Patagonian berries as native food and medicine

Journal of Ethnopharmacology 241 (2019) 111979

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Review

Patagonian berries as native food and medicine Guillermo Schmeda-Hirschmann

a,b,∗

c

d

, Felipe Jiménez-Aspee , Cristina Theoduloz , Ana Ladio

e

T

a

Laboratorio de Química de Productos Naturales, Instituto de Química de Recursos Naturales, Universidad de Talca, 3460000, Talca, Chile Fraunhofer Chile Research Foundation, Centre for Systems Biotechnology (FCR-CSB), Av. del Cóndor 844, Huechuraba, Santiago de Chile, Chile Departamento de Ciencias Básicas Biomédicas, Facultad de Ciencias de la Salud, Universidad de Talca, Talca, Chile d Laboratorio de Cultivo Celular, Facultad de Ciencias de la Salud, Universidad de Talca, 3460000, Talca, Chile e Laboratorio Ecotono, INIBIOMA (CONICET), Universidad Nacional del Comahue, Bariloche, Río Negro, Argentina b c

ARTICLE INFO

ABSTRACT

Keywords: Patagonia Native berries Bioactive compounds Traditional use Polyphenols

Ethnopharmacological relevance: Patagonia is the southernmost part of the South American continent including Chile and Argentina. Berries and wild fruits have been gathered by the native Patagonians as food and medicine for over 14,000 years. The economic potential of the native berries as health promoting and relevant sources of bioactive substances has become apparent with several studies in the last decades. Aim of study: This work aims to provide an insight into the ethnohistorical records of wild edible fruits from Patagonia starting with the archeobotanical studies to the contemporary use of the resources. The chemical and bioactivity studies on the native fruits are presented and discussed. Methodology: A search of electronic databases including Scopus, Scielo, Google Scholar, PubMed, ScienceDirect and SciFinder, as well as hand-search was carried out to perform an integrative review on the native Patagonian berries. Results: The use of native berries as food and medicine by the ancient hunter-gatherer societies can be traced back to the early occupation of Patagonia. The same species used in prehistoric times are still used as food by the contemporary population in this area. Chemical and bioactivity studies have reported remarkable activities in several of the native berries, including calafate (Berberis spp.), native strawberry (Fragaria chiloensis), currants (Ribes spp.), Patagonian raspberries (Rubus spp.) and maqui (Aristotelia chilensis) fruits. The increasing demand for maqui and calafate led to the selection of varieties for commercial production. The fruit constituents show strong antioxidant and inhibitory effect towards enzymes associated with metabolic syndrome, including αamylase, α-glucosidase and lipase. Some berry constituents exert anti-inflammatory effects in vitro. The phytochemicals identified include a wide array of phenolics of different structural skeletons. Changes in composition and bioactivity after simulated gastric and intestinal digestion, as well as colonic fermentation, have been reported in some Patagonian species. Conclusions: Patagonian berries are a relevant source of bioactive compounds with several health promoting properties. The long tradition of use and the interest of the population for their consumption has led to the development of some of this fruits as new potential crops. The ethnobotanical evidence shows a shared knowledge among the different indigenous communities on plant uses according to the local resources, and an integration of the ancient knowledge into the contemporary society. Other species are being investigated to get a more complete picture of the food and medicinal plants from Patagonia.

1. Introduction

south barrier associated to high rainfall in the Pacific area and drier ecosystems in the Atlantic Patagonia. Due to the abundant rain, the western Patagonia present dense forests, while in the eastern Andean slopes, climate is dryer leading to shrub land and grasslands (steppes). The dominant environment is semiarid to arid (Fig. 2). The Patagonian Sub Antarctic forest extends over Andean mountains

Patagonia is the southernmost part of the South American continent and comprises over one million square kilometers of Argentina and the southern portion of Chile. It is located between 37° and 55° S and includes a diversity of habitats (Fig. 1). The Andes form a natural north-

∗

Corresponding author. Laboratorio de Química de Productos Naturales, Instituto de Química de Recursos Naturales, Universidad de Talca, 3460000, Talca, Chile. E-mail address: [email protected] (G. Schmeda-Hirschmann).

https://doi.org/10.1016/j.jep.2019.111979 Received 25 April 2019; Accepted 26 May 2019 Available online 30 May 2019 0378-8741/ © 2019 Elsevier B.V. All rights reserved.

Journal of Ethnopharmacology 241 (2019) 111979

G. Schmeda-Hirschmann, et al.

Fig. 1. Map of South America showing the Patagonia (from Google Maps).

Fig. 2. Landscapes of Patagonia. a) Shrub forest in western Patagonia (Puerto Natales, Ultima Esperanza, Chile); b) Patagonian steppe (eastern Anden slopes); c) Eastern Andean slopes, Cuyin Manzano, Neuquen, National Park Nahuel Huapi; d) Poaceae steppe, Pilcaniyeu, Rio Negro, Argentina. 2

Journal of Ethnopharmacology 241 (2019) 111979

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Table 1 Distribution, life form and fruit type of Patagonian berries. Species Berberidaceae Berberis empetrifolia Lam.

Common names

Distribution in Argentina (RA) and Chile (RCH)

Life form

Fruit type

calafate, michay, zarcilla, montenegro, cherque, calafatillo, mich kan, mich calafate enano, monte negro, calafatillo, zarcillo, monte negro

RA: CAT, CHU, LRI, MEN, NEU, RNE, SCR, SJU, TDF RCH: IV, V, VI, VII, VIII, IX, X, XI, XII, RME RA: CHU, NEU, RNE, SCR, TDF RCH: VI, VII, VIII, IX, X, XI, XII RA: CHU, NEU, RNE, SCR, TDF RCH: VI, VII, VIII, IX, X, XI, XII RA: CHU, NEU, RNE, SCR, TDF RCH: VI, VII, VIII, IX, X, XI, XII RA: CHU, NEU, RNE RCH: VIII, IX, X, XI RA: NEU, RNE; RCH: VII, VIII, IX, X, XII RA: CHU, NEU, RNE, TDF; RCH: VII, VIII, IX, X, XI

shrub

berry

shrub

berry

shrub

berry

shrub

berry

shrub

berry

shrub

berry

shrub

berry

Berberis ilicifolia L.f.

calafate

Berberis microphylla G.Forst=B. heterophylla

michay, michai, calafate Kor, me'ch, michi calafate Mëchai, michay saloll

Berberis microphylla G.Forst=B. buxifolia Lam. Berberis serratodentata Lechl. Berberis trigona Kunze ex Poepp. & Endl. Berberis darwinii Hook. Elaeocarpaceae Aristotelia chilensis (Molina) Stuntz Ericaceae Empetrum rubrum Vahl ex Willd.= Empetrum nigrum var. andinum A.DC. Gaultheria antarctica Hook.f. Gaultheria mucronata (L. f.) Hook. & Arn. = Pernettya mucronata (L. fil.) Gaud Gaultheria phillyreifolia (Pers.)Sleumer

calafate, michay chileno, michay michay, espino, calafate, rullin, chacaihua, michai, michay, klün maqui, maquei, queldron, quellón, koelon, maki, klon, clon, queldón, coclon, Quëlon

RA: CAT, CHU, LPA, LRI, MEN, NEU, RNE, SJU, SLU; RCH: IV, V, VI, VII, VIII, IX, X, XI, RME, IJF

tree or shrub

berry

mutilla, kôl, kôle kapa, sebisa, uvilla de perdicita, brecillo, murtilla de magallanes, mahueng, uvilla, brecillo, malhueng chaura

RA: CHU, MEN, NEU, RNE, SCR, TDF; RCH: V, VII, VIII, IX, X, XI, XII, RME, IJF RA: CHU, RNE, SCR, TDF; RCH: IX, X, XI, XII RA: CHU, NEU, RNE, SCR, TDF; RCH: VIII, IX, X, XI, XII

shrub

drupe

shurb

berry

shrub

berry

shrub

berry

shrub

berry

shrub

berry

shrub

berry

shurb shrub

berry berry

shrub

berry

shrub

berry

tree or shrub

berry

tree or shrub

berry

tree

berry

tree or shrub

berry

shrub shrub

berry berry

shrub shrub

berry berry

perennial plant shrub

conocarp

perennial plant

conocarp

chaura, Schals, shal, chaura chaura, gus, gush, amaiingur chura, chabra chaura, murtillo chaura, manzanita del campo, manzanita

Gaultheria poeppigii DC = Pernettya myrtilloides Zucc. ex Steud. Gaultheria pumila (L.f.) D.J.Middleton

Shal, mutilla, chaura, shanamaim

Grossulariaceae Ribes cucullatum Hook. & Arn.

parrillita, parrilla hoja chica

Ribes densiflorum Phil. Ribes magellanicum Poir.

grosellero parrilla, zarzaparrilla, mulul

Ribes punctatum Ruiz & Pav. = Ribes glandulosum auct. non Ruiz & Pav. Ribes trilobum Meyen Myrtaceae Amomyrtus luma (Molina) D.Legrand & Kausel

grosella, mulul, parrilla

Luma apiculata (DC.) Burret Luma chequen (Mol.) Kaus = Myrceugenella chequen (Molina) Kausel Myrceugenia exsucca (DC.) O.Berg Myrceugenella planipes (H. et A.) Berg Myrteola nummularia (Lam.) O.Berg Ugni candollei (Barn.) Berg Ugni molinae Turcz. Rosaceae Fragaria chiloensis (L.) Mill.

RA: BAI, CHU, NEU, RNE; RCH: VII, IX, X, XI, XII RA: CHU, COR, NEU, RNE, SLU, SCR; RCH: VII, VIII, IX, X, XI RA: CHU, MEN, NEU, RNE, SCR, TDF; RCH: IX, XII

parrilla

RA: CHU, MEN, NEU, RNE, SCR, TDF; RCH: V, VI, VIII, IX, X, XI, XII, RME RA: CHU, NEU; RCH: VIII, IX, X RA: RNE, SCR, TDF; RCH: VI, VII, VIII, IX, X, XI, XII, RME RA: MEN, RNE; RCH: IV, V, VI, VII, VIII, IX, X, RME RCH: IV, V, VII, VIII, ARA, RME

luma, luma blanca, luma colorada, roloncavi, palo madroño, cauchao, cauchahue arrayán, palo colorado, cuthu, quetri, arrayán rojo, temu, arama, quitri, kollimamüll, kütri, temu, temo, kollimamül, collimamil, palo rojo chequén

RA: CHU, NEU, RNE; RCH: VII, VIII, IX, X, XI RA: CHU, NEU, RNE; RCH: IV, V, VI, VII, VIII, IX, X, XI, RME RCH: IV-X

pitra, patagua, pitra, temu, picha, peta, petra, patagua

RA: CHU, NEU, RNE; RCH: IV, V, VI, VII, VIII, IX, X, XI, RME RA: NEU; RCH: VIII, ARA, IX, X, XI RA: NEU, RNE, SCR, TDF; RCH: VIII, IX, X, XI, XII, IJF RCH: VII, VIII, IX, X RA: CHU, NEU, RNE; RCH: V, VI, VII, VIII, IX, X, XI, XII

Peta, peta blanca, mitahue murta, té de Malvinas murta, té de las Malvinas Trautrau, murtilla blanca mutilla uñi, murta frutilla silvestre, llahuén,

Margyricarpus pinnatus (Lam.) Kuntze

perlilla, perla, hierba de la perlilla, yerba de perdiz, manzanita

Rubus radicans Cav.

miño miño, zarza, miñe-miñe

RA: NEU, RNE; RCH: VI, VII, VIII, IX, X, XI, IJF RA: BAI, CHU, COR, ERI, JUJ, LPA, MEN, NEU, RNE, SAL, SLU, SCR, TUC; RCH: IV to X RA: NEU; RCH: IX, X, XI, XII

berry

(continued on next page)

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Table 1 (continued) Species

Common names

Distribution in Argentina (RA) and Chile (RCH)

Life form

Fruit type

Rubus geoides Sm.

frutilla de Magallanes, waásh shal, miñe-miñe, zarza, miñemiñe, frutilla silvestre, belakámaiim, palazaachix, frutilla de la cordillera, frutilla de la zorra, frutilla de Magallanes, frambuesa silvestre

RA: NEU, RNE, SCR, TDF; RCH: VIII, IX, X, XI, XII, IJF

perennial plant

conocarp

RA: Argentina; Provinces of Argentina: CAT (Catamarca), CHU (Chubut), LPA (La Pampa), LRI (La Rioja), MEN (Mendoza), NEU (Neuquén), RNE (Rio Negro), SCR (Santa Cruz), SJU (Jujuy), TDF (Tierra del Fuego). RCH: Chile, Regions of Chile IV- XII, and RME (Metropolitan).

and glacial valleys. The climate is humid and temperate, with an annual rainfall of up to 2000 mm. The vegetation is deciduous or evergreen, with meadows and peat bogs (Fig. 2). In contrast, the Argentinean and central Chilean regions have a Mediterranean type climate, and an annual rainfall between 300 and 900 mm. The vegetation varies from grasslands to spiny steppe scrubs (Barthélémy et al., 2008). Since ancestral times, the entire Patagonia has been inhabited by different native cultures. The largest human groups in this vast territory are the Mapuche and Gününa küna and Aónikenk (commonly named Tehuelches), inhabiting the plains and the Andean slopes of Argentina, the valleys and Sub Antartic forests. Both groups had an ancentral history of cultural interchange and a great movility across the Andes (Del Rio, 2010). They comprised different and complex subgroups: Lafquenches and Williches at the Pacific coast, Pehuenches at the Andean slopes and at the central valley, among others. They occupied an area characterized by Nothofagus, Austrocedrus chilensis and Araucaria araucana forests as part of their cultural landscape. They are considered great explorers of these forests playing a significant role within their cosmology (Molares and Ladio, 2014). The Mapuche and Tehuelche territory, south of the Bío-Bío River in Chile and Rio Negro in Argentina, remained as an independent territory up to the 1880 decade. This situation changed with the military campaigns of Argentina and Chile aiming to incorporate this territory into their newly created countries. Since the 18th century, this area has drastically changed in its social, political, environmental and geographical configuration. The extensive farming model and the intense timber exploitation were imposed in the region, thus incorporating the Patagonian territory into the international capitalist market. During this process, the indigenous populations of the region were decimated and expelled from their lands. The territory was usurped and subdivided mainly into lots controlled by large livestock companies (Del Rio, 2010; Skewes, 2016). The surviving indigenous families that managed to become established in marginal or limited areas, dedicated themselves to livestock breeding as a subsistence activity (Ladio, 2001). Another Patagonian native cultures were the Selknam (also renamed Onas), the Aónikenk at Tierra del Fuego, the sea nomads Haus, Kawashkar (also named Alacaufes) and Yamana (Yagan) at the Pacific Southern cost and the Fueguian channels and fiords (Domínguez Díaz, 2010; Rozzi, 2013). The occupation of Tierra del Fuego by Argentina and Chile took place in the last decades of the 19th and the early 20th century. With the extensive sheep farming and gold exploitation, the native Selknam, Kawashkar and Yamana were decimated by diseases and man hunting. All of these cultures have suffered instances of severe genocide that have drastically eroded their cultural plant patrimony (Molares and Ladio, 2009a, 2009b;Domínguez Díaz, 2010). To date, there is an increasing interest in the study of the potential of Patagonian berries. Therefore, based on an integrative bibliographic review and on our own results, we present an overview of native Patagonian berries which hold most cultural significance, identifying local practices, phytochemical as well as bioactivity information.

2019. The database used were: Scopus (www.scopus.com), Scielo (www. scielo.org), Google Scholar search engine, PubMed, ScienceDirect and SciFinder. For the ethnobotanical part of this review, the key words used were “Patagonian berries”, “Patagonia + ethnobotany” and all plant species/ families considered in the review. Our bibliographic analysis was also enriched with ethnographical, archeological and ethnohistorical documents not included in the above search engines and databases (Molares and Ladio, 2009b). We considered a species as edible when the source referred to the use as food, drink with or without alcohol, sweets, jams, or the consumption of fresh or dried fruit (Ladio, 2006). The use was recorded as medicinal when the literature indicated that it was also considered capable of curing an illness, relieving pain, and treating or counteracting a symptom of any kind (Estomba et al., 2006; Molares and Ladio, 2009a). Scientific names were updated by consulting web databases, such as www.darwin.edu.ar, mpns.kew.org/mpns-portal and www. theplantlist.com. The information gathered from the documents was interpreted qualitatively, including an in-depth content analysis of the studies. It is important to note that our interpretation, in particular of the oldest literature, to fit traditional uses into recognisable western diseases, is a factor that may bias our revision. Some 30 relevant articles from Argentina and Chile were selected, summarizing the use of Patagonian fruits from the Native American to our contemporary society (Tables 1 and 2). This selection is mainly based in field work observations. Thesis were not included. The revised literature covers some 100 years, starting in 1917 (Gusinde, 1917) to the last contributions on Patagonian food plants. All biogeographic zones from the Argentinean and Chilean Patagonia are covered from the ethnobotanical/ethnographical point of view. General information, including the plant scientific names according to the Plant List and their synonyms was included in Table 1 to better understand older literature and correctly differentiate species. The food and other uses of the fruits are presented in Table 2. For the chemical and pharmacological studies on Patagonian fruits, the literature search included all the scientific names and the common names of some species (calafate, maqui, arrayan, etc.). The search was refined using additional keywords such as fruits and different chemical constituents (phenolics, flavonoids, alkaloids, chemical profiling, HPLC, HPLC-MS analysis, biological activity). 3. Results and discussion 3.1. The prehispanic context Estimations of human occupation in Patagonia are between 18,500 and 14,500 BP. The whole territory was scarcely populated. At the time of European arrival, the main groups included the Mapuche and Tehuelche in the continent, as well as the Selknam in Tierra del Fuego. The Kawashkar and Yamana were sea nomads that lived in the coasts of islands and channels. In a study involving HVR-1 mitochondrial sequences from native groups from Patagonia, Crespo et al. (2018) found differentiation among the groups in insular, northern and southern

2. Materials and methods A bibliographical search was carried out during October 2018 and April 4

Conticello et al., (1997), Kutschker et al., (2002), Ladio (2006), Ladio et al., (2007), Ladio and Rapoport (1999), Mösbach (1992); Muñoz et al., (1980), Lozada et al. 2006, Martínez Crovetto (1980), 1982, Ragonese and Martínez Crovetto (1947), Rapoport et al., (1999), Villagrán et al., (1983) Domínguez Díaz (2010), Domínguez et al., (2012), Gusinde (1917), 1982, Ladio and Lozada (2004), Lozada et al. 2006, Martínez Crovetto (1968), 1982, Mösbach (1992), Ragonese and Martínez Crovetto (1947), Rapoport and Ladio (1999), Rapoport et al., (1999)

calafate, mëchai, michay

saloll calafate, michay, michay chileno, calafate, chacaihua, espino michay, michai, klün, rullin

maqui, maquei, maki, clon, coclon, koelon, klon, queldron, queldón, quellón, quëlon

mutilla, mahueng, kôl, kôle, kapa, sebisa, brecillo, murtilla de magallanes, uvilla, uvilla de perdicita

Berberis microphylla G.Forst = B. buxifolia Lam.

Berberis serratodentata Lechl. Berberis trigona Kunze ex Poepp. & Endl. Berberis darwinii Hook.

5

Ericaceae Empetrum rubrum Vahl ex Willd. = Empetrum nigrum var. andinum A.DC.

Elaeocarpaceae Aristotelia chilensis (Molina) Stuntz

Casamiquela (2002), Conticello et al., (1997), Ladio (2001), Ladio and Lozada (2004), Ladio and Rapoport (1999), Lozada et al. 2006, Maldonado (2014), Martínez Crovetto (1968), 1980, 1982, Ragonese and Martínez Crovetto (1947), Rapoport et al., (2003) Mösbach (1992), Muñoz et al., (1980), Martínez Crovetto (1968), Ragonese and Martínez Crovetto 1947, Villagran et al., (1983) Ragonese and Martínez Crovetto (1947) Conticello et al., (1997), Martínez Crovetto (1982) Conticello et al., (1997), Contreras Vega (2007), Ladio and Rapoport (1999), Martínez Crovetto (1980), 1982, Mösbach (1992), Ragonese and Martínez Crovetto (1947), Rapoport et al., (2003), Villagran et al., (1983)

Ciampagna and Capparelli (2012), Conticello et al., (1997), Domínguez Díaz (2010), Lozada et al. 2006, Martínez Crovetto (1968), 1980, 1982, Ragonese and Martínez Crovetto (1947), Rapoport et al., (2003) Ragonese and Martínez Crovetto (1947)

Ethnobotanical references

calafate, kor, me'ch, michay, michi, michai

calafate, calafate enano, calafatillo, cherque, mich kan, michi, michay, monte negro, killei-úmösh, kierr, uva de la cordillera, zarcillo, zarcilla calafate

Common names registered

Berberis microphylla G. Forst = B. heterophylla

Berberis ilicifolia L.f.

Berberidaceae Berberis empetrifolia Lam.

Species

Table 2 Ethnobotanical information on Patagonian berries.

fresh fruits

fresh fruits, sweets, chicha (called tecu), dried fruits, non-alcoholic beverages, ingredient for curanto (leaves)

fresh fruits, chicha, sweets, non-alcoholic beverage, alcoholic beverage as wine

fresh fruits fresh fruit, sweets, chicha

fresh fruits, sweets

fresh fruits, non-alcoholic beverage fresh fruits, sweets, chicha, non-alcoholic beverage, alcoholic beverage as wine

fresh fruits, sweets, jams, chicha, non-alcoholic beverages,

Edible use

Febrifuge, toothache and “aftas” (mouth virosis), chronic diarrhea, enteritis and dysentery, tonic, astringent, vulnerary, sedative, hepatic, analgesic, anti-inflammatory (leaves, stems and fruits)

febrifuge, astringent, anti-inflammatory (leaves and fruits)

febrifuge, diarrhea treatment, tonic (leaves)

febrifuge, digestive (roots)

Medicinal use and ailments treatment

(continued on next page)

sacred plant, wool dye, tinctorial (fruits), veterinary (leaves)

wool dye, tinctorial (violet color with fruits, yellow with roots), ornamental, living fence (plant)

fuelwood, tools, weapons (wood), tinctorial (roots, fruits), tools, knitting needle (spines)

tinctorial (roots, fruits)

Other uses

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6 Gusinde (1917), Muñoz et al., (1980), Mösbach (1992), Conticello et al., (1997), Ladio and Rapoport (1999), Martínez Crovetto (1980), 1982, Ragonese and Martínez Crovetto (1947), Rapoport et al., (1999), Rapoport and Ladio (1999), Villagran et al., (1983)

parrillita, parrilla hoja chica

grosellero parrilla, zarzaparrilla, mulul

grosella, mulul, parrilla

luma, luma blanca, luma colorada, cauchao, cauchahue, chauchau, palo madroño, reloncavi

Grossulariaceae Ribes cucullatum Hook. & Arn.

Ribes densiflorum Phil. Ribes magellanicum Poir.

Ribes punctatum Ruiz & Pav. = Ribes glandulosum auct. non Ruiz & Pav. Ribes cucullatum Hook. & Arn.

Ribes trilobum Meyen Myrtaceae Amomyrtus luma (Molina) D.Legrand & Kausel

chaura, manzanita, manzanita del campo mutilla, chaura, shal, shanamaim

Gaultheria poeppigii DC. = Pernettya myrtilloides Zucc. ex Steud. Gaultheria pumila (L.f.) D.J.Middleton

parrilla

parrillita, parrilla hoja chica

Ladio (2001), Ladio (2006), Ladio and Lozada (2004), Ladio and Rapoport (1999), Lozada et al. 2006, Martínez Crovetto (1980), 1982, Ragonese and Martínez Crovetto (1947), Rapoport et al., (1999), Rapoport and Ladio (1999) Ragonese and Martínez Crovetto (1947) Estomba et al., (2006), Ladio et al., (2007), Ladio and Rapoport (1999), Lozada et al. 2006, Ladio et al., (2007), Ochoa et al., (2010), Martínez Crovetto (1968), 1980, 1982, Muñoz et al., (1980), Ragonese and Martínez Crovetto (1947), Rapoport et al., (1999), Rapoport and Ladio (1999), Villagran et al., (1983) Mösbach (1992), Martínez Crovetto (1982), Ragonese and Martínez Crovetto (1947) Ladio (2001), Ladio, 2006, Ladio and Lozada (2004), Ladio and Rapoport (1999), Lozada et al. 2006, Martínez Crovetto (1980), 1982, Ragonese and Martínez Crovetto (1947), Rapoport and Ladio (1999)

chura, chabra chaura, murtillo, chaura negra

Gaultheria phillyreifolia (Pers.) Sleumer

Ragonese and Martínez Crovetto (1947) Conticello et al., (1997), Domínguez Díaz (2010), Domínguez et al., (2012), Gusinde (1917), Ladio et al., (2007), Mösbach (1992), Muñoz et al., (1980), Ragonese and Martínez-Crovetto (1947), Martínez-Crovetto (1982), Villagrán et al., (1983) Contreras Vega (2007), Mösbach (1992), Muñoz et al., (1980), Ragonese and MartínezCrovetto (1947), Rapoport et al., (1999), Villagran et al., (1983) Gusinde (1917), Ladio and Rapoport (1999), Muñoz et al., 1980, Villagran et al., (1983) Domínguez Díaz (2010), Domínguez et al., (2012), Muñoz et al., (1980), Martínez Crovetto (1968), Ragonese and Martínez Crovetto (1947)

chaura chaura, amaiingur, charan, gus, gush, schals, shal

Gaultheria antarctica Hook.f. Gaultheria mucronata (L. f.) Hook. & Arn. = Pernettya mucronata (L. fil.) Gaud

Ethnobotanical references

Common names registered

Species

Table 2 (continued)

fresh fruits, chicha, nonalcoholic beverages, sweets, alcoholic beverage as wine, dried fruits

fresh fruits, jams, chicha

fresh fruits, dried fruits

fresh fruits fresh fruits, chicha, sweets

fresh fruits, jams, chicha

fresh fruits

fresh fruits, chicha, sweets

fresh fruits, dried fruits

fresh fruits fresh fruits, sweets, chicha

Edible use

stimulating effect, to calm blows pain and inflammation (stems and leaves), astringent (roots)

depurative, urinary, gastrointestinal disorders, gynecologic (leaves and bark)

dysentery and for skin diseases (leaves)

febrifuge, to relieve heart and circulatory system diseases, depurative, allergies (leaves)

depurative, urinary, gastrointestinal disorders, gynecologic (leaves and bark)

febrifuge (leaves)

sores and ulcers (leaves)

Medicinal use and ailments treatment

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wool dye, tinctorial

Other uses

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Ciampagna and Capparelli, 2012, Conticello et al. 1997, Contreras Vega, 2007, Ladio (2001), Ladio and Lozada (2004), Ladio and Rapoport (1999), Lozada et al. 2006, Mösbach (1992), Martínez-Crovetto (1968), 1980, 1982, Molares and Ladio 2009a, b, Molares and Ladio (2014), Muñoz et al., (1980), Ragonese and Martínez Crovetto (1947), Rapoport et al., (1999), Rapoport and Ladio (1999) Ciampagma and Capparelli (2012), Estomba et al., (2006), Muñoz et al. (1980), Martínez Crovetto (1980), 1968, Ochoa et al., (2010), Ragonese and Martínez Crovetto (1947), Rapoport et al., (1999), Rapoport and Ladio (1999) Ladio et al., (2007), Ladio and Rapoport (1999), Martínez Crovetto (1982), Mösbach (1992), Muñoz et al. (1980), Ragonese and Martínez Crovetto (1947), Rapoport and Ladio (1999) Martínez Crovetto (1968), 1980, 1982, Mösbach (1992), Muñoz et al. (1980), Ragonese and Martínez Crovetto (1947), Rapoport et al., (2003), Rapoport and Ladio (1999), Ladio et al., (2007), Ladio and Rapoport (1999)

frutilla silvestre, llahuén, quellen,

mutilla uñi, murta, uñü

Ugni molinae Turcz.

7

perlilla, romerillo, perla, hierba de la perlilla, yerba de perdiz, manzanita, perla

miño miño, zarza, miñe-miñe,

frutilla de Magallanes, waásh shal, miñe-miñe, zarza, frutilla silvestre, belakámaiim, palazaachix, frutilla de la cordillera, frutilla de la zorra, frambuesa silvestre

Margyricarpus pinnatus (Lam.) Kuntze

Rubus radicans Cav.

Rubus geoides Sm.

Rosaceae Fragaria chiloensis (L.) Mill.

trautrau, murtilla blanca

Ugni candollei (Barn.) Berg

pitra, patagua, pitra, temu, picha, peta, petra

peta, peta blanca, mitahue murta, té de Malvinas

Contreras Vega (2007), Muñoz et al., (1980), Martínez Crovetto (1980), Rapoport et al., (1999), Rapoport and Ladio (1999), Villagran et al., (1983) Muñoz et al., (1980), Villagran et al., (1983) Gusinde (1917), Dominguez et al., (2012), Martínez Crovetto (1982), Ragonese and Martínez Crovetto (1947), Rapoport and Ladio (1999) Gusinde (1917), Martínez Crovetto (1982), Mösbach (1992) Villagran et al., (1983), Muñoz et al., (1980), Mösbach (1992), Ladio et al., (2007), Martínez Crovetto (1980), 1982, Ragonese and Martínez Crovetto (1947), Rapoport et al., (1999), Rapoport and Ladio (1999).

chequén

Luma chequen (Mol.) Kaus = Myrceugenella chequen (Molina) Kausel Myrceugenia exsucca (DC.) O.Berg

Myrceugenella planipes (H. et A.) Berg Myrteola nummularia (Lam.) O. Berg

Contreras Vega (2007), Muñoz et al., (1980), Ladio (2001), Ladio and Rapoport (1999), Martínez Crovetto (1982), Ragonese and Martínez Crovetto (1947), Rapoport et al., (1999), Rapoport and Ladio (1999), Villagran et al., (1983) Contreras Vega (2007), Gusinde (1917), Villagrán et al., (1983), Muñoz et al., (1980)

arrayán, arrayán rojo, palo colorado, palo rojo cuthu, quetri, temu, arama, quitri, kollimamüll, kütri temu, temo, kollimamül, collimamil

Luma apiculata (DC.) Burret =Myrceugenia apiculata (DC) Kaus

Ethnobotanical references

Common names registered

Species

Table 2 (continued)

fresh fruit, sweets, cooked fruits

fresh fruit, dried fruits, sweets

fresh fruits

fresh fruits, dried fruit, chicha, jams, liqueurs, syrups, dessert, nonalcoholic beverages

fresh fruits, cooked fruits, sweets, alcoholic beverage called murtao, chicha

fresh fruits

fresh fruits fresh fruits, dried cooked, te

fresh fruits, dried fruits

fresh fruits

fresh fruit, chicha, spirits, non-alcoholic beverages, sweets, petals and flowers to make tortillas

Edible use

diuretic, vulnerary, urinary and appetizer (leaves and roots)

digestive, diarrhea treatment (leaves), obstetric disorders (leaves, roots)

dermatological desorders, rheumatism (leaves)

fortifying tonic (fruits), anti-inflammatory (stems), diarrhea (flowers), gastrointestinal, digestive, respiratory disorders, asthma, tuberculosis, depurative (leaves), astringent, vulnerary (roots), herpes and ulcers (bark)

Medicinal use and ailments treatment

veterinary

tools (wood), living fence (plant)

Other uses

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Patagonia. Interestingly, a common genetic origin of the different populations was reported. The Selknam, Yamanas and Kawashkar showed less diversity probably due to geographic isolation. The human occupation of the Patagonia implied an exploration and colonization process. This process started during the Pleistocene and early Holocene, evidenced in the archeological sites Monte Verde (14,600 BP) in southern Chile, and several places in the Atlantic Patagonia, including Tres Arroyos 1 (12,600 BP) in Tierra del Fuego (Borrero et al., 2019). Exploration and eventual occupation of new territories involves knowledge on the available food resources. For the early hunter-gatherers, availability of safe and non-toxic food plants required trial and error experience to differentiate the edible species from those that needed a detoxifying process before consumption. Displacements on the mainland does not need navigation technology. However, building rafts or canoes was a requirement to explore and eventually occupy the islands along the Pacific coast of Patagonia. The human occupation of the Araucarian islands, at the Pacific coast, was a process associated with the access to marine and coastal resources and took place much later than the exploration of the mainland (Campbell, 2015). The methods used to obtain information on the paleodiets are the analysis of inclusions in coprolites and the study of plant remains in the archeological sites. Archeobotanical studies carried out in Cerro Casa de Piedra, Argentinean Patagonia, allowed the identification of Empetrum rubrum and Gaultheria mucronata (Ericaceae) remains in coprolites, supporting the ancient use of the species as food plants (Martinez Tosto et al., 2016). This site is from the early and middle Holocene (10,690 to 3480 BP). At present, both E. rubrum and G. mucronata can be found in this site. Archeobotanical rests in western Patagonia showed fruits and seeds of Fragaria chiloensis, Berberis spp. and Ericaceae in sites from 11,000–12,000 BP (Borrero et al., 2019). In the Baño 1 site, from the early Holocene, remains from Rubus sp., Ericaceae and Berberis spp. were found (Borrero et al., 2019). Belmar et al. (2017) reported in archeological sites in Aysen (Chile) seeds from Fragaria chiloensis, Berberis spp., Ericaceae, Rubus spp. and Galium spp., among others. The plant use in Argentinean Patagonia from the early- and midHolocene has been described by studying well preserved material from Cerro Casa de Piedra, Santa Cruz Province (Caruso et al., 2018). The plant samples were obtained from stratigraphic levels corresponding to 9640 to 6150 BP and showed plant remains, human and camelid coprolites. Remains from Empetrum rubrum, Berberis spp., Ribes magellanicum and Gaultheria mucronata were found. These species are still used as food. Two Poaceae were also identified, namely Poa ligularis and Stipa tenuis. Ripe Patagonian fruits can be found from spring to winter. For example, the berries from E. rubrum are available from spring to summer, while some Gaultheria fruits from late summer to winter. The human occupation of the sites was seasonal and related with the fruiting time and availability of resources. Other species found in the coprolites, such as Ephedra sp. stems and Azorella monantha leaves, suggest a probable use as medicine (Martínez Tosto et al., 2016). A hut occupation from the Yamana people (1776–1898), who lived as fisher-hunther-gatherers in the Beagle and Fueguian channels, only showed the presence of phytoliths of Poaceae and the fern Blechnum penna marina (Zurro et al., 2009). This supports the fact that the Yamana diet was mainly based in the gathering of seafood, and less use of inland plant resources. Differences can be found between the western and eastern slopes of the Patagonian Andes When comparing the plant remains of edible fruits, in the drier eastern Andes, Berberis spp., Gaultheria, Empetrum and Ribes were found, while in the western Andes, Fragaria chiloensis, Rubus spp, Berberis spp. and Ericaceae were reported, according with a more humid environment (Caruso et al., 2018).

3.2. Traditional uses of berries in Patagonia The Mapuche from Patagonia were agriculturalists and complemented their food supply harvesting wild fruits and vegetables. The protein and fat was obtained by hunting. One of the best studies regarding the plant uses by the Mapuche living in western Patagonia, is the work by Mösbach, compiled in the first half of the 20th century and published in 1992. According to this author, the gathering of wild food resources by the Mapuche was a relevant activity even in the last century. The main staple from gathering activities was the pehuen seed (Araucaria araucana (Mol.) Koch. In the same area where the pehuen seeds were collected, several Ribes spp., Rubus geoides and Fragaria chiloensis were found in abundance. The fermentation of native fruits to obtain “chicha”, an alcoholic beverage, is a cultural practice reported for the Mapuche in Patagonia. Ethnobotanical aspects of fermented food plants and beverages in Europe has been discussed by Soukand et al. (2015). The occurrence of the most available Patagonian berries in Argentina and Chile is shown in Table 1. The tradicional uses are summarized in Table 2. Twenty eight species were found among the taxa analyzed in our ethnobotanical review (Table 2). We did not include species with a very restricted distribution area or only found in the Valdivian forest, as their use was in most cases only occasional. In Mapuche populations from Argentina and Chile, the consumption of wild fruit was a distinctive manifestation of cultural identity, reflecting the characteristics of the local environment, history, and the cosmology of the people. For the Mapuche people the act of eat is considered as “taking energy” or afutun (in Mapudungun, the Mapuche language) in total balance with nature. Therefore, eating plays both a healing and cosmic role when the fruits are collected with respect and only in the quantities required by the family (Ladio and Molares, 2017). It is common among the Mapuche people to ask the plant for “permission” to collect the fruit. This practice is linked with the idea that all living things are connected with a spirit or “pullu”, which is transferred generously during the act of eating. This cosmovison of the vital relations between the elements of nature and the co-inhabitants is found in all the Patagonian indigenous communities of the region (Rozzi, 2016). All the species included in this review are from sub-Antarctic forests. An exception of this is B. microphylla, whose distribution includes the Patagonian steppe and dry forests of Argentina (Table 1, Fig. 2b). The availability of the species is essential in their traditional use: more abundant species are most frequently used (Ladio et al., 2007; Lozada et al., 2006; Molares and Ladio, 2009a, 2009b, 2014). The most frequently cited taxa analyzed in the literature review were Berberis microphylla, Aristotelia chilensis, Fragaria chiloensis, Ribes magellanicum and Ribes cucullatum (Table 2). In the case of F.chiloensis, R. magellanicum and R. cucullatum, they are commonly found in rural and urban peridomestic areas of the region, mainly associated to roadsides, vacant lots and/or human disturbed landscapes (Damascos et al., 1999). Berberis microphylla and A. chilensis are also very cited in the literature and occur mainly in disturbed forests. Studies about plant gathering have shown that long travel times and large distances are only sustainable in the long term when the search of high cultural value species are involved (Ladio and Lozada, 2000; Estomba et al., 2006). Other studies have shown that rural men, women and children still use wild native berries as food. Literature indicates that women are more responsible in the transmission of knowledge regarding plant use within their family and community (Cardoso et al., 2015). Active teaching and imitation, daily stories and conversations are the main dissemination mechanisms (Lozada et al., 2006; Richeri et al., 2013; Neira Ceballos et al., 2012). In the domestic sphere, women are responsible for reproducing recipes for sweets, desserts and medicinal preparations (Richeri et al., 2013; Molares and Ladio, 2014). Therefore,

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women know the features of tinctorial roots and fruits, for example, of different species of Berberis (Neira Ceballos et al., 2012; Cardoso et al., 2015) (Table 2). Therefore, berries are an important part of the living oral traditions and legends of the region, as well as a relevant aspect of the local biocultural heritage.

1 and 2). The main groups of phenolics (anthocyanins, phenylpropanoids, flavonols, flavones, gallic and ellagic acid derivatives) and iridoids occurring in Patagonian berries are summarized in Fig. 3. 3.4.1. Berberidaceae: the calafates (Berberis spp.) The shrubs and bushes belonging to genus Berberis are characteristic species of the Patagonian landscape. They are known under the common name “calafate” and include. Berberis buxifolia Lam. (Fig. 4a), Berberis darwinii Hook (Fig. 4b) and Berberis microphylla G. Forst (Fig. 4c), the latter considered the most palatable. The sweet and aromatic fruits were gathered since pre-historic times and were very appreciated by the early European settlers in Patagonia. There is a traditional believe that if you eat calafate fruits, you will come back to Patagonia. Most studies on Patagonian Berberis fruits are focused on the antioxidant activity of the berries. Ruiz et al. (2010) investigated the anthocyanins and flavonoids of B. microphylla and associated the antioxidant effect with the different groups of chemical constituents of the samples. The hydroxycinnamic acids (HCAs) occurring in the calafate fruit were identified by HPLC-DAD-ESI-MS/MS (Ruiz et al., 2013b). After isolation, several anthocyanin diglycosides and caffeoylglucaric acids were fully characterized by spectroscopic and spectrometric means (Ruiz et al., 2014a, 2014b). Ramirez et al. (2015) compared the anthocyanins of different fleshy fruits occurring in Chile, including B. microphylla. The alkaloid berberine was detected in B. empetrifolia, B. ilicifolia and B. microphylla fruits by Ruiz et al. (2014b). Coridaline was found ony in B. ilicifolia fruits (Ruiz et al., 2014b). The flavonoids occurring in B. empretrifolia, B. ilicifolia and B. microphylla fruits were described by Ruiz et al. (2014b). The simplest flavonoid pattern was found for B. empretrifolia, containing quercetin derivatives, while B. ilicifolia afforded quercetin and isorhamnetin glycosides. The chemical constituents reported so far from calafate fruits are summarized in Table 3. Due to the interest in the fruit at a regional level, a recent work reported the changes in composition of a calafate extract after oral administration in gerbils. The study by Bustamante et al. (2018) shows the structural changes in the different extract constituents after intake. The pharmacokinetic study allowed to disclose the metabolization of calafate phenolics, detecting metabolites in the gerbil plasma. Agronomical studies on Patagonian Berberis are mainly devoted to cultivation of B. microphylla and a comparison of phenolic contents with antioxidant activity of several geographic locations, sometimes with quantification of selected compounds in the fruits (Mariangel et al., 2013). In a study by Ramirez et al. (2015), the antioxidant capacity of six berries, including B. microphylla samples collected in southern Chile was assesed. Berberis microphylla showed the highest scavenging capacity of the DPPH radical, and high reducing power by means of the FRAP assay. In the same way, Ruiz et al. (2013a) showed that in the TEAC assay the best antioxidant capacity was displayed by B. microphylla samples. The highest ORAC values among 120 Chilean fruit species analyzed were found for B. microphylla fruits (Speisky et al., 2012). In a study by Reyes-Farias et al. (2016) on B. microphylla fruits, authors reported that the main anthocyanins was delphinidin-3-glucoside, followed by malvidin-3-glucoside and petunidin-3-glucoside. In the same study, the authors evaluated the effect of calafate extracts in an inflammatory-insulin resistance cell model.The calafate extract diminished the metalloproteinase-9 (MMP-9) gelatinolytic activity, increased the ratio of reduced glutathione/oxidized glutathione (GSH/ GSSG), prevented the caspase-3 activity induced by conditioned medium and LPS, and improved glucose uptake in mouse pre-adipocytes 3T3-L1.

3.3. Local use of Patagonian berries In our literature review, several ways to consume berries were registered. Most of them corresponded to fresh consumption, followed by the preparation of sweets, fermented beverages (“chicha”, wine or liquors), non-alcoholic beverages (juices and syrups) and dried fuits (Table 2). The preference for species that are easily collected or require short preparation times have been documented for local communities of Patagonia (Ladio and Lozada, 2001). This ethnobotanical information has also revealed the importance of the fresh fruit utilization to maintain unaltered the properties of phytocompounds. In order to reduce losses after harvesting and to get food supplies out of season, sweet preparations (preserves, jams, syrups) were also carried out. Rickman et al. (2007) and Howard et al. (2012) concluded that the effect of processing, cooking and storage of fruit species, do not always involve the loss of active substances. The preparation of fermented beverages of most Patagonian berries is well documented. The use of Aristotelia chilensis (maqui) and Fragaria chiloensis fruits to prepare alcoholic beverages combined with corn (Zea mays) has been described in the Mapuche culture and can be traced back to 1000 and 1300 BP in the Mocha Island, Chile (Godoy-Aguirre, 2018). Our review shows the importance of the “chicha”, a traditional fermented or semi-fermented beverage usually derived from wild fruits (mainly F. chiloensis, G. mucronata and Ribes spp.). It is important to note that at present, “chicha” is mainly prepared using wild apples (Malus spp., an exotic Rosaceae) (Ladio and Lozada, 2001). Martínez Crovetto (1982) highlighted that in the past, the Mapuche saved the ferment, prepared with the fruit crushed with water, in order to keep the inoculum for new preparations. This practice shows the significant biocultural role fruits in the maintenance of traditions of high symbolic value. Wafula et al. (2016) reviewed the effects of fermentation on the nutritional and anti-nutritional compositions of some wild vegetables. The authors concluded that the fermentation process seems to reduce phytate and oxalate contents, thereby making minerals more bioavailable. The consumption of “chicha” by native Amerindians in Chile has been revised by Pardo and Pizarro (2005). The use of native berries for medicinal purposes has been described in the Mapuche medical system as: 1) refreshing for fever (for example, Berberis spp and A. chilensis), 2) stimulant and astringent (A. luma, L. apiculata), 3) useful for treating indigestion and diarrhea (F. chiloensis), 4) depurative (R. magellanicum), etc. (Table 2). In addition, the decoction of leaves and roots of F. chiloensis is also described as obstetric and for veterinary purposes (Table 2). 3.4. Chemical and bioactivity studies on Patagonian berries Chemical studies on the content and composition, as well as bioactive properties, can be ound for most of the Patagonian berries traditionally used as food or medicine. However, we could not find reports on the fruit constituents of Berberis darwinii, B. trigona, Margyricarpus pinnatus, Ribes densiflorum and Rubus radicans, so far. We only found a reference on M. pinnatus on the composition of the essential oil obtained from the fruits in a sample from Colombia. The main constituents were sabinene, limonene and pinocarvone (GarciaRoja et al., 2009). The information found on the native fruits is critically analyzed and both chemistry and bioactivity are linked with the potential health promoting properties of the berries. The material is summarized and described by alphabetical order according to the plant families (Tables

3.4.2. Eleocarpaceae: maqui (Aristotelia chilensis) From all the Patagonian berries, perhaps the most investigated from 9

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Fig. 3. Main groups of phenolics (anthocyanins, phenylpropanoids, flavonols, flavones, gallic and ellagic acid derivatives) and iridoids occurring in Patagonian berries.

the point of view of domestication and production, is Aristotelia chilensis (Vogel et al., 2014). The intense deep-purple colored fruits are depicted in Fig. 4e. The maqui berries became popular when markets were looking for new antioxidant products and expanded to more exotic species. One of the first studies that boosted further work in maqui berries was that reported by Miranda-Rottmann et al. (2002). The authors described the capacity of maqui berries and their juice to inhibit LDL oxidation and to protect human endothelial cells against oxidative stress. Rubilar et al. (2011) described the free radical scavenging activity

and the inhibition of α-glucosidase and α-amylase by maqui crude, aqueous and solvent partition extracts. The IC50 for crude maqui fruit was 47.9 μg/mL for α-glucosidase and 41.5 μg/mL for α-amylase. Acarbose, used as a positive control, presented IC50 values of 247.4 μg/ mL for α-glucosidase and 3.4 μg/mL for α-amylase, respectively (Rubilar et al., 2011). Maqui berry extracts inhibited adipogenesis and accumulation of lipids in 3T3-L1 adipocytes. They also showed anti-inflammatory activity on RAW 264.7 macrophages (Schreckinger et al., 2010). A study on the effect of maqui fruit extract on insulin-resistance using cell 10

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models was published by Reyes-Farias et al. (2016). The authors used murine 3T3-L1 pre-adipocytes and RAW264.7 monocytes to disclose the possible effect of the native fruit extracts (A. chilensis and B. microphylla) on extracellular matrix remodeling and adipogenesis. However, instead of concentrations based on extracts w/w yields, authors used as reference 100 μM total polyphenols content of the extracts. The maqui extract modulated MMP-2 activity, reverted the increase in the expression of MCP-1 after treatment with conditioned media and LPS and partially halted the inactivation of IRS-1 by phosphorylation (Reyes-Farias et al., 2016). Aristotelia chilensis fruit extracts decreased the MMP-9 activity, improved the GSH/GSSG ratio and prevented the increase in caspase-3 activity elicited by the conditioned medium and

LPS (Reyes-Farias et al., 2016). Extracts from maqui fruits showed protective effect in an acute ischemia/reperfusion model in rat heart (Céspedes et al., 2008), modulates the expression of inflammation mediators (Cespedes et al., 2017), cyclooxygenase-2, growth of Caco-2 and HT-29 cancer cells (CéspedesAcuña et al., 2018). A review by Misle et al. (2011) summarized the botanical, agronomical information on the plant mainly based in sources published in Spanish, including local journals and thesis. It also presented data on the bioactivity studies on the plant and some general chemical data. The chemical composition of ripe maqui fruits has been intensively investigated. Céspedes et al. (2010) isolated and identified phenolics

Fig. 4. Patagonian berries. a) Berberis buxifolia; b) B. darwinii c) B. microphylla; d) Aristotelia chilensis; e) Empetrum rubrum; f) Gaultheria phillyreifolia; g) G. tenuifolia; h) G. poeppigii; i) Rubus geoides; j) Ribes magellanicum; k) R. punctatum; l) R. cucullatum; m) Fragaria chiloensis ssp. chiloensis f. chiloensis; n) Fragaria chiloensis ssp. chiloensis f. patagonica. 11

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Fig. 4. (continued)

association of traditional uses with bioactivity, we only include some representative reviews. The possible applications of extracts from maqui fruits as nutraceuticals and antioxidants in food and health products can be followed in patent databases. A review on the antioxidant and nutraeutical potential of maqui fruit extracts using a commercial preparation was published by Watson and Schönlau (2015). Looking for new commercial products, maqui berries have been used to design new liquors, including a beverage prepared under the traditional basque “Patxaran” process from Spain. This beverage is appreciated as appetizer and digestive. The original recipe is made macerating Prunus spinosa berries in 25% aqueous ethanol, sugar and anise seeds are added. Gironés-Vilaplana et al. (2015) developed a similar liquour using maqui berries instead of P. spinose, and described the composition, properties and consumer acceptance of both beverages as similar. As berries were also dried for the winter time, the effect of drying on the content and health beneficial effect of the berries is relevant. A study on the changes in compound classes during the drying process of A. chilensis berries was published by Rodriguez et al. (2016). The authors compared the effect of drying at temperatures between 40 °C and 80 °C on the content of several metabolites and antioxidant activity, showing no significant differences within the assayed temperatures. The compounds that grant the claimed health benefits of maqui berries must withstand the digestion process. Lucas-Gonzalez et al. (2016) submitted to in vitro gastrointestinal digestion lyophilized maqui berries in order to determine the recovery and bioaccesbility indexed,

from aqueous and ethanolic extracts from A. chilensis fruits and compared the antioxidant effect of the different fractions using quercetin, tocopherol and BHT as reference compounds. A bioassay-guided study on the cytoprotective and antioxidant compounds from maqui berry allowed the isolation and full identification of a series of phenolics, including anthocyanins, flavonoids, acetophenone/benzaldehyde derivatives, simple phenolics, furfural derivatives and a citric acid derivative (Li et al., 2017). The work by Li et al. (2017) was the first study where the maqui berry constituents were isolated and tested as single constituents in a battery of antioxidant assays. Strong hydroxyl radical scavenging effect was observed and some compounds showed quinone reductase induction effect (Li et al., 2017). In the comparative study carried out by Speisky et al. (2012), maqui berries showed the second best antioxidant activity determined by means of the ORAC assay. Ruiz et al. (2016) reported the HCA and flavonoid composition of the fruit and compared different extraction techniques for the quantification of constituents. The compounds reported in maqui fruits are summarized in Table 4. The anthocyanins from the fruits presented anti-diabetic activity in vivo and in vitro (Rojo et al., 2012). These authors assessed an anthocyanin-rich extract from A. chilensis and the main constituent delphinidin 3-sambubioside-5-glucoside as hypoglycaemic/antidiabetic agents using hyperglycaemic obese mice C57BL/5, as well as rat hepatocytes. The results support the health beneficial effects of the berry and the possible mechanism of action of the maqui anthocyanins. Due to the increasing interest in maqui berries, several reviews have been published in recent years. As the aim of this work is the 12

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Table 3 Constituents reported in Patagonian “calafate” (Berberis) fruits. Compound Anthocyanins Cyanidin-3-glucoside Cyanidin-3-galactoside Cyanidin-3-rutinoside Cyanidin-3-sambubioside Cyanidin 3,5-dihexoside Cyanidin-3,7-β-O-diglucoside Peonidin-3-O-arabinoside Peonidin-3-glucoside Peonidin-3-rutinoside Peonidin-3-O-dihexoside Peonidin 3,5-dihexoside Peonidin-3,7-β-O-diglucoside Dephinidin-3-O-arabinoside Delphinidin pentoside Delphinidin-3-glucoside Delphinidin-3-galactoside Delphinidin-3-rutinoside Delphinidin 3,5-dihexoside Delphinidin 3-rutinoside-5-glucoside Delphinidin-3,7-β-O-diglucoside Petunidin-3-glucoside Petunidin-3-O-galactoside Petunidin-3,5-dihexoside Petunidin-3-rutinoside Petunidin-3,7-β-O-diglucoside Petunidin 3-rutinoside-5-glucoside Petunidin 3-O-(6´´ acetyl) glucoside Malvidin-3-glucoside Malvidin-3-rutinoside Malvidin 3,5-dihexoside Malvidin-3,7-β-O-diglucoside Malvidin 3-rutinoside-5-glucoside Malvidin-3-O-(6´´ coumaroyl)glucoside Malvidin 3-O-(6´´ acetyl) galactoside Flavonoids Kaempferol (K) K-rhamnoside Quercetin (Q) Q-3-O-glucoside (isoquercitrin) Q-3-galactoside Q-3-O-rhamnoside (quercitrin) Q-3-rutinoside Q-3-rutinoside-7-glucoside Q-3-(6″-acetyl)-hexoside 1 Q-3-(6″-acetyl)-hexoside 2 Q-3-malonyl galactoside Q-3-malonyl glucoside Irh-3-O-glucoside Irh-3-galactoside Irh-3-rutinoside Irh-3-rutinoside-7-glucoside Irh-3-(6″-acetyl)-hexoside Irh-3-malonyl galactoside Irh-3-malonyl glucoside Myricetin (My) My-3-O-glucoside My-3-rutinoside My-3-rutinoside-7-glucoside Phenylpropanoids Caffeic acid Coumaric acid Ferulic acid Caffeoylquinic acid derivatives Caffeoylquinic acid isomer 1-3 cis-4-O caffeoylquinic acid 5-O-caffeoylquinic acid cis-5-O-caffeoylquinic acid 4-O-caffeoylquinic acid Dicaffeoylglucaric acid isomer 1-2 3,5-dicaffeoylquinic acid 4,5-dicaffeoylquinic acid Dicaffeoylquinic acid

B. empetrifolia

B. ilicifolia

B. microphylla

Ruiz et al. (2013b)

Ruiz et al. (2013b)

Ruiz et al. (2010);

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Ruiz et al. (2010);

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Ruiz et al., 201b3

Ruiz et al. (2014b) Ruiz et al. (2014b)

Ruiz et al. (2014b) Ruiz et al. (2014b)

Ruiz et al. (2014b)

Ruiz et al. (2014b)

Ruiz et al. (2014b) Ruiz et al. (2014b)

Ruiz et al. (2010) Ruiz et al. (2014a) Ramirez et al. (2015) Ruiz et al. (2010) Ruiz et al. (2010); Ramirez et al. (2015) Ruiz et al. (2010) Ruiz et al. (2014a) Ramirez et al. (2015) Ruiz et al. (2010); Ramirez et al. (2015) Ramirez et al. (2015) Ruiz et al. (2010) Ruiz et al. (2010) Ruiz et al. (2010) Ruiz et al. (2014a) Ruiz et al. (2010) Ramirez et al. (2015) Ruiz et al. (2010) Ruiz et al. (2010); Ramirez et al. (2015) Ruiz et al. (2014a) Ruiz et al. (2010) Ramirez et al. (2015) Ruiz et al. (2010); Ramirez et al. (2015) Ruiz et al. (2010) Ruiz et al. (2010) Ruiz et al. (2014a) Ruiz et al. (2010) Ramirez et al. (2015) Ramirez et al. (2015) Ruiz et al. (2014b); Mariangel et al. (2013) Ruiz et al. (2014b) Mariangel et al. (2013) Ruiz et al., (2010); Ruiz et al. (2014b) Ruiz et al., (2010); Ruiz et al. (2014b) Ruiz et al., (2010); Ruiz et al. (2014b) Ruiz et al., (2010); Ruiz et al. (2014b); Mariangel et al. (2013) Ruiz et al. (2010) Ruiz et al. (2010) Ruiz et al. (2010) Ruiz et al. (2014b) Ruiz et al. (2014b) Ruiz et al., (2010); Ruiz et al. (2014b) Ruiz et al., (2010); Ruiz et al. (2014b) Ruiz et al., (2010); Ruiz et al. (2014b) Ruiz et al. (2010) Ruiz et al. (2010) Ruiz et al. (2014b) Ruiz et al. (2014b) Mariangel et al. (2013) Ruiz et al., (2010); Ruiz et al. (2014b) Ruiz et al., (2010); Ruiz et al. (2014b) Ruiz et al. (2010) Mariangel et al. (2013) Mariangel et al. (2013) Mariangel et al. (2013) Ruiz Ruiz Ruiz Ruiz Ruiz Ruiz Ruiz Ruiz Ruiz

et et et et et et et et et

al. al. al. al. al. al. al. al. al.

(2013b) (2013b) (2013b) (2013b) (2013b) (2013b) (2013b) (2013b) (2013b)

(continued on next page) 13

Journal of Ethnopharmacology 241 (2019) 111979

G. Schmeda-Hirschmann, et al.

Table 3 (continued) Compound Caffeoylglucaric acid isomer 1-4 3-O-trans-caffeoyl glucaric acid 4-O-trans-caffeoyl glucaric acid 5-O-trans-caffeoyl glucaric acid p-coumaroylquinic acid Feruloylquinic acid isomer 1-2 Feruloylcaffeoylquinic acid Chorogenic acid Gallic acid Alkaloids Berberine Corydaline

B. empetrifolia

B. ilicifolia

B. microphylla Ruiz et al. (2013b) Ruiz et al. (2014a) Ruiz et al. (2014a) Ruiz et al. (2014a) Ruiz et al. (2013b) Ruiz et al. (2013b) Ruiz et al. (2013b) Mariangel et al. (2013) Mariangel et al. (2013)

Ruiz et al. (2014b)

Ruiz et al. (2014b) Ruiz et al. (2014b)

Ruiz et al. (2014b)

Table 4 Constituentes reported in “maqui” (Aristotelia chilensis) berries. Compound Anthocyanins Cyanidin Cyanidin-3-O-glucoside Cyanidin 3,5-diglucoside Cyanidin-3-O-sambubioside Cyanidin-3-sambubioside-5-glucoside Delphinidin-3-O-glucoside Delphinidin 3-O-,5-O-diglucoside Delphinidin 3-O-sambubioside Delphinidin 3-O-sambubioside-5-O-glucoside Flavonoids Kaempferol hexoside Quercetin (Q) 3,5-dimethoxyquercetin (Caryatin) Q-3-O-arabinofuranoside Q-3-O-xylopyranoside Q-3-O-rhamnoside Q-3-O-glucoside Q-3-O-galactoside Q-3-O-rutinoside (rutin) Q-6″-O-hexosyl-C-hexoside Q-galloyl glucoside Q-galloyl galactoside Myricetin (My) My pentoside My-glucoside My-galactoside My-rutinoside My-6″-O-hexosyl-C-hexoside My-galloyl hexoside Catechin Epicatechin Procyanidin B-9 Procyanidin trimers Procyanidin tetramers Phenolics 2-O-β-D-glucopyranosyl-4,6-dihydroxybenzaldehyde 4,6-dihydroxy-2-O-(β-D-glucopyranosyl) acetophenone Gallic acid Gallic acid methyl ester 5-Galloylquinic acid p-hydroxybenzoic acid Protocatechuic acid Protocatechuic acid 4-glucoside Protocatechuic acid methyl ester Gentisic acid Sinapic acid p-coumaric acid Ferulic acid Ellagic acid Other compounds Hydroxymethylfurfural Acetyloxymethylfurfural 1,5-dimethyl citrate

Reference Cespedes et al. (2010) Ruiz et al. (2010); Cespedes et al. (2010); Genskowsky et al. (2016); Brauch et al. (2017); Li et al. (2017) Ruiz et al. (2010); Genskowsky et al. (2016); Brauch et al. (2017) Ruiz et al. (2010); Cespedes et al. (2010); Genskowsky et al. (2016); Brauch et al. (2017); Li et al. (2017) Ruiz et al. (2010); Genskowsky et al. (2016); Brauch et al. (2017) Ruiz et al. (2010); Cespedes et al. (2010); Genskowsky et al. (2016); Brauch et al. (2017); Li et al. (2017) Ruiz et al. (2010); Céspedes et al., 2010; Genskowsky et al. (2016); Brauch et al. (2017) Ruiz et al. (2010); Céspedes et al., 2010; Genskowsky et al. (2016); Brauch et al. (2017) Ruiz et al. (2010); Céspedes et al., 2010; Genskowsky et al. (2016); Brauch et al. (2017) Ruiz et al. (2016) Céspedes et al., 2010; Genskowsky et al. (2016); Ruiz et al. (2016) Genskowsky et al. (2016); Li et al. (2017) Li et al. (2017); Ruiz et al., 2016* Li et al. (2017); Ruiz et al., 2016* Ruiz et al. (2016) Genskowsky et al. (2016); Ruiz et al. (2016) Genskowsky et al. (2016); Ruiz et al. (2016); Li et al. (2017) Céspedes et al., 2010; Genskowsky et al. (2016);; Ruiz et al. (2016) Ruiz et al. (2016) Genskowsky et al. (2016); Ruiz et al. (2016) Genskowsky et al. (2016); Ruiz et al. (2016) Céspedes et al., 2010; Genskowsky et al. (2016) Ruiz et al. (2016) Genskowsky et al. (2016); Ruiz et al. (2016) Genskowsky et al. (2016); Ruiz et al. (2016) Ruiz et al. (2016) Ruiz et al. (2016) Ruiz et al. (2016) Céspedes et al., 2010 Céspedes et al., 2010 Céspedes et al., 2010 Céspedes et al., 2010 Céspedes et al., 2010 Li et al. (2017) Li et al. (2017) Céspedes et al., 2010; Li et al. (2017) Li et al. (2017) Ruiz et al. (2016) Céspedes et al., 2010 Li et al. (2017) Ruiz et al. (2016) Li et al. (2017) Céspedes et al., 2010 Céspedes et al., 2010 Céspedes et al., 2010 Céspedes et al., 2010 Genskowsky et al. (2016) Li et al. (2017) Li et al. (2017) Li et al. (2017)

*as pentoside. 14

Delphinidin arabinoside* Delphinidin 3-galactoside* Api rhamnoside Api glucuronide K pentoside K rhamnoside Q arabinoside*, ** Q-pentoside 1 Q-pentoside 2 Q hexoside 1 Q hexoside 2 Q-3-galactoside Q-3-O-rhamnose (quercitrin) Q-3-glucuronide Q-xylopentoside Q rutinoside*,** Q IRh rhamnoside Myr-pentoside 1 Myr-pentoside 2 Myr pentoside 3 Myr-hexoside 1 Myr rhamnoside Myr glucuronide 5-p-coumaroylquinic acid Caffeoyl hexoside derivative 3-caffeoylquinic acid 5-caffeoylquinic acid Caffeoylquinic acid 2 Caffeoylshikimic acid Dihydroxy benzoic acid hexoside Sinapic acid hexoside Sinapic acid hexoside derivative Procyanidin A-type trimer Procyanidin B-type dimer 1 Procyanidin B-type dimer 2 Procyanidin B-type trimer p-coumaroyl monotropein isomer 1

Cyanidin hexoside 2 Cyanidin-3-lathyroside Cyanidin dipentoside Cyanidin di-hexoside Delphinidin pentoside

15 Ruiz et al. (2015)

Ruiz et al. (2015)

Ruiz et al. (2015) Ruiz et al. (2015)

Ruiz et al. (2015) Ruiz et al. (2015)

Ruiz et al. (2015) Ruiz et al. (2015)

Ruiz et al. (2013a); Ruiz et al. (2015)

Ruiz et al. (2013a); Ruiz et al. (2015)

Ruiz et al. (2013a) Ruiz et al. (2013a); Ruiz et al. (2015)

Ruiz et al. (2013a) Ruiz et al. (2015)

Ruiz et al. (2015) Ruiz et al. (2015) Ruiz et al. (2015)

Ruiz et al. (2015) Ruiz et al. (2015) Ruiz et al. (2015)

Ruiz et al. (2013a)

Ruiz et al. (2013a); Ruiz et al. (2015)

Ruiz et al. (2013a) Ruiz et al. (2013a)

Ruiz et al. (2013a); Ruiz et al. (2015)

Ruiz et al. (2013a); Ruiz et al. (2015)

pentoside arabinoside*,** 3-glucoside 3-galactoside*

Cyanidin Cyanidin Cyanidin Cyanidin

G. mucronata

G. antarctica

Compound

Table 5 Constituents reported in Patagonian “chaura” (Gaultheria) fruits.

Mieres-Castro et al. (2019) Mieres-Castro et al. (2019)

al. al. al. al. al. al. al. al. al.

(2019) (2019) (2019) (2019) (2019) (2019) (2019) (2019) (2019)

et et et et et et et et et

al. al. al. al. al. al. al. al. al.

(2019) (2019) (2019) (2019) (2019) (2019) (2019) (2019) (2019)

(continued on next page)

Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro

(2019) (2019) (2019) (2019) (2019) (2019) (2019) (2019) (2019) (2019) (2019) (2019) et et et et et et et et et

al. al. al. al. al. al. al. al. al. al. al. al. Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro

et et et et et et et et et et et et

Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro

(2019) (2019) (2019) (2019) (2019) (2019) (2019) (2019) (2019) (2019) (2019) (2019) (2019)

et et et et et et et et et et et et et

Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro

al. al. al. al. al. al. al. al. al. al. al. al. al.

Mieres-Castro et al. (2019) Mieres-Castro et al. (2019)

Mieres-Castro et al. (2019) Mieres-Castro et al. (2019)

Mieres-Castro et al. (2019)

Mieres-Castro et al. (2019) Mieres-Castro et al. (2019)

(2019) (2019) (2019) (2019) (2019) (2019) (2019) (2019)

Mieres-Castro et al. (2019) Mieres-Castro et al. (2019) Mieres-Castro et al. (2019)

al. al. al. al. al. al. al. al.

Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro

Mieres-Castro et al. (2019) Mieres-Castro et al. (2019)

Mieres-Castro et al. (2019) et et et et et et et et

Mieres-Castro et al. (2019)

Mieres-Castro et al. (2019) Mieres-Castro et al. (2019)

Mieres-Castro et al. (2019)

G. poeppigii

Mieres-Castro et al. (2019) Mieres-Castro et al. (2019)

G. phillyreifolia

G. Schmeda-Hirschmann, et al.

Journal of Ethnopharmacology 241 (2019) 111979

Journal of Ethnopharmacology 241 (2019) 111979

G. Schmeda-Hirschmann, et al.

Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro Mieres-Castro

et et et et et et et et

3.4.3. Ericaceae: the chauras (Gaultheria spp.) and the uvilla (Empetrum rubrum) The most abundant edible Ericaceae species in Patagonia comprise the small Empetrum and Gaultheria fruits (Fig. 4f, g, h and i). They are more frequent in the Andean slopes and in the humid forests of southern Patagonia and Tierra del Fuego. Regarding Empetrum species, the main Patagonian representative is E. rubrum. However, no information about content and composition of secondary metabolites or bioactivity can be found in literature so far. In contrast, different studies have been published on the crowberry Empetrum nigrum L. In a work on four different populations of E. nigrum from Finland, Koskela et al. (2010) described the anthocyanins of the different accessions and showed large variations in the content and composition. The anthocyanins reported for the European accessions included delphinidin, cyanidin, petunidin, peonidin and malvidin hexosides and pentosides (Koskela et al., 2010). Park et al. (2012) studied the phenolics of Empetrum nigrum var. japonicum K. Koch collected in the Jeju Island (Korea). The investigation was carried out with the fruits and leaves. Quercetin and kaempferol were identified as main flavonoid aglycones. The extract showed antioxidant effect and protected cow pulmonary artery endothelial cells against H2O2-oxidative challenge. Wild berries are part of the diet for Native Americans in Alaska. Looking for possible anti-obesity agents and effects on diabetes of Arctic berries, Kellogg et al. (2010) studied the phenolic-enriched extracts (PEE) of Alaskan berries. The PEEs were further partitioned into anthocyanin-enriched and proanthocyanidin-enriched extracts. The procyanidins for E. nigrum included different dimers, trimers and a tetramer based on (epi)catechin and (epi)gallocatechin moieties. The PEE reduced lipid accumulation in 3T3-L1 adipocytes and showed hypoglycaemic effect in vivo in the acute T2DM model. Ogawa et al. (2008) described 13 anthocyanins from Japanese crowberry. The main compounds were cyanidin, delphinidin and peonidin monoglycosides occurring in other samples from Alaska and Korean origin. The growing interest in native Patagonian berries can be perceived in the increasing number of studies on the possible domestication of the species producing larger fruits with better taste. Villagra et al. (2014) reported a comparation on the red, pink and white fruits of the Ericaceae Gaultheria pumila, including size, weight, total soluble content,

Api: apigenin; K: kaempferol; Q: quercetin; IRh: isorhamnetin; Myr: Myricetin.

Ruiz et al. (2015) p-coumaroyl monotropein derivative 1 p-coumaroyl monotropein derivative 2 p-coumaroyl dihydromonotropein isomer 1 p-coumaroyl dihydromonotropein isomer 2 Monotropein 10-trans-p-coumarate (Vaccinoside)* Monotropein 10-trans-cinnamate* 6-α-hydroxy-dihydromonotropein-10-trans-cinnamate* Dihydromonotropein cinnamate Coumaroyl iridoid 535

Ruiz et al. (2015)

G. antarctica Compound

Table 5 (continued)

G. mucronata

al. al. al. al. al. al. al. al.

(2019) (2019) (2019) (2019) (2019) (2019) (2019) (2019)

G. poeppigii G. phillyreifolia

et et et et et et et et

al. al. al. al. al. al. al. al.

(2019) (2019) (2019) (2019) (2019) (2019) (2019) (2019)

the stability of phenolics and the changes induced by the simulated digestion in the antioxidant activity of the samples. The authors demonstrated that the total polyphenol content decreased along with the digestion process. This effect was reflected in the loss of antioxidant capacity of the resulting digested extracts. The bioaccesibility index of phenolics and flavonoids was 78 and 14%, respectively. In another study, Viuda-Martos et al. (2018) studied the protective effects of dietary fiber (sodium carboxymethyl cellulose, xanthan gum and guar gum) on the bioaccesibility and stability of polyphenolic compounds from maqui berry submitted to a simulated gastrointestinal digestion. Dietary fiber increased the bioaccesiblity index of phenolic and flavonoids from maqui berries. This suggest that dietary fiber acts stabilizing the polyphenols during the digestion process, providing better bioaccesbility at the end of the digestion. Domestication efforts to turn maqui into a new crop have been carried out mainly in Chile. The identification of anthocyanins in selected clones of Chilean maqui was described by Brauch et al. (2017) in the Luna Nueva and Morena clones. Both clones are part of the 68 clones kept at the Universidad de Talca, Chile, for fruit production and cultivation studies. As the Argentinean maqui populations also present high diversity (Blackhall et al., 2008), there is potential to find new cultivars/clones with enhanced biological effects and differences in the constituents compared with the Chilean populations. Zuñiga et al. (2017) updated the data on this plant with chemical and pharmacological information on the different plant parts, as well as micropropagation studies. Surprisingly, the traditional claims regarding medicinal uses of this berry have been not fully explored.

16

17

Jiménez-Aspee et al. (2016c) Jiménez-Aspee et al., 2016c

Jiménez-Aspee et al. (2016c)

Jiménez-Aspee et al. (2016c) Jiménez-Aspee et al. (2016c)

et et et et et et et Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee

al. al. al. al. al. al. al.

(2016c) (2016c) (2016c) (2016c) (2016c) (2016c) (2016c)

Ruiz et al. (2013a) Ruiz et al. (2013a)

Ruiz et al. (2013a)

Jiménez-Aspee et al. (2016c)

Jiménez-Aspee et al. (2016c) Jiménez-Aspee et al. (2016c) Jiménez-Aspee et al. (2016c)

Jiménez-Aspee et al. (2016c) Jiménez-Aspee et al. (2016c)

et et et et et et et et et et et et et et et

Jiménez-Aspee et al. (2016c) Jiménez-Aspee et al. (2016c)

Jiménez-Aspee et al. (2016c) Jiménez-Aspee et al. (2016c); Ruiz et al. (2013a) Jiménez-Aspee et al. (2016c); Ruiz et al. (2013a)

Jiménez-Aspee et al. (2016c); Ruiz et al. (2013a)

Jiménez-Aspee et al. (2016c) Jiménez-Aspee et al. (2016c); Ruiz et al. (2013a)

Cyanidin pentoside Cyanidin glucoside Cyanidin pentoside hexoside Cyanidin dihexoside 1 Cyanidin dihexoside 2 Cyanidin rutinoside Cyanidin hexoside derivative Cyanidin malonyl hexoside 1 Cyanidin malonyl hexoside 2 Cyanidin hexoside succinate Delphinidin pentoside Delphinidin glucoside Delphinidin rutinoside Delphindin dihexoside Delphinidin malonyl hexoside Petunidin hexoside Petunidin rhamnoside Petunidin malonyl hexoside Pelargonidin rutinoside Peonidin hexoside Peonidin rutinoside Petunidin rutinoside Malvidin rhamnose pentose Malvidin hexoside

Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee

R. cucullatum Compound

Table 6 Anthocyanins in Patagonian Ribes currants fruits.

R. magellanicum

al. al. al. al. al. al. al. al. al. al. al. al. al. al. al.

(2016c) (2016c); (2016c) (2016c) (2016c) (2016c); (2016c) (2016c) (2016c) (2016c) (2016c) (2016c); (2016c); (2016c) (2016c)

Ruiz et al. (2013a)

3.4.4. Grossulariaceae: the Ribes species Fruits from the genus Ribes are widely cultivated and consumed in the northern hemisphere, especially R. rubrum and R. nigrum fruits. This genus is also represented in the southern hemisphere, particularly in the Patagonia. The most abundant species in Chile are R. magellanicum, R. cucullatum, R. punctatum and R. trilobum (Bañados et al., 2002), while less common taxa include R. valdivianum, R. densiflorum, R. integrifolium, R. parviflorum, R. polyantes and R. bicolor. Altough these fruits are not vastly consumed, they are gathered by local communities and eaten fresh, in preserves and jams or liquors. In the last decade, the production of Ribes is growing in Chile. However, the efforts have been mainly focused in the European species R. rubrum and R. nigrum, without considering the native resources (McLeod et al., 2014). The composition of the fruits from Ribes species growing in Patagonia has been described (Ruiz et al., 2013a, 2015; Jiménez-Aspee et al., 2016b, 2016c). The anthocyanins were isolated and fully characterized as cyanidin and delphinidin glucosides and rutinosides (Jiménez-Aspee et al., 2016c). The content and composition were similar to those of the European species, with the exception of remarkable high amounts of anthocyanins found in Ribes cucullatum. In addition, the main compound present in R. magellanicum and R. punctatum was isolated and identified as 3-caffeoylquinic acid (Jiménez-Aspee et al., 2016c). Minor components included additional hydroxycinnamic acids and flavonols (Ruiz et al., 2015). The full composition of polyphenols found in these fruits is shown in Tables 6 and 7. Regarding the bioactivity, several reports showed the potential of these currants as functional foods. The antioxidant activity of the polyphenol-enriched extracts has been evaluated by different methodologies, including the DPPH, FRAP, TEAC, CUPRAC, scavenging of superoxide anion and ORAC assays (Jiménez-Aspee et al., 2016b, 2016c; Burgos-Edwards et al., 2017). In a comparative study, the Argentinean collections showed higher antioxidant capacities compared to the Chilean samples (Jiménez-Aspee et al., 2016b). In a study with four Ribes species, the highest antioxidant activity was displayed by R. magellanicum, followed by R. cucullatum (Jiménez-Aspee et al., 2016c). In the ORAC-fluorescein assay, the Ribes magellanicum extract showed values comparable to those of Rubus geoides (Ávila et al., 2017). In the study of Jiménez-Aspee et al. (2016c), the authors fractionated the polyphenol-enriched extract into anthocyanins and non-anthocyanin copigment fractions, and evaluated their cytoprotective activity in gastric epithelial AGS cells. The pre-incubation of AGS cells with the copigment fraction from Ribes punctatum showed the best protective activity towards the H2O2 and MGO-induced stress. On the other hand, only the anthocyanins from R. cucullatum showed significant cytoprotection against MGO. Ávila et al. (2017) demonstrated that the cytoprotective effect from Ribes fruit extracts was associated

Jiménez-Aspee et al. (2016c) Jiménez-Aspee et al. (2016c)

R. punctatum

R. trilobum

anthocyanin and pectin in the fruits. However, the identity of the constituents remains to be established. The content and composition of anthocyanins, flavonoids and phenylpropanoids of Gaultheria antarctica and G. mucronata fruits has been described by Ruiz et al. (2013a) and Ruiz et al. (2015), including a coumaroyl iridoid from both species. A recent article describes the constituents of G. phyllireifolia and G. poeppigii fruits (Mieres-Castro et al., 2019). The compounds reported so far are presented in Table 5. The authors fractionated by membrane chromatography the polyphenol-enriched extracts into anthocyanins and copigments for further isolation of main constituents. The anthocyanins were identified as cyanidin and delphinidin arabinosides and galactosides, while in the copigment fraction several flavonoids based on quercetin were identified. The isolation the iridoids monotropein10-trans-cinnamate, monotropein-10-trans-coumarate and 6α-hydroxydihydromonotropein-10-trans-cinnamate was achieved using countercurrent chromatography. Compounds were quantified showing remarkable high levels of iridoids. In addition, the PEEs and fractions showed high antioxidant capacity by means of the DPPH, FRAP, TEAC and ORAC assays (Mieres-Castro et al., 2019).

Jiménez-Aspee et al. (2016c) Jiménez-Aspee et al. (2016c) Jiménez-Aspee et al. (2016c)

Journal of Ethnopharmacology 241 (2019) 111979

G. Schmeda-Hirschmann, et al.

b

18

Q-3-O-glucoside (isoquercitrin) Q hexoside *as galactoside Q dihexoside Q rutinoside Q-3-rhamnoside-7-glucoside Q rutinoside (rutin) Q dihexoside rhamnoside Q-pentoside-rutinoside Q-acetylglucoside Isorhamnetin hexoside Isorhamnetin rhamnoside Myr pentoside Myr rhamnoside * as 3-OMyr hexoside

Q rhamnoside Q hexoside

Coumaric acid acetyldeoxy hexoside Synapoyl hexoside Flavonoids Api pentoside Api hexoside K rhamnoside K hexoside K hexoside K rutinoside K hexoside malonate K-acetylhexoside Q pentoside

5-p-coumaroylquinic acidb

3-p-coumaroylquinic acid

5-O-feruloylquinic acidb

3-O-feruloylquinic acidb

4-O-caffeoylquinic acidb

Caffeoyl hexoside 4 3-Caffeoylquinic acid

Caffeoyl hexoside 2 Caffeoyl hexoside 3

Caffeoyl hexoside 1 3-O-caffeoylquinic acida

Caffeoylquinic acid

Compound

(2016c);

(2016c)

(2016c);

(2016c);

(2016c);

*Ruiz et al. (2015) Jiménez-Aspee et al. (2016c); Ruiz et al. (2015)

Ruiz et al. (2015) Jiménez-Aspee et al. (2016c); Ruiz et al. (2015) Jiménez-Aspee et al. (2016c) Ruiz et al. (2015)

Jiménez-Aspee et al. (2016c); Ruiz et al. (2015) Ruiz et al. (2015) Jiménez-Aspee et al. (2016c); * Ruiz et al. (2015)

Jiménez-Aspee et al. (2016c); Ruiz et al. (2015)

Jiménez-Aspee et al. (2016c) Jiménez-Aspee et al. (2016c); Ruiz et al. (2015) Jiménez-Aspee et al. (2016c)

Ruiz et al. (2015)

Jiménez-Aspee et al. Ruiz et al. (2015) Jiménez-Aspee et al. Ruiz et al. (2015) Jiménez-Aspee et al. Ruiz et al. (2015) Jiménez-Aspee et al. Ruiz et al. (2015) Jiménez-Aspee et al. Ruiz et al. (2015) Ruiz et al. (2015)

Jiménez-Aspee et al. (2016c) Ruiz et al. (2015) Jiménez-Aspee et al. (2016c) Jiménez-Aspee et al. (2016c) Ruiz et al. (2015)

R. cucullatum

Table 7 Flavonols and hydroxycinnamic acids in Patagonian currants (Ribes spp.).

(2016c) (2016c)

(2016c) (2016c)

(2016c)

(2016c);

(2016c) (2016c) (2016c); Ruiz et al. (2015) (2016c)

Ruiz et al. (2015) Ruiz et al. (2015) Jiménez-Aspee et al. Jiménez-Aspee et al. Jiménez-Aspee et al. Jiménez-Aspee et al. Jiménez-Aspee et al.

(2016c) (2016c) (2016c) (2016c) (2016c); Ruiz et al. (2015)

Jiménez-Aspee et al. (2016c) Jiménez-Aspee et al. (2016c) Ruiz et al. (2015) Jiménez-Aspee et al. (2016c); Ruiz et al. (2015)

Jiménez-Aspee et al. (2016c) Jiménez-Aspee et al. (2016c); Ruiz et al. (2015) Ruiz et al. (2015) Jiménez-Aspee et al. (2016c); * Ruiz et al. (2015)

Jiménez-Aspee et al. Jiménez-Aspee et al. Jiménez-Aspee et al. Jiménez-Aspee et al. Ruiz et al. (2015) Jiménez-Aspee et al.

Jiménez-Aspee et al. (2016c)

Jiménez-Aspee et al. (2016c)

Jiménez-Aspee et al. (2016c); Ruiz et al. (2015) Jiménez-Aspee et al. (2016c); Ruiz et al. (2015)

Jiménez-Aspee et al. (2016c); Ruiz et al. (2015) Jiménez-Aspee et al. (2016c); Ruiz et al. (2015) Jiménez-Aspee et al. (2016c); Ruiz et al. (2015) Ruiz et al. (2015)

Jiménez-Aspee et al. Ruiz et al. (2015) Jiménez-Aspee et al. Jiménez-Aspee et al. Ruiz et al. (2015) Jiménez-Aspee et al. Jiménez-Aspee et al. Ruiz et al. (2015)

R. magellanicum

et et et et et

al. al. al. al. al.

(2016c) (2016c) (2016c) (2016c) (2016c)

Jiménez-Aspee et al. (2016c) Jiménez-Aspee et al. (2016c) Jiménez-Aspee et al. (2016c)

Jiménez-Aspee et al. (2016c) Jiménez-Aspee et al. (2016c)

Jiménez-Aspee et al. (2016c) Jiménez-Aspee et al. (2016c)

Jiménez-Aspee et al. (2016c)

Jiménez-Aspee et al. (2016c) Jiménez-Aspee et al. (2016c)

Jiménez-Aspee et al. (2016c)

Jiménez-Aspee et al. (2016c)

Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee

Jiménez-Aspee et al. (2016c)

Jiménez-Aspee et al. (2016c)

Jiménez-Aspee et al. (2016c)

Jiménez-Aspee et al. (2016c)

Jiménez-Aspee et al. (2016c) Jiménez-Aspee et al. (2016c)

Jiménez-Aspee et al. (2016c) Jiménez-Aspee et al. (2016c)

Jiménez-Aspee et al. (2016c) Jiménez-Aspee et al. (2016c)

R. punctatum

et et et et

al. al. al. al.

(2016c) (2016c) (2016c) (2016c)

(continued on next page)

Jiménez-Aspee et al. (2016c) Jiménez-Aspee et al. (2016c)

Jiménez-Aspee et al. (2016c)

Jiménez-Aspee et al. (2016c) Jiménez-Aspee et al. (2016c)

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Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee

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Jiménez-Aspee et al. (2016c) Jiménez-Aspee et al. (2016c)

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Jiménez-Aspee et al. (2016c)

R. trilobum

G. Schmeda-Hirschmann, et al.

Journal of Ethnopharmacology 241 (2019) 111979

Journal of Ethnopharmacology 241 (2019) 111979

Jiménez-Aspee et al. (2016c) Jiménez-Aspee et al. (2016c) Jiménez-Aspee et al. (2016c) Jiménez-Aspee et al. (2016c) Ruiz et al. (2015)

Jiménez-Aspee et al. (2016c) Jiménez-Aspee et al. (2016c)

Jiménez-Aspee et al. (2016c); Ruiz et al. (2015)

Jiménez-Aspee et al. (2016c)

Myr rutinoside Myr hexoside acetate Catechin/Epicatechin hexoside (epi)Catechin-(epi)Catechin Procyanidin B

R. trilobum R. punctatum R. magellanicum R. cucullatum Compound

Table 7 (continued)

G. Schmeda-Hirschmann, et al.

with the activation of intracellular antioxidant defense mechanisms rather than a direct free radical scavenging effect. Theoduloz et al. (2018) reported that the activity of the antioxidant enzymes catalase, superoxide dismutase, glutathione-peroxidase and reductase was induced by the polyphenol-, anthocyanin- and copigment-extracts from Ribes fruits. In the last decade, the use of simulated gastrointestinal models has become a valuable tool to get a first insight into the changes in bioactivity and composition of food extracts when submitted to the digestion process. This approach was successfully carried out by Burgos-Edwards et al. (2017), demonstrating that simulated digestion induced a decrease in the total phenolic and flavonoid content, which was related to a partial loss of the antioxidant activity. Interestingly, the inhibitory activity against metabolic syndrome-associated enzymes partially withstands the gastrointestinal digestion. Despite the changes in bioactivity after the simulated digestion, the inhibitory activity of the polyphenols against α-glucosidase was maintained. In addition, BurgosEdwards et al. (2018) showed that the colonic microbiota from human donors also induced changes in the polyphenolic profile and bioactivity of the fruits from Ribes magellanicum and R. punctatum. Regardless of these modifications, the colonic derived-metabolites were active inhibitors of α-glucosidase, suggesting that fermented polyphenols from both species might help in the prevention of postprandial hyperglycaemia when reaching the small gut after enterohepatic recirculation (Espín et al., 2017). Hence, Patagonian Ribes may be considered as a functional food. However, further in vivo experiments will be needed to confirm these effects. 3.4.5. Myrtaceae fruits The fruits of several myrtaceae are abundant food sources in summer times and in early autumn. They include Amomyrtus luma, Luma apiculata (syn.: Myrceugenella apiculata), Luma chequen and Myrceugenella planipes. The murta berries (Ugni molinae and to a less extent, Ugni candollei), are still highly appreciated. The fruits of A. luma and U. molinae were also fermented into “chicha”. As a result of the interaction with the European settlers and the introduction of alcoholcontaining beverages, the aromatic fruits of A. luma, L. apiculata and U. molinae were macerated into alcohol to obtain liquors. Most chemical and pharmacological studies of Myrtaceae berries have been performed on Luma apiculata, L. chequen and Ugni molinae, in agreement with the larger geographic distribution and tradition of use. The phenolic composition of L. apiculata and L. chequen fruits collected in Chile was described by Simirgiotis et al. (2013) (Table 8). Both extracts presented antioxidant activity in agreement with the high phenolic content and the chemical identity of the fruit constituents. Fuentes et al. (2016) investigated the changes during fruit ripening and also evaluated the polyphenolic content and antioxidant activity of L. apiculata fruit extracts. The methanol extract of the fruit was tested on rat thoracic aorta rings to assess the effect on endothelium-dependent vasodilation under high glucose-induced damage. The L. apiculata fruit extract induced relaxation of precontracted aortic rings reducing the effect elicited by high glucose. The effect was dose-dependant at concentrations of 0.1, 1.0 and 10 mg/mL (Fuentes et al., 2016). The authors identified rutin (Q-3-rutinoside) and anthocyanins (petunidin, peonidin and malvidin glycosides) in the extract. The hypotensive effect of Ugni molinae fruit extracts was determined using the rat aortic ring model including both endothelium-intact and endothelium-removed aortic rings. The extract concentration was expressed as μg GAE/mL and not as mg extract/mL, making it difficult to compare the results with those from other species (Jofré et al., 2016). A dose-response hypotensive effect was observed in rings with intact endothelium, allowing the study of possible mechanisms of action. Jofré et al. (2016) established the vasodilation effect of the extract using selective inibitors of SK (K+/Ca2+) channels of low and high conductance, inhibitors of iNOS and eNOS, and NO-competitive inhibitors of guanylate cyclase. The ED50 of the extract was 1.69 μg GAE/ 19

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Table 8 Constituents reported in Mytaceae fruits: “arrayán” (Luma apiculata), “chequén” (Luma chequen), “huarapo” (Myrteola nummularia) and “murta” (Ugni molinae). Compound Pelargonidin 3-O-arabioside Cyanidin-3-O-arabinoside Cyanidin-3-O-glucoside Cyanidin-3-O- galactoside Cyanidin-3-O-dihexoside Cyanidin-3-rutinoside Cyanidin-3-O-(6´´ succinoyl)glucoside Peonidin-3-O-arabinoside Peonidin-3-O-glucoside Peonidin 3-O-galactoside Delphinidin-3-O-galactoside Delphinidin-3-O-glucoside Dephinidin-3-O-arabinoside Petunidin 3-O- arabinoside Petunidin-3-O-glucoside Petunidin-3-O-galactoside Petunidin-3-O-rutinoside Malvidin 3-O-arabinoside Malvidin-3-O-glucoside Malvidin-3-O-galactoside Malvidin 3-O-(6´´ acetyl) galactoside Peonidin-malvidin 3-O-glucoside Tannins Gallic acid Galloyl/HHDP hexose (pedunculagin I)

L. apiculata

Fuentes et al. (2016) Ramirez et al. (2015) Fuentes et al. (2016) Ramirez et al. (2015); Fuentes et al. (2016) Fuentes et al. (2016) Ramirez et al. (2015) Fuentes et al. (2016) Fuentes et al. (2016) Ramirez et al. (2015)

Ramirez et al. (2015)

M. nummularia

U.molinae

Ruiz et al. (2013a)

Junqueira-Gonçalves et al., 2015 Junqueira-Gonçalves et al., 2015 Ruiz et al. (2010); Junqueira-Gonçalves et al., 2015 Junqueira-Gonçalves et al., 2015

Ramirez et al. (2015)

Ramirez et al. (2015) Ramirez et al. (2015) Ramirez et al. (2015) Ruiz et al. (2010); Ramirez et al. (2015); Junqueira-Gonçalves et al., 2015 Ramirez et al. (2015)

Ruiz et al. (2013a)

Ramirez et al. (2015) Ramirez et al. (2015)

Simirgiotis et al., (2013) (AP)

HHDP-hexose Simirgiotis et al. (2013) Simirgiotis et al., (2013) (Fr, AP)

Unknown gallotannin Galloylquinic acid p-coumaric acid Caffeoylhexoside 1 Caffeoylhexoside 4 Flavonoids Luteolin Luteolin-3-glucoside Kaempferol

Junqueira-Gonçalves et al., 2015

Junqueira-Gonçalves et al., 2015

Simirgiotis (AP) Simirgiotis (AP) Simirgiotis (AP) Simirgiotis

Jofré et al. (2016); Junqueira-Gonçalves et al., 2015

et al., (2013) et al., (2013) et al., (2013) et al. (2013)

Jofré et al. (2016) Simirgiotis et al. (2013) Simirgiotis et al., (2013) (Fr, AP) Simirgiotis et al. (2013)

Ruiz et al. (2015) Ruiz et al. (2015) Ruiz et al. (2015)

K-3-glucoside Quercetin Q-pentoside 1 Q-3-O-ribose Q-3-O-glucoside (isoquercitrin) Q-3-galactoside Q-glucuronide Q-3-O-rhamnose (quercitrin) Q-3-rutinoside (rutin) Q-dirhamnoside Q-3-O-(6″-O-galloyl)-hexose

Simirgiotis et al., (2013) (AP) Simirgiotis et al., (2013) (Fr, AP)

IRh Irh-3-O-(6″-O-galloyl)-hexose Irh-3-O-glucoside Myricetin

Ruiz et al. (2015) Simirgiotis et al., (2013) (AP)

Ruiz et al. (2015)

Simirgiotis et al., (2013) (AP) Fuentes et al. (2016) Simirgiotis et al., (2013) (Fr, AP)

Simirgiotis et al., (2013) (AP)

Junqueira-Gonçalves et al., 2015 Junqueira-Gonçalves et al., 2015 Junqueira-Gonçalves et al., 2015 Ramirez et al. (2015) Ramirez et al. (2015)

Fuentes et al. (2016) Ramirez et al. (2015); Fuentes et al. (2016) Ramirez et al. (2015) Ramirez et al. (2015)

Procyanidin B1

Bis-HHDP hexose Castalagin or vescalagin Catechin Epigallocatechin gallate Furosinin Unknown gallotannin

L. chequen

Simirgiotis (AP) Simirgiotis (AP) Simirgiotis (AP) Simirgiotis (AP)

et al., (2013)

Junqueira-Gonçalves et al., 2015 Junqueira-Goncalves et al., 2015* Junqueira-Gonçalves et al., 2015 Junqueira-Gonçalves et al., 2015 Jofré et al. (2016); Junqueira-Gonçalves et al., 2015 Junqueira-Gonçalves et al., 2015 Jofré et al. (2016); Junqueira-Gonçalves et al., 2015 Jofré et al. (2016); Junqueira-Gonçalves et al., 2015; Shene et al. (2009) Shene et al. (2009) Junqueira-Gonçalves et al., 2015 Junqueira-Gonçalves et al., 2015 Shene et al. (2009)

et al., (2013) et al., (2013) et al., (2013)

My-pentoside 1

Ruiz et al. (2015)

Jofré et al. (2016) Junqueira-Gonçalves et al., 2015

(continued on next page) 20

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Table 8 (continued) Compound

L. apiculata

My-pentoside 2 My-3-O-ribose My-hexoside 1 My-hexoside 2 My-3-O-galactoside (myrcitrin)

Simirgiotis et al., (2013) (Fr, AP)

My-3-O-rhamnoside

Simirgiotis et al., (2013) (Fr, AP)

Laricitrin-(6″-O-galloyl)3-O-hexose

Syringetin-3-O-glucoside Taxifolin pentoside

M. nummularia

Simirgiotis et al., (2013) (AP)

U.molinae

Ruiz et al. (2015)

Simirgiotis et al., (2013) (AP)

Laricitrin-3-O-hexoside

Syringetin

L. chequen

Simirgiotis (AP) Simirgiotis (AP) Simirgiotis (AP) Simirgiotis (AP) Simirgiotis (AP) Simirgiotis (AP)

et al., (2013)

Ruiz et al. (2015) Ruiz et al. (2015)

Shene et al., 2009# Shene et al., 2009#

et al., (2013) et al., (2013) et al., (2013) et al., (2013) et al., (2013) Ruiz et al. (2015)

AP: reported for aerial parts (leaves).* as caffeic acid 3-glucoside; # as glucosides.

mL and the vascular response was associated to the eNOS and guanylate cyclase inhibition. The extract showed no toxicity on HUVEC-C cells up to the highest tested concentration (44 μg GAE/mL) and also presented free radical scavenging activity against ROS. Jofré et al. (2016) reported gallic acid, catechin, quercetin-3-β-D-glucoside, myrcetin, quercetin and kaempferol in the extract of murta investigated for antioxidant and vasodilatation effect in rat aortic rings. The fruits of Ugni molinae were assessed as antioxidants using different assay systems (Rubilar et al., 2011). The crude fruit extract showed inhibitory effect on α-glucosidase with an IC50 of 69.2 μg/mL while the effect on α-amylase was lower, with IC50 > 100 μg/mL. Junqueira-Gonçalves et al. (2015) described antioxidant and antibacterial activity of U. molinae fruit extracts. The antimicrobial effect on E. coli and S. thyphi was carried out using the agar diffusion technique, which is not appropriate. Some 100 μL of the extract obtained from 5 g fresh fruit was reported as “equivalent to the activity of all antibiotics tested” (Junqueira-Gonçalves et al., 2015). However, the antibiotic content in the disks is not informed and the extract volume corresponds to about 20 mg fresh fruit. Overall, the data interpretation is questionable. Shene et al. (2009) compared the antimicrobial effect of EtO:water 1:1 murta fruit extracts with that of gentamicine (10 μg/disk) and penicillin G (10 IU/disk) against S. aureus ATCC 25,923. The authors found similar antimicrobial activity at a concentration/disk equivalent to 18 mg dry fruit/disk. Therefore, the activity (18 mg vs. 10 μg or 10 IU) should be regarded as not relevant as an antimicrobial agent. A recent review on murta summarizes the agronomic, chemical and pharmacological information on this species (López et al., 2018). The interest in murta is growing in Chile and Argentina, and minor scale production in southern Chile is currently carried out. Studies on the effect of different storage methods on the properties and palatability of the berries has been published. The studies include the effect of fruit drying on the bioactivity and functional properties (López et al., 2017), and the bioaccesibility and free radical scavenging effect of the juice extract (Ah-Hen et al., 2018). Further work on murta fruits include studies on the cell wall polysaccharides and pectin extraction (Taboada et al., 2010). In a recent publication, Urquiaga et al. (2017) evaluated the effect of a berry concentrate on the postprandial oxidative stress in healthy human volunteers. The berry concentrate was made by mixing murta, maqui, blackberry, cranberry, blueberry and raspberry. A hamburguer was prepared with 250 g of turkey meat. Volunteers were divided into three meal groups, namely: 1) consuming the turkey burger +500 mL of water; 2) consuming the turkey burger +500 mL of the berry concentrate at 5% w/v; and 3) consuming a turkey burger prepared with 6% of berry concentrate (w/w) + 500 mL of the berry concentrate at

5% w/v. The results showed that meals 2 and 3 decreased the MDA plasma concentration and protein carbonyls, and increased the DPPH antioxidant capacity when compared to meal 1. The decreased posprandial oxidative stress and increased the antioxidant activity in plasma shows he importance of the berry concentrate to halt the oxidative reactions that occur during digestion and thermal processing of the turkey meat. As the study was undertaken with a berry mix, additional work is needed to find out the individual contribution of the constituents. 3.4.6. Rosaceae 3.4.6.1. Fragaria chiloensis. The Chilean strawberry (Fragaria chiloensis) can be found in two botanical forms, namely, the white strawberry (F.chiloensis ssp. chiloensis f. chiloensis) or the red strawberry (F.chiloensis ssp. chiloensis f. patagonica). The colorless fruits can be found growing in Chilean coastal areas, ranging from Maule to Araucania regions, while the red fruits are usually found in the Andean slopes of Chile and the southern Patagonia in Argentina. Both fruits were gathered by native communities due to their sweet taste and pleasant aroma, and are eaten fresh or processed (Schmeda-Hirschmann et al., 2011, 2016). Several studies focused mainly on the physiology of the plant, genetic improvement, pathogen infection and post-harvest management have been compiled in a recent review (Morales-Quintana and Ramos, 2019). In addition, some other studies on the chemical composition and biological activity of the secondary metabolites can be found. The studies included different parts of the plant, with emphasis on the edible pulp. The main difference between white and red fruits is the content of anthocyanins. In the red F. chiloensis ssp. chiloensis f. patagonica collected in Chile, Simirgiotis et al. (2009) described four main anthocyanins, namely: cyanidin-3-O-glucoside, pelargonidin-3-O-glucoside, cyanidin-malonyl-glucoside, pelargonidin-malonyl-glucoside. In the same way, Cheel et al. (2005, 2007) reported that the main anthocyanin in red strawberries were pelargonidin derivatives, followed by cyanidin derivatives; while in the white strawberry (f. chiloensis), only cyanidin derivatives were detected in the achenes of the fruit. The total anthocyanin content of the Chilean collections was higher in the white fruits compared to the achenes from red fruits and the commercial variety F.x ananassa cv. Chandler. On the other hand, the white fruit thalamus contained the lowest total anthocyanin content compared to the red fruits. Redarging other polyphenols, ellagic acid and quercetin glucuronide were the main signals in the HPLC-DAD analysis of white fruit strawberry. Other minor compounds including quercetin, isorhamnetin and kaempferol glycosides, ellagitannins and proanthocyanidins have been reported (Simirgiotis and Schmeda-Hirschmann, 21

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Table 9 Anthocyanins and flavonoids reported in the native strawberry Fragaria chiloensis ssp. patagonica (red) and Fragaria chiloensis ssp. chiloensis (white). Anthocyanins

Red

Cyanidin hexoside Cyanidin-3-O-β-D-glucopyranoside Cyanidin-malonyl-glucoside Pelargonidin-3-o glucoside Pelargonidin derivative Pelargonidin-malonyl- glucoside Flavonoids Apigenin hexoside K pentoside K hexoside 1 K hexoside 2 K glucuronide K acetyl hexoside K hexoside pentoside K rhamnoside hexoside K derivative K coumaroyl-hexoside 1 K coumaroyl-hexoside 2 Q Q pentoside 1

Thomas-Valdés et al., 2019 Simirgiotis and Schmeda-Hirschmann, Simirgiotis and Schmeda-Hirschmann, Simirgiotis and Schmeda-Hirschmann, Thomas-Valdés et al., 2019 Simirgiotis and Schmeda-Hirschmann,

Q Q Q Q Q

pentoside 2 pentoside 3 rhamnoside hexoside glucuronide

Q dihexoside Q rutinoside Q acetyl hexoside Q acetyl hexoside Q derivative IRh pentoside IRh rhamnoside IRh glucuronide IRh acetyl hexoside IRh hexoside pentoside DHQ pentoside 1 DHQ pentoside 2 DHQ hexoside pentoside Taxifolin derivative Tryptophan

White 2010 2010 2010

Simirgiotis and Schmeda-Hirschmann, 2010; Cheel et al. (2005) Simirgiotis and Schmeda-Hirschmann, 2010 Simirgiotis and Schmeda-Hirschmann, 2010

2010

Simirgiotis and Schmeda-Hirschmann, 2010

Thomas-Valdés et al., 2019

Thomas-Valdés et al., 2018; Thomas-Valdés et al., 2019 Thomas-Valdés et al., 2018 Thomas-Valdés et al., 2018, Thomas-Valdés et al., 2019 Thomas-Valdes et al., 2019 Simirgiotis and Schmeda-Hirschmann, 2010 Thomas-Valdés et al., 2018 Thomas-Valdés et al., 2018

Thomas-Valdés et al., 2019 Thomas-Valdés et al., 2019 Simirgiotis and Schmeda-Hirschmann, 2010 Thomas-Valdés et al., 2019 Thomas-Valdés et al., 2019 Simirgiotis and Schmeda-Hirschmann, 2010 Simirgiotis and Schmeda-Hirschmann, 2010 Thomas-Valdés et al., 2019, Simirgiotis and SchmedaHirschmann, 2010 Thomas-Valdés et al., 2019 Thomas-Valdés et al., 2019 Thomas-Valdés et al., 2019 Thomas-Valdés et al., 2019, Simirgiotis et al. (2009) Thomas-Valdés et al., 2019

Thomas-Valdés et al., 2018; Schmeda-Hirschmann et al. (2016) Simirgiotis and Schmeda-Hirschmann, 2010 Simirgiotis and Schmeda-Hirschmann, 2010 Thomas-Valdés et al., 2018 Thomas-Valdés et al., 2018, Simirgiotis and Schmeda-Hirschmann, 2010 Thomas-Valdés et al., 2018, Simirgiotis and Schmeda-Hirschmann, 2010 Thomas-Valdés et al., 2018 Thomas-Valdés et al., 2018 Thomas-Valdés et al., 2018, Simirgiotis and Schmeda-Hirschmann, 2010 Thomas-Valdés et al., 2018, Schmeda-Hirschmann et al. (2016); Simirgiotis and Schmeda-Hirschmann, 2010 Thomas-Valdés et al., 2018 Thomas-Valdés et al., 2018 Thomas-Valdés et al., 2018 Schmeda-Hirschmann et al. (2016) Thomas-Valdés et al., 2018 Thomas-Valdés et al., 2018 Thomas-Valdés et al., 2018, Simirgiotis and Schmeda-Hirschmann, 2010 Thomas-Valdés et al., 2018 Thomas-Valdés et al., 2018 Thomas-Valdés et al., 2018 Thomas-Valdés et al., 2018

Thomas-Valdés et al., 2019

Thomas-Valdés et al., 2019 Thomas-Valdés et al., 2019 Thomas-Valdés et al., 2019

Schmeda-Hirschmann et al. (2016) Cheel et al. (2005)

2010; Thomas-Valdés et al., 2018). In the red strawberry, Simirgiotis et al. (2009) described the occurrence of several ellagitannins, ellagic acid glycosides and quercetin/kaempferol glycosides. Cheel et al. (2005) isolated and characterized three E-cinnamic acid glycosides, tryptophan and the anthocyanin cyanidin-3-O-β-D-glucopyranoside from white-fruited strawberries. The three E-cinnamic derivatives were reported in literature for the first time, and they were only present in the thalamus of the fruits. A summary of the identified compounds is depicted in Table 9 (anthocyanins and flavonoids) and Table 10 (tannins). Several studies reported the antioxidant capacity of the fruit extracts from the white and red native strawberries. The assays included DPPH, FRAP, TEAC, CUPRAC, ORAC, the scavenging of the superoxide anion and the inhibition of lipid peroxidation of red blood cells. Cheel et al. (2005) evaluated the crude, EtOAc and Amberlite-retained extracts in three antioxidant assays, namely, DPPH, superoxide anion scavenging and inhibition of lipid peroxidation. Among them, the Amberlite-retained extract showed the best antioxidant capacity in all the methods evaluated. In addition, the isolated compounds were tested in the same assays, showing that ellagic acid and cyanindin-3-O-β-Dglucopyranoside were the most active compounds in the DPPH and superoxide anion scavenging assays, respectively. In the same way, Simirgiotis et al. (2009) reported the antioxidant activity of different fractions obtained from F. chiloensis f. chiloensis, showing that the best antioxidant capacity was associated to the content of quercetin-3-

glucoside, ellagic acid, cyanidin-3-glucoside and pelargonidin-3-glucoside. Cheel et al. (2007) showed that the antioxidant activity of F. chiloensis f. patagonica was due to an additive effect between the polyphenols from thalamus and achenes, while in F. chiloensis f. chiloensis, the achenes showed the highest antioxidant capacity, which was attributed to their high anthocyanin content. In another study, Simirgiotis and Schmeda-Hirschmann (2010) compared the antioxidant activity of fruits, leaves and rhizomes, showing that the white fruits from F. chiloensis f. chiloensis presented the highest scavenging activity against the superoxide anion. The authors associated the composition of polyphenols present in the fruit to this activity, mainly ellagic acid and flavonoids. In a more recent study, the changes in composition and bioactivity of a polyphenol-enriched extract (PEE) from F. chiloensis f. chiloensis (Thomas-Valdés et al., 2018) and F. chiloensis f. patagonica (ThomasValdés et al., 2019) submitted to a simulated gastrointestinal digestion process. The non-digested PEE (ND-PEE), gastric-digested PEE (GDPEE) and intestinal-digested PEE (ID-PEE) were assessed by means of the DPPH, FRAP, TEAC and superoxide anion scavenging assays. The antioxidant capacity was significantly lost by the digestion process, in all the experimental models for both fruit forms. The authors showed that the lost of activity was correlated to the changes in the total phenolic content of the extracts. In addition, the inhibition of α-glucosidase, α-amylase and pancreatic lipase was evaluated. The ND-PEE, GD-PEE and ID-PEE of both fruit forms were strong inhibitors of α22

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Table 10 Tannins reported in the native strawberry Fragaria chiloensis ssp. patagonica (red) and Fragaria chiloensis ssp. chiloensis (white). Compound Protocatechuic acid pentoside Protocatechuic acid hexoside Dihydroferuloyl hexoside 1 Dihydroferuloyl hexoside 2 Sinapinic acid Hydroxybenzoic acid derivative 1-O-E-Cinnamoyl-β-D-xylopyranoside 1-O-E-cinnamoyl-β-D-rhamnopyranoside 1-O-E-cinnamoyl-α-xylofuranosyl-(1→6)-β-D-glucopyranose Caffeoylquinic acid/chlorogenic acid Caffeoylquinic acid/chlorogenic acid Trigalloyl hexose HHDP galloyl hexose 3 Bis-HHDP galloyl hexoside 1 Bis-HHDP galloyl hexoside 2 Bis-HHDP galloyl hexoside 3 Bis HHDP hexoside 1 Bis HHDP hexoside 2 Bis HHDP hexoside 3 HHDP galloyl hexose 1 HHDP galloyl hexose 2 (epi)catechin (Epi)catechin hexoside (epi)C-(epi)C dimer Procyanidin B Procyanidin tetramer 1 Procyanidin tetramer 2 Ellagic acid Ellagic acid pentoside Ellagic acid hexoside Ellagic acid rhamnoside Ellagitannin 1 Ellagitannin 2 Ellagitannin 3 Ellagitannin 4 Ellagitannin 5 Ellagitannin 6 Ellagitannin 7 Ellagitannin 8 Ellagitannin 9 Ellagitannin 10 Ellagitannin 11

Red

Thomas-Valdés Thomas-Valdés Thomas-Valdés Thomas-Valdés Thomas-Valdés Thomas-Valdés Thomas-Valdés Thomas-Valdés Thomas-Valdés Thomas-Valdés

White

et et et et et et et et et et

al., al., al., al., al., al., al., al., al., al.,

Thomas-Valdés et al., 2018 Thomas-Valdés et al., 2018 Thomas-Valdés et al., 2018 Thomas-Valdés et al., 2018 Schmeda-Hirschmann et al. Schmeda-Hirschmann et al. Cheel et al. (2005) Cheel et al. (2005) Cheel et al. (2005) Schmeda-Hirschmann et al. Schmeda-Hirschmann et al. Thomas-Valdés et al., 2018

2019 2019 2019 2019 2019 2019 2019 2019 2019 2019

(2016) (2016)

Thomas-Valdés et al., 2018 Thomas-Valdés et al., 2018 Thomas-Valdés Thomas-Valdés Thomas-Valdés Thomas-Valdés

Thomas-Valdés et al., 2019 Simirgiotis and Schmeda-Hirschmann, 2010 Simirgiotis and Schmeda-Hirschmann, 2010 Simirgiotis and Schmeda-Hirschmann, 2010 Simirgiotis and Schmeda-Hirschmann, 2010 Thomas-Valdés et al., 2019 Simirgiotis and Schmeda-Hirschmann, 2010 Simirgiotis and Schmeda-Hirschmann, 2010 Simirgiotis and Schmeda-Hirschmann, 2010 Simirgiotis and Schmeda-Hirschmann, 2010 Simirgiotis and Schmeda-Hirschmann, 2010 Simirgiotis and Schmeda-Hirschmann, 2010 Simirgiotis and Schmeda-Hirschmann, 2010 Simirgiotis and Schmeda-Hirschmann, 2010 Simirgiotis and Schmeda-Hirschmann, 2010 Simirgiotis and Schmeda-Hirschmann, 2010 Simirgiotis and Schmeda-Hirschmann, 2010

glucosidase, while they prove to be inactive towards α-amylase. Interestingly, the ND-PEE of the white fruits showed a 70% inhibition of pancreatic lipase at 50 μg/mL, while the red fruits inhibited the enzyme by 40% at the same concentration. The activity was slightly reduced after the gastric digestion step, and almost by 90% at the end of the intestinal phase (Thomas-Valdés et al., 2018, 2019). Furthermore, the authors evaluated the cytoprotective effect of the non-digested and digested PEEs of both fruit forms towards the H2O2-induced damage in AGS cells, showing no significant cytoprotection (Thomas-Valdes et al., 2018, 2019).

(2016) (2016)

et et et et

al., al., al., al.,

2018 2018 2018, Simirgiotis and Schmeda-Hirschmann, 2010 2018

Thomas-Valdés et al., 2018

Thomas-Valdés et al., 2018, Simirgiotis and Schmeda-Hirschmann, 2010; Cheel et al. (2005) Schmeda-Hirschmann et al. (2016); Simirgiotis and SchmedaHirschmann, 2010 Thomas-Valdés et al., 2018 Simirgiotis and Schmeda-Hirschmann, 2010 Simirgiotis and Schmeda-Hirschmann, 2010 Simirgiotis and Schmeda-Hirschmann, 2010

Simirgiotis and Schmeda-Hirschmann, 2010 Simirgiotis and Schmeda-Hirschmann, 2010

geoides Sm. (Rosaceae) are highly appreciated for their pleasant aroma, sweet taste and attractive red color. The wild fruits can be found in the Chilean and Argentinean Patagonia, growing in humusrich soils generally associated to Nothofagus species. The chemical composition of this Patagonian fruit was described by Ruiz et al. (2013a, 2015) and Jiménez-Aspee et al. (2016a), who identified flavonol glycosides, tannins and anthocyanins as main components, among other minor compounds (Table 11). The anthocyanins found were monoglycosides and diglycosides of cyanidin, while the flavonol glycosides were derivatives of quercetin, kaempferol and isorhamnetin (Ruiz et al., 2013a; Jiménez-Aspee et al., 2016a). A more diverse profile was observed in the tannin composition, including lambertianin,

3.4.6.2. Rubus geoides. The fruits from the wild raspberry, Rubus 23

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Table 11 Constituents reported in Rubus geoides fruits. Compound

Reference

Anthocyanins Cyanidin 3-hexoside 1 Cyanidin-3-hexoside 2 Cyanidin 3-glucoside Cyanidin 3-hexoside pentoside 1 Cyanidin-3-hexoside pentoside 2 Cyanidin pentosylhexoside Cyanidin-3-dihexoside Cyanidin-3-sambubioside Cyanidin 3-sophoroside Pelargonidin hexoside Pelargonidin pentosylhexoside Flavonols K-hexoside K-pentoside hexoside 1 K- pentoside hexoside 2 Q-3-galactoside Q-hexoside 1 Q hexoside 2 Q-glucuronide Q hexoside acetate Q hexoside pentoside Q dihexoside Q derivative Q IRh hexoside IRh glucuronide

Jiménez-Aspee et al. Jiménez-Aspee et al. Ruiz et al. (2013a) Jiménez-Aspee et al. Jiménez-Aspee et al. Ruiz et al. (2013a) Jiménez-Aspee et al. Ruiz et al. (2013a) Ruiz et al. (2013a) Ruiz et al. (2013a) Ruiz et al. (2013a)

(2016a) (2016a)

Jiménez-Aspee et al. Jiménez-Aspee et al. Jiménez-Aspee et al. Ruiz et al. (2015) Jiménez-Aspee et al. Jiménez-Aspee et al. Jiménez-Aspee et al. Jiménez-Aspee et al. Jiménez-Aspee et al. Ruiz et al. (2015) Jiménez-Aspee et al. Ruiz et al. (2015)

(2016a) (2016a) (2016a)

(2016a) (2016a) (2016a)

(2016a) (2016a) (2016a) (2016a) (2016a) (2016a)

Jiménez-Aspee et al. (2016a) Jiménez-Aspee et al. (2016a)

Galloylquinic acid Caffeoylhexoside 3 Procyanidins Catechin/epicatechin Catechin (epi)Catechin-(epi)catechin Procyanidin B (epi)Afzelechin/(epi)Catechin Procyanidin trimer 1 Procyanidin trimer 2 Procyanidin trimer 3 Procyanidin derivative Hydrolyzable tannins Castalagin/vescalagin Galloyl-bis-HHDP-glucose E−1 Potentillin/casuarictin isomer E−2 HHDP galloyl glucose derivative E−3 Lambertianin C isomer without ellagic acid E−4 HHDP galloyl glucose derivative E−5 HHDP galloyl glucose derivative E−6 Lambertianin C related isomer without ellagic acid E−7 Galloyl-bis-HHDP-glucose 1 E−8 Galloyl-bis-HHDP-glucose 2 E−9 Galloyl-bis-HHDP-glucose 3 E−10 Lambertianin C isomer without ellagic acid E−11 Lambertianin C isomer without ellagic acid E−13 Lambertianin C isomer without ellagic acid E−12 Ellagitannin Ellagic acid

potentillin, casuarictin and different procyanidin derivatives (JiménezAspee et al., 2016a). The antioxidant capacity of the methanolic extract obtained from the fruits was evaluated by means of the TEAC and CUPRAC assays. In the TEAC assay, the results showed a moderate activity compared to Berberis and Ribes species (Ruiz et al., 2013a), while in the CUPRAC assay the results shown by Ruiz et al. (2015) demonstrated that R. geoides had the best antioxidant capacity compared to Ribes and Gaultheria species. In another study, the phenolic-enriched extract obtained from ripe Rubus geoides fruits was compared with that obtained from the commercial species Rubus idaeus. The antioxidant activity of the extracts, determined by the DPPH, FRAP and TEAC assays, was dependant from the collection place, showing the best activity those samples

Ruiz et al. (2015) Ruiz et al. (2015) Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee

et et et et et et et et

al. al. al. al. al. al. al. al.

(2016a) (2016a) (2016a) (2016a) (2016a) (2016a) (2016a) (2016a)

Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee Jiménez-Aspee

et et et et et et et et et et et et et et et et

al. al. al. al. al. al. al. al. al. al. al. al. al. al. al. al.

(2016a) (2016a) (2016a) (2016a) (2016a) (2016a) (2016a) (2016a) (2016a) (2016a) (2016a) (2016a) (2016a) (2016a) (2016a) (2016a)

collected in northern Patagonia (Jiménez-Aspee et al., 2016a). In addition, the polyphenolic enriched extract from R. geoides showed significant cytoprotective activity towards oxidative and dicarbonyl stress induced by hydrogen peroxide and methylglyoxal, respectively. The experiments were carried out in gastric epithelial AGS cells and the results showed a dose-dependent effect. The pre-treatment of AGS cells with the extracts increased the intracellular glutathione content (Jiménez-Aspee et al., 2016a). Moreover, Ávila et al. (2017) reported that a pre-incubation with the R. geoides polyphenol-enriched extract induced intracellular antioxidant responses in AGS cells, increasing the levels of glyoxalase I and glutathione-S-transferase. The viability of the cells challenged with peroxyl and hydroxyl radicals was associated with the activation of these intracellular detoxifying enzymes. 24

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4. Conclusions

Burgos-Edwards, A., Jiménez-Aspee, F., Theoduloz, C., Schmeda-Hirschmann, G., 2018. Colonic fermentation of polyphenols from Chilean currants (Ribes spp.) and its effect on antioxidant activity and metabolic syndrome-associated enzymes. Food Chem. 258, 144–155. https://doi.org/10.1016/j.foodchem.2018.03.053. Bustamante, L., Pastene, E., Duran-Sandoval, D., Vergara, C., von Baer, D., Mardones, C., 2018. Pharmacokinetics of low molecular weight phenolic compounds in gerbil plasma after the consumption of calafate berry (Berberis microphylla) extract. Food Chem. 268, 347–354. https://doi.org/10.1016/j.foodchem.2018.06.048. Campbell, R., 2015. So near, so distant: human occupation and colonization trajectories on the Araucanian islands (37° 30′ S. 7000–800 cal BP [5000 cal BC–1150 cal AD]). Quat. Int. 373, 117–135. https://doi.org/10.1016/j.quaint.2014.11.060. Cardoso, B., Ochoa, J., Richeri, M., Molares, S., Pozzi, C., Castillo, L., Chamorro, M., Aigo, J., Morales, D., Ladio, A., 2015. El papel de las mujeres y las plantas en la subsistencia de las comunidades rurales de la Patagonia árida de Argentina. Leisa 31 (4), 19–22. Caruso, F.,L., Velázquez, N.J., Martínez, T.,A.C., Yagueddú, C., Civalero, M.T., 2018. Multiproxy study of plant remains from Cerro Casa de Piedra 7 (Patagonia, Argentina). Quat. Int. 463, 327–336. https://doi.org/10.1016/j.quaint.2016.11.005. Part B. Casamiquela, R., 2002. Contribuciones etnobotánicas de la Patagonia, first ed. Centro Nacional Patagonico, Puerto Madryn. Céspedes, C.L., El-Hafidi, M., Pavon, N., Alarcon, J., 2008. Antioxidant and cardioprotective activities of phenolic extracts from fruits of Chilean blackberry Aristotelia chilensis (Elaeocarpaceae), Maqui. Food Chem. 107, 820–829. https://doi.org/10. 1016/j.foodchem.2007.08.092. Céspedes, C.L., Valdez-Morales, M., Avila, J.G., El-Hafidi, M., Alarcón, J., Paredes-López, O., 2010. Phytochemical profile and the antioxidant activity of Chilean wild blackberry fruits, Aristotelia chilensis (Mol) Stuntz (Elaeocarpaceae). Food Chem. 119, 886–895. https://doi.org/10.1016/j.foodchem.2009.07.045. Cespedes, C.L., Pavon, N., Dominguez, M., Alarcon, J., Balbontin, C., Kubo, I., El-Hafidi, M., Avila, J.G., 2017. The Chilean superfruit black-berry Aristotelia chilensis (Elaeocarpaceae), Maqui as mediator in inflammation-associated disorders. Food Chem. Toxicol. 108, 438–450. https://doi.org/10.1016/j.fct.2016.12.036. Céspedes-Acuña, C.L., Xiao, J., Wei, Z.-J., Longsheng, C., Bastias, J.M., Avila, J.G., Alarcon-Enos, J., Werner-Navarrete, E., Kubo, I., 2018. Antioxidant and anti-inflammatory effects of extracts from Maqui berry Aristotelia chilensis in human colon cancer cells. J. Berry Res. 8, 275–296. https://doi.org/10.3233/JBR-180356. Cheel, J., Theoduloz, C., Rodriguez, J., Saud, G., Caligari, P.D.S., Schmeda-Hirschmann, G., 2005. 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The revision on the use of native berries in Patagonia allowed the identification of 28 species mainly used as food, but also as medicinal in Eastern and Western Patagonia. Most of them are available in both sides of the Andes dividing Argentina and Chile. The steppes and shrub landscape in the eastern are ideal places to gather Berberis, Ericaceae and Grossulariaceae. Several species appreciated as edible at present show a very long ethnohistory of use (prehispanic, posthispanic and contemporary), including Berberis, Fragaria, Ribes, Rubus, Gaultheria and Empetrum. The gathering of wild fruits by human populations of Argentina and Chile is a distinctive manifestation of cultural identity, which reflects the local environment, history and cosmology of the people. Chemical and bioactivity studies have been focused mainly in maqui, calafate and the native strawberry because of their potential development into new crops. The chemical constituents show a wide array of compounds belonging to different chemical structures, acting by different and complementary mechanisms. Further studies are required to investigate other species that have not been considered so far. In addition, more studies are needed on the mechanisms of action related to the health promoting properties from these native berries, as well as to encourage the agronomic development of these wild species into commercial crops. Author contributions GSH designed the review and worked up the archeological background and the integrative data interpretation. CT and FJ-A prepared the chemical and pharmacological revision, as well as the artwork. AL wrote the ethnobotanical section. All authors actively participated in the data interpretation and shaped the final version of the manuscript. Acknowledgements Financial support from FONDECYT Projects 1170090 and 11170184 is kindly acknowledged. A.L. thanks CIEFAP and CONICET, Argentina for funding. References Ah-Hen, K.S., Mathias-Rettig, K., Gómez-Pérez, L.S., Riquelme-Asenjo, G., LemusMondaca, R., Muñoz-Fariña, O., 2018. Bioaccessibility of bioactive compounds and antioxidant activity in murta (Ugni molinae T.) berries juices. J. Food Meas. Charac. 12, 602–615. https://doi.org/10.1007/s11694-017-9673-4. Ávila, F., Theoduloz, C., López-Alarcón, C., Dorta, E., Schmeda-Hirschmann, G., 2017. Cytoprotective mechanisms mediated by polyphenols from Chilean native berries against free radical-induced damage on AGS cells. Oxid. Med. Cell. Longev. https:// doi.org/10.1155/2017/9808520. Article ID: 980852058. Bañados, M.P., Hojas, C., Patillo, C., Gonzalez, J., 2002. Geographical distribution of native Ribes species present in the herbarium of Chile. Acta Hortic. (Wagening.) 585, 103–106. https://doi.org/10.17660/ActaHortic.2002.585.13. Barthélémy, D., Brion, C., Puntieri, J., 2008. Plantas de la Patagonia, first ed. Vazquez Mazzini, Buenos Aires. Belmar, P.,C., Méndez, C., Reyes, O., 2017. Hunter-gatherer plant resource use during the Holocene in central western Patagonia (Aisén, Chile, South America). Veg. Hist. Archaeobotany 26, 607–625. https://doi.org/10.1007/s00334-017-0632-0. Blackhall, M., Raffaele, E., Veblen, T.T., 2008. Cattle affect early post-fire regeneration in a Nothofagus dombeyi-Austrocedrus chilensis mixed forest in northern Patagonia, Argentina. Biol. Conserv. 141, 2251–2261. https://doi.org/10.1016/j.biocon.2008. 06.016. Borrero, L.A., Delaunay, A.N., Méndez, C., 2019. Ethnographical and historical accounts for understanding the exploration of new lands: the case of Central Western Patagonia, southernmost South America. J. Anthropol. Archaeol. 54, 1–16. https:// doi.org/10.1016/j.jaa.2019.02.001. Brauch, J.E., Reuter, L., Conrad, J., Vogel, H., Schweiggert, R.M., Carle, R., 2017. Characterization of anthocyanins in novel Chilean maqui berry clones by HPLC-DADESI/MSn and NMR-spectroscopy. J. Food Compos. Anal. 58, 16–22. https://doi.org/ 10.1016/j.jfca.2017.01.003. Burgos-Edwards, A., Jiménez-Aspee, F., Thomas-Valdés, S., Schmeda-Hirschmann, G., Theoduloz, C., 2017. Qualitative and quantitative changes in polyphenol composition and bioactivity of Ribes magellanicum and R. punctatum after in vitro gastrointestinal digestion. Food Chem. 237, 1073–1082. https://doi.org/10.1016/j.foodchem.2017. 06.060.

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