Diversity and origin of medicinal exotic flora in Cape Verde Islands

The Cape Verde archipelago is located in the North Atlantic Ocean, in close proximity to the western African coast, c. 600 km west of Senegal. All the nine inhabited islands are of volcanic origin, namely: Santo Antão, São Vicente, São Nicolau (Northern Islands), Santiago, Fogo, Brava (Southern Islands), and Sal, Boavista and Maio (Eastern Islands) (fig. 1). This archipelago was discovered by Portuguese navigators who, throughout the 15th century, explored the African coast (Albuquerque 1991). Documents relating to its discovery do not record the existence of any traces of human occupation, but mention the existence of several plant species that attracted the attention of their first occupants (Cardoso 1902). The colonization of Cape Verde, which began around 1460 in Santiago Island, was laid by Europeans, mainly Portuguese but also some Spanish, a few Italians, and Africans purchased on the West African coast, especially on the Guinea coast (slave trade) (Ribeiro 1955). The geographical position of Cape Verde in the Atlantic Ocean transformed these islands into an important port of call for the supply and repair of the Portuguese vessels (Carreira 1986). In the main port city of Santiago Island, Ribeira Grande, sailors from Portugal, traders on their way to Central America or Brazil, and travellers returning from the East, exchanged experiences and knowledge and left some plants brought from distant locations that served to prevent and cure most illnesses (Torrão & Soares 2009). Although the introduction of many plants in Cape Verde seems to have been intentional, the availability of old descriptions of the plant uses in these islands is scarce (Duarte & Moreira 2002). In general, the lack of registered thorough sampling until the middle of the 19th century was a result of the fact that botanists visiting this archipelago were only taking advantage of their short stops on the way to more botanically rich regions for collection and study of the local flora (Pettersson 1960). In fact, it was only in the 19th century that these islands began to raise the interest among the naturalists and scientists, and some field expeditions were made by Forbes in 1822, Darwin in 1832, Hooker in 1839, Bolle in 1851, and Welwitsch in 1853 and 1861 (Barbosa 1961). In the 19th and 20th centuries several important works were published (e.g. Webb 1849, Schmidt 1852, Chevalier 1935,


INTRODUCTION
The Cape Verde archipelago is located in the North Atlantic Ocean, in close proximity to the western African coast, c. 600 km west of Senegal.All the nine inhabited islands are of volcanic origin, namely: Santo Antão, São Vicente, São Nicolau (Northern Islands), Santiago, Fogo, Brava (Southern Islands), and Sal, Boavista and Maio (Eastern Islands) (fig.1).This archipelago was discovered by Portuguese navigators who, throughout the 15 th century, explored the African coast (Albuquerque 1991).Documents relating to its discovery do not record the existence of any traces of human occupation, but mention the existence of several plant species that attracted the attention of their first occupants (Cardoso 1902).The colonization of Cape Verde, which began around 1460 in Santiago Island, was laid by Europeans, mainly Portuguese but also some Spanish, a few Italians, and Africans purchased on the West African coast, especially on the Guinea coast (slave trade) (Ribeiro 1955).The geographical position of Cape Verde in the Atlantic Ocean transformed these islands into an important port of call for the supply and repair of the Portuguese vessels (Carreira 1986).In the main port city of Santiago Island, Ribeira Grande, sailors from Portugal, traders on their way to Central America or Brazil, and travellers returning from the East, exchanged experiences and knowledge and left some plants brought from distant locations that served to prevent and cure most illnesses (Torrão & Soares 2009).
Although the introduction of many plants in Cape Verde seems to have been intentional, the availability of old descriptions of the plant uses in these islands is scarce (Duarte & Moreira 2002).In general, the lack of registered thorough sampling until the middle of the 19 th century was a result of the fact that botanists visiting this archipelago were only taking advantage of their short stops on the way to more botanically rich regions for collection and study of the local flora (Pettersson 1960).In fact, it was only in the 19 th century that these islands began to raise the interest among the naturalists and scientists, and some field expeditions were made by Forbes in 1822, Darwin in 1832, Hooker in 1839, Bolle in 1851, and Welwitsch in 1853 and 1861 (Barbosa 1961).In the 19 th and 20 th centuries several important works were published (e.g.Webb 1849, Schmidt 1852, Chevalier 1935, Hansen & Sunding 1993, Brochmann et al. 1997, Paiva et al. 1995-1996, Martins et al. 2002) providing a reasonable insight into the knowledge of the Cape Verde flora.Despite these and other botanical studies, several important issues remain to be considered, namely related to the collection of ethnobotanical data.The few studies available concerning the uses of medicinal plants in this archipelago (namely Barbosa 1961, Gomes et al. 1995, Varela 1999, 2001, and Vera-Cruz 1999) are written in Portuguese, which increases the difficulty for the scientific community to access the information.
Despite the subtropical dry climate that characterizes this archipelago, and which has not allowed the development of abundant vegetation, the Cape Verde flora comprises about 740 spontaneous or naturalized taxa from more than one hundred families, the Asteraceae, Euphorbiaceae, Fabaceae, Malvaceae, Solanaceae, Cyperaceae, and Poaceae being the most well-represented (Duarte et al. 2008).Most of the archipelago's flora is presently composed of exotic naturalized species (Duarte & Romeiras 2009).
Since the Cape Verde Islands were not inhabited up to the end of the 15 th century (Cardoso 1902), it will be helpful to understand how the introduction of plants for medicinal purposes, constituted a factor in defining the present day flora.As such, herein is presented a study that has been developing in the field of characterization of the Cape Verde exotic medicinal flora, in order to understand the traditional use of the exotic medicinal flora that the population of this archipelago still uses and to highlight some features related to their introduction during islands colonization.

MATERIAL AND METHODS
Data was gathered from published research papers on medicinal plant studies in Cape Verde (Barbosa 1961, Gomes et al. 1995, Vera-Cruz 1999, Varela 1999, 2001) and complemented by exhaustive consultation of specimens kept in LISC Herbarium (IICT/Tropical Research Institute), which holds the most important collection of Cape Verde flora.For each taxon, the family, scientific and local name, habit and distribution in Cape Verde (only inhabited islands) and worldwide native range were included in a database.This data was gathered in Chevalier (1935), Brochmann & Rustan (1981), Flora de Cabo Verde (Paiva et al. 1995-1996, Martins et al. 2002), Flore du Sénégal (Berhaut 1971, 1974, 1975a, 1975b, 1976, 1979, Vanden Berghen 1988, 1991), Flora of West Tropical Africa (Hepper 1963, 1968-1972, Hutchinson & Dalziel 1954-1958), Hansen &Sunding (1993), andSánchez-Pinto et al. (2005) as well as in several published papers related with particular taxa.Also data collected in recent field work done by the authors was taken into consideration.Data concerning the origin (native vs. introduced) of the species was mainly obtained from Lobin & Zizka (1987), Ferrão (1993) and Sánchez-Pinto et al. (2005).However with some taxa it was not possible to obtain accurate data since their geographic origin is unknown or doubtful.
The scientific names were revised and updated using online databases such as Tropicos (http://www.tropicos.org).
For the exotic plants used in traditional medicine in Cape Verde, the data was organized in two categories: (a) the naturalized species, i.e. the introduced plants that have shown the  Based on cited bibliography we further analyzed the native distribution range of these exotic medicinal plants.The terminology used follows Morrone (2002), which considers the following world regions: Nearctic, Palaearctic, Neotropical, Afrotropical, Oriental, Australotropical, Andean, Cape or Afrotemperate, and Antarctic.Furthermore some combinations were considered for species with a more wide range of distribution: Cosmopolitan, Pantropical, Afrotropical-Neotropical, Afrotropical-Palaearctic, Afrotropical-Oriental, Oriental-Australotropical and Nearctic-Neotropical.It has to be noted that with some species, especially the widespread, it was not possible to determine the exact range of native distribution.
Moreover, an historic contextualization of the introduction of the medicinal plants in Cape Verde was also carried out using for instance the descriptions of the English Captain Georges Roberts in 1726(in Roberts 1980), or from the naturalist Feijó in 1797, in charge of collecting information on the natural productions and responsible for the first herbarium representing the Cape Verde flora (in Feijó 1986).Other historical documents with descriptions and information referring to the colonization of these islands were used, e.g.Senna 1818(in Senna 1987), Chelmicki &Varnhagen 1841, andValdez 1864.In addition to the mentioned studies and taking into consideration the fact that most of the slaves that initially populated Cape Verde came from Guinea-Bissau, we further compared the exotic medicinal flora of both countries using Catarino et al. (2008) checklist.

Exotic flora used in traditional medicine
A total of 101 naturalized exotic species were reported in traditional medicine in the different islands of Cape Verde.The Dicotyledons with 92 species constitute the highest number of plants used for medicinal purposes.Also nine Monocoty-ledons were reported in our study.Most of these taxa are herbaceous, annual or biannual plants.However, some shrubs (e.g.Vernonia colorata, Opuntia ficus-indica, Jatropha curcas, Lavandula dentata, Indigofera tinctoria, Sesbania grandiflora, Gossypium barbadense, Gossypium hirsutum, Ruta chalepensis, Capraria biflora, Lantana camara), small trees (Leucaena leucocephala, Sapindus saponaria), and trees (Tamarindus indica, Lonchocarpus laxiflorus, Melia azedarach) have also been reported (table 1).
The present study revealed that the naturalized dicotyledonous species belonged to 28 families.The families with a greater number of medicinal species are the Fabaceae with fourteen species, the Asteraceae and the Malvaceae with twelve species each, the Amaranthaceae with eight species, and the Solanaceae with seven species (see table 1).The genera with the highest number of species are: Sida with four species; and Amaranthus and Datura with three species each.When referring to the monocotyledonous species naturalized in Cape Verde, of the five families with plants used in traditional medicine, the Cyperaceae is the family with more species, four taxa.On the other hand, concerning the Poaceae, which exists in large numbers in the archipelago (~ 120 grass species both native and exotic, see Duarte et al. 2008), only one species is referred to as being medicinal, Imperata cylindrica (table 1).Several other uses were registered for the grasses in Cape Verde, namely as pasture and foraging (data not shown).
The analysis of the non-naturalized exotic species with medicinal interest revealed that nineteen taxa belong to the medicinal flora of this archipelago.These taxa are distributed in ten families, of which eight are leguminous species (five Fabaceae and three Mimosaceae) (table 2).Most of these are woody perennial species, being mainly distributed across the islands of Santo Antão and Santiago, where the agricultural activity is higher.

Distribution of Cape Verde's medicinal exotic plants
Regarding the worldwide distribution of the medicinal naturalized species (fig.2) four main groups were observed: (a) Afrotropical species, of which the majority are from West family scientific name (a)  local name native Distribution (b)  habit distribution in Cape Verde (c)     1).Among the species which are distributed between two biogeographical regions there is a predominance of the Afrotropical-Oriental.
From the analyses of the non-naturalized medicinal species used in traditional medicine of Cape Verde it was revealed that the majority are from Neotropical or Oriental (Asia) regions (fig.3); on the other hand species from Palaearctic regions are not numerous, as opposed to what happens with naturalized medicinal species (see fig. 2).The predominance of the elements from Latin America and Tropical Asia is related to the fact that these are the places of origin and domestication of a large number of the species cultivated in the archipelago, like beans (Canavalia ensiformis, Lablab purpureus subsp.purpureus, Phaseolus lunatus), peanuts (Arachis hypogaea) or manioc (Manihot esculenta).
Half of the exotic medicinal species from Cape Verde (tables 1 & 2) is present in Guinea-Bissau (see Catarino et al. 2008), although it was found that only a reduced number are used as medicinal in both countries.For instance: Abrus precatorius (used for male impotence and tooth aches), Spermacoce verticillata (used for kidney problems and belly aches), Chamaecrista absus (to heal furunculous and fever), Chamaecrista nigricans (used to treat wounds, as a purgative, and to treat worm problems), Ocimum basilicum (used to treat colds), Senna occidentalis (for venereal diseases, fevers or eye problems), are some of the species commonly used in the traditional medicine in Guinea-Bissau and Cape Verde Islands.Furthermore, many other species, used as me-dicinal in Cape Verde, are referred to as alimentary (Amaranthus spinosus, Amaranthus viridis, Adansonia digitata), for phytochemical uses (Acanthospermum hispidum, Indigofera tinctoria), or for textile manufacturing (Hibiscus cannabinus, Gossypium hirsutum) in Guinea-Bissau.

DISCUSSION
As a result of human colonization and also of trading routes during the Age of Discoveries, most of the flora of Cape Verde archipelago is presently constituted by exotic naturalized species (Duarte & Romeiras 2009).The use of local flora in folk medicine is common in Cape Verde, and 101 exotic plants, i.e. about 20% of total exotic flora, were reported as medicinal in this archipelago.As a consequence of the hot and dry climatic conditions most of them correspond to annual or biannual herbs as with the overall flora.
Although, the introduction of useful plants in the Cape Verde Islands occurred at the same pace as their occupation (Barcellos 1899), for the 16 th , 17 th and the 18 th centuries, there is no concrete information on medicinal plants used by the populations of this archipelago (Albuquerque 1991).One of the first descriptions of medicinal plants and how the local people used them in healing certain diseases was made by Feijó in 1797(in Feijó 1986).Furthermore, in Filho (1995) an old description (from 1798) reported that an infusion of the leaves of the plant commonly named fedegosa (Chenopodium ambrosioides; see table 1) was used to help in labor, facilitating the uterine contractions: relaxation of the pelvic muscles and increase the resistance of blood vessels to prevent postpartum bleeding.According to Varela (1999Varela ( , 2001)), C. ambrosioides continued to be reported as an important medicinal plant with several applications in Cape Verde as well as in other tropical and subtropical areas.For instance, in Central and South America the leaves and flowers are presently used to stimulate labor, menses regulation and to treat abnormal uterine bleeding (Ososki et al. 2002), and in West Africa is used to stimulate blood flow in the pelvic area and uterus (Berhaut 1974).So, one of the most ancient descriptions about the traditional use of C. ambrosioides in the Cape  Verde Islands seems to reflect the current modern use of this plant in different parts of the world.
As it was noted, the position of these islands in the Atlantic Ocean allowed a rapid colonization, especially during the 18 th -19 th centuries.Several medicinal plants were introduced and adopted by Portuguese immigrants, although the traditional knowledge on the Cape Verde Islands was particularly influenced by African slaves.According to Torrão & Soares (2009), African slaves were subjected to severe workloads and unbearable living conditions and were forced to cure their own illnesses with local medicinal plants.These slaves, that initially colonized this archipelago or whilst en-route to Latin America, brought with them the knowledge of the uses of the local flora which is reflected in the predominance of elements Afrotropical and Neotropical highlighted in our studies.Regarding the exotic flora of Palaearctic distribution it is assumed that this is undoubtedly linked to the introduction of plants by the Portuguese during the whole process of colonization of the islands; species like Foeniculum vulgare, Plantago major or Rosmarinus officinalis are commonly used as medicinal in Portugal.Because of their economical interest, many of the plants were introduced by the Portuguese and other Europeans, which had in this way an important role in defining the composition of the flora of these islands.In this context, Ribeiro (1955) refers to Cape Verde as a centre of concentration and diffusion for plants, animals and men, as probably none other in the tropical regions; and Ferrão (1991) refers to the islands of Cape Verde as playing a role of extraordinary importance in the exchange of plants and worked as 'gardens' of acclimatization for plants from many places.
It was noted that the African slaves have certainly shaped the present day use of medicinal plants in the Cape Verde Islands, where the majority of the rural population still uses some plants to treat diseases.This comes as no surprise as the African continent has a long and impressive list of medicinal plants based on local knowledge (e.g.Burkill 1985, 1994, 1995, 1997, 2000, Schmelzer & Gurib-Fakim 2008).In Africa, traditional healers and remedies made from plants play an important role in the health of millions of people (e.g.Ayensu 1978).Every region has a form of traditional medicine, which varies from one community to another and is deeply rooted in a specific socio-cultural context (Oliver-Bever 1986, Rukangira 2001).For instance the roots and leaves of Abrus precatorius subsp.africanus, a tropical plant found in almost all of the West African countries are used in Cape Verde for conjunctivitis and skin diseases (Varela 1999(Varela , 2001)).According to the Flora of Senegal (Berhaut 1976) this plant is widely used for broad applications such as: respiratory infections and cough; to cure anaemia; abortifacient.Meanwhile, in Guinea-Bissau, the dried root is used for "toothache and stomach aches", and it is also understood to have an aphrodisiac effect (Catarino et al. 2006).Likewise, Jatropha curcas (Parawira 2010), a Euphorbiaceae described as medicinal in Cape Verde has an actual worldwide economic importance.This species is a drought-resistant perennial shrub, adapted to the arid and semi-arid conditions of all the Cape Verde Islands.The oil of its seeds can be combusted as fuel without being refined and used in folk medicine as a laxative or purgative (Figueiredo 1996).
The infant mortality in Cape Verde is among the very lowest in the West African region, the major health problems are related either with childhood diseases (e.g.diarrhoea, respiratory infections and cough), fevers, skin infections, urinary diseases or eye inflammations (Varela 1999(Varela , 2001)).Most of these diseases are caused by poor hygiene, particularly the lack of treated water in rural areas.It is to be noted that Cape Verde has a relatively low prevalence of HIV/AIDS (Larsen et al. 1998), limited cases of malaria have been reported in Santiago Island, and tuberculosis appears only from time to time (Wessel et al. 1999) contrary to the other Sub-Saharan African countries.So, in Cape Verde the situation is not as serious as in other African countries; nevertheless, medical facilities in this archipelago are limited.For instance, there are only two central hospitals (in Mindelo, São Vicente Island and in Praia, Santiago Island); and Brava and Santo Antão no longer have functioning airports, and air evacuation, only by helicopters, is extremely difficult from these two islands.So, the cost of pharmaceuticals, the difficulty of reaching the two central hospitals, as well as limited availability of doctors, especially in the rural areas, most likely contributes to the widespread continued use of plants for medicinal purposes in this archipelago.
Finally, we would like to clarify that very few papers concerning aspects of the folk plant traditions have been published for Cape Verde Islands.Moreover interviews with traditional healers from these islands have scarcely been done and so, further field studies must be organized for a better characterization of the medicinal Cape Verde flora.

Figure 1 -
Figure 1 -Geographic location of Cape Verde archipelago in the North Atlantic Ocean.

Figure 2 -
Figure 2 -Distribution of naturalized exotic species used in traditional medicine in Cape Verde Islands.

Figure 3 -
Figure 3 -Distribution of non-naturalized exotic species used in traditional medicine in Cape Verde Islands.

Table 1 -Checklist of the exotic naturalized medicinal plants of Cape Verde Islands. (
Morrone (2002)n which the introduced status in Cape Verde is somewhat doubtful are marked with an asterisk (*), (b), in the case of recent nomenclatural changes, synonyms commonly employed in Cape Verdean botanical literature are included; (c), the terminology used followsMorrone (2002).Whenever possible, the distribution of each taxon concerns to its native geographic range; (d), Cape Verde Islands abbreviations: A, Santo Antão; V, São Vicente; N, São Nicolau; S, Sal; B, Boavista; M, Maio; T, Santiago; F, Fogo; and Br, Brava.

Table 2 -Checklist of the exotic cultivated medicinal plants of Cape Verde Islands
Morrone (2002)ase of recent nomenclatural changes, synonyms commonly employed in Cape Verdean botanical literature are included; (b), the terminology used followsMorrone (2002).Whenever possible, the distribution of each taxon concerns to its native geographic range; (c), Cape Verde Islands abbreviations: A, Santo Antão; V, São Vicente; N, São Nicolau; S, Sal; B, Boavista; M, Maio; T, Santiago; F, Fogo; and Br, Brava.