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Journal of Ethnopharmacology 110 (2007) 235–249

Insect management products from Malian traditionalmedicine—Establishing systematic criteria for

their identification

Ashley D. Lehman a, Florence V. Dunkel a,∗, Robyn A. Klein a, Saidou Ouattara b,Drissa Diallo c, Kadiatou Toure Gamby b, Moussa N’Diaye b

a Department of Plant Sciences and Plant Pathology, 119 Plant BioScience Building, Montana State University,Bozeman, MT 59717-3150, United States

b Institut d’Economie Rurale, BP 258, Rue Mohamed V, Bamako, Malic Department of Traditional Medicine, Institut National de Recherche en Sante Publique (INRSP), BP 1746, Bamako, Mali

Received 2 March 2006; received in revised form 10 May 2006; accepted 10 June 2006Available online 21 October 2006

bstract

In material-resource poor countries like Mali, traditional practices incorporate the use of plants for medicinal purposes. Ethnobotanical researchas documented traditional uses of plants, while concomitant studies by natural product chemists, ethnobotanists, and microbiologists have verifiedhe efficacy of using traditional medicinal plants that have proven antimicrobial activity. These plants may also be used to protect agriculturalrops pre-harvest and post-harvest from insect herbivory. In Mali, subsistence farmers, regional scientists, and extension specialists rely on locallants for many medicinal needs and are amenable to using traditional plant materials for insect pest management. The goal of this research was toevelop Integrated Pest Management (IPM) strategies using Malian traditional medicine as a discovery lead. The discovery premise was based ondentifying plants through a matrix approach utilizing agricultural scientists, traditional practitioners, and subsistence farmers. We hypothesizedhat plants used in traditional medicine with antimicrobial activity lead to potential insect pest management agents. To test our hypothesis, weeveloped a four-step process for selecting Malian plant species. Seven criteria were selected to create a systematic matrix to identify the mostromising plant materials for practical, affordable, ecologically-sound insect management by Malian farmers. In the first step of the process, we

eveloped a list of 294 medicinal Malian plant species which were evaluated using the matrix. Sixty-seven plant species met our main criteria. Afterhe environmental soundness of these species was evaluated using four minor criteria, 50 species emerged from this pre-chemical, pre-bioassayrocess for further consideration in IPM programs in Mali.

2006 Elsevier Ireland Ltd. All rights reserved.

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eywords: Subsistence farmers; Traditional medicine; Antimicrobial; Adaptog

. Introduction

Mali is an ethnically and politically stable African coun-ry where inhabitants are primarily subsistence farmers. Millet,orghum, rice, maize, and cotton are among the major crops,hile cowpeas, tomatoes, squash, okra, peppers, and hibis-

us are important traditional garden crops. Green beans arerecently discovered cash crop that subsistence farmers are

ttempting to sell in organic European markets. Between 1989

∗ Corresponding author. Tel.: +1 406 994 5065; fax: +1 406 994 7600.E-mail address: ueyfd@montana.edu (F.V. Dunkel).

Ii(2Mio

378-8741/$ – see front matter © 2006 Elsevier Ireland Ltd. All rights reserved.oi:10.1016/j.jep.2006.06.016

ytoecdysteroid; Pest management

nd 1993, more than 10,000 farmers were trained in Integratedest Management (IPM) techniques as a safer, less expensive,nd more environmentally-sound system of pest managementDiarra and Kamissoko, 1993). Since 1993, Mali’s agriculturalrograms have focused on improving the adoption rate of IPMechniques. A participatory process for developing effectivePM methods was created by Malian and US scientists work-ng with subsistence farmers in collaborative on-farm researchErbaugh et al., 1995–1996; Moore et al., 2001; Gamby et al.,

002a,b). For dissemination of the resulting IPM “packages,”alians used farmer field schools (a farmer-to-farmer teach-

ng and learning process) (Gamby et al., 2002c) and a seriesf sets of posters for individual learning by literate, as well

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36 A.D. Lehman et al. / Journal of Et

s non-literate, Bambara farmers (Gamby and Dunkel, 2001).n our on-farm IPM research and dissemination, we noticedhat frequent suggestions were made by Malian scientists thatocal plant materials were available for pest management. Thisnformation spawned relatively rapid adoption of these mate-ials into the on-farm research and then into the IPM trainingackages.

Passing traditional practices of personal health and insectest management to the next generation is an ancient customn most indigenous cultures (International Council for Science,002). Knowledge of the efficacy of indigenous plant medicines now broadly supported by scientific research and has beenhown to be crucially important to pharmacology as well aso agriculture (Zhang, 2002; Newman et al., 2003; Strobel andaisy, 2003; Buenz et al., 2005). Paying attention to clues of

ndigenous traditional practices has uncovered novel pest man-gement ideas such as the use of Tetradenia riparia Hochst.odd. (Lamiaceae) (Dunkel et al., 1990; Weaver et al., 1992)nd Ocimum canum Sims. (Lamiaceae) (Weaver et al., 1994a)o protect stored beans against bruchids. Recently, scientists haveeen reporting consultations with traditional healers (Belmainnd Stevenson, 2001). For example, in Mali, farmers often com-ine local plants used in traditional medicine and apply themo crops for pest management. One practitioner reported that heombines powdered Ziziphus mauritiana Lam. (Rhamnaceae)ith Vitellaria paradoxa C.F. Gaertn. (syn. Butyrospermumaradoxum C.F. Gaertn. Hepper) (Sapotaceae) to produce aore effective insecticide (Cisse, 2004). Local farmers observed

hat Vitellaria paradoxa has a stronger insecticidal effect whenounded into a paste instead of a powder. Malian scientists arepplying this traditional knowledge to pesticidal research forrotection of Sorghum bicolor (L.) Moench (Poaceae) (Traore,002). Laboratory studies confirm that plant preparations varyn effectiveness depending on preparation technique and endse of insecticide (Dunkel, 1994, 1997; Dunkel and Sears,998).

There seems to be no organized, stepwise methodologyeported to identify traditional medicinal plants that may havensect pest management activity. The reported primary processessed to identify new materials for IPM have been the labori-us, high-throughput screening of mass-produced combinatorialhemical libraries (Newman et al., 2003) and insect bioassays.ajor pharmaceutical and pest management product compa-

ies continue to de-emphasize natural products programs, andhe number of new active substances from mass-screening ofombinatorial libraries hit a 20-year low of 37 in 2001 andontinued to decline (Class, 2002). Nevertheless, companiesnvolved in natural product drug discovery and possibly thosenvolved in natural product insecticide or insect bioactive mate-ials discovery use a highly organized approach to reduce timeo find a biologically active compound and put it into drug orest management development (Heinrich et al., 2004). Severalompanies now market natural product libraries and banks of

icrotiter plates with pure natural products in individual wells atknown concentration. To rapidly identify local plants for use byubsistence farmers worldwide, and incorporate products fromhese plants into local integrated pest management research, a

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armacology 110 (2007) 235–249

impler method of identifying potential bioactive candidates iseeded.

Exploration of local medicinal plants as a method to iden-ify novel, plant-based insect management products is not aotally new idea (Chariandy et al., 1999; Jayasekara et al., 2005).or example, Ageratum conyzoides L. (Asteraceae) has beensed as an antimicrobial in Chinese medicine as well as beingntercropped in citrus orchards to increase predatory mite pop-lations (Kong et al., 2005). There are several main modesf action in plant-based medicine that are also effective innsects. For example, plants defending humans against harm-ul bacteria, protozoa, and fungi, may in turn, disrupt or killpecific microorganisms that serve as mutualistic microorgan-sms on which pest insect species depend for life itself (Bigit al., 2004; Bostanian et al., 2005). Other pest insect speciesepend on microorganisms only during times of stress (Dunkel,969). Local scientists, in collaboration with Malian subsis-ence farmers can identify the most likely plant candidates usingow-tech methods with these plants to protect crops againstnsects. We suggest a process markedly different from testingombinatorial libraries, and a process that preceeds laboratoryioassays.

We therefore, tested the hypothesis that: (a) plant species withnsect management potential may have already been identifiedmong the indigenous traditional medicines of Mali and (b) atepwise matrix process can differentiate medicinal plants withhe potential for insect management. Our matrix process createsdatabase of plant species for laboratory and field evaluation.ur objective is to develop effective, locally available, plant-ased insect pest management products that can be producedith low labor input and that will be accepted and used by Malian

ubsistence farmers.

. Methodology

.1. Overview

A series of steps was designed to consolidate a searchf the peer-reviewed literature and interviews with agricul-ural scientists, traditional practitioners, and local subsis-ence farmers (Fig. 1). Plant species were selected based onhree main criteria: traditional medicinal use; antimicrobialctivity; and insect defense activity. A list resulted in plantpecies likely to have insect management activity in labora-ory and field investigations (Table 2). Species that have par-icularly environmentally-sound profiles were noted within theist.

.2. Step 1. Search peer-reviewed literature for Malianraditional plant use and bioactivity; interview Malianraditional practitioners; interview scientists; interviewarmers; search literature for selection criteria used todentify insect pest management mechanisms of action

The first step involved five procedures conducted simultane-usly over 2 years resulting in an initial pool of Malian plantpecies. Step 1a required a search of peer-reviewed literature

A.D. Lehman et al. / Journal of Ethnopharmacology 110 (2007) 235–249 237

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ig. 1. Method for selection of medicinal plants of Mali with pest managementor potential of managing insect pests.

or documentation of traditional use, antimicrobial and/or anti-nsect activity of plants found in Mali. Step 1b was to interviewraditional medicine practitioners in Mali and request sugges-ions on plant species they use or recommend. Step 1c was tonterview Malian scientists to gather their recommendations oflant species. The interviewer clarified to the interviewee thatll information was meant to be employed by the subsistencearmers of Mali. The interviewer was careful not to coerce thenterviewees. An individual interview was performed and theollowing questions were asked:

. What are the strongest antibacterial plants used in Bamako,Mali?

. Which plant species are used for pesticides against cropinsects?

. What are the medicinal plants used as an antibiotic or anti-fungal in Bamako, Mali?

rwan

tial: a four-step process to identify local, plant-based materials to be evaluated

. How are these plant medicines prepared and applied?

. What part of the plant is used?

. What is the local Bambara name for the plant species?

Dr. Drissa Diallo, Head of the Department of Traditionaledicine in the National Institute of Public Health Research

INRSP), and Saidou Ouattara, the medicinal plant specialist atnstitut d’Economie Rurale (IER), were consulted concerningocal medicinal and traditional uses. Step 1d was to interview

alian farmers for similar recommendations of plants to add tour initial list. This survey was informal and included Malian sci-ntists and technicians who provided translation from Bambara.ombinations of scientist and farmer-derived information was

eceived, such as from Malian weed biologist, Moussa N’Diaye,ho is testing a natural pesticide which has reduced Striga

nd increased crop production. This pesticide is a mixture of aon-native plant, Azadirachta indica A. Juss. (Meliaceae), and

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Table 1Examples of plants with microbe defense and insect defense activity

Species, common name, and family Microbe defense activity Insect defense activity

Acorus calamus L., calamus (Araceae) Oil, medicinal and antimicrobial (Rani et al., 2003) Oil, insecticidal (Rani et al., 2003)Allium sativum L., garlic (Liliaceae) Extract and essential oil inhibits mycelial growth and/or spore germination

(Huang and Chung, 2003)Insecticidal (Huang and Chung, 2003)

Amorpha fruticosa L., false indigo (Fabaceae) Rotenone in seeds, roots, leaves antimicrobial (Gao et al., 2003/2004) Rotenone in seeds, roots, leaves; controls bruchids (Gao et al., 2003/2004)Anacardium occidentale L., cashew (Anacardiaceae) Gum exudates vs. Aspergillus flavus, Colletrotrichum musae, Verticillium sp.

(Marques et al., 1992); methanol bark extract active broad spectrumantibacterial (Akinpelu, 2001)

Oviposition deterrent for Callosobruchus maculatus (Echindu, 1991; Marqueset al., 1992); feeding deterrent of larval Crimissa cruralis (Marques et al.,1992); insecticidal for Aedes aegypti larvae (de Mendonca et al., 2005)

Anethum graveolens L., dill (Apiaceae) Antimycobacterial (Stavri and Gibbons, 2005) Volatile oils active against Lucilia sericata (Mazyad et al., 1999);Parasarcophaga dux (Khalaf, 2004)

Annona glabra L., pond apple (Annonaceae) Seed, bark, roots, fruit: antimicrobial, antimalarial (Rupprecht et al., 1990) Ethanol stem extract larvicidal for Aedes aegypti (de Mendonca et al., 2005)Artemisia tridentata Nutt. spp. vaseyana, sage (Asteraceae) Traditional use: colds, pneumonia, tuberculosis (Hart, 1976; Dunkel and

Sears, 1998)Fumigative adulticide (Dunkel and Sears, 1998)

Azadirachta indica A. Juss, neem (Meliaceae) (easily cultivated) Inhibits mitosis in protozoa (Fritzsche and Cleffmann, 1987); antibacterialagainst dental caries (Pai et al., 2004)

Antifeedant (Radcliffe et al., 1990); growth regulator, oviposition deterrent(Jenkins et al., 2003); reproductive hormone disruption, inhibition ofoogenesis (Rembold and Sieber, 1981a); neuroendocrine control ofmetamorphosis (Redfern et al., 1981); ecdysis (Mordue Luntz et al., 1986)

Brassica spp., mustard (Brassicaceae) Extract and essential oil inhibits mycelial growth and/or spore germination(Huang and Chung, 2003)

Insecticidal (Huang and Chung, 2003)

Cassia (species not specified) Extract and essential oil inhibits mycelial growth and/or spore germination(Huang and Chung, 2003)

Insecticidal (Huang and Chung, 2003)

Cinnamomum zeylanicum Ulrich, cinnamon (Lauraceae) Volatile oil fraction causes stasis growth in Aspergillus flavus, inhibitsEscherichia coli growth (Lopez et al., 2005); inhibits mycelial growth and/orspore germination (Huang and Chung, 2003)

Oral adulticide: Rhyzopertha dominica (Dunkel et al., unpublished; Huangand Chung, 2003)

Clitoria ternatea L., butterfly pea (Fabaceae) Finotin inhibits growth of Rhizoctonia solani, Fusarium solani,Colletotrichum lindemuthianum, Xanthomonas axonopodis pv. phaseoli(Kelemu et al., 2004)

Finotin inhibits bruchids, Zabrotes subfasciatus, Acanthoscelides obtectus(Kelemu et al., 2004)

Mentha rotundifolia (L.) Huds., Moroccan mint (Lamiaceae) Essential oil, Aspergillus niger, Escherichia coli, Bacillus subtilus (El-Archet al., 2003)

Essential oil: Rhyzopertha dominica, Sitophilus oryzae (El-Arch et al., 2003)

Monarda fistulosa L., horsemint (Lamiaceae) Inhibits growth of Staphylococcus aureus (Rogosca and Rogosca, 2000) Insect repellant (Hart, 1976); fumigative adulticide (Weaver et al., 1995)Ocimum canum Sims., African mint (Lamiaceae) Fungitoxic against Pythium spp. (Pandey and Dubey, 1994) Fumigative and contact adulticide (Weaver et al., 1991, 1994a)Olea sp. L., olive (Oleaceae) Oil inhibits mycelial growth and/or spore germination (Huang and Chung,

2003)Hydrolytic compounds insecticidal (Huang and Chung, 2003)

Origanum sp. L., oregano (Lamiaceae) Extract and essential oil inhibits mycelial growth and/or spore germination(Huang and Chung, 2003)

Insecticidal (Huang and Chung, 2003)

Ricinus communis L., castor (Euphorbiaceae) Essential oil inhibits mycelial growth and/or spore germination (Huang andChung, 2003)

Oviposition deterrent, ovicidal, insecticidal in Callosobruchus chinensis(Upansani et al., 2003); insecticidal (Huang and Chung, 2003)

Syzygium aromaticum (L.) Merr. & L.M. Perry, clove (Myrtaceae) Volatile fraction inhibits growth in Aspergillus flavus, Escherichia coli,Bacillus cereus, Candida albicans, Yersinia enterocolitica (Lopez et al.,2005)

Inhibited growth in Culex pipiens larvae (El Hag et al., 1999); repelled threespecies of mosquito (Trongtokit et al., 2005)

Tagetes minuta L., marigold (Asteraceae) Antibacterial: Bacillus subtilis, Escherichia coli, Pseudomonas aeruginosa,Staphlococcus spp. (Tereschuk et al., 1997)

Contact adulticide (Weaver et al., 1994c)

Tetradenia riparia Hochst. Codd., umuruvumba (Lamiaceae) Antimicrobial (Van Puyvelde, 1986; Dunkel et al., 1990) Contact adulticide (Dunkel et al., 1990; Weaver et al., 1994b)Thujopsis dolabrata var. hondai Makino, aomori hiba (Cupressaceae) Antifungal: wood rotting fungi (Okabe et al., 2004) Termites (Okabe et al., 2004)Zingiber officinale Roscoe, ginger (Zingiberaceae) Antibacterial against Staphylococcus aureus, S. pyogenes, S. pneumoniae,

and Haemophilus influenzae (Akoachere et al., 2002)Repellent against Bemisia argentifolii (Zhang et al., 2004)

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Table 2Malian plant species that meet the Main Criteria (traditional use, antimicrobial activity, insect management activity), and the Minor Criteria, exceptions notedFamily and species Traditional use Microbe defense activity Insect defense activity

AizoaceaeGlinus oppositifolius (L.) Aug. DC. Headache, rheumatism, fevers (Iwu, 1993); pain, inflammation, fever,

malaria, wounds, diarrhea, intestinal parasites, skin disorders(Inngjerdingen et al., 2005)

Antifungal, molluscicidal (Diallo et al., 2001) Larvicidal against Aedes aegypti, Anopheles gambiae, Culexquinquefasciatus (Diallo et al., 2001)

AmaranthaceaeAchyranthes aspera L.a Arthritis, muscular pains (Iwu, 1993) Ecdysteroid positive (Lafont et al., 2003)Amaranthus spinosus L. Gastrointestinal disorders, hemorrhoids, arthritis (Iwu, 1993) Ecdysteroid positive (Lafont et al., 2003)Amaranthus viridis L. Coughs, purgative (Iwu, 1993) Ecdysteroid positive (Lafont et al., 2003)Celosia trigyna L. Vermifuge (Adamu et al., 2005) Inhibits Pseudomonas aeruginosa and Escherichia coli (Adamu et al.,

2005)Anacardiaceae

Anacardium occidentale L. Arthritis, colds (Iwu, 1993); arterial hypotension (Ouattara, 1997) Gum exudate inhibits Aspergillus flavus, Colletrotrichum musae,Verticillium sp. (Marques et al., 1992); broad spectrum antibacterial(Akinpelu, 2001)

Oviposition deterrent to Callosobruchus maculatus (Echindu, 1991;Marques et al., 1992); feeding deterrent of larval Crimissa cruralis(Marques et al., 1992); insecticidal to Aedes aegypti larva (deMendonca et al., 2005)

Spondias mombin L. Diarrhea (Iwu, 1993); wounds (Diallo et al., 2002; Inngjerdingen etal., 2004)

Insecticidal (Pieters and Vlietinck, 2005)

AnnonaceaeAnnona senegalensis Pers. Parasites (Ouattara, 1997); wounds, (Diallo et al., 2002;

Inngjerdingen et al., 2004); diarrhea, gonorrhea (Adamu et al., 2005)Antimicrobial (Adamu et al., 2005)

ApocynaceaeAdenium obesum (Forssk.) Roem. & Schult. Wounds, ulcers, caries, cardiac tonic (Iwu, 1993) Antimicrobial (Adamu et al., 2005)

AristolochiaceaeAristolochia albida Duch. Stomach tonic, malarial fevers, parasites (Iwu, 1993) Antimicrobial (Adamu et al., 2005)

AsclepiadaceaeCalotropis procera (Aiton) W.T. Aiton Conjunctivitis, wounds, venereal disease (Iwu, 1993); wounds

(Inngjerdingen et al., 2004)Antimicrobial (Adamu et al., 2005)

AsteraceaeVernonia colorata (Willd.) Drakec Febrifuge, tonic (Iwu, 1993); malaria (Ouattara, 1997); wounds

(Diallo et al., 2002)Inhibits gram positive bacteria (Rabe et al., 2002)

BignoniaceaeNewbouldia laevis (P. Beauv.) Seem. ex

BureauFebrifuge, wounds, stomachache (Iwu, 1993); dysentery, worms,sexually transmitted diseases (Burkill, 1985)

Inhibited Bacillus subtilis and Escherichia coli, antifungal (Gafner etal., 1996)

Highly effective against adult nematode, Haemonchus contortus(Hounzangbe-Adote et al., 2005)

Stereospermum kunthianum Cham. Skin eruptions, venereal disease, wounds, coughs (Iwu, 1993);wounds (Diallo et al., 2002; Inngjerdingen et al., 2004)

Antimicrobial (Adamu et al., 2005)

CapparaceaeCrataeva adansonii DC. syn. C. religiosa

G. Forst.Earache, wounds (Iwu, 1993) Ecdysteroid positive (Lafont et al., 2003)

CelastraceaeMaytenus senegalensis (Lam.) Exell Dysentery, colic (Iwu, 1993); wounds (Diallo et al., 2002); eye

infections (Matu and van Staden, 2003)Antibacterial (Matu and van Staden, 2003)

Pilostigma thonningii (Schum.) M. Redh Toothache, chest pain (Adamu et al., 2005) Inhibits Pseudomonas aeruginosa and Escherichia coli (Adamu et al.,2005)

ChenopodiaceaeChenopodium ambrosioides L. Wounds (Diallo et al., 2002) Ecdysteroid positive (Lafont et al., 2004)

CochlospermaceaeCochlospermum tinctorium A. Richa Burns, stomachache, urethritis, diarrhea (Iwu, 1993); hepatitis

(Ouattara, 1997); wounds (Diallo et al., 2002); malaria,hepatoprotective (Nergard et al., 2005); schistosmiasis (Adamu et al.,2005)

Antimicrobial (Adamu et al., 2005)

CombretaceaeAnogeissus leiocarpus (DC.) Guill. & Perr.c Infections, hepatitis (Ouattara, 1997); wounds (Diallo et al., 2002;

Inngjerdingen et al., 2004); dysentery, coughs, diarrhea (Adamu et al.,2005)

Antimicrobial (Sanogo et al., 1998; Adamu et al., 2005) Antihelminthic, not insectical (Hammond et al., 1997)

Combretum molle R. Br. ex G. Don Wounds (Diallo et al., 2002) Antibacterial (Geyid et al., 2005)

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Table 2 (Continued )

Family and species Traditional use Microbe defense activity Insect defense activity

Guiera senegalensis J.F. Gmel. Wounds (Diallo et al., 2002; Inngjerdingen et al., 2004); cough,syphilis, diarrhea, leprosy (Adamu et al., 2005)

Inhibits Pseudomonas aeruginosa and Staphylococcus aureus(Sanogo et al., 1998; Adamu et al., 2005); antimalarial activity(Ancolio et al., 2002)

Pteleopsis suberosa Engl. & Dielsc Wounds (Diallo et al., 2002) Moderate bacterial activity against Staphylococcus aureus (Sanogo etal., 1998)

Terminalia avicennioides Guill. & Perr. Wounds (Diallo et al., 2002); dysentery (Adamu et al., 2005) Inhibits Pseudomonas aeruginosa and Escherichia coli (Adamu et al.,2005); inhibits Staphylococcus aureus (Akinyemi et al., 2005)

ConvolvulaceaeIpomoea batatas (L.) Poir Purgative, tonic (Iwu, 1993) Ecdysteroid positive (Lafont et al., 2004)

EbenaceaeDiospyros mespiliformis Hochst. ex A. DC. Fevers, dysentery, vermifuge (Iwu, 1993); hypertension (Ouattara,

1997); wounds (Diallo et al., 2002)Antibacterial (Sanogo et al., 1998); inhibits Proteus mirabilis (Adamuet al., 2005)

EuphorbiaceaeAcalypha wilkesiana Mull. Arg.a Antimycotic, wounds (Iwu, 1993) Inhibits Staphylococcus aureus (Akinyemi et al., 2005)Bridelia ferruginea Benth. Coughs, diabetes, external application (Iwu, 1993); wounds (Diallo et

al., 2002)Antimicrobial (Akinpelu and Olorunmola, 2000; Talla et al., 2002)

Euphorbia balsamifera Aiton Anthelmintic (Iwu, 1993); wounds (Inngjerdingen et al., 2004) Antimicrobial (Adamu et al., 2005)Euphorbia hirta L.a Coughs, asthma, anthelmintic, stomachache, eye infections (Iwu,

1993); entamebiasis, (Ouattara, 1997)Antimicrobial (Adamu et al., 2005)

Jatropha curcas L. Fevers, veneral diseases, dysentery (Iwu, 1993); wounds (Diallo et al.,2002)

Inhibits Staphylococcus aureus and Escherichia coli (Adamu et al.,2005)

Ricinus communis L. Wounds (Iwu, 1993); constipation (Ouattara, 1997) Inhibits mycelial growth and/or spore germination (Huang andChung, 2003)

insecticidal (Huang and Chung, 2003); active against Callosobruchuschinensis oviposition deterrent, ovicidal, insecticidal (Upansani et al.,2003)

FabaceaeAbrus precatorius L. Bronchial diseases, vermifuge, trachoma (Iwu, 1993) Antimicrobial (Adamu et al., 2005)Arachis hypogaea L. Wounds (Diallo et al., 2002) Ecdysteroid positive (Lafont et al., 2004)Cassia occidentalis L. Malaria (Ouattara, 1997); ringworm (Adamu et al., 2005) Inhibits Proteus mirabilis and Escherichia coli (Adamu et al., 2005)Daniella oliveri Hutch. & Dalzielc Toothache (Adamu et al., 2005) Weak inhibition of P. mirabili, P. aeruginosa, Staphyloccocus aureus,

and Escherichia coli (Adamu et al., 2005)Insecticide (Tamboura et al., 1998; Traore, 2002)

Entada africana Guill. & Perr.c Hepatitis (Ouattara, 1997); wounds (Inngjerdingen et al., 2004) Antimicrobial (Adamu et al., 2005)Erythrina senegalensis DC. Jaundice (Adamu et al., 2005) Active against gram positive bacteria and methicillin resistant

Staphylococcus aureus (Kone et al., 2004)Parkia biglobosa (Jacq.) R. Br. ex G. Donb Hypertension, hepatitis (Ouattara, 1997); wounds (Inngjerdingen et

al., 2004)Inhibits Bacillus cereus, Staphylococcus aureus, Escherichia coli(Ouoba et al., 2005)

Pilostigma thonningii (Schum.) M. Redh Malaria, cough, dysentery, wounds, helminthiasis (Togola et al., 2005) Antibacterial (Togola et al., 2005) Caused larval paralysis in Haemonchus contortus (Togola et al., 2005)Tamarindus indica L. Wounds (Inngjerdingen et al., 2004) Antimicrobial (Adamu et al., 2005) Insecticidal (Araujo et al., 2005)

LoganiaceaeAnthocleista djalonensis A. Chev. Worms (Iwu, 1993) Staphylococcus, Escherichia coli (Togola et al., 2005)

MalvaceaeSida acuta Burm. f.a Wounds (Diallo et al., 2002) Ecdysteroid positive (Lafont et al., 2004)

MeliaceaeAzadirachta indica A. Juss.d Wounds (Inngjerdingen et al., 2004); malaria (Adamu et al., 2005) Inhibits mitosis in protozoa (Fritzsche and Cleffmann, 1987); dental

caries (Pai et al., 2004); antimicrobial (Adamu et al., 2005)Antifeedant (Radcliffe et al., 1990); growth regulator, ovipositiondeterrent (Jenkins et al., 2003); reproductive hormone disruption;inhibition of oogenesis (Rembold and Sieber, 1981a); neuroendocrinecontrol of metamorphosis (Redfern et al., 1981); ecdysis (MordueLuntz et al., 1986)

Trichilia emetica Vahl. Antiparasitic (Iwu, 1993); wounds (Diallo et al., 2002);gastrointestinal infections, fever, respiratory infections (Diallo et al.,2003); malaria, respiratory infections, intestinal worms (Germano etal., 2005)

Antibacterial, antifungal, antiviral (Champagne et al., 1992);antibacterial (Germano et al., 2005)

Insect antifeedant (Champagne et al., 1992)

Trichilia roka (Forssk.) Chiov.c Fever, malaria, wounds (Maiga et al., 2005) Lethal to schistosomula of Schistosoma haematobium (Sparg et al.,2000)

Antifeedent, Nakatana et al., 1985)

MoringaceaeMoringa oleifera Lam.d Diarrhea (Adamu et al., 2005) Inhibits Pseudomonas aeruginosa (Adamu et al., 2005)

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MyrtaceaePsidium guajava L. Dysentery, fevers, stomach tonic (Iwu, 1993); wounds (Diallo et al.,

2002)Inhibits Proteus mirabilis (Adamu et al., 2005)

Syzygium guineese (Willd) DC. Abdominal pain, carminative (Iwu, 1993) Antibacterial (Geyid et al., 2005)

NyctaginaceaeBoerhavia diffusa L.a Dysmenorrhea, jaundice, asthma (Iwu, 1993) Ecdysteroid positive (Lafont et al., 2004)

OleaceaeOlea europaea L. Inflammation (Iwu, 1993) Inhibits mycelial growth and/or spore germination (Huang and

Chung, 2003)Insecticidal (Huang and Chung, 2003)

Ximenia americana L. Wounds (Diallo et al., 2002; Inngjerdingen et al., 2004) Active against Enterococcus faecalis and Streptococcus pyrogenes(Kone et al., 2004)

Inhibited hatching of Clavigralla tomentosicollis (Fatope et al., 2000)

OpiliaceaeOpilia celtidifolia (Guill. et Perr.) Endl. ex

Walp.cHypertension, jaundice (Ouattara, 1997); wounds (Diallo et al., 2002;Inngjerdingen et al., 2004)

Anthelmintic (Togola et al., 2005)

PoaceaeCymbopogon citratus (DC.) Stapf Fevers, jaundice, diarrhea (Iwu, 1993) Larvicidal (Cavalcanti et al., 2004)

RhamnaceaeZizyphus mauritiana Lam. Wounds (Diallo et al., 2002; Inngjerdingen et al., 2004) Antimicrobial (Adamu et al., 2005)Zizyphus mucronata Willd. Colds, fevers (Iwu, 1993); gonorrhea (Adamu et al., 2005) Antimicrobial (Adamu et al., 2005)

RubiaceaeCrossopteryx febrifuga (Afzel. ex G. Don)

Benth.Fevers, antiviral (Iwu, 1993); hypertension, parasites (Ouattara,1997); wounds (Diallo et al., 2002)

Moderate activity against Staphylococcus aureus (Sanogo et al., 1998)

Mitracarpus scaber Zucc. ex Schult. &Schult. f.a

Dermatitis (Ouattara, 1997); sore throat, leprosy, wounds, dysentery(Jegede et al., 2005)

Active against Pseudomonas aeruginosa (Jegede et al., 2005)

Nauclea latifolia Sm. syn. Sarcocephaluslatifolius (Sm.) Bruce.c,d

Malaria (Ouattara, 1997); worms, fever (Onyeyili et al., 2001) Antimalarial (Onyeyili et al., 2001) Prevents nematode egg hatch (Onyeyili et al., 2001)

TiliaceaeGrewia mollis Juss. Wounds (Iwu, 1993); gonorrhea (Adamu et al., 2005) Antimicrobial (Adamu et al., 2005)

VerbenaceaeLippia adoensis Hochst. Fungal skin infections, wounds (Tadeg et al., 2005) Antimicrobial (Tadeg et al., 2005)Lippia chevalieri Moldenke Malaria (Ouattara, 1997) Antimicrobial (Bassole et al., 2003)Lippia multiflora Moldenke.d Pneumonia, fever, headache (Iwu, 1993) Antimicrobial (Bassole et al., 2003) Insecticidal (Koumaglo et al., 1996); pediculocidal, scabicidal

(Oladimeji et al., 2000)Vitex doniana Sweet Coughs, skin infections (Iwu, 1993); wounds (Diallo et al., 2002) Antimicrobial (Adamu et al., 2005)Vitex madiensis Oliv. Wounds (Diallo et al., 2002) Ecdysteroid positive (Lafont et al., 2004)

ZingiberaceaeZingiber officinale Roscoe Carminative, diuretic, antiemetic (Iwu, 1993) Antimicrobial (Adewunmi et al., 1990; Adamu et al., 2005; Thongson

et al., 2005)Oviposition deterrent (Echindu, 1991

ZygophyllaceaeBalanites aegyptiaca Del.b Wounds (Inngjerdingen et al., 2004) Antimicrobial (Adamu et al., 2005) Larvicidal against Culex pipiens (Chapagain and Wiesman, 2005)a Invasive tendencies (Dembele, 2005).b Protected status (Anon., 1999).c Toxic properties (Maiga et al., 2005).d Easily cultivated (Eugene et al., 1998; ASNAPP, 2003).

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armer-produced potash, made from the ash of millet, corn ororghum stalks (Martin et al., 2004). Step 1e involved searchinghe insect pest management literature to understand the various

echanisms of action of plant products used in insect pest man-gement (Regnault-Roger et al., 2005, and references within).or example, plant material and their extracts have been used

o: deter, kill, and interfere with feeding, growth and devel-pment, mating, oogenesis, oviposition, reproduction, molting,nd mutualistic bacterial and fungal organisms of the insectTable 1).

.3. Step 2. Create an initial list and select criteria

As there is no official flora of Mali, various plant lists,atabases, reports, theses, books, and journal papers were con-ulted to form a list of plant species used in traditional medicinen Mali that have antimicrobial or insect activity (Watt andreyer-Brandwijk, 1962; Koumare, 1968; Kerharo and Adam,974; Ayensu, 1978; Oliver-Bever, 1986; Malgras, 1992; Iwu,993; Ouattara, 1997; Burkill, 2000; Neuwinger, 2000; Traore,002; Lafont et al., 2004; CAB Direct, 2005). Additional speciesere added from interviews with Malian farmers, traditionaledicine practitioners, and scientists. The initial compiling of

lant species was accumulated through a literature search andnterviews. The result was a list of 294 plant species in 78 plantamilies. The Missouri Botanical Gardens Tropicos databaseas used as the authority for nomenclature. Three criteria were

hosen to select plant species for the final list. These are doc-mented: history of traditional use for human health (Mainriterion #1); microbe defense activity (Main Criterion #2);

nsect defense activity (Main Criterion #3). Four additionalriteria were also selected: non-invasive (Minor Criterion #1)Akobundu and Agyakwa, 1989); not protected, threatened, orndangered (Minor Criterion #2) (Anon., 1999); no documentedoxic properties (Minor Criterion #3) (Maiga et al., 2005); easilyultivated (Minor Criterion #4).

.4. Step 3. Subject list of Malian plant species to criteria

The list of 294 Malian plant species resulting from Steps 1a–das then subjected to the three main criteria: published evidencef traditional use, antimicrobial, or anti-insect activity. Impor-ant resources on African plant species were consulted (Watt andreyer-Brandwijk, 1962; Koumare, 1968; Kerharo and Adam,974; Ayensu, 1978; Burkill, 1985–2000; Oliver-Bever, 1986;algras, 1992; Diarra and Kamissoko, 1993; Iwu, 1993; Diallo,

000; Neuwinger, 2000; Traore, 2002). The libraries of the Insti-ut d’Economie Rurale and the Falculte de Medicine were alsoearched to document bioactivity of Malian plant species. Itas noted that some plant species synthesize insect hormones

ecdysteroids) which can disrupt insect molting and discouragehytophagy (Lafont and Dinan, 2003). These phytoecdysteroidompounds have beneficial activity in humans (and other mam-

als), and as such, are often found in plants used in traditionaledicine. Therefore, all 294 species obtained in Step 1 were

ntered into the EcdyBase online database to identify potentialcdysteroid-containing species (Lafont et al., 2004). The list of

atst

armacology 110 (2007) 235–249

94 species was reviewed by Malian scientists using the sevenriteria.

First, those species with no documented evidence of tradi-ional use (Main Criterion #1) were eliminated from the list.hen all those species not passing Main Criterion #2 or Mainriterion #3 were eliminated from the list. On the final list

Table 2), the four minor criteria were noted but no plants wereliminated from the list because they did not pass any of theour Minor Criteria. To make the final list, a species had to have

ain Criterion #1 and also either Main Criterion #2 or #3. Poten-ially invasive species, protected species, those with documentedoxic responses, and/or those not easily cultivated, remained onhe final list but were noted as such. The environmentally-soundhoices, therefore, recommended for further evaluation are thosen Table 2 without designated cautions.

.5. Step 4. List of Malian plant species with potential pestanagement uses

We developed and tested a model and so the literature was notompletely exhausted for each of the initial 294 species. Thus,pecies eliminated from the initial list due to lack of antimicro-ial or anti-insect activity may be returned to the short list inhe future as more evidence is accumulated to support criteria.hus, three criteria were used to make the next list of poten-

ial species (Table 2): documented history of traditional use foruman health; microbe defense activity; and/or insect defensectivity.

. Results

In the development of this model most species were obtainedrom a literature search and interviews with scientists. These dataere collated as follows. In Step 1a, 128 species were identifiednly from the literature. In Step 1b, with traditional medicineractictioners, 7 species were identified. In Step 1c with Maliancientists, 137 species were identified. In Step 1d with Malianarmers, 22 species were identified. Some of these species weredentified in more than one step. When combined, there were94 different species entering Step 2a.

Although relatively few species (29; 9.9%) were identifiedn Steps 1b and 1d, the anecdotal information given providedwealth of opportunities for discovery leads. From the initial

ist of 294 plant species traditionally used for health remedies inali, 67 species belonging to 33 families (22%) met the threeain Criteria of documented use in traditional medicine as well

s antimicrobial and/or anti-insect activity. Of the plants that metwo of the three Main Criteria (Table 2), 53 species (18%) hadocumented microbe defense activities, while 26 species (9%)ad negative effects on insect pests. Pesticidal properties of 20pecies were documented from Malian research (Diallo et al.,001; Traore, 2002).

Species with ecdysteroid compounds were included in the

nti-insect activity category because of their anti-insect poten-ial. Of the 67 species that passed the three Main Criteria, 10pecies (3%) used in traditional Malian medicine were ecdys-eroid positive (Dinan and Lafont, 2004). These are indicated

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n Table 2 in the anti-insect activity column. In the original listf 294 species generated in Step 1, there were 13 additionalalian genera that are ecdysteroid positive but did not pass the

ocumented traditional medicine category (Main Criterion #1).hese genera are: Aerva sp. Forssk., Amaranthaceae; Asparagusp. L., Liliaceae; Bidens sp. L., Asteraceae; Brassica sp. L., Bras-icaceae; Cassia sp. L., Fabaceae; Centaurea sp. L., Asteraceae;iospyros sp. L., Ebenaceae; Gossypium sp. L., Malvaceae;rewia sp. L., Tiliaceae; Hibiscus sp. L., Malvaceae; Pandi-ka sp. (Moquin-Tandon) Hook. f., Amaranthaceae; Phaseolusp. L., Fabaceae; Pulicaria sp. Gaertn., Asteraceae.

The list of 294 species was also subjected to the four Minorriteria selected in Step 3. Of the initial list of 294 species, 238

pecies were found to be non-invasive (56 or 19% of the initialist were invasive). The scientific director of IER, Dr. Bouremaembele, helped determine invasive or weed-like tendencies of

he species by cross-referencing with the Guide des adventices’Afrique de l’ouest (Akobundu and Agyakwa, 1989). Onlyeven species of the second list (Table 2) were found to havenvasive tendencies. Of these remaining 60 species without cau-ions, 58 species were found not to have protected, threatenedr endangered status. Endangered Mali plant species is theesponsibility of The Direction Nationale de la Conservation dea Nature (DNCN) Bamako, Mali. DNCN develops protectiveaws for endangered plant and animal species in Mali. Somepecies on the initial list of 294 plant species were found tar-eted for protection, but none were threatened or endangeredhen reviewed by the DNCN. The DNCN and the publication,ecueil Des Textes Legislatifs et Reglementaires en Matiere deestion Des Ressources Naturelles (Anon., 1999), were con-

ulted. This process identified three protected species, all trees,n our initial list: Vitellaria paradox, Khaya senegalensis, andarkia biglobosa. The initial list of 294 included three treepecies [Afzelia africana (Fabaceae), Khaya senegalensis (Meli-ceae), Pterocarpus santalinoides (Fabaceae)] appearing on thenternational Union for Conservation of Nature and Naturalesources list of threatened species (IUCN, 2006). The initial

ist of 294 also contained two rare species, Balanites aegypti-ca (Zygophyllaceae) and Calotropis procera (Asclepiadaceae)eported by Dr. Drissa Diallo (2005) of INRSP. Of these sevenpecies, only two species, Parkia biglobosa and Balanites aegyp-iaca, met the Main Criteria and remained on the list (Table 2).o documented toxicity was found in 275 of the initial list of94 species (Maiga et al., 2005). Eight of the 67 species thatassed the three Main Criteria had indications in the literaturef mild toxic side effects when used as traditional medicine.hese species are noted in Table 2 and did not overlap with

he species on the list of 67 with other cautions. Ease of cul-ivation of these Malian medicinal plants should be a criterionsed in the future. We found only two publications document-ng ease of cultivation of these 294 species. One of the authors,aidou Ouattara (IER), also provided information on ease ofultivation of these plants from his own unpublished research at

ER-Sotuba. Eleven species from the list of 294 were cited inhe literature as easy to cultivate (Eugene et al., 1998; ASNAPP,003). Only four of these made it to the list of 67 and are sooted.

sSt

armacology 110 (2007) 235–249 243

Therefore, 50 of the 294 species passed six of the seven cri-eria used. Table 2 contains 67 antimicrobial and/or anti-insectpecies with documented use in traditional medicine of Maliith 7 invasive species, 2 protected species, and 8 potentially

oxic species. None of these 17 species overlapped. These par-icular species were noted, but not removed from the initialist. We noted in Table 2 the four species with documentedase of cultivation. Therefore, we concluded this stage of theesearch with a list of 50 environmentally-sound species highlyecommended for further evaluation. Of these 50 species with-ut cautions noted, three are particularly easy to cultivate: Lippiaultiflora (Verbenaceae); Moringa oleifera (Moringaceae); andzadirachta indica (Meliaceae).

. Discussion

The methodology we developed follows recent ethnobotan-cal recommendations to select plant species using stringentxclusion criteria at the beginning of the research process, alongith ‘an interest in the people whose knowledge and identity

re embodied in these plants’ (Cordell and Colvard, 2005; Etkinnd Elisabetsky, 2005; Graz et al., 2005). A list has been devel-ped of 67 promising species of which 50 species are highlyecommended leads for new, local insect-active materials thatould be incorporated into Malian farmers’ IPM strategies. Newest insects and new cash crops with new pest complexes areontinuing to develop in the agricultural areas of Mali (Gambyt al., 2002a; Thera et al., 2002). This list of promising andighly recommended species could be useful for Malians ashey develop integrated management packages to manage newests.

As other scientists and farmers begin to use this list, andmore extensive survey of traditional medicine practitioners

nd farmers is made using this model in Mali, we have sev-ral suggestions. All four Minor Criteria (invasiveness, pro-ective status, toxicity, ease of cultivation) can be used toeduce the size of the final list before proceeding to bioas-ays and farmer trials. Practicality, ease of extraction, andlant species containing ecdysteroids should be added as Minorriteria.

.1. Invasiveness

Non-native plants cultivated for insect management may havenvasive tendencies. At the same time local weeds may bexploited for pest management. Striga spp. Lour (Scrophulari-ceae) is a serious plant parasite on crops, sometimes requiringarmers to abandon their fields. Yet, some species of Striga aresed in African villages for microbial infections (Dada et al.,002).

.2. Overharvesting/protection

Encouraging use of wild plant products could cause problemsuch as local overharvesting (Belmain and Stevenson, 2001).ome species on the initial list of 294 plant species were found

argeted for protection when reviewed by the DNCN and sub-

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44 A.D. Lehman et al. / Journal of Et

ected to the IUCN list (2006). However, lack of surveys specifico all local regions makes it difficult to ascertain if these or otherpecies are at risk from overharvesting. Protection should bessessed for each species on a regional or local level. Cultivationf medicinal plants has been initiated by Institut d’Economieurale (IER) in Mali in an effort to decrease risk of overharvest-

ng wild plants.

.3. Toxic or harmful

Despite safeguards, potential harm to farmers and livestocks another important consideration in encouraging use of locallant products for insect pest management. Many insects haveeen effectively and safely managed with natural plant com-ounds (Mulla and Su, 1999; Belmain and Stevenson, 2001).lants that have a history of medicinal use are likely to be safer

han those with no history of use (Fabricant and Farnsworth,001). Nonetheless, a survey of potentially harmful plants soldn the market in the Bamako district in Mali identified 19pecies that have a potential for causing problems such as diar-hea or vomiting (Maiga et al., 2005). These considerationsre based on ingestion, which may not be a high risk fac-or in the application of an insect management product, butould pose a serious problem for application on edible crops.liminating poor candidates before screening compounds and

unning field trials increases success rates (Cordell and Colvard,005).

.4. Easily cultivated

In Mali, most traditional medicines from plants are pro-uced from wild-collected sources. For the time being, wild-ollecting will continue to be used for plant-based insect man-gement. Use of trees, especially three Meliaceae species onhe list (Table 2), needs to be accomplished sustainably. Inarticular, the three species on the final list without other cau-ions, Moringa oleifera, Lippia multiflora, and Azadirachtandica, need to be particularly targeted for further research.zadirachta indica is already widely used in Mali and through-ut the tropical world as an insect management material (Eugenet al., 1998) and appears here in this model-building andodel-testing process as a “control.” Although the other 47

pecies have not had published records on their ease of culti-ation, they need to remain in the highly recommended cate-ory.

.5. Practicality

Most of the population of Mali are small-scale, subsistencearmers (estimated 70% of the population). Simply to survive,ubsistence farmers must produce and preserve enough food forheir family for the entire year. Their lack of cash and tech-ological resources require that pest management strategies be

ractical. New IPM strategies must not require any monetaryesources or major expenditures of time during the subsistencearmers’ period for planting (June/July) or harvest of the mainrains (October/November).

ag2a

armacology 110 (2007) 235–249

.6. Easily extracted

The majority of Malian villagers use a mortar and pestleo pulverize plants for food and biopesticides. Simple waterxtraction of raw plant material is feasible for biopesticide prepa-ation. Cold manual presses used to extract oil from seeds suchs sesame, peanut, neem, and cotton, are produced locally inamako and Mopti (Herz, 1995) and have been acquired by

armer associations throughout Mali. The fact that Malians com-only use such low-tech methods for plant extraction suggests

hat practical methods would be more easily accepted to producensecticides and insect-deterrent products. For example, cost-ree, on-farm-produced, plant-based pest management materialsere readily accepted when introduced to subsistence farmers

n Mali (N’Diaye, 2005).

.7. Ecdysteroids

Integrated pest management methods have also focused onnhibition or disruption of molting hormones (Guerrero andosell, 2005). Ecdysteroids upregulate chitinase mRNA, cleav-

ng chitin polymers during the molting process (Fukamizond Kramer, 1987), as in the epidermis of the tobacco horn-orm, Manduca sexta L. (Sphingidae) (Kramer et al., 1993).he effects of ecdysteroids on eukaryotes are well documented

Dinan and Lafont, 2004). Ingested by humans and other mam-als, ecdysteroids have been shown to enhance memory, reducealnutrition, anemia, and asthenia—an activity referred to as

daptogenic (Klein and Dunkel, 2003; Lafont and Dinan, 2003;athori and Pongracz, 2005). Dietary supplements includingcdysteroid compounds are marketed for enhancing athletickills and increasing resistance to stress (Lafont and Dinan,003; Klein, 2004). Some plants synthesize ecdysteroids. Asn example, if a plant is used in traditional Malian medicine fornhancement of memory or to improve nutrition, it is possiblehat this activity may be due to ecdysteroid compounds. If so,hat plant may also cause ecdysis disruption in insect pests. Thus,

edicinal plants used for enhancement of memory or muscleay provide promising leads for insect pest management. Par-

icular attention should be paid to the 10 ecdysteroid species inable 2.

.8. Traditional medicine as a discovery lead fornsect-active materials

The world-wide rate of peer-refereed articles document-ng the dual antimicrobial and anti-insect properties of plantsas tripled between the 1980s and 2005 (CAB Direct, 2005).triking parallels exist between plant compounds that inhibitr kill microbes as well as insects. Usnic acid, a chemicalound in lichens, has both antimicrobial and anti-insect prop-rties (Ingolfsdottir, 2002). Cyclotide compounds produced byembers of the Rubiaceae and Violaceae families have both

ntimicrobial properties and a potent inhibitory effect on therowth and development of lepidopteran larvae (Jennings et al.,001). Persea americana Mill. (Lauraceae) was found activegainst six human tumor cell lines as well as against yellow

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ever mosquito larva (Oberlies et al., 1998). Artemisia triden-ata subsp. vaseyana (Rydb.) Beetle (Asteraceae) (Dunkel andears, 1998), Tagetes minuta L. (Asteraceae) (Kumar et al.,000), and Monarda fistulosa L. (Lamiaceae) (Weaver et al.,995) have both antimicrobial activity and potential pest man-gement application. Table 1 illustrates more plants with paral-el antimicrobial and antipesticidal activity. This work definesinsect defense activity’ as: insecticidal by disruption of internalutualistic microorganisms; directly toxic to nervous system,

uch as in acetyl cholinesterase inhibition; disruption of repro-uctive or developmental hormones; antifeedant; ovipositionnd other deterrents. Proven mechanisms of insect bioactiv-ty in plant material include: oviposition deterrent chemicalsJenkins et al., 2003); fumigation (brief exposure to volatileompounds released from broken plant trichomes) (Dunkel andears, 1998); contact insecticides such as pyrethrums fromhrysanthemum cinerarifolium (Casida and Quistad, 1995) andxtracts of Tagetes minuta (Weaver et al., 1994c); growth regula-ors such as juvenile hormone mimics from balsam fir and otherlant species (Beckage, 1998) and phytoecdysteroids (Lafontnd Dinan, 2003) that prevent adult molting and inhibit ooge-esis (Rembold and Sieber, 1981b); antifeedants (Radcliffe etl., 1990); and repellents (Zhang et al., 2004). One of the mostnteresting mechanisms of insect management is the antimicro-ial effect of plant products on obligate mutualistic protozoa,acteria, and fungi in insects. One such example is the use oforbic acid, produced by Sorbus americanum to purge black car-et beetles of their intestinal commensals that aid them duringtarvation periods (Dunkel, 1969) and purge cigarette beetles ofheir mutualistic fungi (Milne, 1961, 1963, 1964). Thus, medic-nal plants used for microbe-caused pathologies may provideromising leads for insect pest management.

The case for expanding, not decreasing the search for novelgents from plants has been made by both drug (Cragg et al.,997; Lee, 2004) and pest management disciplines (Regnault-oger et al., 2005). Cragg et al. (1997) reported that 30% ofpproved drugs for the period 1983–1992 were derived fromatural products, including plants. This percentage rises to0% for the period 1989–1995. Managing insect pests withlants, either in whole form or extract, is not only commonn material-resource poor countries such as in Africa (Weavert al., 1994b,c), but also in modernized countries such asrance (Regnault-Roger and Hamraoui, 1993). Selection oflant species based on ethnomedical information is highly suc-essful according to the drug discovery experience of Fabricantnd Farnsworth (2001). Thus it should also hold true for theevelopment of local plant-based pest management products.arallel antimicrobial and insect bioactivity should come as nourprise, since humans share approximately 60% of their genesith plants and yeast (Nakagami et al., 2005). Coupling these

hared traits with ethnomedical knowledge in a set of steps todentify the most likely plant species with insect managementpplication is a novel idea.

At least 35,000 plant species are used in traditional herbaledicine throughout the world (Kong et al., 2003). It is possible

hat additional species will be found in use in Mali. The matrixriteria applied in this investigation can easily be used to add

OCio

armacology 110 (2007) 235–249 245

r subtract plant species. The initial plant list can be applied ton vitro or field experiments using low-tech methods familiar to

alian farmers. More plant species can be added to the resultingist as they meet the criteria and fit into the evaluation matrix oflants for pest management potential. Low-tech methods canhen be investigated, similar to the use of the neem and potasherbicide used in Bamako (Martin et al., 2004). Since the rawaterial to be used by Malian farmers would be locally available,

here is no problem with importation.

. Conclusion

Mali was chosen as a country system to test our hypothesis,o build the resulting model, and to use the model to construct aatabase. The abundance of ethnomedical information in thecientific literature can be compiled into a useable form foroth scientists and farmers. We discovered 67 plant species withnsect management potential that have already been identifiedy indigenous traditional medicine. We recommend 50 of thesepecies as environmentally-sound choices. We made these dis-overies by using the matrix process we developed. Therefore,e accept our hypothesis. The next step in Mali will be to put

he 50 plant species through laboratory bioassays and farmervaluation with the current Malian pest insects. We further pro-ose that this model can be used in other material-resource poorountries with a rich history of traditional medicine practices.his method is meant to apply low-technology pest manage-ent strategies in a holistic manner. Applying local knowl-

dge of the Malian people combined with outside tools isikely to produce practical, locally-achievable pest managementolutions.

cknowledgements

Our deep appreciation to Assa Kante, IER, and Sidy Ba, Uni-ersity of Bamako, Institute of Agriculture (IPR/IFRA), whoelped with arrangements in Bamako; and Neuhan Cisse, tra-itional Bambara medicine practitioner, Bamako, Mali; Thentegrated Pest Management (IPM) Collaborative Researchupport Project (IPM CRSP) which is an initiative of thegency for International Development (AID), Grant LAG-196-G-00-3053-00, Title XII, and the Board of Internationalood and Agriculture Development and Economic Coopera-

ion (BIFADEC), the participating U.S. universities and otherollaborating institutions (Dunkel, Co-P.I.); USDA-CSREESigher Education Challenge Grant, No. 2002-38411-12114

Discovery-Based Undergraduate Opportunities: Collaborativeesearch Support Programs (CRSPs)” (Dunkel, P.I.); Montanatate University Undergraduate Scholars Program, 2004–2005Lehman); Montana Agricultural Experiment Station (No. 161,unkel); and the University Cooperation in Development, ALO

Special Initiative 2004). This publication was made possi-le, in part, through support provided by USAID through the

ffice of Higher Education for Development (HED) underooperative Agreement HNE-A-00-97-00059-00. The opin-

ons expressed do not necessarily reflect the views of USAIDr HED.

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46 A.D. Lehman et al. / Journal of Et

ppendix A. Supplementary data

Supplementary data associated with this article can be found,n the online version, at doi:10.1016/j.jep.2006.06.016.

eferences

damu, H.M., Abayeh, O.J., Agho, M.O., Abdullahi, A.L., Uba, A., Dukku,H.U., Wufem, B.M., 2005. An ethnobotanical survey of Bauchi State herbalplants and their antimicrobial activity. Journal of Ethnopharmacology 99,1–4.

dewunmi, C.O., Oguntimein, B.O., Furu, P., 1990. Molluscicidal and antis-chistosomal activities of Zingiber officinale. Planta Medica 56, 374–376.

kinpelu, D.A., 2001. Antimicrobial activity of Anacardium occidentale bark.Fitoterapia 72, 286–287.

kinpelu, D.A., Olorunmola, F.O., 2000. Antimicrobial activity of Bridelia fer-ruginea fruit. Fitoterapia 71, 75–76.

kinyemi, K.O., Oladapo, O., Okwara, C.E., Ibe, C.C., Fasure, K.A., 2005.Screening of crude extracts of six medicinal plants used in South-WestNigerian unorthodox medicine for anti-methicillin resistant Staphylococ-cus aureus activity. BMC Complementary and Alternative Medicine,doi:10.1186/1472-6882-5-6.

koachere, J.F., Ndip, R.N., Chewi, E.B., Ndip, L.M., Njock, T.E., Anong,D.N., 2002. Antibacterial effect of Zingiber officinale and Garcinia kolaon respiratory tract pathogens. East African Medical Journal 79, 588–592.

kobundu, I.O., Agyakwa, C.W., 1989. Guide des Adventices d’Afrique del’ouest. Institut International d’Agriculture Tropicale, Ibadan, Nigeria.

ncolio, C., Azas, N., Mahiou, V., Ollivier, E., Di Giorgio, C., Kieta, A.,Timon-David, P., Balansard, G., 2002. Antimalarial activity and extractsand alkaloids isolated from six plants used in traditional medicine in Maliand Sao Tome. Phytotherapy Research 16, 646–649.

non., 1999. Recueil des textes legislatifs et reglementaires en matiere de ges-tion des Ressources Forestieres, Fauniques et Halieutiques. In: DirectionNationale de la Conservation de la Nature. Ministere de l’Environnement,Bamako, Mali.

raujo, C., Bezerra, I.W.L., Oliveira, A.S., Moura, F.T., 2005. In vivo bioin-secticidal activity toward Ceratitis capitata (fruit fly) and Callosobruchusmaculatus (cowpea weevil) and in vitro bioinsecticidal activity toward dif-ferent orders of insect pests of a trypsin inhibitor purified from tamarind tree(Tamarindus indica) seeds. Journal of Agricultural and Food Chemistry 53,4381–4387.

SNAPP, 2003. Agribusiness in Sustainable Natural African Plant Products.yensu, E.S., 1978. Medicinal Plants of West Africa. Reference Publications,

Inc., Algonac, Michigan.assole, I.H.N., Ouattara, A.S., Nebie, R., Ouattara, C.A.T., Kabore, Z.I., Traore,

S.A., 2003. Chemical composition and antibacterial activities of the essentialoils of Lippia chevalieri and Lippia multiflora from Burkina Faso. Phyto-chemistry 62, 209–212.

athori, M., Pongracz, Z., 2005. Phytoecdysteroids—from isolation to theireffects on humans. Current Medicinal Chemistry 12, 153–172.

eckage, N.E., 1998. Insect growth regulators. In: Rechcigl, J.C., Rechcigl,N.A. (Eds.), Biological and Biotechnological Control of Insect Pests. LewisPublishers, Boca Raton, FL, pp. 123–137.

elmain, S., Stevenson, P., 2001. Ethnobotanicals in Ghana: reviving and mod-ernising age-old farmer practice. Pesticide Outlook, 233–238.

igi, M.F.M.A., Torkomian, V.L.V., de Groote, S.T.C.S., Hebling, M.J.A.,Bueno, O.C., Pagnocca, F.C., Fernandes, J.B., Vierira, P.C., da Silva,M.F.G.F., 2004. Activity of Ricinus communis (Euphorbiaceae) and rici-nine against the leaf-cutting ant Atta sexdens rubropilosa (Hymenoptera:Formicidae) and the symbiotic fungus Leucoagaricus gongylophorus. Pest

Management Science 60, 933–938.

ostanian, N.J., Akalach, M., Chiasson, H., 2005. Effects of a Chenopodium-based botanical insecticide/acaricide on Orius insidiosus (Hemiptera:Anthocoridae) and Aphidius colemani (Hymenoptera: Braconidae). PestManagement Science 61, 979–984.

D

D

armacology 110 (2007) 235–249

uenz, E.J., Johnson, H.E., Beekman, E.M., Motley, T.J., Bauer, B.A., 2005. Bio-prospecting Rumphius’s Ambonese herbal: Volume I. Journal of Ethnophar-macology 96, 57–70.

urkill, M.H., 1985/2000. Useful Plants of West Tropical Africa. Royal BotanicGardens, Kew, London.

AB Direct, 2005. CAB International. http://www.cabdirect.org.asida, J.E., Quistad, G.B., 1995. Pyrethrum Flowers: Production, Chemistry,

Toxicology and Uses. Oxford University Press, New York.avalcanti, E.S.B., de Morais, S.M., Lima, M.A.A., Santana, E.W.P., 2004. Lar-

vicidal activity of essential oils from Brazilian plants against Aedes aegyptiL. Memorias Do Instituto Oswaldo Cruz 99, 541–544.

hampagne, D.E., Koul, O., Isman, M.B., Scudder, G.G.E., Towers, G.H.N.,1992. Biological activity of limonoids from the Rutales. Phytochemistry 31,377–394.

hapagain, B., Wiesman, Z., 2005. Larvicidal effects of aqueous extractsof Balanites aegyptiaca (desert date) against the larvae of Culex pipiensmosquitoes. African Journal of Biotechnology 4, 1351–1354.

hariandy, C.M., Seaforth, C.E., Phelps, R.H., Pollard, G.V., Khambay, B.P.,1999. Screening of medicinal plants from Trinidad and Tobago for antimicro-bial and insecticidal properties. Journal of Ethnopharmacology 64, 265–270.

isse, N., 2004. Personal communication. Traditional Bambara (Malian)medicine practitioner, Bamako, Mali.

lass, S., 2002. Pharma overview. Chemical Engineering News 80, 39–49.ordell, G.A., Colvard, M.D., 2005. Some thoughts on the future of ethnophar-

macology. Journal of Ethnopharmacology 100, 5–14.ragg, G.M., Newman, D.J., Snader, K.M., 1997. Natural products in drug

discovery and development. Journal of Natural Products 60, 52–60.ada, J.D., Alade, P.I., Ahmad, A.A., Yadock, L.H., 2002. Antimicrobial activ-

ities of some medicinal plants from Soba-Zaria, Nigeria. Nigerian QuarterlyJournal of Hospital Medicine 72, 55–56.

e Mendonca, F.A., da Silva, K.F., Dos Santos, K.K., Ribeiro, Junior, K.A.,Sant’Ana, A.E., 2005. Activities of some Brazilian plants against larvae ofthe mosquito Aedes aegypti. Fitoterapia 76, 629–636.

embele, B., 2005. Scientific Director, Institut d’Economie Rurale of Mali,personal communication.

iallo, D., 2000. Ethnopharmacological survey of medicinal plants in Mali andphytochemical study of four of them: Glinus oppositifolius (Aizoaceae),Diospyros abyssinica (Ebenaceae), Entada africana (Mimosaceae), Trichiliaemetica (Meliaceae). Doctorate Thesis. Universite de Lausanne, Switzer-land, p. 221.

iallo, D., Marston, A., Terreaux, C., Toure, B.Y., Paulsen, B.S., Hostettmann,K., 2001. Screening of Malian medicinal plants for antifungal, larvicidal,molluscicidal, antioxidant and radical scavenging activities. PhytotherapyResearch 15, 401–406.

iallo, D., Sogn, C., Samake, F.B., Paulsen, B.S., Michaelsen, T.E., Keita, A.,2002. Wound healing plants in Mali, the Bamako region. An ethnobotani-cal survey and complement fixation of water extracts from selected plants.Pharmaceutical Biology 40, 117–128.

iallo, D., Paulsen, B.S., Liljeback, T.H.A., Michaelsen, T.E., 2003. The Malianmedicinal plant Trichilia emetica; studies on polysaccharides with comple-ment fixing ability. Journal of Ethnopharmacology 84, 279–287.

iarra, L., Kamissoko, M., 1993. IPM status report in Mali. In: United Nations,Food and Agriculture Organization Global IPM Meeting, Bangkok, Thai-land.

inan, L., Lafont, R., 2004. Compilation of the literature reports for theeffects of ecdysteroids on algae, vascular plants, microbes, insects andmammals, their biotechnological applications and their biological activities.http://www.ecdybase.org/.

unkel, F.V., 1969. Symbiotic associations between the black carpet beetle,Attagenus megatoma, and microorganisms with particular reference to theeugregarine, Pyxinia frenzeli. Ph.D. Thesis. University of Wisconsin.

unkel, F.V., Weaver, D., Rusuku, G., Kimpe, N., Puyvelde, L., 1990. Antimicro-bial and insecticidal activity of the essential oil fom the leaves of Tetradenia

riparia. Planta Medica 56, 645.

unkel, F.V., Weaver, D.K., Weaver, T.W.III., 1994. Insecticidal or insect behav-iorally active preparations from aromatic plants. U.S. Patent No. 05,306,497.

unkel, F.V., Weaver, D.K., Weaver, T.W.III., 1997. Insecticidal or insect behav-iorally active preparations from aromatic plants. U.S. Patent No. 5,591,435.

hnoph

D

E

E

E

E

E

E

F

F

F

F

G

G

G

G

G

G

G

G

G

G

H

H

H

H

H

H

I

II

I

I

I

J

J

J

J

K

K

K

K

K

A.D. Lehman et al. / Journal of Et

unkel, F.V., Sears, L.J., 1998. Fumigant properties of big mountain sagebrush,Artemisia tridentata Nutt. ssp. vaseyana (Rydb.) Beetle for stored graininsects. Journal of Stored Products Research 34, 307–321.

chindu, T.N.C., 1991. Ginger, cashew and neem as surface protectants of cow-peas against infestation and damage by Callosobruchus maculatus (Fab).Tropical Science 31, 209–211.

l-Arch, M., Satrani, B., Farah, A., Bennani, L., Boriky, D., Mohamed, F.,Mohamed, B., Mohammed, T., 2003. Chemical composition, antimicrobialand insecticide activities of Mentha rotundifolia essential oil from Morocco.Acta Botanica Gallica 150, 267–274.

l Hag, E.A., Nadi, A.H., Zaitoon, A.A., 1999. Toxic and growth retardingeffects of three plant extracts on Culex pipiens larvae (Diptera: Culicidae).Phytotherapy Research 13, 388–392.

rbaugh, M., Dunkel, F., Diarra, A., Gamby, M., Kyamanywa, S., 1995–1996.Africa region annual report: An overview. IPM CRSP Third Annual Report.http://www.ag.vt.edu/ipmcrsp/annrepts/annrep96/annrpt96af.html.

tkin, N.L., Elisabetsky, E., 2005. Seeking a transdisciplinary and culturallygermane science: the future of ethnopharmacology. Journal of Ethnophar-macology 100, 23–26.

ugene, S.B., Bhatnagar, D., Jacobsen, M., Metcalf, R.L., Saxena, R.C., Unande,D., Vietmeyer, N.D., 1998. Neem: A Tree for Solving Global Problems.Cornucopia Press Subiaco, Australia.

abricant, D.S., Farnsworth, N.R., 2001. The value of plants used in traditionalmedicine for drug discovery. Environmental Health Perspectives 109, 69–75.

atope, M.O., Adoum, O.A., Takeda, Y., 2000. C(18) acetylenic fatty acids ofXimenia americana with potential pesticidal activity. Journal of Agriculturaland Food Chemistry 48, 1872–1874.

ritzsche, U., Cleffmann, G., 1987. The insecticide azadirachtin reducespredominantly cellular RNA in Tetrahymena. Naturwissenschaften 74,191–192.

ukamizo, T., Kramer, K.J., 1987. Effect of 20-hydroxyecdysone on chitinaseand �-N-acetyl-glucosaminidase during the larval-pupal transformation ofManduca sexta (L). Insect Biochemistry 17, 547–550.

afner, S., Wolfender, J.L., Nianga, M., Stoeckli-Evans, H., Hostettmann, K.,1996. Antifungal and antibacterial napthoquinones from Newbouldia laevisroots. Phytochemistry 42, 1315–1320.

amby, K.T., Dunkel, F.V., 2001. Development and dissemination of integratedpackages for insect and disease management. In: Integrated Pest Man-agement Collaborative Research Support Program. Eighth Annual Report,Virginia Tech, Blacksburg, PA, pp. 176–181.

amby, K.T., Foster, R., Thera, A., Moore, K., Caldwell, J., Sissako, H., Yeboah,A., 2002a. Development of an integrated package for management of diseaseand insect pests on green beans. In: Integrated Pest Management Collab-orative Research Support Program. Ninth Annual Report, Virginia Tech,Blacksburg, VA, pp. 225–228.

amby, K.T., Noussourou, M., Foster, R., Traore, S., Sissako, H., Westwood, J.,Yeboah, A., 2002b. Development of an integrated package for managementof insects and weeds affecting hibiscus. In: Integrated Pest ManagementCollaborative Research Support Program. Ninth Annual Report, VirginiaTech, Blacksburg, VA, pp. 228–231.

amby, K.T., N’Diaye, M., Sidibe, I., Foster, R., Moore, K., Hipkins, P., West-wood, J., Traore, A., Sissoko, H., 2002c. Dissemination of green bean IPMpackages through farmer field schools. In: Integrated Pest Management Col-laborative Research Support Program. Ninth Annual Report, Virginia Tech,Blacksburg, VA, pp. 239–240.

ao, H.H., Li, W., Yang, J., Wang, Y., Guo, G.Q., Zheng, G.C., 2003/2004.Effect of 6-benzyladenine and casein hydrolysate on micropropagation ofAmorpha fruticosa. Biologia Plantarum 47, 145–148.

ermano, M.P., D’Angelo, V., Sanogo, R., Catania, S., Alma, R., De Pasquale,R., Bisignano, G., 2005. Hepatoprotective and antibacterial effects ofextracts from Trichilia emetica Vahl. (Meliaceae). Journal of Ethnophar-macology 96, 227–232.

eyid, A., Abebe, D., Debella, A., Makonnen, Z., Aberra, F., Teka, F., Kebede,

T., Urga, K., Yersaw, K., Biza, T., Mariam, B.H., Guta, M., 2005. Screeningof some medicinal plants of Ethiopia for their anti-microbial properties andchemical profiles. Journal of Ethnopharmacology 97, 421–427.

raz, B., Diallo, D., Willcox, M., Giani, S., 2005. Screening of traditional herbalmedicine: first, do a retrospective study, with correlation between diverse

K

armacology 110 (2007) 235–249 247

treatments used and reported patient outcome. Journal of Ethnopharmacol-ogy 101, 338–339.

uerrero, A., Rosell, G., 2005. Biorational approaches for insect control byenzymatic inhibition. Current Medicinal Chemistry 12, 461–469.

ammond, J.A., Fielding, D., Bishop, S.C., 1997. Prospects for plantanthelmintics in tropical veterinary medicine. Veterinary Research Com-munications 21, 213–228.

art, J., 1976. Montana Native Plants and Early Peoples. Montana HistoricalSociety, Helena, MT, p. 45.

einrich, M., Barnes, J., Gibbons, S., Williamson, E.M., 2004. Fundamentals ofPharmacognosy and Phytotheraphy. Churchill Livingstone, St. Louis, MO.

erz, J., 1995. How to use your ram press. Enterprise Works Worldwide.http://www.enterpriseworks.org/success mali.asp.

ounzangbe-Adote, M.S., Paolini, V., Fouraste, I., Moutairou, K., Hoste, H.,2005. In vitro effects of four tropical plants on three life-cycle stages of theparasitic nematode, Haemonchus contortus. Research in Veterinary Science78, 155–160.

uang, J.W., Chung, W.C., 2003. Management of vegetable insect diseases withplant extracts. In: Huang, H.C. (Ed.), Advances in Plant Disease Manage-ment. Research Signpost Publishers, Kerala, India, pp. 153–163.

nternational Union for Conservation of Nature and Natural Resources,2006. 2006 IUCN Red List of Threatened Species. IUCN, http://www.iucnredlist.org.

ngolfsdottir, K., 2002. Usnic acid. Phytochemistry 61, 729–736.nngjerdingen, K., Nergard, C.S., Diallo, D., Mounkoro, P.P., Paulsen, B.S.,

2004. An ethnopharmacological survey of plants used for wound healing inDogonland, Mali, West Africa. Journal of Ethnopharmacology 92, 233–244.

nngjerdingen, K., Debes, S.C., Inngjerdingen, M., Hokputsa, S., Harding, S.E.,Rolstad, B., Michaelsen, T.E., Diallo, D., Paulsen, B.S., 2005. Bioactivepectic polysaccharides from Glinus oppositifolius (L.) Aug. DC., a Malianmedicinal plant, isolation and partial characterization. Journal of Ethnophar-macology 101, 204–214.

nternational Council for Science, 2002. ICSU Series on Science for Sus-tainable Development No. 4: Science Traditional Knowledge and Sus-tainable Development. http://www.icsu.org/2 resourcecentre/RESOURCElist base.php4?rub=8.

wu, M.M., 1993. Handbook of African Medicinal Plants. CRC Press, BocaRaton, FL.

ayasekara, T.K., Stevenson, P.C., Hall, D.R., Belmain, S.R., 2005. Effect ofvolatile constituents from Securidaca longepedunculata on insect pests ofstored grain. Journal of Chemical Ecology 31, 303–313.

egede, I.A., Kunle, O.F., Ibrahim, J.A., Ugbabe, G., Okogun, J.I., 2005. Pharma-cognostic investigation of leaves of Mitracarpus vilosus (S.W.) DC. AfricanJournal of Biotechnology 4, 957–959.

enkins, D., Dunkel, F.V., Gamby, K.T., 2003. Storage temperature of neemkernel extract: Differential effects on oviposition deterrency and larval tox-icity of Callosobruchus maculatus (F.) (Coleoptera: Bruchidae). Journal ofEnvironmental Entomology 32, 1283–1289.

ennings, C., West, J., Waine, C., Craik, D., Anderson, M., 2001. Biosynthesisand insecticidal properties of plant cyclotides: the cyclic knotted proteinsfrom Oldenlandia affinis. Proceedings of the National Academy of SciencesUSA 98, 10614–10619.

elemu, S., Cardona, C., Segura, G., 2004. Antimicrobial and insecticidal pro-tein isolated from seeds of Clitoria ternatea, a tropical forage legume. PlantPhysiology and Biochemistry 42, 867–873.

erharo, J., Adam, J.G., 1974. La Pharmacopee senegalaise traditionelle. In:Plantes Medicales et Toxiques. Editions Vigot, Freres, Paris.

halaf, A.F., 2004. Enzyme activity in the flesh fly Parasarcophaga dux Thom-son influenced by dill compounds, myristicin and apiol. Journal of theEgyptian Society of Parasitology 34, 255–264.

lein, R.A., Dunkel, F.V., 2003. New pest management frontiers: linking plantmedicine to traditional knowledge. American Entomologist 49, 7–18.

lein, R., 2004. Phytoecdysteroids. Journal of the American Herbalists Guild

5, 18–28.

one, W.M., Atindehou, K.K., Terreaux, C., Hostettmann, K., Traore, D., Dosso,M., 2004. Traditional medicine in North Cote-d’Ivoire: screening of 50medicinal plants for antibacterial activity. Journal of Ethnopharmacology93, 43–49.

2 hnoph

K

K

K

K

K

K

L

L

L

L

M

M

M

M

M

M

M

M

M

M

M

M

N

N

N

N

N

N

O

O

O

O

O

O

O

P

P

P

R

R

R

R

48 A.D. Lehman et al. / Journal of Et

ong, C., Hu, F., Xu, X., Zhang, M., Liang, W., 2005. Volatile allelochemi-cals in the Ageratum conyzoides intercopped citrus orchard and their effectson mites Amblyseius newsami and Panonychus citri. Journal of ChemicalEcology 31, 2193–2203.

ong, J.-M., Goh, N.-K., Chia, L.-S., Chia, T.-F., 2003. Recent advances intraditional plant drugs and orchids. Acta Pharmacologica Sinica 24, 7–21.

oumaglo, K.H., Akpagana, K., Glitho, A.I., Garneau, F.X., Gagnon, H., Jean,F.-I., Moudachirou, M., Addae-Mensah, I., 1996. Geranial and neral majorconstituents of Lippia multiflora Moldenke leaf oil. Journal of Essential OilResearch 8, 237–240.

oumare, M., 1968. Contribution a l’etude pharmacologique de Guiera sene-galensis. Doctorate Thesis. University of Toulouse, France.

ramer, K.J., Corpuz, L., Choi, H.K., Muthukrishnan, S., 1993. Sequence ofa cDNA and expression of the gene encoding epidermal and gut chiti-nases of Manduca sexta. Insect Biochemistry and Molecular Biology 23,691–701.

umar, A., Dunkel, F.V., Broughton, M.A., Sriharan, S., 2000. Effect of rootextracts of Mexican marigold. Tagetes minuta (Asterales: Asteraceae) onsix nontarget aquatic macroinvertebrates. Environmental Entomology 29,140–149.

afont, R., Dinan, L., 2003. Practical uses for ecdysteroids in mammals includ-ing humans: an update. Journal of Insect Science 3, 1–30.

afont, R., Harmatha, J., Marion-Poll, F., Dinan, L., Wilson, I.D., 2004. TheEcdysone Handbook, third ed. http://ecdybase.org.

ee, K.-H., 2004. Current developments in the discovery and design of new drugcandidates from plant natural product leads. Journal of Natural Products 67,273–283.

opez, P., Sanchez, C., Batlle, R., Nerın, C., 2005. Solid- and vapor-phase antimi-crobial activities of six essential oils: susceptibility of selected foodbornebacterial and fungal strains. Journal of Agricultural and Food Chemistry 53,6939–6946.

aiga, A., Diallo, D., Fane, S., Sanogo, R., Paulsen, B.S., Cisse, B., 2005. A sur-vey of toxic plants on the market in the district of Bamako, Mali: traditionalknowledge compared with a literature search of modern pharmacology andtoxicology. Journal of Ethnopharmacology 96, 183–193.

algras, D.R.P., 1992. Arbres et Arbustes Guerisseurs des Savanes Maliennes.Karthala, Paris.

arques, M.R., Albuquerque, L.M.B., Xavier-Filho, J., 1992. Antimicrobialand insecticidal activities of cashew tree gum exudate. Annals of AppliedBiology 121, 371–377.

artin, M.S., Goble, A.R., N’Diaye, M., Dembele, B., Gamby, K., Mullins,D., Fell, R., Westwood, J.H., 2004. Characterization of foliar-applied potashsolution as a non-selective herbicide in Malian agriculture. In: Abstractsof the 4th International Weed Science Congress, Durban, South Africa,p. 87.

atu, E.N., van Staden, J., 2003. Antibacterial and anti-inflammatory activitiesof some plants used for medicinal purposes in Kenya. Journal of Ethnophar-macology 87, 35–41.

azyad, S.A., El-Serougi, A.O., Morsy, T.A., 1999. The efficacy of the volatileoils of three plants for controlling Lucilia sericata. Journal of the EgyptianSociety of Parasitology 29, 91–100.

ilne, D.L., 1961. The mechanism of growth retardation by nicotine in thecigarette beetle, Lasioderma serricorne F. South Africa Journal of Agricul-tural Science 4, 277–278.

ilne, D.L., 1963. A study of the nutrition of the cigarette beetle, Lasiodermaserricorne F., (Coleoptera: Anobiidae) and a suggested new method for itscontrol. Journal of the Entomological Society of Southern Africa 26, 43–63.

ilne, D.L., 1964. Food preservatives as insecticides against Tribolium con-fusum DuVal., T. castaneum Herbst., and Lasioderma serricorne F. SouthAfrica Journal of Agricultural Science 7, 79–86.

oore, K.M., Gamby, K.T., Sissoko, H.T., Dembele, B., Thera, A.T., N’Diaye,M., Ba, A., Mullins, D., Hipkins, P., Cobb, J., Westwood, J., Caldwell,J., Sidebe, I., Diallo, M.K., 2001. Participatory assessment. In: Integrated

Pest Management Collaborative Research Support Program. Eighth AnnualReport, Virginia Tech, Blacksburg, VA, pp. 187–189.

ordue Luntz, A.J., Evans, K.A., Charlett, M., 1986. Azadirachtin, ecdysteroidsand ecdysis in Locusta migratoria. Comparative Biochemistry and Physiol-ogy 85, 297–301.

R

armacology 110 (2007) 235–249

ulla, M.S., Su, T., 1999. Activity and biological effects of neem productsagainst arthropods of medical and veterinary importance. Journal of theAmerican Mosquito Control Association 15, 133–152.

akagami, H., Pitzschke, A., Hirt, H., 2005. Emerging MAP kinase pathwaysin plant stress signaling. Trends in Plant Science 10, 339–346.

akatana, M., Iwashita, T., Naoki, H., Hase, T., 1985. Structure of a limonoidantifeedent from Trichilia roka. Phytochemistry 24, 195–196.

’Diaye, M., 2005. Institut d’Economie Rurale, Bamako, Mali, personal com-munication.

ergard, C.S., Diallo, D., Inngjerdingen, K., Michaelsen, H., Matsumoto, T.,Kiyohara, H., Yamada, H., Paulsen, B.S., 2005. Medicinal use of Cochlosper-mum tinctorium in Mali. Anti-ulcer-, radical scavenging- and immunomod-ulating activities of polymers in the aqueous extract of the roots. Journal ofEthnopharmacology 96, 255–269.

euwinger, H.D., 2000. African Traditional Medicine: A Dictionary of PlantUse and Applications. Medpharm, Scientific Publishers Stuttgart, St. Leon-Rot, Germany.

ewman, D.J., Cragg, G.M., Snader, K.M., 2003. Natural products as sourcesof new drugs over the period 1981–2002. Journal of Natural Products 66,1022–1037.

berlies, N.H., Rogers, L.L., Martin, J.M., McLaughlin, J.L., 1998. Cytotoxicand insecticidal constituents of the unripe fruit of Persea americana. Journalof Natural Products 61, 781–785.

kabe, T., Morita, Y., Inamori, Y., Narita, K., Ishida, N., 2004. Wood extractsfrom Aomori Hiba (Hinokiasunaro)—the insecticidal and preservativeeffects of Aomori Hiba oil. Aroma Research 5, 325–332.

ladimeji, F.A., Orafidiya, O.O., Ogunniyi, T.A.B., Adewunmi, T.A., 2000.Pediculocidal and scabicidal properties of Lippia multiflora essential oil.Journal of Ethnopharmacology 72, 305–311.

liver-Bever, B., 1986. Medicinal Plants in Tropical West Africa. CambridgeUniversity Press, Cambridge, UK.

nyeyili, P.A., Nwosu, C.O., Amin, J.D., Jibike, J.I., 2001. Anthelmintic activ-ity of crude aqueous extract of Nauclea latifolia stem bark against ovinenematodes. Fitoterapia 72, 12–21.

uattara, S., 1997. Liste de quelques plantes medicinales et leurs utilizations.In: Final Report for Medicinal Species Project, Institut d’Economie Rurale,Bamako, Mali.

uoba, L.I.I., Diawara, B., Annan, N.T., Poll, L., Jakobsen, M., 2005.Volatile compounds of Soumbala, a fermented African locust bean (Parkiabiglobosa) food condiment. Journal of Applied Microbiology 99, 1413–1421.

ai, M.R., Acharya, L.D., Udupa, N., 2004. Evaluation of antiplaque activityof Azadirachta indica leaf extract gel—a 6-week clinical study. Journal ofEthnopharmacology 90, 99–103.

andey, V.N., Dubey, N.K., 1994. Antifungal potential of leaves and essential oilsfrom higher plants against soil phytopathogens. Soil Biology Biochemistry26, 1417–1421.

ieters, L., Vlietinck, A.J., 2005. Bioguided isolation of pharmacologicallyactive plant components, still a valuable strategy for the finding of newlead compounds? Journal of Ethnopharmacology 100, 57–60.

abe, T., Mullholland, D., van Staden, J., 2002. Isolation and identifica-tion of antibacterial compounds from Vernonia colorata leaves. Journal ofEthnopharmacology 80, 91–94.

adcliffe, E.B., Dunkel, F.V., Strozk, P., Adam, S., 1990. Antifeedant effect ofneem, Azadirachta indica A.Juss., kernel extracts on Kraussaria angulifera(Krauss) (Orthoptera: Acrididae), a sahelian grasshopper. Tropical Agricul-ture 68, 95–101.

ani, A.S., Satyakala, M., Murty, U.S.N., 2003. Acorus calamus Linn: an impor-tant medicinal plant and source of a potent biopesticide. Proceeding of theNational Academy of Sciences India. Section B, Biological Sciences 73,1–15.

edfern, R.E., Warthen Jr., J.D., Uebel, E.C., Mills Jr., G.D., 1981. Theantifeedant and growth-disrupting effects of azadirachtin and Spodoptera

frugiperda and Oncopeltus fasciatus. In: Schmutterer, H., Ascher, K.R.S.,Rembold, H. (Eds.), Natural Pesticides from the Neem Tree (Azadirachtaindica A. Juss). GTZ Press, Eschborn, West Germany, p. 129.

egnault-Roger, C., Hamraoui, A., 1993. Efficacy of plants from south ofFrance used as traditional protectant of Phaseolus vulgaris L. against its

hnoph

R

R

R

R

R

S

S

S

S

T

T

T

T

T

T

T

T

T

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A.D. Lehman et al. / Journal of Et

bruchid Acanthoscelides obtectus Say. Journal of Stored Products Research29, 259–264.

egnault-Roger, C., Philogene, B.J.R., Vincent, C., 2005. Botanicals: Yester-day’s and today’s promises. In: Biopesticides of Plant Origin. LavoisierPublishing Inc., Secaucus, NJ, pp. 1–15.

embold, H., Sieber, K.P., 1981a. Inhibition of oogenesis and ovarian ecdys-teroid synthesis by azadirachtin in Locusta migratoria. Zeitschrift Fur Natur-forschung C: A Journal of Biosciences 36, 466.

embold, H., Sieber, K.P., 1981b. Effect of azadirachtin on oocyte developmentin Locusta migratoria migratorioides. In: Schmutterer, H., Ascher, K.R.S.,Rembold, H. (Eds.), Natural Pesticides from the Neem Tree (Azadirachtaindica A. Juss). GTZ Press, Eschborn, West Germany, p. 75.

ogosca, M., Rogosca, R., 2000. Antimicrobial activity of Monarda fistulosa L.extract and its therapeutic use. In: The First Conference on Medicinal andAromatic Plants of Southeast European Countries, Yugoslavia, P-109, pp.1–4.

upprecht, J.K., Hui, Y.H., McLaughlin, J.L., 1990. Annonaceous acetogenins:a review. Journal of Natural Products 53, 237–278.

anogo, R., Crisafi, G., Germano, M.P., De Pasquale, R., Bisignano, G., 1998.Evaluation of Malian traditional medicines: screening for antimicrobialactivity. Phytotherapy Research 12, S154–S156.

parg, S.G., Van Staden, J., Jager, A.K., 2000. Efficiency of traditionally usedSouth African plants against schistosomiasis. Journal of Ethnopharmacology73, 209–214.

tavri, M., Gibbons, S., 2005. The antimycobacterial constituents of dill(Anethum graveolens). Phytotherapy Research 19, 938–941.

trobel, G., Daisy, B., 2003. Bioprospecting for microbial endophytes andtheir natural products. Microbiology and Molecular Biology Reviews 67,491–502.

adeg, H., Mohammed, E., Asres, K., Gebre-Mariam, T., 2005. Antimicrobialactivities of some selected traditional Ethiopian medicinal plants used in thetreatment of skin disorders. Journal of Ethnopharmacology 100, 168–175.

alla, E., Djamen, D., Djoulde, D.R., Tatsadjeu, L., Tantoh, D., Mbafor, J.T.,Fomum, Z.T., 2002. Antimicrobial activity of Bridelia ferruginea leavesextracts. Fitoterapia 73, 343–345.

amboura, H., Kabore, H., Yameogo, S.M., 1998. Ethnomedecine veterinaire etpharmacopee traditionnelle dans le plateau central du Burkina Faso: cas dela province du Passore. Biotechnology, Agronomy Society and Environment2, 181–191.

ereschuk, M.L., Riera, M.V.Q., Guillermo, R., Castro, L.R., Abdala, R., 1997.Antimicrobial activity of flavonoids from leaves of Tagetes minuta. Journalof Ethnopharmacology 56, 227–232.

hera, A.T., Gilbertson, R.L., Gamby, K.T., Sissoko, H.T., Foster, R., Youm,O., 2002. Management of whitefly and aphid-transmitted virus diseases of

tomato. In: Integrated Pest Management Collaborative Research SupportProgram. Ninth Annual Report, Virginia Tech, Blacksburg VA, pp. 233–235.

hongson, C., Davidson, P.M., Mahakarnchanakul, W., Vibulsresth, P., 2005.Antimicrobial effect of Thai spices against Listeria monocytogenes andSalmonella typhimurium DT104. Journal of Food Protection 68, 2054–2058.

Z

Z

armacology 110 (2007) 235–249 249

ogola, A., Diallo, D., Dembele, S., Barsett, H., Paulsen, B.S., 2005. Ethnophar-macological survey of different uses of seven medicinal plants from Mali,(West Africa) in the regions Doila, Kolokani and Siby. Journal of Ethnobi-ology and Ethnomedicine, doi:10.1186/1746-4259-1-7.

raore, I., 2002. Utilisation des especes de plantes pesticides dans la conser-vation des grains et semences du sorgho (Sorghum bicolor (L.) Moench).Memoire de Dea: Option Protection des Vegetaux. Thesis. Universite duMali.

rongtokit, Y., Rongsriyam, Y., Komalamisra, N., Apiwathnasorn, C., 2005.Comparative repellency of 38 essential oils against mosquito bites. Phy-totherapy Research 19, 303–309.

pansani, S.M., Kotkar, H.M., Mendki, P.S., Maheshwari, V.L., 2003. Partialcharacterization and insecticidal properties of Ricinus communis L. foliageflavonoids. Pest Management Science 59, 1349–1354.

an Puyvelde, L., 1986. Active principles of Tetradenia riparia. I. Antimi-crobial activity of 8(14),15-sandaracopimaradiene-7�,18-diol. Journal ofEthnopharmacology 17, 269–275.

att, J.M., Breyer-Brandwijk, M.G., 1962. Medicinal and Poisonous Plants ofSouth Africa, second ed. E and S Livingstone LTD, Edinburgh, London.

eaver, D.K., Dunkel, F.V., Ntezurubanza, L., Jackson, L.L., Stock, D.T., 1991.The efficacy of linalool, a major component of freshly-milled Ocimumcanum Sims (Lamiaceae), for protection against post harvest damage bycertain stored product Coleoptera. Journal of Stored Product Research 27,213–220.

eaver, D.K., Dunkel, F.V., Cusker, J.L., VanPuyvelde, L., 1992. Ovipositionpatterns in two species of bruchids (Coleoptera: Bruchidae) as influenced bythe dried leaves of Tetradenia riparia. Journal of Environmental Entomology21, 1121–1129.

eaver, D.K., Dunkel, F.V., Potter, R.C., Ntezurubanza, L., 1994a. Contact andfumigant efficacy of powdered and intact Ocimum canum Sims (Lamiales:Lamiaceae) against Zabrotes subfasciatus (Boheman) adults (Coleoptera:Bruchidae). Journal of Stored Product Research 30, 243–252.

eaver, D.K., Dunkel, F.V., Van Puyvelde, L., Richards, D.C., Fitzgerald, G.W.,1994b. Toxicity and protectant potential of the essential oil of Tetradeniariparia (Lamiales: Lamiaceae) against Zabrotes subfasciatus (Coleoptera:Bruchidae) infesting dried pinto beans (Fabales: Leguminosae). Journal ofApplied Entomology 118, 179–196.

eaver, D.K., Wells, C.D., Dunkel, F.V., Bertsch, W., Sing, S.E., Sriharan, S.,1994c. Insecticidal activity of floral, foliar, and root extracts of Tagetes min-uta (Asterales: Asteraceae) against adult Mexican bean weevils (Coleoptera:Bruchidae). Journal of Economic Entomology 87, 1718–1725.

eaver, D.K., Phillips, T.W., Dunkel, F.V., Nance, E.L., Grubb, R.T., 1995.Dried leaves from Rocky Mountain plants decrease infestation by storedproduct beetles. Journal of Chemical Ecology 21, 127–142.

hang, J.T., 2002. New drugs derived from medicinal plants. Therapie 57,137–150.

hang, W., McAuslane, H.J., Schuster, D.J., 2004. Repellancy of ginger oil toBemisia argentifolii (Homoptera: Aleyrodidae) on tomato. Journal of Eco-nomic Entomology 97, 1310–1318.