Journal of Ethnopharmacology 155 (2014) 1332–1341

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Journal of Ethnopharmacology
journal homepage: www.elsevier.com/locate/jep

Research Paper

An ethnopharmacological assessment of the use of plants against

parasitic diseases in humans and animals
Flávia dos Santos Silva a, Ulysses Paulino Albuquerque a,n, Livio Martins Costa Júnior b,
Aldilene da Silva Lima b, André Luiz Borba do Nascimento a, Júlio Marcelino Monteiro c
a
Laboratório de Etnobiologia Aplicada e Teórica (LEA), Departamento de Biologia, Universidade Federal Rural de Pernambuco, Rua Dom Manoel de Medeiros,
s/n, Dois Irmãos, CEP 52171-900 Recife, PE, Brazil
b
Laboratório de Parasitologia (LAPA), do Centro de Ciências Agrárias e Ambientais, CCAA - UFMA, Maranhão, Brazil
c
Universidade Federal do Piauí, Campus Professora Cinobelina Elvas, Bom Jesus, PI, Brazil

art ic l e i nf o a b s t r a c t

Article history: Ethnopharmacological relevance: Ethnobotanical surveys are detecting an increasing frequency of exotic
Received 4 April 2014 plant species in pharmacopeias, which has led researchers to investigate the role of such species in
Received in revised form traditional medical systems. According to the diversification hypothesis, exotic species are included to
7 July 2014
complete pharmacopeias, i.e., to treat diseases for which no native species are known, thus broadening
Accepted 17 July 2014
Available online 27 July 2014
the scope of the plant repertoire.
Materials and methods: The present study was conducted at two rural communities in northeastern
Keywords: Brazil aiming at a survey of the plants known or used by the population to treat endo- and ectoparasitic
Brazil diseases in humans and animals. In addition, plant extracts exhibiting acaricide activity were assessed
Ethnoveterinary
using the engorged female immersion and larval packet tests (LPT).
Traditional botanical knowledge
Results: The results of the present study showed a tendency for native species to be used against
Tick
Insecticidal activity ectoparasites and exhibit a broader scope of use compared to exotic species. In turn, exotic species were
predominantly indicated to treat diseases caused by endoparasites, although there was an overlap of
native and exotic species relative to some therapeutic purpose, e.g., ticks. Only two of the plant species
tested exhibited acaricide activity (Nicotiana glauca Graham and Croton blanchetianus Baill.), and in both
cases, the activity was weak.
Conclusion: The ethnobotanical data do not fully support the suggested hypothesis. Overall, the wide
versatility of exotic species was not exclusively used to treat parasitic diseases in humans and animals. In
addition, the selection of acaricide plants based on the ethnopharmacological study generated
uninteresting results.
& 2014 Elsevier Ireland Ltd. All rights reserved.

1. Introduction
The search for plants that are potentially useful against dis-
eases, e.g., parasitic diseases, has recently increased because of the
resistance of parasites to available synthetic agents (see Echevarria
et al. (1996), Martins (2006), and Molento (2009)). Lans and Tumer
(2011) showed that using plant products against parasites reduces
drug use in animal health care, and plant products are also
relevant from an environmental perspective because they do not
contaminate the soil.
Ethnobotanical studies provide a satisfactory approach to disco-
vering novel active substances because they investigate the knowl-
edge of individuals who utilize plants. The selection of plants by
n
Corresponding author.
E-mail address: upa@db.ufrpe.br (U.P. Albuquerque).
human populations has been a target of studies that aim to assess the
process involved in elaborating pharmacopeias and identifying
species with the greatest potential for bio-prospecting. In that regard,
some authors have questioned the role of exotic species in local
medical systems (Alencar et al., 2010; Medeiros et al., 2013). Until
recently, the inclusion of exotic species in local medical systems was
considered to denote cultural loss (Caniago and Sibert, 1998). From a
chemical perspective, Albuquerque (2006) formulated the diversifi-
cation hypothesis, according to which exotic species might be
introduced in a given culture to diversify its pharmacopoeia.
Albuquerque's (2006) hypothesis was tested by Alencar et al.
(2010) at a semi-arid site in northeastern Brazil. These authors
observed evidence that support the diversification hypothesis
because the exotic species examined exhibited greater chemical
diversity compared to the native species. Thus, exotic species
might be introduced to ensure a supply of substances to treat
diseases for which no native species are known.

http://dx.doi.org/10.1016/j.jep.2014.07.036
0378-8741/& 2014 Elsevier Ireland Ltd. All rights reserved.
 F.d.S. Silva et al. / Journal of Ethnopharmacology 155 (2014) 1332–1341 1333

Therefore, the aims of the present study were to investigate
(1) whether there are differences in the diversity of uses for exotic
species that fight parasitic diseases in humans and animals
compared to native species and (2) whether there is specificity
for using of exotic or native plant species indicated for parasitic
diseases. In addition, we tested the acaricide activity of the plant
species that were directly reported against ticks.
type BSh in Köppen's classification, with an average annual
temperature of 23.1 1C (Itep/Lamepe, 2007). The area vegetation
is hypo-xerophilous Caatinga (savanna like vegetation) and con-
tains deciduous and sub-deciduous species (Lins Neto et al., 2012).
The two communities share several traits, including their distance
from urban areas, location by the Letreiro Mountains (690 m high)
(Almeida et al., 2011) and vegetation comprised of shrubs and trees,
which supply the residents with plants to satisfy various needs.

2. Materials and methods 2.1.1. Carão site

2.1. Study location
This study was conducted in two rural communities, Carão Site
and Letreiro Site, located in Altinho County, Pernambuco (north-
eastern Brazil) (Fig. 1) 162 km from Recife, which is the state
capital. This area has a hot, semi-arid climate that corresponds to
Carão is located 16 km from the next town (081 350 S and 361
050 W) between two low mountains. Agriculture in this area fulfills
human and animal subsistence. Livestock are partially fed plants
extracted from anthropogenic areas, such as on the sides of roads
and cultivated land where maize (Zea mays L.) and Barbary
figs (Opuntia ficus-indica (L.) Mill) are grown (Santos et al.,
2009). The use of plants in daily sustenance most likely generated

Fig. 1. Location of the Carão and Letreiro communities, Altinho, Pernambuco (Northeast Brazil).
Source: Alencar et al. (2010).
1334 F.d.S. Silva et al. / Journal of Ethnopharmacology 155 (2014) 1332–1341
wide botanical experience for the population. Most of the animals
raised in this area are cattle, whereas sheep, swine and poultry are
less common.
The community residents perform different activities, including
agriculture, trade, teaching and civil construction, among others. A
resident association holds monthly meetings to discuss matters of
local interest. Primary care is provided by a Family Health Program
(FHP) unit (Silva et al., 2011), in which a doctor and nurse see
patients on a monthly and weekly basis, respectively. In addition,
two community health agents perform house calls.
2.1.2. Letreiro site
Letreiro is located 9 km from Altinho (81 330 S and 361 50 W)
and includes dwellings and pasture areas distributed along a
central road that leads to the city center. Livestock farming of
cattle and sheep is most widely performed at Letreiro, whereas
swine and goats are less common. To reduce costs, cattle are fed
some cactus species, such as blue columnar cactus (Pilosocereus
pachycladus F. Ritter), mandacaru (Cereus jamacaru DC.) and
Barbary fig (Opuntia ficus-indica (L.) Mill.).
2.2. Data collection
2.2.1. The collection of ethnobotanical data
An ethnobotanical study was conducted in both communities
with individuals older than 18 years old. These individuals were
visited in their homes to explain the study aims and procedures,
and those who were interested in participating signed an informed
consent form to comply with regulations (National Health Council
Resolution no. 466 from December 12, 2012). Socioeconomic
information was then recorded before ethnobotanical data were
collected, which was performed using semi-structured interviews
(Albuquerque et al., 2014). The guiding question in the interviews
was “What plants do you know and/or use for any purpose?” To
supplement the information, participants were asked which com-
ponents they used from the aforementioned plants, what purpose
they served and where they were collected and prepared. The
guided field-walk method was then used to validate the verna-
cular/popular names of the plants (Albuquerque et al., 2014) as
well as collect additional information, such as procedure, help the
informants remember the names of the plants and collect botani-
cal materials for taxonomic identification.
The initial stage of data collection consisted of recording the
general uses of plants. The second stage was performed with
participants who fulfilled at least one of the following criteria:
raised local domestic animals; was a key-informant on medicinal
plants, who was selected based on the quality and amount of data
provided in the initial study stage; and was considered a local
specialist according to the results obtained using the “snowball”
sampling technique (Albuquerque et al., 2014). In this stage of the
study, free lists were elaborated on and semi-structured inter-
views were conducted to collect information on plants with
possible anti-parasitic activities. Regarding the participants who
raised cattle, additional information was collected relative to the
type and number of animals they raised and the duration of that
activity. In order to collect information about parasites, we used
local terms recorded in the first interview.
All the plants indicated in the interviews were collected,
botanized and included in the collection of Professor Vasconcelos
Herbarium, Federal Rural University of Pernambuco (Universidade
Federal Rural de Pernambuco—UFRPE), and copies were included
in the collection of Professor Geraldo Mariz Herbarium, Federal
University of Pernambuco (Universidade Federal de Pernambuco—
UFPE) and Agronomic Institute of Pernambuco (Instituto Agronô-
mico de Pernambuco—IPA). The plants were identified using
comparisons with herbarium materials, expert advice and a survey
of the specialized literature.
2.2.2. Plant selection to obtain extracts for in vitro testing of activity
against the tick Rhipicephalus microplus (Canestrini, 1887)
Plants used against cattle ticks, Rhipicephalus microplus, were
selected from the ethnobotanical survey to investigate the resis-
tance of Rhipicephalus microplus (Stone and Haydock, 1962;
Drummond et al., 1973) to these plants in engorged female
immersion and larval packet tests (LPT).
Extracts were prepared from the plant components indicated
by the participants. The samples were collected from at least three
individuals of each species, dried at room temperature, ground
and subjected to extraction using a hydroalcoholic solvent (70%
methanol). Maceration was performed using serial filtration 48 h
after extraction and then every 24 h for approximately 10 days.
Finally, the extract was evaporated using a rotary evaporator.
2.2.3. Larval packet test (LPT)
The LPT was performed according to the technique formulated
by Stone and Haydock (1962) and modified by the Food and
Agriculture Organization FAO (1984) and Leite (1988). Approxi-
mately 100 tick larvae aged 14 to 21 days, obtained in laboratory
conditions, were placed on two 2  2 cm filter papers impregnated
with 400 ml of plant extract dissolved in 70% ethanol to a
concentration of 100 mg/ml. This solvent (70% ethanol) was used
as a negative control. Further tests were performed with various
extract concentrations (200, 150, 100, 75, 50, 25 and 10 mg/ml) as
a function of the mortality observed in the initial test. Four
repetitions were performed with each extract concentration. The
impregnated larvae were placed in a BOD (Biochemical Oxygen
Demand) incubator at 27 71 1C and a relative humidity of Z 80%
for 24 h. The living and dead larvae were then counted.
2.2.4. Engorged female immersion test
This test was performed with plant extracts dissolved in 70%
ethanol and a control group. Each test was performed with groups
of ten engorged Rhipicephalus microplus females, according to the
procedure described by Drummond et al. (1973). The ticks,
obtained from artificial infestations, were initially dried and
weighed to obtain a homogeneous group weight. Each group
was immersed in 4 ml of extract solution at concentrations of
200, 150, 100, 50 and 10 mg/ml for 5 min, and the control group
was only immersed in 70% ethanol. The ticks were then dried and
placed in a BOD incubator at 27 71 1C and a relative humidity of
Z80% for oviposition. The resulting eggs were weighed and placed
in syringes sealed with hydrophilic cotton for incubation and
larval eclosion. The larvae were counted under a stereoscopic
microscope, and the product efficiency (PE) was calculated using
the formula of Drummond et al. (1973): PE ¼RE of control group-
 RE of treated  100/RE of control group, where Reproductive
Efficiency (RE) ¼weight of eggs multiplied by the percentage of
hatched eggs and 20,000 (estimated number of eggs per gram of
eggs)/weight of engorged females.
2.3. Data analysis
The plant species were classified by their origin, native or
exotic. Native species were defined as plants that occurred
spontaneously in South America, and exotic species were plants
that originated on other continents (Alencar et al., 2010).
A Chi-square test with a 95% confidence level (α o0.5) was
used to determine whether there was a difference in the propor-
tion of native and exotic species richness in either community or
among the plants used to fight parasites in humans and animals. A
 F.d.S. Silva et al. / Journal of Ethnopharmacology 155 (2014) 1332–1341 1335

G-test was used to determine whether there was a difference in
the number of native and exotic species indicated against ecto-
and endoparasites affecting humans and animals. In addition, the
G-test on the contingency tables (Ayres et al., 2007) was used to
determine whether there was a difference in the proportion of
exotic and native species used for each parasitic disease. A
Kruskal–Wallis test (with p o0.05 significance) was used to
determine whether an exotic species used against parasites in
humans, animals or both exhibited a wider scope of use compared
to native species in either community. All analyses were per-
formed using the BioEstat 5.0 software (Ayres et al., 2007).
The concentration required to kill 50% of the tick larvae
(Effective Concentration—EC50) was assessed using Software
GraphPad Prism 6.0.
3. Results
3.1. The richness of plants used as anti-parasitic agents
A wide diversity of plant species with possible anti-parasitic
activities in humans and animals was observed in both commu-
nities. Altogether, 53 ethnospecies were recorded at Carão, 43 of
which were identified: 40 at the level of species (nine exotic and
31 native) and three at the level of genus, corresponding to 26
different botanical families. Thirty-five ethnospecies were
recorded at Letreiro, 26 of which were identified: 24 at the level
of species (11 exotic and 13 native) and two at the level of genus,
corresponding to 21 different botanical families.
The participants cited plants used to fight endoparasites, such
as amebae and worms, and ectoparasites, including lice, cattle
flies, furuncular myiasis, ticks and fleas (see Table 1). The species
with the highest number of anti-parasitic uses noted in the Carão
and Letreiro communities included Aloe vera (L.) Burm.
f. (Carão ¼10 uses; Letreiro¼ 15 uses), Chenopodium ambrosioides
L. (Carão ¼9; Letreiro ¼4), Nicotiana glauca Graham (Carão ¼4;
Letreiro¼6) and Libidibia ferrea (Mart. ex Tul.) L. P. Queiroz
(Carão¼ 4; Letreiro¼5).

Altogether, 189 individuals, distributed across 61 dwellings,
were located in Carão. A total 112 people have over eighteen years
of age, eight individuals refused to participate or left the study;
therefore, 104 participants were interviewed (68 females and 36
males). In Letreiro, from 162 in total, 115 individuals were older
than 18 years and resided in 53 dwellings. Only 73 individuals,
corresponding to 77% of the adult population, participated in the
study (41 females and 32 males). Regarding the remaining
residents, some had moved to another location (n¼ 20), refused
to participate (n ¼14) or were not home (n ¼8). In the second
stage, 30 participants were selected from the Carão residents, 27 of
whom agreed to participate in the study, and 40 were selected
from the Letreiro population, 36 of whom agreed to participate.
3.2. Are species richness and the number of uses higher among exotic
plant species?
In Carão, the proportion of native species used to fight parasites
was higher (χ² ¼12.1, p o0.01). The results from the Letreiro
community did not indicate a difference between the proportion
of exotic and native species (χ² ¼0.167, p 40.05). A separate
analysis of the proportion of native and exotic species used to
treat parasitic diseases in humans or animals showed that the
proportion of native species indicated by Carão residents was
higher compared to exotic species (χ²¼ 6.76, p o0.01) but did not
differ relative to the treatment of animals (χ² ¼3.571, p4 0.05). The
proportion of native and exotic species noted in Letreiro did not

Table 1
Medicinal plants used against parasitic diseases in two rural communities in NE Brazil.

Family/species/voucher Status Vernacular names Parts Hosts Ectoparasites Endoparasites Method of preparation NR
used

Amaranthaceae
Chenopodium ambrosioides L. (UFP 54230) E Mastruz Lf, Tw, People Ameba, Raw, maceration and 34
In worms triturated in milk
Lf, Tw Cattle, goat, Worms Triturated in water,
chicken, pig, maceration and decoction
sheep

Annonaceae
Annona squamosa L. (not collected) E Pinha Lf, Sd People Louse Maceration and soak 3
Lf Goat Louse Triturated in water

Apocynaceae
n
Aspidosperma pyrifolium Mart. (not N Pereiro Bk People Tick Soak 10
collected)
Bk, Lf Goats, horse, Louse, tick, louse Soak
cattle eggs of animals
Calotropis procera (Aiton) Aiton (not E Algodão de seda Lt Cattle, goat, pig Myiasis Raw 3
collected)

Araceae
Anthurium affine Schott (not collected) N Tanharão, milho St, Fr, Cattle, goat, pig, Myiasis Raw 3
de urubu Rt horse

Compositae
Bidens bipinnata L. (PEUFR 49837) N Carrapicho Rt People Ameba Decoction 1
Helianthus annuus L. (not collected) E Girassol Sd People Worms Maceration 1

Cactaceae
Melocactus zehntneri (Britton & Rose) N Coroa de frade Cl People Worms Decoction 1
Luetzelb. (not collected)

Leguminosae
Senna spectabilis var. excelsa (Schrad.) H. N Canafístula Fw, Rt People Worms Decoction 2
S. Irwin & Barneby (PEUFR 48673)
1336 F.d.S. Silva et al. / Journal of Ethnopharmacology 155 (2014) 1332–1341

Table 1 (continued )

Family/species/voucher Status Vernacular names Parts Hosts Ectoparasites Endoparasites Method of preparation NR
used

Caricaceae
Carica papaya L. (PEUFR 48666) N Mamão Bk People Worms Raw 2

Celastraceae
Maytenus rigida Mart. (PEUFR 46182) N Bom nome NI Cattle Worms NI 1

Convolvulaceae
Operculina macrocarpa (L.) Urb. (not N Batata de purga Rt, Lf, People Wworms Maceration 8
collected) Bk

Cucurbitaceae
Cucumis anguria L. (not collected) N Chuchuzinho do Fr Cattle, goat Tick Raw 1
mato
Cucurbita pepo L. (not collected) E Jerimum caboclo Sd People Worms Infusion and decoction 1
Momordica charantia L. (not collected) E Melão de são Fr People Ameba, Raw and maceration 5
caetano worms
Tw Horse Worms Soak
Wilbrandia sp (not collected) N Cabeça de nego Rt Donkey, horse, Worms Raw and soak 6
cattle, chicken
NI Cattle Myiasis NI

Euphorbiaceae
nn
Croton blanchetianus Baill. (PEUFR N Marmeleiro, Bk Goats, horse, Louse, tick, louse Soak 3
48713) marmeleiro cattle eggs of animals
branco
Bk People Ameba Decoction and soak
Croton rhamnifolius Willd. (not collected) N Velame Lf Chicken Louse of chicken Raw 1
Jatropha curcas L. (PEUFR 49602) N Pião manso Fr Pig Worms Raw 1
Jatropha gossypiifolia L. (PEUFR 48660) N Pião roxo Bk People Worms Decoction 1
Jatropha mollissima (Pohl) Baill. (PEUFR N Pião brabo Bk People Worms Raw with water 1
48661)
n
Manihot dichotoma Ule (PEUFR 48717) N Maniçoba Lf, Rt, Cattle, goat, pig, Tick, louse, myiasis Raw 3
Rr chicken
chicken louse soak
Manihot esculenta Crantz (not collected) N Mandioca Lf, Rt, Cattle Tick Worms Raw 6
Rr
Ricinus communis L. (UFP 54257) N Mamona Fr, Bk Horse Worms Soak 2
do Fr
Chicken Louse Burned

Leguminosae
Amburana cearensis (Allemão) A.C.Sm. N Imburana açú Bk People Worms Decoction 1
(PEUFR 50486)
n
Anadenanthera colubrina (Vell.) Brenan N Angico Bk, Lf Cattle Tick Maceration and soak 2
(PEUFR 48714)
Libidibia ferrea (Mart. ex Tul.) L. P. Queiroz N Jucá Fr, Bk Cattle, sheep, Worms Soak, decoction, raw 13
(UFP54214) goat, chicken

Lamiaceae
Mentha sp. (not collected) E Hortelã da Lf Lf, Tw People Ameba, Infusion, maceration, 17
miúda worms decoction
Cattle, goat, pig Worms Triturated
Ocimum gratissimum L. (not collected) E Louro Lf People Worms Decoction 1

Amaryllidaceae
Allium sativum L. (not collected) E Alho Bb People Ameba, Maceration, decoction 9
worms and raw
Bb cattle tick, furuncular raw
myiasis, flies of cattle
Bb pig louse raw

Meliaceae
Cedrela odorata L. (UFP 54191) N Cedro Bk Chicken Worms Soak 1
n
Melia azedarach L. (not collected) E Lírio, lírio de Lf Cattle Tick, flies of cattle Soak 2
bolinha, neem

Leguminosae
Mimosa tenuiFwa (Willd.) Poir. (PEUFR N Jurema preta de Lf Cattle Tick Worms Decoction 1
50871) espinho

Musaceae
Musa  paradisiaca L. (not collected) E Banana prata Magará People Worms Raw 2

Myrtaceae
Eugenia sp. (not collected) N Pirim Bk People Worms NI 1

Nyctaginaceae
Boerhavia diffusa L. (not collected) E Pega pinto (erva Rt People Worms Decoction 1
tostão)
 F.d.S. Silva et al. / Journal of Ethnopharmacology 155 (2014) 1332–1341 1337

Table 1 (continued )

Family/species/voucher Status Vernacular names Parts Hosts Ectoparasites Endoparasites Method of preparation NR
used

Plantaginaceae
Scoparia dulcis L. (UFP 53449) E Vassoura de Tw People Worms Decoction 1
botão

Rhamnaceae
n
Ziziphus joazeiro Mart. (UFP 46189) N Juá Bk People Tick Soak 2
Bk Cattle, goat Tick, louse Soak
Bk Donkey, horse Worms Grated bark to soak

Rubiaceae
Spermacoce verticillata L. (not collected) N Vassourinha de Wp People Worms Decoction 2
botão

Rutaceae
Citrus limon (L.) Osbeck (not collected) E Limão Fr Chicken Louse of chicken Raw 1

Sapotaceae
Sideroxylon obtusifolium (Roem. & Schult.) N Quixaba Bk People Worms Decoction 1
T.D.Penn. (UFP 54175)

Solanaceae
n
Capsicum frutescens L. (UFP 54144) E Pimenta Fr People Worms Raw 2
malagueta
Fr, Bk Cattle Flies of cattle, tick, Triturated in water
flea
Fr Chicken Worms Raw
nn
Nicotiana glauca Graham. (UFP46506) N Fumo Lf People To chase ticks, louse Raw 3
Lf Cattle Tick, flies of cattle Tincture
Lf Chicken To chase louse Dried
Solanum aculeatissimum Jacq. (not N Gogóia Rt, Bk People Worms Raw, decoction 2
collected)
Solanum americanum Mill. (UFP 54176) N Erva moura Bk People Worms Raw 1

Verbenaceae
Cajanus cajan (L.) Huth (PEUFR 49847) E Feijão de corda Sd Cattle Worms Maceration 1
Lippia gracilis Schauer (IPA 81233) N Alecrim Lf Cattle, horse Myiasis Maceration 1
Lippia microphylla Cham. (UFP 54198) N Alecrim de flepa Lf Cattle Myiasis Maceration 1

Vitaceae
Cissus simsiana Schult. & Schult. f. (IPA N Parreira Bk Cattle Myiasis Raw 1
81219)

Xanthorrhoeaceae
Aloe vera (L.) Burm. f. (not collected) E Babosa, erva Lf People Ameba, 41
babosa worms
Lf Cattle, goat, Worms Decoction, maceration,
horse, pig, sheep raw, soak
Undetermined Couve branco Bk People Worms Triturated with water 1
Carrapateiro Lf Cattle Worms Maceration and soak 1
Papaconha Rt People Worms Maceration with honey, 6
decoction
Papaconha branca Rt People, cattle, Worms Dried after maceration 1
goat
Prumera Lf, Fr People, cattle, Worms Maceration 3
chicken
Jacatiá Bk People Worms Raw 1
Jerimu Sd People Worms Maceration
Sacatinga Tw Chicken Louse of chicken Raw 1
Vassourinha de Rt People Worms Decoction
botão da branca

Pharmacologycal study.
NR: Number of respondents by species; N: Native; E: Exotic; NI: uninformed; Bk: bark; Bb: bulb; Cl: cladodes; Wp: whole plant; Fw: flower; Ft: fruit; Fr: fruit rind;
In: inflorescence; Lf: leaves; Lt: latex; Rt: roots; Rr: root rind; Sd: seeds; St: stem; Tw: twig.
n
Larval packet test.
nn
Larval packet test and engorged female immersion test.

differ relative to the treatment of either humans or animals
(humans: χ² ¼1.667, p 40.05; animals: χ² ¼2.25, p 40.05)
(Table 2). These results indicated that the proportion of exotic
species known to treat parasitic diseases was not emphasized in
either community, i.e., was not significantly higher compared to
native species.
The scope of therapeutic indications noted for native and exotic
species was compared (Table 3). In Carão, the number of uses
attributed to exotic plant species relative to parasitic diseases was
significantly higher compared to native species as a whole
(humans and animals) (H ¼9.01; p ¼0.003) and in humans alone
(H ¼8.41; p¼ 0.004) (Table 3) but not in animals alone (H¼ 0.70;
p¼ 0.402). The residents of Carão appeared to choose exotic
species to treat a wide scope of parasitic diseases, whereas the
contribution of native and exotic species for treatment was similar
in Letreiro.
1338 F.d.S. Silva et al. / Journal of Ethnopharmacology 155 (2014) 1332–1341

3.3. Is there specificity for using native or exotic plant species against 3.4. In vitro testing of activity against the tick Riphicephalus
some parasitic diseases? microplus

The analysis of exotic vs. native species used against parasitic
diseases in both communities (Fig. 2) showed that only exotic
species were indicated (Allium sativum L. and Aloe vera (L.) Burm.
f.) relative to two conditions, furuncular myiasis, popularly known
as flystrike, and fleas, respectively. Exotic species were predomi-
nantly used for amebiasis (G ¼6.44, p¼ 0.01) and stable fly
(G ¼8.26, p ¼0.004) at Carão; similar results were not observed
at Letreiro. Only native species were indicated to fight louse eggs
in animals (Aspidosperma pyrifolium, Croton blanchetianus and
Ziziphus joazeiro) and ticks in humans (Aspidosperma pyrifolium,
Nicotiana glauca and Ziziphus joazeiro) (Fig. 2). Relative to other
therapeutic targets, the proportion of native species was higher
compared to exotic species at Carão but similar in Letreiro (p40.05).
Despite an overlap in the use of native and exotic species, some
exotic species were attributed a larger scope of use. The most
frequently indicated species used against endoparasites (in
humans and animals) at Carão were exotic, Chenopodium ambro-
sioides (n¼ 24 indications) and Aloe vera (n ¼24), whereas the
native species Manihot esculenta (n ¼4) and Aspidosperma pyrifo-
lium (n ¼5) were most frequently indicated for ectoparasites. In
Letreiro, the most frequently indicated species used against
endoparasites were exotic, Aloe vera (n¼ 25) and Chenopodium ambro-
sioides (n¼18), and the native species Aspidosperma pyrifolium (n¼ 5)
and Nicotiana glauca (n¼ 8) were used for ectoparasites.
The analysis of the proportion of exotic and native species
indicated in both communities (Table 4) was not significantly
different relative to ectoparasites that affect both humans and
animals (G ¼0.172; p ¼0.895) or animals alone (G ¼0.114;
p ¼0.735) or to endoparasites that affect both humans and animals
(G ¼2.08; p ¼0.148), humans alone (G ¼ 2.201; p ¼0.137) or animals
alone (G ¼ 0.172; p ¼0.678).
A total of 11 plants were indicated against ticks, but only nine
(two exotic and seven native) were available for collection and
assessment: Anadenanthera colubrina (leaves and bark), Aspidos-
perma pyrifolium (leaves and bark), Capsicum frutescens (fruit),
Croton blanchetianus (bark), Manihot dichotoma (leaves), Manihot
esculenta (leaves and roots), Nicotiana glauca (leaves), Ziziphus
joazeiro (bark) and Melia azedarach (leaves).
Among all the extracts tested at 100 mg/ml that were indicated
as acaricide, only those from the native species Croton blanchetia-
nus (78%) and Nicotiana glauca (27%) were efficient. The remaining
extracts did not cause larval death. Most likely, the active princi-
ples in those extracts were poorly efficient or in too low concen-
tration; thus, higher concentrations might be necessary to cause
larval death.
The species that exhibited efficiency in the abovementioned
test were subjected to further testing at the following concentra-
tions: Croton blanchetianus - 200, 150, 100, 75, 50, 25 and 10 mg/ml
and Nicotiana glauca - 250, 200, 150, 100 and 75 mg/ml. The tested
concentrations of Nicotiana glauca were higher because the

Table 2
Plant species used as antiparasitic agents and the number species indicated for the
treatment of parasitic diseases in humans and animals in two rural communities in
northeastern Brazil.

Local Number of species

People Animals

E N E N
(n¼ 13) (n¼ 20) (n¼ 12) (n¼ 21)

Carão 6 17 8 18
Letreiro 9 5 5 10
Fig. 2. The number of exotic and native species used against parasites affecting
N¼ Native; E ¼ Exotic. humansn and animalsnn at two rural communities in northeastern Brazil.

Table 3
An analysis of variance of the knowledge of anti-parasitic uses of plants in humans exhibited by two rural communities in northeastern Brazil.

Local/Total diversity of uses Uses

General (n¼ 33) People Animals

(people and animals) (n¼ 6) (n ¼29)
x7 SDn x7 SDn x7 SDn

Native Exotic Native Exotic Native Exotic

Carão (n¼ 28) 2.337 1.79a 5.447 3.43b 1.23 7 0.56a 2.677 1.50b 2.94 71.89a 3.87 7 2.30a
Letreiro (n¼15) 2.077 1.65a 2.90 7 4.18a 1.20 7 0.44a 2.007 1.33a 2.08 71.50a 1.25 7 0.50a

n
Equal letters in the same row correspond to identical use (overall, humans and animals) and the absence of significant differences between the data based on a
Kruskal–Wallis test (po 0.05). SD: standard deviation.
 F.d.S. Silva et al. / Journal of Ethnopharmacology 155 (2014) 1332–1341 1339

Table 4 Damme (2011) observed many species from this family, which
The richness of exotic and native species indicated to fight against ecto- and were associated with several types of chemical compounds,
endoparasites affecting humans and animals in two rural communities in north-
demonstrating their relevance in veterinary medicine, as natural
eastern Brazil.
pesticides and in human medicine. According to Seigler (1994), the
Number of cited species wide scope of medicinal uses attributed to Euphorbiaceae might
be because of its broad variety of secondary metabolites, including
Ectoparasites Endoparasites alkaloids, tannins and terpenes. Seigler's data indicate that species
Exotic Native Exotic Native
belonging to Euphorbiaceae might exhibit anti-parasitic properties.
Some studies have been conducted on several traditional
C L C L C L C L populations to document the presence of species with potential
anti-parasitic properties (Hammond et al., 1997; Farooq et al.,
General 6 4 18 8 6 8 18 7
2008). For instance, Diehl et al. (2004) consider the ethnobotanical
Animals 4 4 15 8 6 2 8 3
People 2 – 8 1 6 9 11 4 approach as advantageous for listing species with anti-helminthic
activity. When assessing ethno-veterinary practices used to con-
C ¼Carão community; L¼ Letreiro community. trol chicken parasites in Eastern Cape, South Africa, Mwale and
Masika (2009) observed that an increase in the incidence of
corresponding diseases led the local population to locate and use
Table 5
The efficiency of Croton blanchetianus Baill. and Nicotiana glauca Graham extracts plants to combat them. In Kenya, one of the main ectoparasites
against tick Rhipicephalus microplus (Canestrini, 1887) larvae. that affects cattle, the ticks, are controlled using extracts from
traditional plants (Njoroge and Bussmann, 2006).
Concentration (mg/ml) Mortality (%) Using plants might be particularly relevant among populations
Croton blanchetianus Nicotiana glauca
far from urban areas (Vandebroek et al., 2004). Mafimisebi et al.
(2012) observed that even the distance from veterinary healthcare
250 – 63.27 services might influence the use of medicinal plants. This result
200 44.00 51.84 might account for the fact that the residents of Letreiro, which is
150 36.21 57.31
closer to Altinho, had an initial resource of conventional drugs
100 42.80 46.46
75 25.94 44.54 when initial outbreaks of stable fly disease appeared following the
50 11.31 – introduction of infested cattle. Proximity to an urban area might
25 2.44 – also explain the narrow scope of plants known for that purpose by
10 0.00 –
the local community.

4.2. Are the diversity and number of uses attributed to exotic species
Table 6
to combat parasitic diseases greater compared to native species?
The product efficacy (PE) of Croton blanchetianus Baill. and Nicotiana glauca Graham
extracts relative to Rhipicephalus microplus engorged females.
Within the set of plants reported as anti-parasitic agents for
Croton blanchetianus Nicotiana glauca humans and animals, the number of exotic species was not
Concentration mg/ml remarkable compared to native ones. The presence of such species,
% PE % PE
according to Medeiros et al. (2013), is a reflection of the natural
200 31.87 53.89 progression of pharmacopeias. Therefore, to interpret the presence
150 25.26 29.14 of exotic species as a positive or negative phenomenon, scientists
100 21.55 22.64 must investigate their corresponding context. The results of the
50 18.30 16.37
10 8.33 9.27
present study show that Carão residents indicated exotic species
for a larger number of parasitic diseases compared to native
species. That result is notable because although there were fewer
mortality rate at 100 mg/ml was low. Overall, the results indicated exotic compared to native species in that community, the former
that the larval mortality rate was gradual at lower concentrations were more versatile and fulfilled a broader range of therapeutic
(Table 5). Both Croton blanchetianus and Nicotiana glauca were targets. This fact might indicate that exotic species were tested
only positive in concentrations less than 100 and 50 mg/ml. against parasitic diseases for which no native plant was indicated,
The EC50 concentrations for Nicotiana glauca and Croton blan- e.g., furuncular myiasis and fleas. Similar results were not detected
chetianus extracts were 91 and 67 mg/ml, respectively. The mod- at Letreiro, possibly because of its closer proximity to an urban
erate acaricidal activity of them was reinforced by the results from area, which facilitated the use of conventional drugs at the
the engorged female test (Table 6). Both extracts were most expense of medicinal plants, as indicated above.
effective during the reduction of oviposition and hatchability in The data collected in the present study do not allow us to infer
high concentrations conclusions of how the exotic species became included in the
repertoire of anti-parasitic methods. Perhaps exotic plants were
introduced to broaden the scope of the local medical system and
4. Discussion increase its versatility, as Medeiros et al. (2013) suggested. Once a
disease category is attributed to a wide variety of exotic species,
4.1. The diversity of plants used as anti-parasitic agents the latter might reduce the pressure of using native species. In a
recent study conducted in South Africa, exotic species performed
Family Euphorbiaceae was distinct in terms of the number of an important role in reducing the pressure of using native species
species indicated at both communities, which reinforces its (Semenya et al., 2012).
medicinal and veterinary potential. Euphorbiaceae was also nota- The diversity of native species used as anti-parasitic agents did
ble in other studies conducted at communities in the Caatinga area not appear to be affected by the presence of exotic species. Even
(Albuquerque et al., 2007) and outside Brazil (Gakuya et al., 2012). when the data corresponded to a specific spatial and temporal
In a review of the medicinal use of Euphorbiaceae, Mwine and Van setting, they did not support the hypothesis that the presence of
1340 F.d.S. Silva et al. / Journal of Ethnopharmacology 155 (2014) 1332–1341
exotic species in a pharmacopeia might lead to the loss of knowl-
edge relative to the therapeutic uses of native species (Amorozo,
2002). The presence of exotic species might be a reflection of a
cultural adaptation to control the spread of disease within a given
population (Thomas, 2001). Such an adjustment in the use of
plants performed by different populations was identified in a
review of the medicinal Mapuche Fwa in Argentina and Peru
(Morales and Ladio, 2009). The results of that study showed that
the number of exotic species recently increased is included in
pharmacopeias to treat novel diseases.
Another notable role that exotic species might have in traditional
medical systems is to share the pressure of using native plants. A
recent study conducted in South Africa observed that exotic species
might significantly reduce the pressure of using native species
(Semenya et al., 2012). These data support the utilitarian redundancy
model suggested by Albuquerque and Oliveira (2007), which states
that the pressure of use decreases in the presence of numerous
species used for the treatment of an identical therapeutic target.
Therefore, the presence of exotic species in a pharmacopeia might
represent an adaptive strategy of socio-ecological systems because
the global reduction of native forests makes access to “native
medicinal plants” more difficult. Therefore, human populations
might have recourse to exotic species, most of which are cultivated
close to their homes to optimize foraging. Harvest time is a variable
that might be accounted for when harvesting medicinal plants by
human communities (Soldati and Albuquerque, 2012).
Therefore, the study of the diversity of native relative to exotic
species per disease category might provide relevant data to
understand the patterns of knowledge and medicinal use of such
species and changes in pharmacopeias. The results of the present
study suggest that the introduction of exotic species might
diversify the therapeutic system by (1) increasing the versatility
of the category of use and (2) enabling the treatment of parasitic
diseases for which no native species is available.
4.3. Is there specificity for the use of native or exotic plant species to
fight some parasitic diseases?
Although the scope of use exhibited some overlap for exotic and
native species, each was the only species indicated to fight some
parasitic diseases. This result, in addition to the fact that a wide variety
of both types of species are indicated for diseases, might suggest that
over time, and as a function of adjustments within the medical system,
exotic species are included in the repertoire of plants that are useful to
fight parasitic diseases for which few native species are known. An
increase in the number of plants available to treat parasitic diseases
most likely makes the control of such diseases more certain because
whenever one species is scarce, another plant might be used. In the
case of the Caatinga area, which exhibits seasonality in its climate,
exotic species might control the incidence of some diseases in the dry
season when the required native species are not available. However,
that hypothesis must be tested.
Overall, it should be noted that some native species were attributed
more uses against ectoparasites compared to exotic species, whereas
the latter were attributed more uses against endoparasites compared
to the former, thus showing that some species had a more relevant
role in the treatment of some diseases. Albuquerque et al. (2009)
observed that a wide variety of exotic plants were included in the
treatment of diseases in humans but not for veterinary use, which
disagrees with the results of the present study.
4.4. Acaricide potential of plant species and animal health care
The wide variety of species indicated as acaricide agents in both
communities showed that the residents had access to traditional
medicine for animal health care. Traditional medicine was not the
only option because some informants reported a preference for
conventional drugs, which they judged to be more efficient and
practical. Attempts to control parasites are triggered by losses in
productivity and the transmission of pathogenic agents that are
fatal for tick-infested livestock (Graf et al., 2004), whereas the use
of conventional drugs often increases the number of cattle tick
resistant populations (Junior and Oliveira, 2005).
Research with that focus is necessary, possibly as a function of the
absence of studies with an ethno-veterinary focus. According to a
review study conducted by Alves et al. (2010) relative to the plants
used for animal health care in Latin America, few records of
ixodicides are available. Few studies conducted in Brazil have
recorded plants used as acaricides, particularly in the Caatinga.
Despite their wide biological and cultural diversity, few ethnobota-
nical and pharmacological studies have been conducted in such areas
in general (Albuquerque et al., 2007) or have targeted medicinal
plants in particular, although such studies are highly relevant to the
discovery of new pharmaceutical products (Almeida et al., 2006).
The predominance of native species in both communities and
the efficiency exhibited by some plants against cattle tick indicate
their potential relevance. Among the plants assessed for such
purpose in the present study, only two native species (Nicotiana
glauca and Croton blanchetianus) exhibited ixodicide activity in the
LPT and engorged female test. Although the uses of those plant
species were not widely known by the residents in the commu-
nities, the results of the present study indicate the relevance of
including scarcely indicated species because their uses might have
always been restricted to the community members who indicated
them. It is noteworthy to observe that among the species indicated
with possible acaricide activity in the communities, tests assessing
the activity of raw extracts were only reported relative to Melia
azedarach in the literature (Borges et al., 2003). That extract
proved efficient on in vitro larvae and in the engorged female
immersion test, which was shown by larval death and the
reduction of egg production.
Based on the data described above, it might be concluded that
including exotic species to fulfill therapeutic indications of native
species is not systematically based on efficiency criteria. Inefficient
species might have indirect actions against parasites, e.g., by
repelling them. The species indicated in both communities might
possibly be efficient during the tick larval stage only because
engorged females migrate to the soil, which the informants might
have incorrectly interpreted as an effect of the plants. The extracts
that had no acaricidal activity may be being influenced by the
extraction method, which can vary among the species. It is
important to emphasize that the results of this study may not be
reflected on the different ways of local use.
Regarding the extracts that exhibited promising acaricide
active, it would be notable to investigate their active principles
separately. In a study of Nicotiana glauca toxicity, Furer et al. (2011)
identified a toxic active principle, anabasine, which is a pyridine
alkaloid; however, it is not yet known whether anabasine is
associated with the larvicidal effect of that plant.
Acknowledgments
The authors are grateful to the Carão community in face of the
receptive welcome, like, the City of Altinho, in the person of the
Secretary of Agriculture, Mr. Miguel Andrade Jr., for the logistical
support. The Health Workers from Carão Community, Mr. Inaldo and
Mr. Alexandre, for the support. The following researchers from the
Laboratory of Applied and Theoretical Ethnobiology (LEA) for support
in ethnobotanical data collection and researchers from the Laboratory
Animal Parasitology (LPA). To CNPq (471989/2012-6) and FACEPE
(APQ-1264-2.05/10) for financial support.
 F.d.S. Silva et al. / Journal of Ethnopharmacology 155 (2014) 1332–1341
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