vulgare, Silybum marianum, and Sonchusoleraceus (Aceituno-Mata 2010; Tardıo et al. 2005) are good candidates for wildcollection with commercial purposes. Although the collection of Alliumampeloprasum might be considered destructive, our experience shows that manysmall bulbs produced around the central bulb remain in the collecting place.Moreover, wild populations also include smaller individuals that are not selectedby the gatherers, allowing its self-regeneration.

Wild food harvesting could be developed in the framework of the organic marketand sustainable harvest certification in order to assure sustainability and food quality(Muller 2009). Organic wild collection is a very broad concept which encompassesfood resources collected in pastures, uncultivated lands, and other areas of theagriculture landscape (IFOAM 2006). Organic certification can be applied to wildharvested plants, as provided in legal organic regulations at the regional (CAEM 2010)and international (e.g., EU Regulations EEC 834/07 and 889/08) scales. Likewise,many private organic standards have arisen that have additional requirements forwild harvesting (e.g., Certification of Environmental Standards [CERES] in Germany;Ekologisk Produktion Certifierad [KRAV] in Sweden; Bio-Suisse in Switzerland), as wellas others focused on sustainable harvest certification of wild products in a broadersense, including other uses apart from food (FairWild Foundation 2010).

All these certification systems could foster safe and appropriate marketing ofwild vegetables as fresh or processed products. In fact, recent changes in marketdemands are influencing the reevaluation of wild foods, which are served in localrestaurants as unique traditional delicacies. The wild food and drink sectorseems to be a successful, profitable, and expanding one. More than 300 wildproducts are currently being produced for the global organic market, includingmedicinal and aromatic plants, nuts, fruits, and mushrooms collected in forestedareas (IFOAM 2006). Because of the contamination risks that weedy vegetablesare potentially exposed to, such as car exhaust, agrochemicals, and other sourcesof pollution, the specific standards for the collection of weedy vegetablesgrowing on agricultural areas need to be more extensively developed in order toavoid unsafe consumption of wild edibles. In this way, the combination oforganic farming and wild collection of weedy edibles in the same plots could bean interesting alternative to guarantee food safety.

Wild Collection for Self-Consumption

Generally, small amounts of plant material are required to fulfill domesticharvesting needs. According to our yield and plant density estimations, theruderal species herein studied are suitable to be harvested regularly for self-consumption without endangering their populations. Those species have been


traditionally collected and their populations do not seem to have suffered fromthis exploitation. Therefore, wild edibles could be harvested as useful resourcesin the effort to achieve food security and sovereignty. The maintenance oftraditional practices, like gathering wild plants, has shown to operate as animportant reservoir of useful knowledge, preventing its erosion. In central Spain,wild edibles have been an important dietary supplement in springtime,coinciding with a seasonal period of scarcity of cultivated vegetables (Acei-tuno-Mata 2010). Nowadays, these practices can be interesting for food securityas a buffer against times of food shortage or food crisis, such as the famineperiods that happened in some parts of Europe in the nineteenth and twentiethcenturies (Łuczaj et al. 2012). Although the economic potential of foraging wildedibles is unknown, it could be significant for domestic economies, as suggestedby the economic benefits of Spanish home gardens (Reyes-Garcıa et al. 2012).Vogl-Lukasser et al. (2010) report that some weeds spontaneously emerging inAustrian Alpine home gardens are tolerated because they are seen as anopportunity for increasing the number of useful plants and saving money. Inhome gardens, foraging wild edibles could also be transformed into a valuableenvironmental educational tool to promote traditional ecological knowledge andthe conservation of wild species and their associated habitats (Sanderson andPrendergast 2002). Since wild foraging is not risk-free, however, competentidentification of plants should be encouraged, especially for urban or untrainedcollectors, in order to avoid accidental poisoning by toxic look-alike species(Colombo et al. 2010).

Conclusion

This work aims to contribute to the knowledge and valorization oftraditionally consumed wild vegetables. Despite their great nutritional interest,wild vegetables are still an undervalued food resource and very little is knownabout their production and sustainable exploitation. As far as we know, thispaper provides the first quantitative data on the natural yields and availability of15 Mediterranean wild green vegetables. Due to the great heterogeneity of thespecies with respect to life and growth forms, we have developed a basic yieldevaluation methodology for wild vegetables that can be applied in other surveys.

According to local people, changes in land uses and management practiceshave diminished in some cases the local availability of these plants, especiallydue to the abandonment of traditional agricultural practices, contamination risks,and the urbanization of agricultural lands. Nevertheless, the edible yield of theseplants was found to be considerably high in most cases, revealing the potentialof traditional wild vegetables to increase food diversity. Some of the mostappreciated of the still-collected species, such as Scolymus hispanicus and Silenevulgaris, showed low production rates. This finding suggests that species yielddoes not drive the selection of wild edible plants.

Traditional harvesting offers sociocultural, economic, and ecological benefitsto local communities. It also contributes to the conservation of bioculturaldiversity and promotes cultural empowerment to resist acculturation. Moreover,


commercial wild collection and organic farming are feasible alternatives that canpromote food quality and rural economic growth. Natural yields of wild edibleplants can be compared with those obtained under agricultural conditions.Additionally, consumer acceptance should be assessed by sensory evaluationpanels when considering their interest as potential new crops.

Acknowledgments

Financial support for this project was granted by the ERDF and the Spanish Ministryof Education and Science (CGL2006-09546/BOS and CSO2011-27565). We want to thankS. Gonzalez and A. Velez del Burgo for collaborating in the fieldwork and the SpanishMeteorological State Agency (AEMET) for providing meteorological data. We are alsograteful to the Department of Nutrition and Bromatology II of the UniversidadComplutense de Madrid, especially to M. C. Sanchez-Mata, M. Camara, V. Fernandez,P. Morales, P. Garcıa and B. Ruiz for performing the plant nutritional analysis of thisproject. Finally, we thank the reviewers for their very appropriate and insightfulcomments.

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