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Medicinal Plants and Herbal Drugs: An Overview

• First Online: 28 March 2021

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• Burhan Ahad 3 ,
• Waseem Shahri 3 ,
• Humeera Rasool 3 ,
• Z. A. Reshi 3 ,
• Sumaiyah Rasool 4 &
• Tufail Hussain 5  

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4 Citations

Medicinal plants, which represent one of the greatest assets of ecosystem, have found their utilization in human life and healthcare system since early days of mankind and have still maintained their importance in modern times by virtue of maintaining their basic therapeutic curative role. Numerically constituting a large group of world flora, medicinal plants form the source for large variety of herbal drugs used for medicinal purposes. Cultivation of medicinal plants being a promising alternative to wild collection enables not only conservation of natural genetic variability and survival of critically endangered, vulnerable, endangered, endemic and rare species but also symbolizes a potent economy branch for pharmaceutical industry as source of their quality raw material. Medicinal plants owe their curative value to naturally occurring biologically active ingredients in them, i.e. the primary and secondary metabolites which obtained either in pure or combined form with other molecules form a pivotal source of drug lead compounds. Growth and development of medicinal plants and medicinally active chemical metabolites found in them are influenced by the abiotic factors and biotic factors. The resurgence in recognizing medicinal plants as a source of drugs and other products is mainly due to their effectiveness, with no to little side effects associated with their application and as an alternate to high-cost synthetic drugs. Though herbal medicine has become more mainstream world over during the last few decades, their safety, quality and effectiveness still remain a key issue. The renewed interest in medicinal plants expanded their market demand which however coupled with their already rather limited availability and potential overharvesting have brought about alarming biodiversity problems sounding the need to evaluate and conserve our old prized natural germplasm.

This chapter deals with stocking of knowledge regarding use of medicinal plants, their correct identification, their chemical constitution, factors involved in their quality production and also that of naturally occurring bioactive principles, as well concerns with regard to their quality and control parameters thereof . The chapter also gives insight into their conservation aspect especially from the viewpoint of sustainability as they represent the substantial proportion of the global drug market.

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Burhan Ahad, Waseem Shahri, Humeera Rasool & Z. A. Reshi

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Ahad, B., Shahri, W., Rasool, H., Reshi, Z.A., Rasool, S., Hussain, T. (2021). Medicinal Plants and Herbal Drugs: An Overview. In: Aftab, T., Hakeem, K.R. (eds) Medicinal and Aromatic Plants. Springer, Cham. https://doi.org/10.1007/978-3-030-58975-2_1

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Phytochemical analysis of some selected traditional medicinal plants in Ethiopia

• Misganaw Gedlu Agidew 1  

Bulletin of the National Research Centre volume  46 , Article number:  87 ( 2022 ) Cite this article

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This review of relevant medicinal plants is based on the fundamental knowledge accumulated by indigenous people of Ethiopia and to identify which types of selected medicinal plants for phytochemical analysis were analyzed and which one is not analyzed at Ethiopian levels. In this review, the most traditional medicinal plant species found and used in Ethiopia are chosen.

The qualitative phytochemical analysis, some of which are the most important phytochemicals such as phenolic, tannins, alkaloids, saponins, cardiac glycosides, steroids, terpenoids, flavonoids, phlobatannins, anthraquinones, and reducing sugars are studied by the researcher. Most studies have revealed that some phytochemicals are present in some medicinal plants while some are absent. The phytochemical properties of some species were studied like Artemisia afra (Ariti), Aloe Vera (Erret), Yzygium guineense (Dokuma), Ruta chalepensis (Tenadam), Ocimum grattissimum (Damakese), Nigella sativa (Tikur Azmud), Lepidium sativum (Feto), Hagenia abyssinica (Kosso), Croton macrostachyus (Bisana), and Rhamnus prinoides (Gesho).

Conclusions

This review has shown that traditional medicinal plants whose phytochemical properties are not studied have various medicinal purposes like treating mastitis, preventing boils, hemorrhoids, congestion, headache, hepatitis, liver, vertigo, stomatitis, kidneys, liver, and vision for treating anemia, hemorrhoid coughs, fluxes, and stomatitis in most animals and human beings. So that identifying the plants based on the investigation and analysis of phytochemical properties of such plant species are more important than Ethiopian levels.

Medicinal plants still play important roles in the daily lives of people living in developing countries of Asia and Africa, including Ethiopia. Medicinal plants not only serve as complements or substitutes for modern medical treatments, which are often inadequately available but also enhance the health and security of local people. Thus, these plants play indispensable roles in daily life and are deeply connected to diverse social, cultural, and economic events associated with life, aging, illness, and death (JAFICOAF 2008). Medicinal plants are used to treat and diagnose diseases and infections. From ancient times, plants have been rich sources of effective and safe medicines (Russell-Smith et al. 2006 ).

The world health organization (WHO) defined traditional medicine as the total combination of knowledge and practices that can be formally explained or used in the prevention and elimination of physical, mental, or social imbalance and relying exclusively on practical experience and observation handed down from generation to generation, whether verbally or in writing. About 75–90% of the rural population in the world (excluding western countries) relies on traditional medicines as their only health care system. This is not only because of poverty where people cannot afford to buy expensive modern drugs, but traditional systems are also more culturally acceptable and meet the psychological needs in a way modern medicine does not (Fassil Kibebe 2001 ).

Ethnomedicinal practices are believed to be one of the potential bases for the development of safe and effective treatments. Ethiopia has a long history of a traditional health care system, but studies on traditional medicinal plants (TMP) have been limited in comparison to the country’s multiethnic, cultural, and flora diversity (Fentahun et al. 2017 ), Also, the use of medicinal plants to treat infections is an old practice in large parts of Ethiopia to solve health problems for livestock and humans (Redda et al. 2014 ; Giday et al. 2009 ; Regassa 2013 ; Abera 2014 ; Tamene 2020 ; Mulatu 2020 ).

Increasing traditional medicines and natural plant products

The main phytochemical components, present in medicinal plants are tannins, alkaloids, saponins, cardiac glycosides, steroids, terpenoids, flavonoids, phlobatannins, anthraquinones, and reducing sugars. As proposed by WHO, the primary health care of most population of developing countries depend on traditional medicines and mostly natural plant products (Vines 2004 ). Like the worldwide countries, populations of Ethiopia use traditional medicines in both rural and urban areas. Traditional practice and activities have a long history in many areas in the Ethiopia and it will continue to give useful and applicable tools for treating disease (Helen et al. 2019 ).

Different traditional medicinal plant species are studied by different researchers in the world and in the Ethiopian. Ethiopia comprises people with many languages, cultures, and beliefs. This makes for a rich and diverse knowledge and practice of traditional medicine, including herbal remedies (Helen et al. 2019 ). There are different literature reviews that investigated and studied the Ethnobotanical and Ethnopharmacological evidence of some Ethiopian medicinal plants traditionally used for the Treatment of Cancer, skin problems, leprosy, and external parasites, Evil eye, and wound treatment in the Ethiopia. However, there is no report that could show phytochemical composition and its expanded pharmacological application in the folk medicine of some traditional medicinal plants in the country of Ethiopia. Moreover, this knowledge of identifications of studied and unstudied phytochemical composition of medicinal plants in Ethiopia can serve as the baseline data for researchers and analyzers for the further study of traditional medicinal plants in Ethiopia (Helen et al. 2019 ).

The medicinal power of traditional plants species lies in phytochemical components that cause definite pharmacological action on the human body (Naseem 2014 ). Based on their metabolism activity in the plant, phytochemicals components are generally can be mainly divided into two groups, which are primary which has mainly sugars, amino acids, chlorophyll and proteins, and secondary constituents while secondary constituents consist of alkaloids, flavonoids, saponins, tannins, phenolic compounds and many more (Krishnaiah 2007 ).

The most important components of the medicinal plant were isolated by the extraction methods by using the right solvent. Each researcher in the published articles in this review, different methods of extraction such as ethanol, methanol, chloroform, acetone, hexane, petroleum ether, ethyl acetate, and aqueous (water) were used to the phytochemical composition of plant species. The objective of this review was to collect and summarize the information about the medicinal plant and to classify the plants based on the studies of their phytochemical composition as well as this provides information for the research community to conduct further scientific investigations in Ethiopia’s medicinal plants.

Materials and methods

In this review, the data and information on the traditional medicinal plants in Ethiopia were collected from the published papers, which are available online in different forms such as books, published articles, and research reports. Different online sources such as Google Scholar and gray literature were the source of published articles by browsing the different words or terms like medicinal plants and Ethiopian traditional plants. For this review, scientific name, family name, local name, and important, obtained from the published articles that were obtained online, and the data are shown in Table 23 .

There are various traditional medicinal plants used to treat different illnesses and diseases in Ethiopia which did not describe plant species by scientific names; and review articles, are excluded. For this review paper, a total of 53 plant species that are recognized and grown in Ethiopia are documented. From those plant species, the phytochemical composition of some plant species is studied by a researcher and some are not studied. The most important components of the medicinal plant were isolated by the extraction methods by using different solvents. In all reported literature, different solvent such as ethanol, methanol, chloroform, acetone, hexane, petroleum ether, ethyl acetate, and water was used as solvent.

The main aim of this review is to collect and summarize the information about the medicinal plant and to classify the plants based on the studies of their phytochemical composition as well as to provide information for the research community to conduct further scientific investigations on the Ethiopia medicinal plants.

Results and discussions

Phytochemical analysis.

Traditional medicine plays a significant role in the healthcare of the people in developing countries, including Ethiopia, and medicinal plants provide a valuable contribution to this practice (Tesfahuneygn and Gebreegziabher 2019 ). In this review, around 33 medicinal plants species were identified from published articles. The different parts of the plant such as root, leaves, and fruit, in which these different parts have many traditional values, pharmacological uses, and phytochemical constituents were mentioned. From few medication values of plant parts, to treat rheumatism, madness, snakebite, chest pain, jaundice chest pain, malaria, headache, cough, etc. All the medicinal plants are shown in the table form with the scientific name, families, local name, and importance. Most plants were reported and investigated in Ethiopia. As reported by many authors, some medicinal plants with their scientific name, family, local name and their importance are shown in Table 23 , and these plant species listed in this review were often used by the people in Ethiopia.

Phytochemicals

Analysis of the phytochemical properties of the medicinal plants used to show and isolate the drug, lead compounds and components from the parts of the plant. The unique biological activity of the plants can be identified by their phytochemicals properties. Most parts of the plants used for the analysis of the phytochemical properties were leaves, roots, stem barks, and fruits. In this review, medicinal plants were investigated for phytochemical constituents of ethanol, methanol, chloroform, acetone, hexane, petroleum ether, ethyl acetate, and aqueous (water) extraction of different phytochemicals.

In this review, the most published articles recognized the presence of phytochemical components in the plants was indicated by the positive sign (+) and the absence of phytochemical components in the plants, by the negative sign (−) as shown in table.

Alkaloids are one of the main and largest components produced by plants, and they are metabolic byproducts that are derived from the amino acids (Naseem 2014 ). Based on the published articles in these reviews, alkaloids were extracted from the different parts of the plants using different solvents such as ethanol, methanol, chloroform, acetone, hexane, petroleum ether, ethyl acetate, and aqueous (water). These types of solvents extract phytochemical components from medicinal plants like leaves, roots, stem bark, and fruits.

Flavonoids consist of a large group of polyphenol compounds having a benzoyl-γ-pyrone structure and are ubiquitously present in plants. They are synthesized by the phenylpropanoid pathway. Available reports tend to show that secondary metabolites of a phenolic nature including flavonoids, are responsible for the variety of pharmacological activities (Mahomoodally et al. 2005 ; Pandey 2007 ). Flavonoids are hydroxylated phenolic substances and are known to be synthesized by plants in response to microbial infection (Dixon et al. 1983 ). In this review, flavonoids were detected in most plant species but in some medicinal plants were not present the same plant but different solvents like eucalyptus and Agenda Abyssinia leaves.

The term tannin is widely applied to a complex large biomolecule of polyphenol nature having sufficient hydroxyls and other suitable groups such as carboxyl to form strong complexes with various macromolecules (Navarrete 2013 ). In this present review, tannins were detected in most plant species like peel and juice of Citrus medica, mango ( Mangifera indica L .) leaves, Avocado fruit ( Persea Americana ), Dioscorea alata leaf , of Leucas aspera L . leaf and root, Ocimum gratissimum Linn leaf, Rhamnus prinoides root, extract of Rhizomes , Zingiber officinale and Curcuma longa and also for different solvent give different response for the same plant species like Bersama abyssinica leaf, F lax seeds , Nigella sativa , Ruta chalepensis leaves, and Syzygium guineense and not totally detected in part of plants like Lepidium sativum seeds and love Gilbetii root. Tannins are generally used in the tanning process and used as healing agents in inflammation, burn, piles, and gonorrhea (Boroushaki et al. 2016 ).

Saponins are an important group of plant secondary metabolites that are widespread throughout the plant kingdom. Saponins are basically phytochemicals that are found in most vegetables, beans, and herbs (Francis et al. 2002 ; Haralampidis et al. 2002 ). In this review, saponins were detected in most medicinal plants like citrus fruit juice , of Mango ( Mangifera indica L .) leaves, Avocado fruit ( Persea americana ), Leucas aspera L . leaf, and root, Rhamnus prinoides root, Bitter ( Vernonia amygdalina ) leaf and Stem bark of Vernonia amygdalina in common plant species and some plants were shown different results, that depends on solvent and also not totally detected in part of the plant such as Bersama abyssinica leaf, Dioscorea alata leaf, love Gilbertii root, and Flax seeds .

The word steroid is derived from sterol, which is a natural or synthetic chemically active hormone-like element. A steroid is one of a large group of chemical substances classified by a specific carbon structure. Steroids include drugs used to relieve swelling and inflammation, such as prednisone and cortisone; vitamin D; and some sex hormones, such as testosterone and estradiol (Hill et al. 2007 ). For this review, Steroids were detected in most plant species like citrus fruit juice , peel and juice of citrus Medica , Flaxseeds , Nigella sativa , Ocimum gratissimum Linn leaf, Syzygium guineans root, and Root and Stem bark of Vernonia amygdalina in common plant species while in some plant species were shown variable result that depends on the given solvents and not totally detected in the part of the plant like Rhamnus prinoides root.

Terpenoids are small molecular products synthesized by plants and are probably the most widespread group of natural products. Terpenoids show significant pharmacological activities, such as antiviral, antibacterial, antimalarial, anti-inflammatory, inhibition of cholesterol synthesis, and anti-cancer activities (Boroushaki et al. 2016 ). As mentioned earlier, Terpenoids were detected in most analysis plant species such as citrus fruit juice , Hagenia abyssinica leaves, Leucas aspera L . leaf and root, Flax seeds , Ocimum gratissimum linn leaf, Ruta chalepensis leaves, and Syzygium guineans root while in some plants its result depends on the types of solvents.

Phenolic compounds are secondary metabolites, which are produced in the shikimic acid of plants and pentose phosphate through phenylpropanoid metabolization (Derong Lin et al. 2016 ). In this review, phenolic was detected in most the medicinal plants like citrus fruit juice, peel and juice of citrus medica, mango ( Mangifera indica L .) leaves and Avocado fruit ( Persea Americana ), eucalyptus leaves, Flax seeds , Rhamnus prinoides root, of Rhizomes , Zingiber officinale, and Curcuma longa but some medicinal plant is given different response and depend on the solvents.

Even though there are so many medicinal plants in Ethiopia, this review of the phytochemical analysis shows that some medicinal plants were studied by the investigator in different areas of Ethiopia, while some traditional plants are not studied. According to the data of published articles, the extraction techniques of the medicinal plants were mainly digestion and aqueous-alcohol extraction. From Tables show that phytochemical investigation results are available in the Ethiopia area levels.

Above the Table 1 , phytochemical screening of alkaloids, tannins, saponins, flavonoids, phenols and phytosterols were the secondary metabolites found in the crude extract of Echinops amplexicaulis , Ruta chalepensis , and Salix subserrata . The methanol extracts of Echinops amplexicaulis and Salix subserrata contain most of the secondary metabolites.

In terms of the qualitative phytochemical investigation of the medicinal plants, the medicinal plants extract had different phytochemicals constituents such as saponins, tannins, alkaloids, terpenoids, anthraquinones, phenolic compounds, cardiac glycosides, and flavonoids (Table 2 ).

Phytochemical investigations from these medicinal plants have shown a large number of organic complex and biologically active compounds.

The results of the qualitative phytochemicals analysis showed that the leaf extracts of Lippia adonis var. koseret also indicated the presence of tannins, flavonoids, polyphenols, alkaloids and saponins, while in the case of ethyl acetate alkaloids were not detected and tannins were absent in petroleum ether extract (Table 3 ). Amino acids and carbohydrates were absent in all three extracts.

In this review, phytochemical screening of Bersama abyssinica leaf in Table 4 shown that the most published articles recognized the presences of specific phytochemical components in the plants was indicated by the positive sign (+) and the absence of phytochemical components in the plants, by the negative sign (−). These phytochemical constituents in Bersama abyssinica leaf were shown variable results that depend on the given solvents and are not totally detected in Bersama abyssinica leaf.

The results in Table 5 show that there are phytochemical components in Citrus fruit juice concentrates. These phytochemical constituents all are found in citrus fruit juice concentrates except cardiac glycosides were not detected in lemon and they indicated highly medicinal values. It can be suggested that the presence of phenols, alkaloids, flavonoids, saponins, steroids, and reducing sugar in Citrus fruit juice indicates are highly medicinal value.

From Table 6 , flavonoids, phenols, tannins, steroids, coumarin and cardioactive glycosides: have shown positive tests of ethyl acetate, and methanol extracts of peel and juice of citrus medica, while some phytochemical positive test and totally not detected like (anthraquinones, alkaloids, and terpenoids). These secondary metabolites are known to be biologically active and play significant roles in the bioactivity of medicinal plants because the medicinal values of the medicinal plant lie in these phytochemical compounds which produce a definite and specific action on the human body.

Based on the given data from Table 7 , phytochemical screening of ethanol extract of mango ( Mangifera indica L .) leaves and Avocado ( Persea americana ) fruits almost all are were detected but terpenoids were not detected in Mango ( Mangifera indica L .). The phytochemical are naturally occurring chemicals in plants which serve as medicinal for the protection of human disease; the phytochemicals are nonnutritive plants chemical that have protection or disease preventive properties.

In this review, the phytochemical analysis revealed the presence of flavonoids, phenols, and tannins while the terpenoids positive test of methanol extract and the remaining phytochemical components are were not detected. These results show that phytochemical depend on solvents (Table 8 ).

Table 9 , the presence of flavonoid, tannin, and phenol in methanol extract. The acetone extract obtained from the eucalyptus leaves was screened for phytochemicals. Qualitative phytochemical screening of acetone extract of eucalyptus leaves demonstrated the presence of saponins, carbohydrate, tannin, and phenol, while quinone, fat, protein, and flavonoid were absent.

In this review, the methanol, ethanol, n-hexane, and petroleum ether extract obtained from the Hagenia abyssinica leaves were screened for various phytochemicals from Table 10 . Qualitative phytochemical screening of methanol extract of Hagenia abyssinica leaves demonstrated the presence of saponins, flavonoids, phenols, terpenoids, steroids, and glycosides, while tannins, anthraquinones, and alkaloids were absent. Phytochemical analysis of ethanol extract of Hagenia abyssinica leaves demonstrated the presence of saponins, tannins, phenols, terpenoids, and alkaloids, while steroids, glycosides and phlobatannins were absent. A similarity that phytochemical screening of n -hexane extract of Hagenia abyssinica leaves demonstrated the presence of flavonoids, anthraquinones and terpenoids but saponins, tannins, alkaloids, steroids, glycosides, and phlobatannins are not detected and Hagenia abyssinica leaves extracted by petroleum ether were obtained presence of phytochemical only saponins and terpenoids, while other phytochemicals are not detected.

Phytochemicals screening in the plant extracts revealed the presence of flavonoid, stereol and polyterpenes, and saponified present in both methanol and ethyl acetate extract of Lepidium sativum s eeds and also flavonoids were present in petroleum ether extract of Lepidium sativum seeds while other phytochemical components were not detected (Table 11 ).

In this review, phytochemical screening of the aqueous, methanol, and hexane extracts of Leucas aspera L . leaf and root revealed the presence of various medically active constituents from Table 12 . Almost all phytochemical compounds present in the aqueous, methanol, and hexane extracts of Leucas aspera L . leaf and root were identified except cholesterol and steroids in the parts of leaf and root by aqueous. These plants indicate highly medicinal values.

Phytochemical screening of the love Gilbertii root suggests the presence of major phytochemicals in the root extracts (Table 13 ). Dichloromethane: methanol of roots showed the presence of alkaloids, anthraquinones, and flavonoids whereas; tannins, saponins, and terpenoids were not presented.

As result in Table 14 , screening for phytochemicals in the plant extracts almost all presents in both acetone and methanol extracts of Flax seeds, while some phytochemical is not detected like tannins, saponins in acetone extract of Flax seeds and also saponins were presented by methanol extract of flaxseeds. In addition to this phytochemicals screening of ethanol and water extract of flaxseeds almost phytochemical components presents and some phytochemicals not totally detected. These secondary metabolites are known to be biologically active and play significant roles in the bioactivity of medicinal plants because the medicinal values of the medicinal plant lie in these phytochemical compounds which produce a definite and specific action on the human body.

This review was shown in the (Table 15 ) phytochemical analysis of petroleum ether and ethyl acetate seed extract of Nigella sativa contains tannins, steroids, terpenoids and alkaloids, flavonoids, phenol, glycosides and steroids were found in the extract and are potent methanol soluble while some phytochemicals were not presented since it depends on the solvents.

In the present review, phytochemical screening of methanol and aqueous extracts of Ocimum gratissimum Linn leaf showed that the presence of tannins, phlorotannins, steroids, terpenoids, flavonoids and cardiac glycosides with steroidal ring whereas, saponins and sugar were not present in methanol solvent and also alkaloids were not absent in Table 16 . These detected phytochemical compounds are known to have beneficial importance in medicinal as well as physiological activities. In this manner, isolating and identifying these bioactive compounds, new drugs can be formulated to treat various diseases and disorders.

Table 17 shows the phytochemicals detected in Rhamnus prinoides root extract. Tests for triterpenes, saponins, tannins, phenols, glycosides, cardiac glycosides, and resins were positive in both aqueous and methanol/water extracts. Alkaloids were detected only in the methanol/water extract while steroids, flavonoids, flavones, and anthraquinones were not detected in both aqueous and methanol/water extracts. These phytochemicals may be responsible for the medicinal value of Rhamnus prinoides .

Phytochemical screening of ethanol/water (1:1) extract of Rhizomes, Zingiber officinale, and Curcuma longa showed the presence of phenolic, flavonoids, glycosides, and tannins whereas alkaloids were not present (Table 18 ).

The phytochemical analysis of Ruta chalepensis leaves extract in methanol showed that phytochemical components include; alkaloids, flavonoids, terpenoids, cardiac glycosides, phenols, saponins, tannins and anthraquinones and steroids were not present. Steroids, terpenoids and saponins were additionally present in both ethyl acetate and acetone extract, and also flavonoids, terpenoids, and anthraquinones were detected in the n-hexane extract, while others were not totally found in Table 19 .

In Table 20 , the presence of steroids, terpenoids, saponins, flavonoids, flavonoids, tannins, alkaloids, phenol, and glycosides were present in both dichloromethane/methanol and methanol extracts and steroids and terpenoids also were present in n-hexane extract whereas other phytochemicals components were not detected.

From Table 21 , it can be seen that the sample extracts showed positive tests for the presence of alkaloids, saponin, tannins, phlorotannin, glycosides, and flavonoids except for anthraquinones. Therefore, Bitter ( Vernonia amygdalina ) is the most frequently used for medicinal purposes.

In this review, the results revealed the presence of alkaloids, steroids, glycosides, saponin, and phlorotannin methanol extracts from the root and stem bark of Vernonia amygdalina whereas only tannins and phenols were not detected (Table 22 ). Therefore, the phytochemical screening results reveals that the presence of these phytochemical constituents supports the use of the Vernonia amygdalina plant in folklore medications and it is probable that these phytochemicals are responsible for the healing properties.

A total of 53 traditional medicinal plants were identified in this review. All of the reviewed plants have direct traditional uses for treating either ailment with cancer-like symptoms (determined by the traditional practitioner) or for laboratory-confirmed cancer cases. Medicinal plants have continued to be the most affordable and easily accessible source for the treatment of several human and livestock ailments in Ethiopia. Besides treating cancer, the plants selected in this review are also cited for their various traditional uses, including for the treatment of eczema, leprosy, rheumatism, gout, ringworm, diabetes, respiratory complaints, warts, hemorrhoids, syphilis, and skin diseases (Table 23 ). The output calls for the need for further phytochemical and pharmacological investigation giving priority to those plants which have been cited most for their use to treat cancer.

In Ethiopia, there are increasing demands for many most popular, more available, and effective plant species by the people. As stated by the different authors in the above Tables, different phytochemicals were investigated in different plant species with different solvent concentrations. Even though different phytochemicals were analyzed for different plant species, their concentration varied from one plant species to another plant species for different parts of the plant. Based on the above information from the Table, one type of phytochemical cannot be detected in all plant species and the concentration of one phytochemical content varies from one part of the plant to another part which mean the concentration of one phytochemical content in leaves can vary from the concentrations of phytochemical contents in root and fruits. Generally, even though there are various medicinal plants in Ethiopia, there are no studies that show enough information about qualitative and quantitative phytochemical contents for most plant species in the country. This may be due to the lack of enough laboratory facilities and modern technology available in the country for improving the synthesis and extraction of phytochemical components for developing the new drug product and drug leading compounds from the different parts of the medicinal plants by the government and private company.

In conclusion, this study showed the wide use of medicinal plants in Ethiopia. Even though there is a wealth of indigenous knowledge transfer is declining from generation to generation as a result of oral transmission. Human beings around the world have spent their lives for a long time to discovering a new drug to diagnose, prevent and treat various diseases. To save their lives from dangerous diseases, a new and powerful drug must be discovered and developed from the different parts of the plant. In order to future promote for development of new drug synthesis and extraction of bioactive components from the parts of the plant, availability, and value of information is very important. From tables, phytochemicals analysis of different medicinal plants revealed the presence of various bioactive compounds such as polyphenols, flavonoids, phenolic compounds alkaloids, saponins, tannins, phlobatannins, glycosides, anthraquinones, steroids, terpenoids, and triterpene. Based on the above data available in the review, most phytochemical components of traditional medicinal plants in Ethiopia are not analyzed. This leads to more traditional plants in Ethiopia are not being recognized by the international scientific organization, not how to use medicinal plants for disease treatment and they do not have scientific names. This review recommended finding further most common medicinal plants to investigate in scientific research and to governing them in the scientific naming system and as well as further studies should focus on green synthesis of heavy metals on different types of medicinal plants in Ethiopia. Based on this review, the studied phytochemical characteristics of medicinal plants in Ethiopia are few, so further study could be needed for examining, and characterizing the properties of unrecognized plant species in Ethiopia.

Availability of data and materials

The datasets used during the current study are available online in different forms such as books, various published journals and google scholar.

Abbreviations

Cirsium Englerianum

Cucumis Pustulatus

Discopodium Penninervium

Euphorbia Depauperata

Lippia Adoensis

Polysphaeria Aethiopica

Rumex Abyssinica

World Health Organization

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First and foremost, I would like to praise the Almighty God, and his wife Elsa Aweke for bestowing upon my health, strength, patience and protection throughout my study period.

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Agidew, M.G. Phytochemical analysis of some selected traditional medicinal plants in Ethiopia. Bull Natl Res Cent 46 , 87 (2022). https://doi.org/10.1186/s42269-022-00770-8

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Worldwide research trends on medicinal plants.

1. Introduction

2. materials and methods, 3.1. global evolution trend, 3.2. global subject category, 3.3. distribution of publications by countries, 3.4. institutions (affiliations), 3.5. authors, 3.6. keywords, 3.6.1. global perspective, 3.6.2. keywords related to plants, 3.7. clusters, 3.8. collaboration network of countries, 4. conclusions, author contributions, acknowledgments, conflicts of interest.

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Salmerón-Manzano, E.; Garrido-Cardenas, J.A.; Manzano-Agugliaro, F. Worldwide Research Trends on Medicinal Plants. Int. J. Environ. Res. Public Health 2020 , 17 , 3376. https://doi.org/10.3390/ijerph17103376

Salmerón-Manzano E, Garrido-Cardenas JA, Manzano-Agugliaro F. Worldwide Research Trends on Medicinal Plants. International Journal of Environmental Research and Public Health . 2020; 17(10):3376. https://doi.org/10.3390/ijerph17103376

Salmerón-Manzano, Esther, Jose Antonio Garrido-Cardenas, and Francisco Manzano-Agugliaro. 2020. "Worldwide Research Trends on Medicinal Plants" International Journal of Environmental Research and Public Health 17, no. 10: 3376. https://doi.org/10.3390/ijerph17103376

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• Published: 25 April 2018

Quantitative study of medicinal plants used by the communities residing in Koh-e-Safaid Range, northern Pakistani-Afghan borders

• Wahid Hussain 1 ,
• Lal Badshah 1 ,
• Manzoor Ullah 2 ,
• Maroof Ali 3 ,
• Asghar Ali 4 &
• Farrukh Hussain 5  

Journal of Ethnobiology and Ethnomedicine volume  14 , Article number:  30 ( 2018 ) Cite this article

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The residents of remote areas mostly depend on folk knowledge of medicinal plants to cure different ailments. The present study was carried out to document and analyze traditional use regarding the medicinal plants among communities residing in Koh-e-Safaid Range northern Pakistani-Afghan border.

A purposive sampling method was used for the selection of informants, and information regarding the ethnomedicinal use of plants was collected through semi-structured interviews. The collected data was analyzed through quantitative indices viz. relative frequency citation, use value, and family use value. The conservation status of medicinal plants was enumerated with the help of International Union for Conservation of Nature Red List Categories and Criteria (2001). Plant samples were deposited at the Herbarium of Botany Department, University of Peshawar for future reference.

One hundred eight informants including 72 male and 36 female were interviewed. The informants provided information about 92 plants species used in the treatment of 53 ailments. The informant reported maximum number of species used for the treatment of diabetes (16 species), followed by carminatives (12 species), laxatives (11 species), antiseptics (11 species), for cough (10 species), to treat hepatitis (9 species), for curing diarrhea (7 species), and to cure ulcers (7 species), etc. Decoction (37 species, i.e., 40%) was the common method of recipe preparation. Most familiar medicinal plants were Withania coagulans , Caralluma tuberculata , and Artemisia absinthium with relative frequency (0.96), (0.90), and (0.86), respectively. The relative importance of Withania coagulans was highest (1.63) followed by Artemisia absinthium (1.34), Caralluma tuberculata (1.20), Cassia fistula (1.10), Thymus linearis (1.06), etc. This study allows identification of novel uses of plants. Abies pindrow , Artemisia scoparia , Nannorrhops ritchiana , Salvia reflexa , and Vincetoxicum cardiostephanum have not been reported previously for their medicinal importance. The study also highlights many medicinal plants used to treat chronic metabolic conditions in patients with diabetes.

Conclusions

The folk knowledge of medicinal plants species of Koh-e-Safaid Range was unexplored. We, for the first time, conducted this quantitative study in the area to document medicinal plants uses, to preserve traditional knowledge, and also to motivate the local residents against the vanishing wealth of traditional knowledge of medicinal flora. The vast use of medicinal plants reported shows the significance of traditional herbal preparations among tribal people of the area for their health care. Knowledge about the medicinal use of plants is rapidly disappearing in the area as a new generation is unwilling to take interest in medicinal plant use, and the knowledgeable persons keep their knowledge a secret. Thus, the indigenous use of plants needs conservational strategies and further investigation for better utilization of natural resources.

The residents of remote areas mostly depend on folk knowledge of medicinal plants to cure different ailments. Plants not only provide food, shelter, fodder, drugs, timber, and fuel wood, but also provide different other services such as regulating different air gases, water recycling, and control of different soil erosion. Hence, phytodiversity is required to fulfill several human daily livelihood needs. Millions of people in developing countries commonly derive their income from different wild plant products [ 1 ]. Ethnomedicinal plants have been extensively applied in traditional medicine systems to treat various ailments [ 2 ]. This relationship goes back to the Neanderthal man who used plants as a healing agent. In spite of their ancient nature, international community has recognized that many indigenous communities depend on biological resources including medicinal plants [ 3 ]. About 80% of the populations in developing countries rely on medicinal plants to treat diseases, maintaining and improving the lives of their generation [ 4 , 5 ]. The people, in most parts of the world particularly in rural areas, rely on traditional medicinal plants’ remedies due to easy availability, cultural acceptability, and poor economic conditions. Out of the total 422,000 known angiosperms, more than 50,000 are used for medicinal purposes [ 6 ]. Some 75% of the herbal drugs have been developed through research on traditional medicinal plants, and 25% of prescribed drugs belong to higher plants [ 7 ]. Traditional knowledge has a long historical cultural heritage and rich natural resources that have accumulated in the indigenous communities through oral and discipleship practices [ 8 ]. Traditional indigenous knowledge is important in the formulation of herbal remedies and isolates bioactive constituents which are a precursor for semisynthetic drugs. It is the most successful criterion for the development of novelties in drugs [ 9 , 10 , 11 ]. Traditional knowledge can also contribute to conserve and sustain the use of biological diversity. However, traditional knowledge, especially herbal health care system, has declined in remote communities and in younger generations as a result of a shift in attitude and ongoing socio-economic changes [ 12 ]. The human communities are facing health and socio-economic problems due to changing environmental conditions and socio-economic status [ 13 ]. The tribal people have rich unwritten traditional medicinal knowledge. It rests with elders and transfers to younger orally. With rapid economic development and oral transmitted nature of traditional knowledge, there is an urgent need to systematically document traditional medicinal knowledge from these communities confined in rural and tribal areas of the world including Pakistan. The Koh-e-Safaid Range is one of the remote tribal areas of Pakistan having unique and century-old ethnic characteristics. A single hospital with limited insufficient health facilities is out of reach for most inhabitants. Nature has gifted the area with rich diversity of medicinal plants. The current advancement in the use of synthetic medicines has severely affected the indigenous health care system through the use of medicinal traditional practices in the area. The young generation has lost interest in using medicinal plants, and they are reluctant to practice traditional health care system that is one of the causes of the decline in traditional knowledge system. Quantitative approaches can explain and analyze the variables quantitatively. In such approach, authentic information can be used for conservation and development of existing resources. Therefore, the present research was conducted in the area to document medicinal uses of local plants with their relative importance, to record information for future investigation and discovery of novelty in drug use, and to educate the locals about the declining wealth of traditional and medicinal flora from the area.

Ethnographic and socio-economic background of the study area

Koh-e-Safaid Range is a tribal territory banding Pakistan with Afghanistan in Kurram Agency. It lies between 33° 20′ to 34° 10′ N latitudes and 69° 50′ to 70° 50′ E longitudes (Fig.  1 ).This area is federally administered by the Government of Pakistan. The Agency is surrounded on the east by Orakzai and Khyber agencies, in the southeast by Hangu district, and in the south by North Waziristan Agency and Nangarhar and Pukthia of Afghanistan lies on its west. The highest range of Koh-e-Safaid is Sikaram peak with, 4728 m height. The Agency is well-populated with many small fortified villages receiving irrigation water from Kurram River that flows through it. The weather of the Agency is mostly pleasant in summer; however, in winters, freezing temperature is experienced, and sometimes falls to − 10 °C. The weather charts website “Climate-Charts” ranked it as the fourth coldest location in Pakistan. Autumn and winter are usually dry seasons while summer and spring receive much of the precipitation. The total population of the Agency according to the 2017 censuses report is 253,478. Turi, Bangash, Sayed, Maqbal, Mangel, Khushi, Hazara, Kharote, and Jaji are the major tribes in the research area. The joint family system is practiced in the area. Most of the marriages are held within the tribe; however, there is no ban on the marriages outside the tribe. Marriage functions are communal whereby all relatives, friends, and village people participate with songs, music, and dances male and female separately. The death and funeral ceremonies are jointly attended by the friends and relatives. The people of the area follow Jirga to resolve their social and administrative problems. This is one of the most active and strong social institutions in the area. Economically, most people in the area are poor and earning their livelihoods by menial jobs. The professional includes farmers, pastoralists, shopkeepers, horticulturists, local health healers, wood sellers, and government servants. In the adjoining areas of the city, pastorals keep domestic animals and are considered a better source of income.

Map of the study area and area location in Pakistan

Sampling method

The study was conducted through purposive sampling by informants’ selection method. The selection of informants was primary based on the ethnomedicinal plants and their willingness to share the information. The selection criteria include people who prescribe recipes for treatment; people involved in buying, collection, or cultivation of plants; elder members of above 60 years age; and young literate members. The participants were traditional healers, plant collectors, farmers, traders, and selected knowledgeable elders above 60 years age and young ones. The interviews were conducted in local Pashto language in the local dialect. The informants were involved in the gathering of data with a consent of village tribe chieftains called Maliks.

Data collection

Semi-structured open-ended interviews were conducted for the collection of ethnomedicinal information from April 2015 to August 2017. Informants from 19 localities were interviewed including Sultan, Malikhail, Daal, Mali kali, Alam Sher, Kirman, Zeran, Malana, Luqman Khail, Shalozan, Pewar, Teri Mangal, Bughdi, Burki, Kharlachi, Shingak, Nastikot, Karakhila, and Parachinar city (Fig.  1 ). The objectives of this study were thoroughly explained to all the informants before the interview [ 14 ]. Data about medicinal plants and informants including local names of plants, preparation of recipes, storage of plant parts, informant age, occupation, and education were collected during face-to-face interviews. A questionnaire was set with the following information: informant bio-data, medicinal plant use, plant parts used and modes of preparation, and administration of the remedies. Plants were confirmed through repeated group discussion with informants [ 15 , 16 ]. For the identification of plants, informants were requested for transect walks in the field to locate the cited plant for confirmation.

Collection and identification of medicinal plants

The medicinal plants used in traditional treatment of ailments in the study area were collected with the help local knowledgeable persons, traditional healers, and botanists. The plants were pressed, dried, and mounted on herbarium sheet. The field identification was confirmed by a taxonomist in the Herbarium Department of Botany, University of Peshawar. The voucher specimens of all species were numbered and deposited in the Herbarium of Peshawar University (Fig.  2 ).

Landscape of Kurram Valley ( a winter, b summer). c , d Traditional healers selling herbal drugs on footpath. e Trader crushing Artemisia absinthium for marketing. f Principal author in the field during data collection. g , h Plant collectors in subalpine zone. i Lilium polyphyllum rare species distributed in subalpine zone. j Ziziphora tenuior endangered species of subtropical zone

Data analysis

The information about ethnomedicinal uses of plants and informants included in questionnaires such as botanical name, local name, family name, parts used, mode of preparation, use reports, frequency of citation, relative importance, and voucher number were tabulated for all reported plant species. Informants’ use reports for various ailments and frequency of citation were calculated for each species. The relative importance of species was calculated according to use-value formula (UV = UVi/Ni) [ 17 ], where “UVi” is the number of citations for species across all informants and “Ni” the number of informants. The citation probability of each medicinal plant across all informants was equal to avoid researchers’ biasness. Family use value was calculated using the formula FUV = UVs/Ns, where “UVs” represent the sum of use values of species falling within family, and Ns represents the number of species reported for the family. The conservation status of wild medicinal plants species was enumerated by applying International Union for Conservation of Nature (IUCN) criterion (2001) [ 18 ].

Informants’ knowledge about medicinal plants and their demography

A total of 108 including 72 male and 36 female informants were interviewed from 19 locations. The three groups of male respondents were falling in the age groups of 21 to 40, 41 to 60, and 61 to 80 years having the numbers of 19, 19, and 34, respectively. Among the female respondents, 10 aged 21 to 40, 14 aged 41 to 60, and 12 aged 61 to 80 years. Among the informants, 15 males were illiterate, 34 were matriculate, 13 were intermediate, and 10 were graduates. Among the females, 19 were illiterate, 16 were matriculate, and only 1 was graduate (Table  1 ). Informants were shepherd, healers, plant collectors, gardeners, and farmers. Twenty-eight informants of above 60 years age, living a retired life, were also interviewed. It was found that males were more knowledgeable than females. Furthermore, health healers were more knowledgeable.

Diversity of medicinal plants

A total of 92 medicinal species including 91vascular plant species belonging to 50 families and 1 mushroom Morchella of Ascomycetes of family Morchellaceae were reported (Table  2 ) . Asteraceae had eight species followed by seven species of Lamiaceae and Rosaceae. Three species were contributed by each of Moraceae, Asclepiadaceae, Polygonaceae, Brassicaceae, Solanaceae, Cucurbitaceae, and Liliaceae. Of the remaining eight families, namely, Poaceae, Pinaceae, Zingiberaceae, Chenopodiaceae, Plantaginaceae, Apiaceae, Fabaceae, and Zygophyllaceae, each one contributed two species [ 19 , 20 ]. Asteraceae, Lamiaceae, and Rosaceae were also reported with a high number of plants used for medicinal purposes. The reported plants were collected both from the wild (86.9%) and cultivated (13.1%) sources. However, greater percentage of medicinal plants from wild sources indicated higher species’ diversity in the study area. The 62 herbs species, 16 tree, 12 shrubs, and 2 undershrubs species were used in medicinal preparation for remedies.

Plant parts used in preparation of remedies

The plant parts used in the preparation of remedies were root, rhizome, bulbils, stem, branches, leaves, flowers, fruits, seeds, bark, resin, and latex. The relative use of these plant parts is shown in (Fig.  3 ). Fruits were frequently used plant part (26 species), followed by leaves (23 species) and remaining parts (21 species).

Plant parts used in the formulation of remedies

Preparation and mode of administration of remedies

The collection of data for the preparation of remedies from medicinal plants is extremely important. Such information is essential for identification of active ingredients and intake of relevant amount of drug. The present research observed seven methods for preparing recipes. It included decoction, powder, juice, infusions, roast, and ash methods (Fig.  4 ). The 37 species (40%) were most frequently used for the preparation of remedies. A plant part is boiled while infusion is obtained by soaking plant material in cold or hot water overnight. Eleven species (14%) are in powdered form, 11species (14%) in vegetable form, 7 species (9%) in juice form, 7 species (9%) in infusions form, 3 species (4%) in roasted form, and 1 species (2%) in ash form were used. Twenty-seven plant parts were used directly. It included wild fruits that were consumed for their nutritional and medicinal purpose. The most frequently used mode of administration of remedies was oral intake practice of 74 species (79%) followed by both orally and topically practice of 11 species (12%) and topically of 8 species (9%) (Fig.  5 ).

Different modes of drug formulation

Route of administration of drugs

Medicinal plants use categories

The inhabitants used medicinal plants in the treatment of 53 health disorders. The important disorders were cancer, diabetic, diarrhea, dysentery, hepatitis, malaria, and ulcer (Table.  3 ). These disorders were classified into 17 categories. Among the ailments, most plants were used for the treatment of digestive problems mainly as carminative (12 species), diarrhea (11 species), laxative (11 species), ulcer (7 species), appetizer (5 species), colic pain (4 species), and anthelmintic (4 species). Such higher use of plants for the treatment of digestive problems had been reported in ethnobotanical studies conducted in another tribal area of Pakistan [ 21 ]. The other categories (18 species) were used to treat respiratory disorders, followed by endocrine disorders (16 species); antiseptic and anti-inflammatory (15 species); circulatory system disorders (15 species); integumentary problems (15 species); antipyretic, refrigerant, and analgesic (9 species); and hepatic disorders (9 species). However, among the ailments, the highest number of plants were used in the treatment of diabetes (16 species), followed by antiseptic (11 species), cough (10 species), hepatitis (9 species), and ulcer (7 species). Among the remaining species, the informants reported three and two species used against malaria and cancer, respectively (Table  3 ).

Quantitative appraisal of ethnomedicinal use

Based on the quantitative indices, the analyzed data showed that few plants were cited by the majority of the informants for their medicinal value. Seventeen plant species with the highest citation frequency are shown in (Fig.  6 ). The highest citation frequency was calculated for Withania coagulans (0.96), followed by Caralluma tuberculata (0.90), and Artemisia absanthium (0.86). The high values of these species indicated that most of the informants were familiar with their medicinal value. However, the familiarity of these three plants could be linked to their collection for economic purposes [ 22 ]. Withania coagulans (1.63), Artemisia absinthium (1.34), Caralluma tuberculata (1.20), Cassia fistula (1.10), and Thymus linearis (1.06) were reported having the highest used values for medicinal purposes (Fig.  7 ). All these species were used for the cure of three or more diseases. The powdered fruit of Withania coagulans is used for the cure of stomach pain, constipation, diabetes, and ulcer. The next highest use value was calculated for Artemisia absinthium with five medical indications as diabetes, malaria, fever, blood pressure, and urologic problems. Among the remaining three plants, Caralluma tuberculata is used for diabetes, cancer, and stomachic problems, and as blood purifier; Cassia fistula for colic pain and stomach pain and as a carminative agent; and Thymus linearis for cough and as carminative and appetizer. Lowest use value was calculated for Rununculus muricatus (0.04) with next three species having same lowest use value: Abies pindrow (0.05), Lepidium virginicum (0.05), and Oxalis corniculata (0.05). Highest family use value was calculated for Juglandaceae (0.86), followed by Cannabaceae (0.78), Apiaceae (0.75), Asclepiadaceae (0.71), Fumariaceae (0.71), Berberidaceae (0.70), Fabaceae (0.67), Punicaceae (0.65), Solanaceae (0.64), and Asteraceae (0.61). This is the first study that presents a quantitative value of medicinal plants used in the investigated area.

Medicinal plants with highest relative frequency citation

Medicinal plants with highest relative importance

Conservation status of the medicinal flora

Plant preservation means the study of plant declination, their causes, and techniques to protect rare and scarce plants. Plant conservation is a fairly new field that emphasizes the conservation of biodiversity and whole ecosystems as opposed to the conservation of individual species [ 23 ]. The ex situ conservation must be encouraged for the protection of medicinal plants [ 24 ]. In the present case, the area under study is under tremendous anthropogenic pressure as well. Therefore, ex situ conservation of endangered species is recommended. The woody plants, cut down for miscellaneous purposes, are facing conservational problems. Sayer et al. [ 25 ] reported that large investments are being made in the establishment of tree plantation on degraded area in Asia [ 25 ]. Alam and Ali stressed that proper conservation studies are almost negligible in Pakistan [ 26 ]. Same is the case with the study area as no project has been initiated for the conservation of forest or vegetation so far. Anthropogenic activities, small size population, distribution in limited area, and specificity of habitat were observed as the chief threats to endangered species.

According to IUCN Red List Criteria (2001) [ 18 ] conservation status of 80 wild medicinal species have been assessed based on availability, collection status, growth status, and their parts used. The remaining 12 medicinal plants were cultivated species. Of these, 7 (8.7%) species are endangered, 34 (42.5%) species are vulnerable, 29 (36.2%) species are rare, 9 (11.2%) species are infrequent, and only 1 (1.3%) species is dominant. The endangered species were Caralluma tuberculata , Morchella esculenta , Rheum speciforme , Tanacetum artemisioides , Vincetoxicum cardiostephanum , Withania coagulans , and Polygonatum verticillatum.

Traditional medicines are a vital and often underestimated part of health care. Nowadays, it is practiced in almost every country of the world. Its demand is currently increasing rapidly in the form of alternative medicine [ 20 ]. Ethnomedicinal plants have been widely applied in traditional medicine systems to treat various ailments. About 80% of the populations in developing countries rely on medicinal plants to treat diseases, maintaining and improving the lives of their generation [ 19 ]. Traditional knowledge has a long historical cultural heritage and rich natural resources that has accumulated in the indigenous communities through oral and discipleship practices [ 8 ]. Traditional indigenous knowledge is important in the formulation of herbal remedies and isolates bioactive constituents which are a precursor for semisynthetic drugs. It is the most successful criterion for the development of novelties in drugs [ 11 ]. A total of 92 medicinal species including 91 vascular plant species belonging to 50 families and 1 mushroom Morchella of Ascomycetes of family Morchellaceae were reported (Table  2 ) . The current study reveals that the family Asteraceae represents eight species followed by seven species of Lamiaceae and Rosaceae each which showed a higher number of medicinal plants. Three species were contributed by each of Moraceae, Asclepiadaceae, Polygonaceae, Brassicaceae, Solanaceae, Cucurbitaceae, and Amaryllidaceae. While the remaining eight families, namely, Poaceae, Pinaceae, Zingiberaceae, Chenopodiaceae, Plantaginaceae, Apiaceae, Fabaceae, and Zygophylaceae, contributed two species each. Asteraceae, Lamiaceae, and Rosaceae were also reported with a high number of plants used for medicinal purposes. Indigenous use of medicinal plants in the communities residing in Koh-e-Safid Range of Pakistan is evident. Traditional health healers are important to fulfill the basic health needs of the economically poor people of the area. The high dependency on traditional healers is due to limited and inaccessible health facilities. Most people either take recipes from local healers or select wild medicinal plants prescribed by them. Some elders also knew how to preserve medicinal plant parts for future use. Traditional knowledge of medicinal plants is declining in the area due to lack of interest in the young generation to acquire this traditional treasure. Furthermore, most traditional health healers and knowledgeable elders hesitate to disseminate their recipes. Therefore, traditional knowledge in the area is diminishing as aged persons are passing away. Vernacular names of plants are the roots of ethnomedicinal diversity knowledge [ 27 ]. They can clear the ambiguity in the identification of medicinal plants within an area. It also helps in the preservation of indigenous knowledge of medicinal plants. The medicinal plants were mostly reported with one specific vernacular name in the investigated area. While Rosa moschata and Rosa webbiana were known by same single vernacular name as Jangle Gulab. Few species were known by two vernacular names: Curcuma longa as Korkaman or Hildi, Ficus carica as Togh or Anzer, Fumaria indica as Chamtara or Chaptara, Marrubium vulgare as Dorshol or Butaka, Solanum nigrum as Bartang or Kharsobay, Teucrium stocksianum as Harboty or Gulbahar, and Thymus linearis as Paney or Mawory. The informants also mentioned different vernacular names for species even belonging to single genus; Plantago lanceolata as Chamchapan or Ghuyezaba and Plantago major as Ghazaki or Palisepary. Majority of the species commonly had a single name. However, local dialects varied in few species, i. e., Withania coagulans was known by three names: Hapyanaga, Hafyanga, and Shapynga, Caralluma tuberculata as Pamenny or Pawanky, Foeniculum vulgare as Koglany or Khoglany, and Viola canescens was called as Banafsha or Balamsha. The species with high use value need conservation for maintaining biodiversity in the study area. However, in the present case, no project or programs for the conservation of forest or vegetation are operating. Grazing and unsustainable medicinal uses were observed as the chief hazard to highly medicinal plant species. The higher use of herbs can be attributed to their abundance, diversity, and therapeutic potentials as antidiabetic, antimalarial, antipyretic, antiulcerogenic, antipyretic, blood purifier, and emollient and for blood pressure, hepatitis, stomach pain, and itching. Aloe vera , cultivated for ornamental purpose, is used as wound healing agent. Among the plant parts, the higher use of fruit may relate to its nutritional value. The aerial parts of the herbaceous plants were mostly collected in abundance and frequently used for medicinal purposes. In many recipes, more than one part was used. The utilization of roots, rhizomes, and the whole plant is the main threat in the regeneration of the medicinal plants [ 28 ]. In the current study, decoction was found to be the main method of remedy preparation as reported in the ethnopharmacological studies from other parts [ 29 , 30 , 31 ]. Fortunately, we collected important information like preparation of remedies and their mode of administration for all the reported plants. However, the therapeutic potential of few plants are connected to their utilization method. A roasted bulb of Allium cepa is wrapped on the spine-containing wound to release the spine. The leaf of Aloe vera containing viscous juice is scratched and wrapped on a wound. The latex of Calotropis procera is first mixed with flour and then topically applied on the skin for wound healing. Infusion of Cassia fistula fruit’s inner septa is prepared for stomach pain and carminative and colic pain in children. The fruit of Citrullus colocynthis boiled in water is orally taken for the treatment of diabetes. Grains of Hordeum vulgare are kept in water for a day, and its extraction is taken for the treatment of diabetes. The decoction of Seriphidium kurramensis shoots are used as anti-anthelmintic and antimalaria. The leaves of Juglans regia are locally used for cleaning the teeth and to prevent them from decaying. Furthermore, its fruit is used as brain tonic, and its roasted form is useful in the treatment of dysentery. The roots of Pinus wallichiana are cut into small pieces and put into the pot. The cut pieces are boiled, and the extracted liquid is poured into the container. One drop of the extracted liquid is mixed with one glass of milk and taken orally once a day as blood purifier. An infusion of Thymus linearis aerial parts is prepared like hot tea and is drunk for cough and as appetizer and carminative. A decoction of Zingiber officinale rhizome is drunk at night time for relief of cough. Medicinal plants are still practiced in tribal and rural areas as they are considered as main therapeutic agents in maintaining better health. Such practices have been described in the ethnobotanical studies conducted across Pakistan. The current study reveals several plant species with more than one medical use including Artemisia absanthium , Cichorium intybus , Fumaria indica , Punica granatum , Tanacetum artemisioides , Teucrium stocksianum , and Withania coagulans . Their medicinal importance can be validated from indigenous studies conducted in various parts of the country. Amaranthus viridis leaf extract is an emollient and is used for curing cough and asthma as well [ 32 ]. Artemisia absanthium is used for the treatment of malaria and diabetes [ 33 , 34 , 35 , 36 ]. Cichorium intybus is used against diabetes, malaria, and gastric ulcer, and it is also used as digestive and laxative agent [ 28 , 37 , 38 , 39 , 40 , 41 ]. Leaves of Cannabis sativa are used as bandage for wound healing; powdered leaves as anodyne, sedative, tonic, and narcotic; and juice added with milk and nuts as a cold drink [ 42 ]. Whole plant of Fumaria indica [ 36 ] and Tanacetum artemisioides [ 43 ] is used for treating constipation and diabetes, respectively. Dried rind powder and fruit extract of Punica granatum are taken orally for the treatment of anemia, diarrhea, dysentery, and diabetes [ 44 , 45 , 46 , 47 ]. A decoction of aerial parts of Teucrium stocksianum is used for curing diabetes [ 29 , 48 ]. Withania coagulans is known worldwide [ 38 , 49 ] as a medicinal plant, whose fruit decoction is best remedy for skin diseases and diabetes. Its seeds are used against digestive problems, gastritis, diabetes, and constipation [ 21 , 28 , 50 ]. Our results are in line with the traditional uses of plants in the neighboring counties [ 8 ]. For example, Fumaria indica is used as blood purifier, and Hordeum vulgare grains decoction for diabetes; Juglans regia bark for toothaches and scouring teeth; Mangifera indica seed decoction for diarrhea; Solanum nigrum extract for jaundice; and Solanum surattense fruit decoction for cough have been documented in the study (40) . Such agreements strengthen our results and provide good opportunity to evaluate therapeutic potential of the reported plants. Three plants species Adiantum capillus-veneris , Malva parviflora , and Peganum harmala have been documented for their medicinal use in the ethnobotanical study [ 51 ]. According to this, the decoction of the aerial parts of Adiantum capillus-veneris is used for the treatment of asthma and dyspnea. Malva parviflora root and flower are used for stomach ulcers. Peganum harmala fruit powder and decoction are used for toothache, gynecological infections, and menstruation. The dried leaves of Artemisia absanthium is used to cure stomach pain and intestinal worm while an inflorescence paste prepared from its fresh leaves is used as wound healing agent and antidiabetic [ 52 , 53 ]. The bulb of Allium sativum is used in rheumatism while its seed vessel mixed with hot milk is useful for the prevention of tuberculosis and high blood pressure. The fruit bark of Punica granatum is used in herbal mixture for intestinal problems [ 54 ]. Avena sativa decoction is used for skin diseases including eczema, wounds, irritation, inflammation, erythema, burns, itching, and sunburn [ 55 ]. Foeniculum vulgare and Lepidium sativum are used for the treatment of diabetes and renal diseases [ 53 ]. Verbascum thapsus leaves and flowers can be used to reduce mucous formation and stimulate the coughing up of phlegm. Externally, it is used as a good emollient and wound healer. Leaves of Thymus linearis are effective against whooping cough, asthma, and round worms and are an antiseptic agent [ 21 ]. Berberis lycium wood decoction with sugar is the best treatment for jaundice. Chenopodium album has anthelmintic, diuretic, and laxative properties, and its root decoction is effective against jaundice. The whole plant decoction of Fumaria indica is used for blood purification. Dried leaves and flowers of Mentha longifolia are used as a remedy for jaundice, fever, asthma, and high blood pressure [ 36 ]. Morus alba fruit is used to treat constipation and cough [ 42 ]. Oxalis corniculata roots are anthelmintic, and powder of Chenopodium album is used for headache and seminal weakness [ 47 ]. Boiled leaves of Cichorium intybus are used for stomachic pain and laxative while boiled leaves of Plantago major are used against gastralgia [ 56 ]. Viola canescens flower is used as a purgative [ 32 ]. The above ethnomedicinal information confirms the therapeutic importance of the reported plants. The reported plant species show biological activities which suggest their therapeutic uses. The aqueous extract of Allium sativum has been studied for its lipid lowering ability and was found to be effective at the amount of 200 mg/kg of body weight. It also has significant antioxidant effect and normalizes the activities of superoxide dismutase, catalase, glutathione peroxidase, and glutathione reductase in the liver [ 57 ]. An extract of Artemisia absanthium antinociception in mice has been found and was linked to cholinergic, serotonergic, dopaminergic, and opioidergic system [ 58 ]. The ethanolic extract of Artemisia absanthium at a dose of 500 and 1000 mg/kg body weight has reduced blood glucose to significant level [ 59 ]. The hepatoprotective activity of crude extract of aerial parts of Artemisia scoparia was investigated against experimentally produced hepatic damage through carbon tetrachloride. The experimental data showed that crude extract of Artemisia scoparia is hepatoprotective [ 60 ]. Ethanolic and aqueous extracts from Asparagus exhibited strong hypolipidemic and hepatoprotective action when administered at a daily dose of 200 mg/kg for 8 weeks in hyperlipidemic mice [ 61 , 62 ]. The extract of Calotropis procera was evaluated for the antiulcerogenic activity by using different in vivo ulcer in pyloric-ligated rats, and significant protection was observed in histamine-induced duodenal ulcers in guinea pigs [ 63 ]. Cannabidiol of Cannabis sativa was found as anxiolytic, antipsychotic, and schizophrenic agent [ 64 ]. Caralluma tuberculata methanolic extract of aerial parts (500 mg/kg) in fasting blood glucose level in hyperglycemic condition decreased up to 54% at fourth week with concomitant increase in plasma insulin by 206.8% [ 65 ]. The aqueous and methanol crude extract of Celtis australis , traditionally used in Indian system of medicine, was screened for its antibacterial activity [ 66 ]. Cichorium intybus L. whole plant 80% ethanolic extract a percent change in serum glucose has been observed after 30 min in rats administrated with vehicle, 125, 250, and 500 mg notified as 52.1, 25.2, 39, and 30.9%, respectively [ 67 ]. Citrullus colocynthis fruit, pulp, leaves, and root have significantly decreased blood glucose level and restored beta cells [ 30 , 68 , 69 , 70 ]. The two new aromatic esters horizontoates A and B and one new sphingolipid C were isolated from Cotoneaster horizontalis . The compounds A and B showed significant inhibitory effects on acetylcholinesterase and butylcholinesterase in a dose-dependent manner [ 71 ]. The alkaloids found in Datura stramonium are organic esters used clinically as anticholinergic agents [ 72 ]. The methanolic extract of Momordica charantia fruits on gastric and duodenal ulcers was evaluated in pylorus-ligated rats; the extract showed significant decrease in ulcer index [ 73 ]. Antifungal activity of Nannorrhops ritchiana was investigated against fungal strains Aspergillus flavus , Trichophyton longifusis , Trichophyton mentagrophytes , Aspergillus flavus , and Microsporum canis were found susceptible to the extracts with percentage inhibition of 70–80% [ 74 ]. The inhibitory effects of Olea ferruginea crude leaf extract on bacterial and fungal pathogens have been evaluated [ 75 ]. The aqueous extract of Plantago lanceolata showed that higher doses provide an overall better protection against gastro-duodenal ulcers [ 76 ]. The oral and intraperitoneal management of extracts reduced the gastric acidity in pylorus-ligated mice [ 77 ]. The antiulcer effect of Solanum nigrum fruit extract on cold restraint stress, indomethacin, pyloric ligation, and ethanol-induced gastric ulcer models and ulcer healing activity on acetic acid-induced ulcer model in rats [ 78 , 79 ]. The antifungal activity (17.62 mm) of Viola canescens acetone extract 1000 mg/ml against Fusarium oxysporum has been observed [ 80 ]. Leaf methanolic extract of Xanthium strumarium has inhibited eight pathogenic bacteria at a concentration of 50 and 100 mg/ml [ 81 ]. Aqueous extract of the fruits of Withania coagulans in streptozotocin-induced rats at dose of 1 g/kg for 7 days has shown significant decrease ( p  < 0.01) in the blood glucose level (52%), triglyceride, total cholesterol, and low density lipoprotein and very significant increase ( p  < 0.01) in high density lipoprotein level [ 31 ]. This shows that further investigation on the reported ethnomedicinal plants can lead to the discovery of novel agents with therapeutic properties.

In the current study, conservation status of 80 medicinal species was reported which was growing wild in the area. The information was collected and recorded for different conservation attributes by following International Union for Conservation and Nature (2001) [ 18 ]. It was reported that seven species (8.7%) were endangered due to the much collection, anthropogenic activities, adverse climatic conditions, small size population and distribution in limited area, specificity of habitat, and over grazing in the research area. However, the below-mentioned species were found to be endangered: Caralluma tuberculata , Morchella esculenta , Rheum speciforme , Tanacetum artemisioides , Vincetoxicum cardiostephanum , Withania coagulans , and Polygonatum verticillatum . Unsustainable use and lack of suitable habitat have affected their regeneration and pushed them to endangered category. Traditional knowledge can also contribute to conservation and sustainable use of biological diversity [ 19 , 20 ].

Novelty and future prospects

Ethnomedicinal literature research indicated that five plant species, Abies pindrow , Artemisia scoparia , Nannorrhops ritchiana , Salvia reflexa , and Vincetoxicum cardiostephanum , have not been reported previously for their medicinal importance from this area. The newly documented uses of these plants were Abies pindrow and Salvia reflexa (antidiabetic), Artemisia scoparia (anticancer), Nannorrhops ritchiana (laxative), and Vincetoxicum cardiostephanum (chest problems). Adiantum capillus-veneris is reported for the first time for its use in the treatment of skin problems. These plant species can be further screened for therapeutic agents and their pharmacological activities in search of novel drugs. The study also highlights 16 species of antidiabetic plants Caralluma tuberculata , Momordica charantia , Marrubium vulgare , Artemisia scoparia , Melia azedarach , Salvia reflexa , Citrullus colocynthis , Tanacetum artemisioides , Quercus baloot , Olea ferruginea , Cichorium intybus , Artemisia absinthium , Hordeum vulgare , Teucrium stocksianum , Withania coagulans , and Abies pindrow . Except sole paper from District Attack, Pakistan [ 28 ], such a high number of antidiabetic plants have not been reported previously from any part of Pakistan in the ethnobotanical studies.

Traditional knowledge about medicinal plants and preparation of plant-based remedies is still common in tribal area of Koh-e-Safaid Range. People due to closeness to medicinal plants and inaccessible health facilities still rely on indigenous traditional knowledge of plants. The role of traditional healers in the area is observable in primary health care. The locals used medicinal plants in treatment of important disorders such as cancer, diabetes, hepatitis, malaria, and ulcer. The analyzed data may provide opportunities for extraction of new bioactive constituents and to develop herbal remedies. The study also confirmed that the communities residing in the area have not struggled for conservation of this traditional treasure of indigenous knowledge and medicinal plants. Medicinal plant diversity in the remote and backward area of Koh-e-Safaid Range has great role in maintaining better health conditions of local communities. Therefore, conservation strategies should be adopted for the protection of medicinal plants and traditional knowledge in the study area to sustain them in the future.

Abbreviations

Family use value

International Union for Conservation of Nature

The number of informants

Represent the number of species reported for the family

The number of citations for a species across all informants

Represent sum of use values of species falling within family

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Acknowledgements

This work is part of the Doctoral research work of the principal (first) author. The authors also acknowledge the participants for sharing their valuable information.

Authors’ contribution

WH conducted the collection of field data and wrote the initial draft of the manuscript. LB supervised the project. MU and MA helped in the field survey, sampling, and identification of taxon. AA and FH helped in the data analysis and revision of the manuscript. All the authors approved the final manuscript after revision.

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Hussain, W., Badshah, L., Ullah, M. et al. Quantitative study of medicinal plants used by the communities residing in Koh-e-Safaid Range, northern Pakistani-Afghan borders. J Ethnobiology Ethnomedicine 14 , 30 (2018). https://doi.org/10.1186/s13002-018-0229-4

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Pharmacological and behavioral investigation of putative self-medicative plants in Budongo chimpanzee diets

Contributed equally to this work with: Elodie Freymann, Fabien Schultz

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* E-mail: [email protected] (EF); [email protected] (FS)

Affiliation Primate Models for Behavioural Evolution Lab, Institute of Human Sciences, Department of Anthropology and Museum Ethnography, University of Oxford, Oxford, United Kingdom

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Affiliations Primate Models for Behavioural Evolution Lab, Institute of Human Sciences, Department of Anthropology and Museum Ethnography, University of Oxford, Oxford, United Kingdom, Gorongosa National Park, Sofala, Mozambique, Interdisciplinary Centre for Archaeology and the Evolution of Human Behaviour, University of Algarve, Faro, Portugal

Roles Funding acquisition, Supervision, Writing – review & editing

Affiliations Ethnopharmacology & Zoopharmacognosy Research Group, Department of Agriculture and Food Sciences, Neubrandenburg University of Applied Sciences, Neubrandenburg, Germany, ZELT–Center for Nutrition and Food Technology gGmbH

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Affiliation Ethnopharmacology & Zoopharmacognosy Research Group, Department of Agriculture and Food Sciences, Neubrandenburg University of Applied Sciences, Neubrandenburg, Germany

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Affiliations Wild Minds Lab, School of Psychology and Neuroscience, University of St Andrews, St Andrews, United Kingdom, Budongo Conservation Field Station, Masindi, Uganda

Affiliation Wildlife Research Center, Inuyama Campus, Kyoto University, Inuyama, Japan

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Affiliation Budongo Conservation Field Station, Masindi, Uganda

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Affiliations Budongo Conservation Field Station, Masindi, Uganda, Czech University of Life Sciences Prague, Prague, Czech Republic

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Affiliations Budongo Conservation Field Station, Masindi, Uganda, Department of Comparative Cognition, Institute of Biology, University of Neuchâtel, Neuchâtel, Switzerland

Roles Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Writing – original draft, Writing – review & editing

Affiliations Ethnopharmacology & Zoopharmacognosy Research Group, Department of Agriculture and Food Sciences, Neubrandenburg University of Applied Sciences, Neubrandenburg, Germany, Pharmacognosy and Phytotherapy, School of Pharmacy, University College of London, London, United Kingdom

• Elodie Freymann, 
• Susana Carvalho, 
• Leif A. Garbe, 
• Dinda Dwi Ghazhelia, 
• Catherine Hobaiter, 
• Michael A. Huffman, 
• Geresomu Muhumuza, 
• Lena Schulz, 
• Daniel Sempebwa, 

• Published: June 20, 2024
• https://doi.org/10.1371/journal.pone.0305219
• Reader Comments

Wild chimpanzees consume a variety of plants to meet their dietary needs and maintain wellbeing. While some plants have obvious value, others are nutritionally poor and/or contain bioactive toxins which make ingestion costly. In some cases, these nutrient-poor resources are speculated to be medicinal, thought to help individuals combat illness. In this study, we observed two habituated chimpanzee communities living in the Budongo Forest, Uganda, and collected 17 botanical samples associated with putative self-medication behaviors (e.g., bark feeding, dead wood eating, and pith-stripping) or events (e.g., when consumer had elevated parasite load, abnormal urinalysis, or injury). In total, we selected plant parts from 13 species (nine trees and four herbaceous plants). Three extracts of different polarities were produced from each sample using n -hexane, ethyl acetate, and methanol/water (9/1, v/v ) and introduced to antibacterial and anti-inflammatory in vitro models. Extracts were evaluated for growth inhibition against a panel of multidrug-resistant clinical isolates of bacteria, including ESKAPE strains and cyclooxygenase-2 (COX-2) inhibition activity. Pharmacological results suggest that Budongo chimpanzees consume several species with potent medicinal properties. In the antibacterial library screen, 45 out of 53 extracts (88%) exhibited ≥40% inhibition at a concentration of 256 μg/mL. Of these active extracts, 41 (91%) showed activity at ≤256μg/mL in subsequent dose-response antibacterial experiments. The strongest antibacterial activity was achieved by the n- hexane extract of Alstonia boonei dead wood against Staphylococcus aureus (IC50: 16 μg/mL; MIC: 32 μg/mL) and Enterococcus faecium (IC50: 16 μg/mL; MIC: >256 μg/mL) and by the methanol-water extract of Khaya anthotheca bark and resin against E . faecium (IC50: 16 μg/mL; MIC: 32 μg/mL) and pathogenic Escherichia coli (IC50: 16 μg/mL; MIC: 256 μg/mL). We observed ingestion of both these species by highly parasitized individuals. K . anthotheca bark and resin were also targeted by individuals with indicators of infection and injuries. All plant species negatively affected growth of E . coli . In the anti-inflammatory COX-2 inhibition library screen, 17 out of 51 tested extracts (33%) showed ≥50% COX-2 inhibition at a concentration of 5 μg/mL. Several extracts also exhibited anti-inflammatory effects in COX-2 dose-response experiments. The K . anthotheca bark and resin methanol-water extract showed the most potent effects (IC50: 0.55 μg/mL), followed by the fern Christella parasitica methanol-water extract (IC50: 0.81 μg/mL). This fern species was consumed by an injured individual, a feeding behavior documented only once before in this population. These results, integrated with associated observations from eight months of behavioral data, provide further evidence for the presence of self-medicative resources in wild chimpanzee diets. This study addresses the challenge of distinguishing preventative medicinal food consumption from therapeutic self-medication by integrating pharmacological, observational, and health monitoring data—an essential interdisciplinary approach for advancing the field of zoopharmacognosy.

Citation: Freymann E, Carvalho S, Garbe LA, Dwi Ghazhelia D, Hobaiter C, Huffman MA, et al. (2024) Pharmacological and behavioral investigation of putative self-medicative plants in Budongo chimpanzee diets. PLoS ONE 19(6): e0305219. https://doi.org/10.1371/journal.pone.0305219

Editor: Armel Jackson Seukep, University of Buea, CAMEROON

Received: January 9, 2024; Accepted: May 25, 2024; Published: June 20, 2024

Copyright: © 2024 Freymann et al. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All relevant data are within the manuscript and its Supporting Information files.

Funding: Funding for this project was granted by the the Clarendon Fund at the University of Oxford (to EF), the British Institute of Eastern Africa (to EF), Keble College at the University of Oxford (to EF), Boise Trust Fund (to EF), German Federal Ministry of Education and Research (13FH026IX5, PI: L-AG and Co-I: FS) (to LAG, FS) and Neubrandenburg University of Applied Sciences (grant # 13310510) (to LAG, FS).

Competing interests: The authors have declared that no competing interests exist.

Introduction

‘Medicinal foods’ refer to resources in the diet that have potential curative value due to the presence of plant secondary metabolites (PSMs) [ 1 , 2 ]. PSMs are compounds that usually occur only in special, differentiated cells [ 3 ] and which help plants defend against predators, pathogens, and competitors [ 4 – 7 ]. PSMs can have a range of functions, including the inhibition of microbial, fungal, and competitor growth [ 8 ]. While some PSMs can be toxic at high doses, these compounds can also promote the health of human and non-human consumers [ 8 – 10 ]. Research suggests 15–25% of primate and other mammalian diets consist of medicinal foods [ 9 , 11 ]. These resources likely play a critical role in animal health-maintenance by passively preventing or reducing the impact of parasitic infections or other pathogens [ 9 – 14 ].

While most animals likely consume foods with medicinal properties as part of their normal diets, fewer species have been shown to engage in therapeutic self-medication. Huffman [ 15 ] defines this type of self-medicative behavior as the active extraction and ingestion, by an ill individual, of medicinal resources with little nutritional value. Instead of an individual passively benefiting from a plant’s medicinal properties through normal feeding, this form of self-medication requires basic awareness of the resource’s healing properties. One of the best-studied animals to engage in this form of self-medication is our closest living relative: the chimpanzee.

Wild chimpanzees ( Pan troglodytes ), across at least sixteen field sites [ 15 ] have demonstrated therapeutic self-medication using two well-established self-medicative behaviors: leaf swallowing [ 16 , 17 ] and bitter-pith chewing [ 18 ]. Leaf swallowing, first reported by Wrangham [ 19 , 20 ] and described by Wrangham & Nishida [ 21 ], involves the careful selection and ingestion of whole, hispid leaves. This behavior was later demonstrated to expel internal parasites (i.e. Oesophagostomum sp. and Bertiella studeri ) from the gut [ 16 , 17 , 22 , 23 ]. The functional mechanism responsible for this anthelminthic effect is considered to be primarily “mechanical” [ 9 ] as, rather than a chemical compound, the leaf’s indigestibility, brought about by the trichomes on its surface—stimulates gut motility in the swallower [ 17 , 23 , 24 ].

The second established behavior is bitter-pith chewing, which involves the stripping of outer bark and leaves from the soft new stem growth of the shrub, Vernonia amygdalina , exposing the inner pith. Individuals chew the pith and ingest only the bitter juices while spitting out the fibers [ 18 , 25 ]. Bitter-pith chewing is considered ‘phytochemical’ self-medication [ 9 ], as its anthelminthic effect appears to be the result of bioactive PSMs [ 26 – 29 ]. This behavior’s medicinal effect was associated with a significant drop in the infection intensity of Oesophagostomum stephanostomum nematodes [ 25 ], suggesting that the bitter compounds directly affect the adult worms. This hypothesis was supported by in vivo studies conducted by Jisaka et al. [ 30 ], demonstrating that extracts from the pith permanently paralyzed adult Schistosome parasites. V . amygdalina is also used to aid gastrointestinal discomfort and other signs of parasitosis in humans and livestock, symptoms also displayed by chimpanzees ingesting the plant’s bitter pith [ 9 , 18 , 25 , 31 ]. The bitter piths of other plant species are reported to be chewed by chimpanzees across field sites but detailed studies on their medicinal properties have yet to be conducted [ 9 ].

Beyond these two established behaviors, not much is known about the phytochemical self-medicative repertoires of wild chimpanzees, although some behaviors associated with the ingestion of specific plant parts or processing techniques have been recommended for further investigation [ 9 , 15 , 32 ]. One of these behaviors is bark feeding, which involves the ingestion of living stem bark and/or cambium [ 33 ], and which has been observed in at least eleven established field sites [ 33 – 43 ]. Bark feeding has been suggested as a medicinal behavior in chimpanzees and other primates, used to aid in the chemical control of intestinal nematode infection and to relieve gastrointestinal upset [ 9 ]. Bark is characteristically highly fibrous, heavily lignified, sometimes toxic, relatively indigestible, and nutrient-poor [ 44 ]. However, the contribution of bark in chimpanzee diets and toward general health is still poorly understood [though see: 45 ]. In this study, the bark of eight species ingested by Budongo chimpanzees ( Scutia myrtina , Cynometra alexandri , Alstonia boonei , Ficus exasperata , Ficus variifolia , Syzygium guineense , Desplatsia dewevrei , Khaya anthotheca) was screened for antibiotic and anti-inflammatory properties, to better understand the function of bark feeding behaviors and the role this behavior may play in the health maintenance of chimpanzees. For the species K . anthotheca , we tested a mixture of bark and congealed resin, which Budongo chimpanzees were observed to particularly target throughout the study period.

Another putative self-medicative behavior is dead wood eating [ 9 , 35 ], which involves the consumption of decomposing cambium from dead trees. To date, the majority of studies examining this behavior in apes have focused on exploring potential mineral and nutritional benefits, rather than investigating pharmacological properties [ 46 – 49 ]. Many of these studies suggest that dead wood is exploited by chimpanzees as a source of sodium in environments where this mineral is otherwise scarce [ 48 , 49 ]. Our study evaluates the pharmacology of two species of dead wood ( A . boonei and Cleistopholis patens) consumed by the Sonso community of chimpanzees to determine whether this behavior may have multiple functions or health benefits.

The ingestion of pith material from other species has also been suggested as putatively self-medicative [ 34 , 50 , 51 ]. However, unlike V . amygdalina bitter-pith, some of these plant piths appear bland or tasteless. While Wrangham et al. have previously suggested that pith is likely a high-fiber fallback food [ 52 ], De la Fuente et al. review several pith species targeted by chimpanzees with proposed medicinal properties [ 32 ]. In our study, two species of non-bitter piths ( Marantachloa leucantha and Acanthus polystachyus) , were collected for pharmacological assessment. M . leucantha was observed on several occasions being stripped, masticated, and spat out after the juice was extracted from the pith, whereas A . polystachyus was observed being stripped, masticated, and swallowed. Both of these species are also ingested by chimpanzees in Kibale National Park, Uganda [ 52 ].

Establishing phytochemical self-medicative behaviors in wild animals is difficult and time consuming, as the burden of proof is high, self-medicative events can be rare relative to other behaviors, and methods often require multidisciplinary expertise and collaboration [ 9 ]. Past studies have utilized ethnopharmacological methods to determine specific medicinal properties of foods consumed by primates [ 11 ], greatly advancing our understanding of the relationship between primate diets and health. However, a key challenge for establishing novel self-medicative behaviors is differentiating between medicinal food consumption and therapeutic self-medication. While pharmacological data interpreted on its own is crucial for establishing the presence of medicinal resources in chimpanzee diets, the integration of observational and health monitoring data is needed to parse therapeutic self-medicative behaviors from normal feeding behaviors with inadvertent health benefits. Furthermore, the importance of collecting in situ samples from the locations where putative self-medicative behaviors are observed is paramount, as ecological, climatic, and anthropogenic variables can cause variation in the bioactivity of plants across habitats [ 53 ].

In total, we investigated the bioactivity of 51 plant extracts produced from 17 part-specific samples (across 13 species), collected in the Budongo Forest. Each extract was tested for inhibition of bacterial growth as well as anti-inflammatory COX-2 inhibition activity. Due to limitations in scope, funding, and the unavailability of anthelminthic assays for wild animal parasites, none were not conducted in this study, restricting specific identification of parasiticidal behaviors. Assay results are reported and contextualized in this study with direct behavioral evidence and health monitoring data.

Materials and method

Study site and subjects.

Behavioral data, health monitoring metrics, and botanical samples were collected from the Budongo Central Forest Reserve in Uganda (1°35′– 1°55′ N, 31°18′–31°42′ E). An overview of methodological workflow can be found in S2 Fig . The Budongo Conservation Field Station (BCFS) site, founded in 1990, is composed of continuous, semi-deciduous forest and contains two habituated Eastern chimpanzee ( Pan troglodytes schweinfurthii ) communities [ 54 ]. The Sonso community has been studied continuously since 1992, and the ages, social relationships, demographics, and diet of its members are well documented [ 55 , 56 ]. The Sonso population was ~68 individuals at the time of data collection, and the home range covered an area of ~5.33 km 2 [ 57 ]. Waibira, a larger group of at least 105 individuals, was more recently habituated, with consistent data collection beginning in 2011. The Waibira maximum home range area was ~10.28 km 2 [ 57 ].

Behavioral data collection

All samples were collected in the Budongo Forest within the Sonso home range, based on behavioral observations from the study period and supporting evidence from the site’s long-term data of their use. Behavioral and health data were collected from two neighboring chimpanzee communities, each for one four-month field season (Sonso: June-October 2021, Waibira: June-October 2022). Data collected between June-September 2021 informed subsequent plant sample collection for pharmacological analysis, which occurred in early September 2021. Behavioral data collected after sample collection provided additional behavioral context for ingestion of these species. Behavioral data were collected between 07:00 and 16:30 in Sonso and between 06:30 and 17:00 in Waibira using day-long focal animal follows sensu Altman et al. [ 58 ]. This data was recorded using Animal Observer (AO) on iPad and ad libitum feeding events were recorded for any unusual feeding behaviors, including but not limited to bark ingestion, dead wood eating, pith stripping, and geophagy. All feeding events were filmed on a Sony Handycam CX250. We prioritized focal follows on individuals with wounds, high or diverse parasite loads identified through on-going monitoring, or known ailments. However, consecutive day follows of priority individuals were not always possible—or were avoided when they might contribute to increased stress in particularly vulnerable individuals. Throughout the study, using this protocol, 27 Sonso individuals (♂:11; ♀:16) and 24 Waibira individuals (♂:14; ♀:10) were observed. Authors collecting behavioral data were blind to pharmacological results during both study periods.

Health monitoring

Individual health data were recorded in both communities, including opportunistic macroscopic and microscopic fecal analysis and urinalysis testing. While anthelminthic assays were not run in this study, parasite load was opportunistically assessed to provide additional health context for each observation. As the presence of certain helminths may impair a host’s immunological response to bacterial, viral, and protozoal pathogens [ 59 ], parasite load can provide a proxy measurement for overall health. Similarly, a reduced immune system and increased stress caused by co-infections could render a host more susceptible to virulent endoparasites [ 60 , 61 ]. When helminths and/or proglottids were found in samples, they were collected and preserved in ethanol for later identification. To quantify parasite loads, fecal samples were analyzed using the McMaster Method [ 9 , 25 , 62 ]. Urinalysis samples were taken opportunistically using multi-reagent Urine Dipstick Test 9-RC for Urotron RL9 to assess the health and physiological status of group members following methods established by Kaur & Huffman [ 63 ]. Urinalysis metrics considered in this study included: leukocytes (LEU) associated with pyuria caused by UTI, balanitis, urethritis, tuberculosis, bladder tumors, viral infections, nephrolithiasis, foreign bodies, exercise, glomerulonephritis, and corticosteroid and cyclophosphamide use; blood (BLO) associated with peroxidase activity of erythrocytes, and UTIs; and ketones (KET) associated with pregnancy, carbohydrate-free diets, starvation, and diabetes [ 64 ]. Test results were interpreted in situ using a colorimetric scale. We considered a result ‘abnormal’ if the colorimetric scale indicated a positive result when the expected result was negative or if the result was outside the specified test parameters according to the manufacturer.

Plant sample selection for bioactivity testing

Plants were selected for pharmacological testing after three months of data collection in the Sonso community. We selected 10 samples (from 9 species) based on direct observations during this period. These observations included individuals targeting plant parts associated with putative self-medicative behaviors (i.e., bark feeding, dead wood eating, pith-stripping) or sick/wounded individuals seeking out unusually consumed resources. We then selected an additional five species, the ingestion of which had not been directly observed, for testing based on their historical inclusion in Sonso chimpanzees’ bark feeding repertoire. GM, who has worked at the field station for over thirty-years, has previously observed bark feeding on each of these selected species. These historic observations enabled collection of bark samples from specific trees known to have been previously stripped. In two cases, leaf samples were collected from tree species that were also selected for bark samples ( S . guineense and F . exasperata) . While neither Sonso nor Waibira chimpanzees have been observed ingesting the leaves of S . guineense , a sample was collected to enable comparison of bioactivity across plant parts. F . exasperata leaves are consumed in both communities; however, we found no behavioral evidence for use in unusual contexts. In some cases, direct observation of an event involving one of the collected species occurred after botanical collection was complete. These post hoc behavioral observations are reported in this paper, although they did not impact sample selection.

Collection of sample material

Plants were collected from the Sonso community home range following best practice procedures [ 65 ], using sustainable harvesting methods [ 66 ]. See S1 File for more information. Voucher accession numbers are reported in Table 3 . Digital images of voucher specimens can be found in S3 Fig . The currently recognized scientific names of each species were confirmed on https://mpns.science.kew.org/ . Plant family assignments were done in accordance with The Angiosperm Phylogeny Group IV guidance [ 67 ].

Ethnobotanical literature review

We conducted a post-hoc ethnomedicinal review of all species collected for this study using Google Scholar, PROTA, and Kokwaro’s ethnomedicinal pharmacopeia [ 68 ]. To search databases, we used scientific names and synonyms for each plant as keywords [ 65 ].

Plant processing and extractions

At Neubrandenburg University of Applied Sciences, samples were ground using a food processor. Extractions were produced using two solvents and a solvent mixture ( n -hexane, ethyl acetate, and methanol/water ( v/v 9/1)), allowing for the selective isolation of components with varying solubilities and polarities. Methanol-water, the solvent with the highest polarity, generally extracts primary plant metabolites (e.g., polar compounds such as proteins, amino acids, and carbohydrates). Nonpolar solvents like n- hexane extract nonpolar compounds like lipids, making n-hexane a preferred solvent for oil or wax extraction. Extractions with each solvent were achieved through double maceration of new material (non-successively). Extraction suspensions were placed on a shaker at 80 rpm at room temperature for minimum 72h, followed by vacuum filtration. Processes were repeated with the leached material. Filtrates were then combined and dried using a vacuum evaporator, labeled, and stored at -20°C until needed for assays.

Sample solution preparation

To create sample solutions, each crude extract was dissolved in DMSO (Carl Roth) at a concentration of 10 mg/mL. To ensure a homogenous solution, samples were mixed with a vortex mixer and, if necessary, treated with sonication at room temperature or up to 55°C for samples with low solubility. Each extract solution was then tested for inhibition of bacterial growth as well as anti-inflammatory COX-2 inhibition activity. Solutions were stored at -20°C when not in use.

Antibacterial susceptibility tests

A. bacterial strains..

For antibacterial assays, eleven multidrug-resistant clinical isolate strains from nine species were used. This process increased the study’s applicability for early-stage drug discovery, specifically relevant to the threat of antimicrobial resistance (AMR). Seven of these strains (from six species) are classified as ESKAPE pathogens, including Enterococcus faecium (DSM 13590), Staphylococcus aureus (DSM 1104; DSM 18827), Klebsiella pneumoniae (DSM 16609), Acinetobacter baumannii (DSM 102929), Pseudomonas aeruginosa (DSM 1117), and Enterobacter cloacae (DSM 30054), meaning they are highly virulent and resistant to antibiotics [ 69 ]. A strain of the foodborne pathogen Escherichia coli (DSM 498) with AMR as well as a non-resistant E . coli strain (DSM 1576) were also included in the study. Although not an ESKAPE pathogen, E . coli is widely known for causing bacterial diarrhea and AMR strains are a major cause of urinary tract infections [ 70 , 71 ]. Strains of Stenotrophomonas maltophilia (DSM 50170) and Salmonella enterica subsp. enterica (DSM 11320) were also tested. More information on specific clinical isolates/strains, their individual resistance profiles, and antibiotics used can be found in the S5 & S6 Tables in S2 File . Clinical and Laboratory Standards Institute (CLSI) guidelines for broth microdilution testing (M100-S23) were followed [ 72 ].

b. Growth inhibition screening and dose-response study.

The broth dilution in vitro methods for bacterial susceptibility assessment have previously been described by Schultz et al. [ 69 ]. The standardized bacterial working cultures were pipetted into sterile 96-well microtiter plates (Greiner Bio-One International, CELLSTAR 655185). Extracts and antibiotic (64–1 μg/mL), vehicle and sterility controls, were then added into respective wells. Initial optical density measurement (600 nm) was performed, accounting for absorbance of extracts. Plates were incubated at 37°C for 18 h, except for A . baumannii which was incubated for 22h in accordance with strain characteristics ( S5 Table in S2 File ) . After incubation, a final optical density reading (600 nm) was conducted. Percent inhibition values were calculated and the IC 50 and MIC values were determined [ 69 , 73 ]. The IC 50 value is defined as the lowest concentration at which an extract showed ≥ 50% inhibition, and the MIC is the lowest concentration at which an extract displayed ≥ 90% inhibition. A total of 51 samples underwent single-dose pre-screening for growth inhibition (in triplicate) at the concentration of 256 μg/mL on eleven pathogens. Samples showing ≥40% growth inhibition were further tested in a dose-response study with two-fold serial dilution at descending concentrations from 256 to 4 μg/mL. The dose-response experiments were done as biological replicates on separate days in triplicate (technical replicates) to validate reproducibility. Positive controls (antibiotics) and negative controls (vehicle control and sterile media control) were always included. Further details on bacteria standardization can be found in S1 File . Information on plate setup for bacterial library screens and dose-response assays can be found in S4 Fig .

COX-2 inhibition assay

Anti-inflammatory assays were assessed using an in vitro COX inhibitor screening assay kit (Cayman Item No: 701080), with modifications previously described in Schultz et al. [ 74 ]. All extracts were first screened in duplicate for inhibition against human recombinant COX-2 at an initial concentration of 50 μg/mL. For extracts exhibiting at least 50% inhibition, the concentration was then lowered to 10 μg/mL, 5 μg/mL, and 2.5 μg/mL. The most active extracts were taken to dose-response experiments for determination of IC 50 values ( Table 5 ). The assay was done in two steps: 1) the COX reaction step in which the prostaglandin H 2 (PG) was produced (which was further reduced to the more stable prostaglandin F 2α by addition of stannous chloride), and 2) an acetyl choline esterase competitive ELISA step to quantify the produced prostaglandin and calculate a potential enzyme inhibition caused by the extracts. The pure compound and selective COX-2 inhibitor DuP-769 was included as a positive control. DMSO was included as the vehicle control for determining 100% enzyme activity. Information on ELISA plate setup for anti-inflammation assays can be found in S5 Fig .

Ethics statements

Behavioral data used in this study were collected with the approval of the Uganda Wildlife Authority (permit #: COD/96/05) and the Uganda National Council for Science and Technology (permit #: NS257ES). Exportation of samples for pharmacological testing were conducted under UNCST permit #: NS104ES. Behavioral data collection adhered to International Primatological Society’s Code of Best Practice for Field Primatology [ 75 ]. No exported samples were listed under CITES. Plant samples were exported in collaboration with Makerere University (permit #: UQIS00005033/93/PC), issued by the Ugandan government, and transported to Neubrandenburg University of Applied Sciences in accordance with the Nagoya Protocol. A CUREC was approved by the University of Oxford (Ref No.: SAME_C1A_22_080). The authors report no conflict of interest.

Behavioral observations

Several unusual feeding events and putative self-medicative behaviors were recorded over 116 total field days. Table 1 reports all species collected for pharmacological testing and provides behavioral justifications for collection. Images from some of these events can be found in S1 Fig .

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https://doi.org/10.1371/journal.pone.0305219.t001

Individuals with injuries were directly observed ingesting K . anthotheca bark and resin, W . elongata young leaves, C . alexandri bark, and C . parasitica ferns. Individuals exhibiting respiratory symptoms were observed ingesting C . alexandri bark and K . anthotheca bark and resin. Individuals with abnormal urinalysis results (e.g., positive for leukocytes, elevated ketones, and presence of blood) were observed feeding on C . patens dead wood, K . anthotheca bark and resin, and M . leucantha pith. Individuals with recent cases of diarrhea were observed consuming A . boonei and C . patens dead wood, K . anthotheca bark and resin, and W . elongata leaves. Parasitological analyses further suggest individuals with varying degrees of endoparasite infections consumed S . myrtina and C . alexanderi bark, A . boonei and C . patens dead wood, K . anthotheca bark and resin, W . elongata leaves, as well as A . polystachyus and M . leucantha pith. On a day when two individuals were observed leaf swallowing, a scientifically established self-medicative behavior, one was observed consuming K . anthotheca bark and resin, while the other was observed stripping A . polystachyus pith prior to the event. Ingestion of F . variifolia , D . dewevrei , and S . guineense bark were never directly observed during the study period. Examples of bark feeding, dead wood eating, and pith-stripping marks are shown in Fig 1 .

[ a ]: Evidence of F. exasperata bark feeding [ b ] Evidence of C. patens dead wood eating [ c ] Evidence M. leucantha pith-stripping and wadging.

https://doi.org/10.1371/journal.pone.0305219.g001

Ethnobotanical review

Based on our analysis of ethnomedicinal literature spanning various African regions from 1976 to 2022, 11 out of the 13 species tested also had documented ethnomedicinal uses ( Table 2 ).

https://doi.org/10.1371/journal.pone.0305219.t002

Production of extracts and sample information

Taxonomic information and extraction details for the 13 plant species studied, including the plant family, local name (when available), plant part used, solvent for extraction, yield of extraction, extract identification numbers (extract IDs), herbarium accession numbers, and collection location are summarized in Table 3 . Overall, the highest extraction yields were obtained with methanol-water (9/1) as a solvent. The yields from methanol-water extractions for C . parasitica , F . exasperata leaves, and S . guineense stem bark were higher than the other extractions from these samples. The plant samples which had higher yield values with n -hexane, such as the leaves of W . elongata and bark extract of A . boonei , likely have a higher content of lipids (i.e., fatty molecules).

https://doi.org/10.1371/journal.pone.0305219.t003

Library screening against multidrug-resistant human and food bacterial pathogens

Initial screening of extracts involved checking for growth inhibition against each bacterium at a concentration of 256 μg/mL. In total, 45 of the 51 plant extracts (88%) showed activity ≥40% inhibition against at least one of the 11 strains and were thus considered active and brought to dose-response experiments to determine their IC 50 value and MIC. Results from the library screening are reported in S1 Table in S2 File . As all tested plant species in the library screen had at least one extract that was active ( in vitro ) against at least one bacterial strain, no entire species was eliminated for further experimentation. However, as no extracts (at any concentration) inhibited the growth of K . pneumoniae , no further tests were conducted on this bacterium. The extract active against the most bacterial strains (n = 11) was the methanol-water extract of S . guineense stem bark (mwE098a, active against eight strains), followed by the methanol-water S . guineense leaves (mwE098b), the ethyl acetate P . patens dead wood, and the n -hexane A . boonei dead wood (hE092b) extracts, which were each active against seven, seven, and six strains, respectively. The only extract that demonstrated significant inhibition against P . aeruginosa at the highest test concentration was the methanol-water extract from S . guineense bark (mwE098a). This was also the only extract to display significant inhibition at 256 μg/mL against E . cloacae . Of all bacteria in this study, the two strains of E . coli (DSM 498 and DSM 15076) were the most susceptible, with at least one extract from all plant species inhibiting their growth. The E . coli strain with nine known antibiotic resistances (DSM 15076) surprisingly showed growth inhibition in 80% of tested extracts.

Dose-response antibacterial experiments

In dose-response assays, 41 out of the 45 tested extracts (91%) showed activity at ≤256μg/mL, though not all extracts reached MIC values (see Table 4 ). The results, along with standard deviations, are reported in S2 Table in S2 File , while S3 Table in S2 File provides a summary of the number of strains each extract was active against. The strongest in vitro growth inhibition was reported for the methanol-water extract of K . anthotheca bark and resin (mwE088) against Gram-positive E . faecium and the n- hexane extract of A . boonei dead wood (hE092b) against Gram-positive S . aureus (DSM 1104). Both extracts had low IC 50 values of 16 μg/mL (showing strong inhibition), with MIC values of 32 μg/mL against respective strains. E . faecium showed the most general susceptibility to K . anthotheca , with all extracts of this species achieving MIC values (mwE088: 32 μg/mL, eE088: 64 μg/mL, hE088: 128 μg/mL). The ethyl acetate extract of A . boonei dead wood (eE092b) also strongly inhibited the growth of E . faecium (IC 50 : 16 μg/mL; MIC: 64 μg/mL), as did the n- hexane extract of A . boonei dead wood, producing an IC 50 value of 16 μg/mL but failing to reach a MIC value. S . aureus (DSM 1104) was also highly susceptible to the ethyl acetate extracts of A . boonei dead wood (IC 50 : 32 μg/mL; MIC: 128 μg/mL).

https://doi.org/10.1371/journal.pone.0305219.t004

Only one extract, the methanol-water extract of S . guineense bark (mwE098a), was active against the gram-negative P . aeruginosa . This extract exhibited moderate growth inhibition (IC 50 : 64 μg/mL) with no MIC value reached. Despite E . coli (DSM 498) being highly susceptible on the library screen, only two extracts, the methanol-water extract of A . boonei dead wood (mwE092b; IC 50 : 256 μg/mL) and the methanol-water extract of S . guineense leaves (mwE098b; IC 50 : 128 μg/mL), reached IC 50 values at the concentration range tested, with no MICs reached. Interestingly, the strain of E . coli with nine known resistances (DSM 1576) was more susceptible, with 89% (N = 40) of extracts achieving IC 50 values ≤ 256 μg/mL. The most active extract against this strain was the methanol-water extract of K . anthotheca (mwE088; IC 50 : 16 μg/mL; MIC: 256 μg/mL). S . guineense exhibited the highest overall inhibition of S . maltophilia , with all extracts except hE098a displaying IC 50 values of ≤ 256 μg/mL against the bacterium. At the concentration range tested, no extracts yielded MIC values for S . aureus (DSM 18827), A . baumannii , E . cloacae , P . aeruginosa or E . coli (DSM 498).

Anti-inflammatory COX-2 inhibition library screen

Results from the in vitro COX-2 inhibition library screen at descending concentrations are reported in S4 Table in S2 File . At the initial concentration of 50 μg/mL, 43 out of 51 extracts (84%) exhibited an enzyme inhibition of at least 50%, displaying anti-inflammatory activity. This included at least one extract of every plant species. In the next stage of screening, at 10 μg/mL, 18 samples were eliminated. During the final step, at 5 μg/mL, five more were eliminated. The remaining 17 extracts from 10 plant species which displayed inhibition ≥50% at 5 μg/mL, were then introduced to dose-response experiments. The ethyl acetate S . myrtina bark extract (eE089b) was taken to the COX-2 dose-response despite not showing inhibition past 50 μg/mL, as it almost reached the selection limit during analysis and had a relatively high standard deviation. No extracts from W . elongata , C . patens or D . dewevrei showed COX-2 inhibition at 5 μg/mL and thus were excluded from further testing.

COX-2 inhibition dose-response experiments

The most active COX-2 inhibitors were extracts from K . anthotheca (mwE088; hE088; eE088), C . parasitica (mwE087; hE087), F . exasperata (hE093a; eE093a), S . myrtina (hE089a; eE089b), F . variifolia (eE097; hE097), A . polystachyus (hE099; eE099), M . leucantha (hE094), S . guineense (hE098a), A . boonei (hE092b), and C . alexandri (hE096). Results are reported in Table 5 . The strongest COX-2 inhibitor was the K . anthotheca methanol-water bark and resin extract (mwE088) (IC 50 of 0.55 μg/mL), followed by the C . parasitica methanol-water fern extract (mwE087) (IC 50 of 0.81 μg/mL). In contrast, all extracts of the species W . elongata , C . patens , and D . dewevrei failed to show ≥50% inhibition, mostly at the second screening concentration (10 μg/mL). W . elongata extracts notably showed low activity in both antibacterial and COX-2 inhibition assays.

https://doi.org/10.1371/journal.pone.0305219.t005

Plant species with strong pharmacological activity

This study provides the first pharmacological and behavioral evidence of its kind, based on in situ sampling, for the medicinal benefits of bark feeding, dead wood eating, and non-bitter pith stripping behaviors in Budongo chimpanzees. In the following sub-sections, we describe and discuss specific results from five of the tested plant species in further detail. For scope, we selected the two species with the strongest antibacterial properties ( K . anthotheca and A . boonei ) to profile, both of which were the only species to reach 40% inhibition at 16 μg/mL. We also selected C . parasitica to discuss as this species, along with K . anthotheca , exhibited the strongest anti-inflammatory properties. We then discuss results from our S . guineense samples, as this species was effective against the most bacterial strains in our antibacterial assays. Lastly, we selected S . myrtina , as we have behavioral evidence and health data that anecdotally support the use of this species for therapeutic self-medication by Budongo chimpanzees.

Alstonia boonei . Numerous in vitro and in vivo studies, reviewed by Adotey [ 76 ], have reported pharmacological activity in A . boonei bark. However, none of these studies investigated dead wood samples of A . boonei . Consistent with these findings, we found high levels of antibacterial and anti-inflammatory activity in the extracts of this species. Interestingly, extracts from A . boonei dead wood generally exhibited higher activity than living bark. This difference could be due either to a change in active ingredient composition, or possible fungal growth following the tree’s death. While the A . boonei dead wood n -hexane extract (hE092b) exhibited strong growth inhibition against S . aureus (DSM 1104; DSM 18827) and E . faecium at low concentrations in the dose-response assays, the n -hexane bark extract (hE092a) showed no activity <256 μg/mL. Similarly, the ethyl acetate extract of dead wood (eE092b) also strongly inhibited S . aureus (DSM 1104) (IC 50 : 16 μg/mL; MIC: 128 μg/mL) and E . faecium (IC 50 : 16 μg/mL; MIC: 64 μg/mL), while the ethyl acetate bark extract of this species did not even exhibit enough inhibition in the antibacterial library screen to be taken to dose-response assays. However, the methanol-water extract of A . boonei bark (mwE092a) did show activity against E . coli (DSM 498) (IC 50 : 128 μg/mL), as did the methanol-water dead wood extract (mwE092a) (IC 50 : 128 μg/mL), with no MIC values reached in either case. Overall, extracts from A . boonei displayed more potent activity in Gram-positive bacteria, although this effect is more apparent in dead wood than stem bark. In the COX-2 inhibition assays, the n -hexane extract of A . boonei dead wood also showed strong anti-inflammatory inhibition, while the n -hexane extract of the bark only exhibited weak inhibition (at the highest test concentration of 50 μg/mL).

A . boonei is a known medicinal plant across East Africa, commonly used for a variety of reproductive, bacterial, and gastro-intestinal issues, as well as for snake bites, asthma, and dizziness [ 68 , 76 , 77 ]. The bark and latex are intensely bitter, a reliable signal of the presence of bioactive secondary compounds and toxicity [ 94 – 96 ]. Budongo chimpanzees in both communities have been reported to consume both bark and dead wood of A . boonei , often travelling long distances to access these trees and only consuming small amounts of bark per feeding bout [ 45 ]. In an observation reported in this study (see Table 1 : A . boonei , Case 1 ), three males ingested A . boonei dead wood while outside the community’s core area for 1-minute. Two days before the event, one of the individuals had been observed with diarrhea, while also shedding visible tapeworm proglottids ( Bertiella sp.). This sample also contained unidentified protozoa, and Taenia sp. eggs. Pebsworth et al. [ 34 ] also reported an event in which four adult males, all with diverse parasite loads, traveled to a large A . boonei tree and ingested bark.

In the long-term site data, A . boonei bark ingestion was only documented 17 times between 2008–2021 [ 45 ], although this behavior was not systematically reported. In addition, the direct observation of only one A . boonei dead wood eating event, and no A . boonei bark ingesting events over the two four-month periods of observation in this study, suggest that consumption of this species is relatively rare across both communities. While specific pathogenic catalysts for selection of this species remain unknown, based on pharmacological, ethnobotanical, and behavioral data, we propose that A . boonei may be a therapeutic self-medicative resource for Budongo chimpanzees. The relatively strong inhibitory activity of this species against S . aureus , a bacteria associated with causing contamination on the skin leading to chronic wounds [ 97 ], as well as its anti-inflammatory properties, suggests that A . boonei ingestion may have beneficial effects in wound care contexts.

Khaya anthotheca . Previous studies have demonstrated that K . anthotheca bark contains biologically active compounds like gedunins, mexicanolide, phragmalin, and andirobins [ 98 ]. One limonoid identified in the species, anthothecol, has anti-cancer properties [ 99 ]. A study by Obbo et al. [ 100 ] on K . anthotheca bark collected in the Budongo Forest, found strong antiprotozoal activity against Plasmodium falciparum (IC 50 0.96 μg/mL) and Trypanosoma brucei rhodesiense (IC 50 5.72 μg/mL). A related species, K . senegalensis , has been shown to cause cell lysis in some gram-negative bacteria, including Salmonella Typhimurium , Escherichia coli , Shigella sp. and Salmonella sp., by targeting cytoplasmic membranes [ 101 ].

In our antibacterial library screen, of all extracts tested, only the methanol-water extract inhibited growth of A . baumannii (although no IC 50 values were reached in dose-response). The methanol-water extract also inhibited the growth of E . coli (DSM 498) in the library screen, as did the ethyl acetate (eE088) extract, though again no IC 50 values were reached. In our antibacterial dose-response assays, all extracts of K . anthotheca stem bark and resin exhibited strong inhibition against the Gram-positive E . faecium . The most active extract against this strain, which was also the strongest antibacterial result reported in this study, was methanol-water (mwE088) (IC 50 : 16 μg/mL; MIC: 32 μg/mL). All extracts of this species were also found to inhibit E . coli (DSM 1576) in the dose-response experiments, with the methanol-water extract once again also showing the strongest inhibition (IC 50 : 16 μg/mL; MIC: 256 μg/mL). This extract also inhibited the growth of S . maltophilia (IC 50 : 64 μg/mL) in the library screen. Only weak inhibition was found against the food pathogen S . enterica ( n -hexane extract, IC 50 : 256 μg/mL).

K . anthotheca exhibited potent anti-inflammatory activity. Of all extracts tested, the methanol-water K . anthotheca extract (mwE088) displayed the strongest COX-2 inhibition activity (IC 50 : 0.55 μg/mL). Past phytochemical studies on methanol and ethanol-water stem bark extracts from the related species, K . senegalensis , revealed many phenolic compounds, including flavonoids and tannins e.g., [ 101 , 102 ]. Flavonoids act on the inflammatory response, and may block molecules like COXs, cytokines, nuclear factor-кB and matrix metalloproteinases [ 103 ]. Some tannins have also been proven to have strong free radical-scavenging and antioxidant activities [ 104 ]. These compounds are antagonists of particular hormone receptors or inhibitors of particular enzymes such as COX enzymes [ 103 ]. If Khaya species are phytochemically similar, this could help explain K . anthotheca ’s strong COX-2 inhibitory activity.

Across Africa, K . anthotheca is traditionally used for ailments including allergies, fever, headaches, jaundice, bacterial infections, and as a disinfectant for bleeding wounds [ 105 – 107 ]. Our behavioral observations suggest that this species is also a common resource for Sonso chimpanzees, with a total of 65 feeding events recorded throughout the first field season. Of these events, several involved individuals with imbalanced health states (see Table 1 : K . anthotheca ) . On at least three independent occasions, K . anthotheca bark and resin were consumed by wounded individuals. Two adult females on different days tested positive for leukocytes on urinalysis tests within hours of ingesting K . anthotheca , suggesting the presence of infection. One of these individuals was also experiencing severe diarrhea the day prior, the other was found to have trace levels of blood in her urine. A juvenile female with a persistent cough was also observed consuming K . anthotheca bark. On several occasions individuals with high parasite loads or diverse species infection were observed targeting this resource while shedding tapeworm proglottids ( Bertiella sp.). An elderly female was also observed eating bark and resin a few hours prior to leaf-swallowing, a well-established self-medicative behavior known to rid the gut of endoparasites [ 9 , 23 ]. The frequency of K . anthotheca ingestion in the Sonso diet during this period, suggests that individuals have consistent exposure to the antibacterial and anti-inflammatory compounds present in this species. Whether this is a case of passive prevention through intake of a medicinal food, or therapeutic self-medication for a common and wide-spread condition will need further investigation. If used therapeutically, our results suggest this species could be used for treating wounds, bacterial or infections, and/or reducing internal parasite loads.

Christella parasitica.

Extracts of C . parasitica produced notably high anti-inflammatory activity in COX-2 testing, with the methanol-water extract (mwE087) achieving an IC 50 value of 0.81 μg/mL. This same extract, however, exhibited the lowest general activity in the antibacterial library screen. The only antibacterial activity from this species was on E . coli (DSM 498) by the ethyl acetate and n- hexane extracts (eE087; hE087), and on E . coli (DSM 1576) by the n-hexane extract (hE087). The n -hexane extract reached an IC 50 of 128 μg/mL in dose-response assays with no MIC value. Prior to this study, there had been limited pharmacological testing on C . parasitica (though see [ 108 ]), so comparison across studies is not possible.

When we considered the associated behavioral observation involving C . parasitica , we found a notable relevance to our pharmacological results (see Table 1 : C . parasitica , Case 1 ). This observation involved a wounded Sonso adult male (PS) travelling outside of his core area with a large group. It was unclear if this was an inter-community patrol. PS had been observed earlier in the day with a severe hand injury which impacted his mobility, though no open wound was observed. PS separated himself from the group and moved a few meters to a patch of ferns where he began consuming the leaflets. The bout lasted approximately 3-minutes. No other group members were observed feeding on this species, and this was only the second case of fern ingestion reported in Budongo in over 30-years of observations (unpublished site data). Health states of individuals from the past event were unfortunately not recorded. Whether or not C . parasitica ’s highly anti-inflammatory properties were the principal motivator for the selection of this species remains unknown, however, regardless of intention, this plant may have benefitted PS by reducing pain and swelling in his injured hand.

Syzygium guineense.

S . guineense bark and leaves have both previously been found to exhibit a range of pharmacological activity, reviewed by Uddin et al. [ 109 ]. The antioxidant, analgesic, and anti-inflammatory activities of this plant have been attributed to flavonoids, tannins, saponins, carbohydrates, alkaloids, and cardiac glycosides in the extracts [ 109 – 112 ]. In our assays, S . guineense bark exhibited high antibacterial growth inhibition effects in vitro . The methanol-water bark extract (mwE098a) showed some level of inhibition against all bacteria tested in the dose-response assays, except for E . faecium and S . enterica . This was also the only extract, out of all tested, to inhibit growth of P . aeruginosa (IC 50 : 64 μg/mL; MIC: >256 μg/mL) a pathogen known to cause infections in the blood, lungs, and other body parts after surgeries [ 113 ], and was one of two extracts to reach a MIC value against S . maltophilia (IC 50 : 32μg/mL; MIC: 256 μg/mL). The other extract to reach a MIC value was the ethyl acetate S . guineense bark extract (eE098a; IC 50 : 64 μg/mL; MIC: 256 μg/mL). All bark and leaf extracts showed strong inhibition against E . coli (DSM 1576) in the dose-response assays, with the strongest results coming from the methanol-water extracts (mwE098a and mwE098b). All bark and leaf extracts of this species, except for the n -hexane bark extract (hE098a), inhibited E . cloacae , and were the only extracts in the study to do so. E . cloacae , while part of normal intestinal flora, can cause UTI’s and respiratory infections in humans [ 114 ]. S . guineense extracts were also the only extracts to inhibit A . baumannii at a concentration <256 μg/mL, with the methanol-water bark extract showing the strongest inhibition. A . baumannii can cause infections in wounds, blood, urinary tracts, and lungs [ 115 ]. The efficacy of methanolic extracts from this species suggests that the active compounds are polar molecules. In the anti-inflammatory COX-2 inhibition dose-response assays, only the n -hexane bark extract displayed strong inhibitory effects (IC 50 : 2.42 μg/mL), while the other extracts failed to exhibit significant activity during the pre-screening or ≥ 50% inhibition at 10 μg/mL. The COX-2 inhibition assays showed no inflammatory inhibition amongst leaf extracts at tested concentrations.

S . guineense can be found throughout Sub-Saharan Africa and is a common traditional medicine, for malaria [ 116 ]. The bark is also used for stomach aches, diarrhea, internal parasites, and infertility [ 68 , 109 ]. Ingestion of S . guineense bark is rare in Budongo, with no direct observations in either community throughout the study period, and only six total cases between 2008–2021 documented in the site’s long-term data. No observations of leaf ingestion of this species have ever been reported. The infrequent ingestion of S . guineense bark implies a more targeted use, making it unlikely to be a medicinal food. Instead, our pharmacological findings make this resource a strong candidate as a putative, therapeutic self-medicative resource. Unfortunately, as there is currently no health data associated with individuals who have recently consumed S . guineense bark, we do not yet know which properties chimpanzees may be targeting. However, based on pharmacological results, we recommend further investigation into this species as a curative agent for respiratory-related infections.

Scutia myrtina.

Kritheka et al. [ 117 ] in their study on the bioactivity of S . myrtina , found in vivo evidence that this species possesses dose-dependent anti-inflammatory, antimicrobial, and antifungal properties. Across our antibacterial assays, the bark sample of this species collected from the stem inhibited E . faecium (eE089a) and E . coli DSM 1576 (eE089a; mwE089a) in dose-response tests at concentrations ≤256 μg/mL. The refuse sample, collected from the ground below the plant’s stem, inhibited A . baumannii (hE089b), E . faecium (eE089b), and E . coli DSM 1576 (mwE089b; eE089b; hE089b) in dose-response tests below the specified concentration. Interestingly, the refuse sample inhibited more bacteria species overall than the fresh bark. The most potent antibacterial growth inhibition effects came from the ethyl acetate bark sample against E . faecium (eE089a; IC 50 : 64 μg/mL), though no MIC value was reached. In the COX-2 inhibition assays, the n- hexane bark extract had the fifth strongest inhibitory effect in vitro (hE089a; IC 50 : 1.19 μg/mL) out of all samples, while the ethyl acetate refuse bark sample was less potent, though still moderately active (E089b; IC 50 : 7.49 μg/mL).

As far as the authors know, this is the first published report presenting both behavioral and pharmacological evidence for S . myrtina bark as a putative medicinal resource amongst free-ranging chimpanzees (though see [ 118 ] for evidence based on food-combinations). Our behavioral observations indicate that an individual with a diverse and intense parasite infection deliberately sought out the bark of this species. The Budongo chimpanzees may, therefore, utilize S . myrtina as an anthelminthic. Across traditional accounts from multiple regions, S . myrtina is commonly used by people as an anthelminthic to treat intestinal worms [ 68 ], while aerial parts are also used to treat various bacterial infections. As we were not able to conduct urinalysis on the consumer during or after this event, we cannot determine whether the individual also harbored a bacterial infection at the time of ingestion. However, this possibility cannot be ruled out. Based on these findings, we propose S . myrtina be added to the list of putative chimpanzee self-medication behaviors as a treatment for internal parasites, and we encourage further exploration into the other specific chimpanzee health conditions that this species may help ameliorate.

Assessment of putative self-medicative behaviors

We synthesized pharmacological and behavioral evidence to assess therapeutic use of species associated with bark feeding, dead wood eating, and pith stripping behaviors. A summary of the antibacterial and anti-inflammatory results for each species is reported in S3 Table in S2 File . Overall, stem bark and dead wood samples were notable for their activity. Bark samples from every species showed >40% antibacterial inhibition against at least one bacterial strain. This activity was also true of the dead wood samples. When plant parts of the same species were tested ( S . guineense and F . exasperata ), barks generally exhibited more potent antibacterial and COX-2 inhibition activity than the leaves, likely to do with the higher concentration of plant secondary metabolites in bark. Our findings offer strong support that bark and dead wood eating of certain species could constitute novel self-medicative behaviors in wild chimpanzees. We also encourage more investigation into the bioactivity of non-bitter pith stripping, as the pith of A . polystachius showed strong antibacterial activity against E . faecium (hE099; IC 50 : 32 μg/mL; MIC: 128 μg/mL), and the piths of both A . polystachius and M . leucantha demonstrated significant anti-inflammatory properties at low concentrations. Future primatological research should prioritize the establishment of multi-disciplinary long-term projects that look systematically at health states of individuals who engage in bark, dead wood, and pith ingestion behaviors. We also encourage further pharmacological testing on other species used for these behaviors in Budongo and across primate field sites.

Drug discovery

Multidisciplinary studies on this topic have potential to lead to the discovery of new medicines which may benefit our own species [ 119 – 122 ]. Historically, PSMs have played a major role in the development of modern human medicine, and even today, a large portion of medicines are derived either directly or indirectly from plants and other natural materials [ 123 – 127 ]. Antimicrobial resistance is rising to dangerously high levels according to the World Health Organization [ 128 ] requiring the rapid creation of new antibacterial treatments. Infections caused by multi-drug resistant bacteria kill hundreds of thousands of people annually. Our findings of strong antibacterial growth inhibition across numerous plant species growing in Budongo have promising implications for our ability to discover novel compounds in existing forest habitats. Extracts should also be tested against additional bacteria and for anti-virulence effects, e.g., inhibition and disruption of biofilm formation, quorum sensing and toxin production, pursuing development of new therapeutic strategies that apply less evolutionary pressure, likely resulting in emergence of less antibiotic resistances in the future. Phytochemical characterization using advanced techniques, such as LC-ToF-MS and NMR, as well as potentially AI-assisted untargeted metabolomics approaches, are now needed to identify substances present in the most active extracts. This may eventually lead to the isolation and structure elucidation of yet unknown active ingredients and make way for determining their pharmacological selectivity and toxicity, while also taking potential synergistic effects into account.

Simultaneously, we are currently faced with a pressing need for more effective treatments to combat symptoms of acute inflammation and mediate long-term consequences of chronic inflammatory diseases [ 129 ]. The prostaglandin-producing cyclooxygenase-2 (COX-2) mediates and regulates pain, fever, wound inflammation, and many other medical disorders, as it plays a crucial role in the host organism’s defense against pathogens and injury. COX-2 inhibition has the same mechanism of action as non-steroidal anti-inflammatory drugs (NSAIDs). While inflammation is a normal part of the body’s defense against injury or infection, it can be damaging when occurring in healthy tissues or over a protracted period. Chronic inflammation can lead to cardiovascular diseases (CVD) and cancer, the two leading global causes of death [ 130 ]. Past studies have shown that the IC 50 values of Aspirin and ibuprofen (pure compounds and common NSAIDs) are 210 μg/mL and 46 μg/mL respectively for COX-2, and 5 μg/mL and 1 μg/mL respectively for COX-1 [ 131 , 132 ]. The in vitro COX-2/COX-1 selectivity ratio for Aspirin and ibuprofen is 42 and 46 respectively. Surprisingly, the 17 most active extracts in our COX-2 assays display lower IC 50 values than these popular NSAIDs, meaning our extracts have more potent inhibitory effects on the inhibition of COX-2 than the most common anti-fever and anti-pain drugs on the market. While COX-1 assays were beyond the scope of this study, future research should investigate COX-1 inhibition activity of these 17 extracts to calculate COX-2/COX-1 selectivity ratios. Doing so will allow for preliminary assessment of potential side effects, selectivity, and efficacy before future in vivo experiments can commence.

Future directions

Future research on this topic would benefit from the inclusion of control samples (plants or plant parts not consumed by chimpanzees); however, in this study, assay costs were a prohibiting factor. Additional information regarding the nutritional and mineral content of the species mentioned in this study is needed to better understand the motivations for ingestion. However, bioactivity and nutritional/mineral content are by no means mutually exclusive. It is, therefore, highly likely that these resources provide multiple benefits to consumers.

Future studies should also consider ecological variables. For example, different individual plants of the same species should be tested across habitat types to determine whether bioactivity varies based on location, age, life history, or time of harvest. Situating samples in their ecological context will provide a better understanding of whether chimpanzees select resources based on species alone, or other more nuanced criteria. Lastly, climatic studies in combination with pharmacological testing should examine how climate change may impact bioactivity of these plants, as shifting weather patterns have already been shown to alter nutritional content [ 133 ]. This information will be critical for establishing protected habitats that can sustain healthy, wild, primate populations.

Conclusions

As we learn more about the pharmacological properties of plants ingested by chimpanzees in the wild, we can expand our understanding of their health maintenance strategies. Our results provide pharmacological evidence, from in vitro assays of plant parts consumed by wild chimpanzees collected in situ , for the presence of potent bioactive secondary plant metabolites in Budongo chimpanzee diets for a variety of potential illnesses previously not considered. Whether these resources are consumed intentionally as a form of therapeutic self-medication or passively as medicinal foods, must be assessed on a case-by-case basis, taking behavioral observations into account.

For the field of zoopharmacognosy to progress, we encourage continued multidisciplinary collaboration between primatologists, ethnopharmacologists, parasitologists, ecologists, and botanists [ 9 ]. Beyond improving our broad understanding of chimpanzee health maintenance, multidisciplinary studies will benefit our own species, potentially leading to the discovery of novel human medicines to combat the looming problem of growing drug-resistance. For this to happen, however, it is imperative that we urgently prioritize the preservation of our wild forest pharmacies as well as our primate cousins who inhabit them.

Materials availability

Voucher specimens for each species were deposited at the Makerere University Herbarium in Kampala, Uganda for taxonomic identification and storage. A duplicate set was deposited at the University of Oxford Herbarium for permanent storage.

Supporting information

S1 fig. budongo chimpanzees consuming resources tested in this study..

a.) IN eating K . anthotheca bark and resin b.) MZ eating S . myrtina bark c.) KC stripping A . polystachyus pith d.) MB eating C . patens dead wood e.) OZ eating S . guineense bark (post-study period) g.) MZ eating F . exasperata bark.

https://doi.org/10.1371/journal.pone.0305219.s001

S2 Fig. Generalized multi-method workflow used in this study.

https://doi.org/10.1371/journal.pone.0305219.s002

S3 Fig. Voucher samples collected in duplicate.

a . ) C . alexandri (00243133G) b . ) A . polystachius (00243136J) c . ) W . elongata (00243129L) d . ) C . parasitica (00243122E) e . ) K . anthotheca (00243123F) f . ) F . variifolia (51195) g . ) M . leucantha (51203) h . ) A . boonei (51204) i . ) D . dewevrei (00243132F) j . ) S . guineense (00243135I) k . ) S . myrtina (00243128K) l . ) F . exasperata (00243130D).

https://doi.org/10.1371/journal.pone.0305219.s003

S4 Fig. Plate layouts for growth inhibition assays.

[Top] Library Screen: done in 96-wells-mikrotiterplate; AB: Antibiotic as positive control; DMSO: vehicle control / negative control; GC: growth control: containing working culture, to check whether the bacterium grew/active; [Bottom] Dose-Response: done in descending concentration of samples, DMSO, and antibiotic. MB: Media blank, consisted of CAMHB as negative/ sterile media control; DMSO as negative/ vehicle control; GC: growth control, consisted of working culture.

https://doi.org/10.1371/journal.pone.0305219.s004

S5 Fig. ELISA assay setup for anti-inflammatory assay.

https://doi.org/10.1371/journal.pone.0305219.s005

S1 File. Supplementary materials: Methods .

https://doi.org/10.1371/journal.pone.0305219.s006

S2 File. Supplementary tables.

https://doi.org/10.1371/journal.pone.0305219.s007

Acknowledgments

We are grateful to all the field staff working in Budongo who provided invaluable instruction and guidance, generously sharing both scientific insight and traditional knowledge. This study could not have been done without their contributions. Specifically, we would like to thank members of the Perspectives Collective: Chandia Bosco, Monday Mbotella Gideon, Adue Sam, Asua Jackson, Steven Mugisha, Atayo Gideon, and Kizza Vincent, and Walter Akankwasa, as well as site director David Eryenyu. We would also like to thank Godwin Anywar for his assistance with plant identification at the Makerere Herbarium, Stephen Harris at the University of Oxford’s Herbarium for his facilitation of voucher storage, and the Natural History Museum in London for their aid in parasite identification. We are grateful to Vernon Reynolds who founded the field site and to the Royal Zoological Society of Scotland for providing core support. We also gratefully acknowledge the Uganda Wildlife Authority and the Uganda National Council for Science and Technology for granting permission to conduct research in Uganda. Lastly, thank you to the staff and students at Neubrandenburg University of Applied Sciences who made this collaboration possible, and to research assistant, Finn Freymann, for his help with botanical extractions.

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• Iran J Pharm Res
• v.11(1); Winter 2012

Introduction of Medicinal Plants Species with the Most Traditional Usage in Alamut Region

Maryam ahvazi.

a Department of Herbarium, Institute of Medicinal Plants, ACECR, Karaj, Iran.

Farahnaz Khalighi-Sigaroodi

b Department of Pharmacognosy and Pharmaceutics, Institute of Medicinal Plants, ACECR, Karaj, Iran

Mohammad Mahdi Charkhchiyan

c Research Institute of Forests and Rangeland, Ghazvin.

Faraz Mojab

d School of Pharmacy and Pharmaceutical Sciences Research Center, Shahid Beheshty University of Medical Sciences, Tehran, Iran.

Vali-Allah Mozaffarian

e Research Institute of Forests and Rangeland, Tehran, Iran.

Hamideh Zakeri

f Cell Line Engineering, Sigma Aldrich Biotechnology Division. St Louis, USA.

The ethnobotany of the medicinal plants of Alamut region is important in understanding the cultures and traditions of Alamut people. This study documents 16 medicinal plant species, most commonly used by the indigenous people of Alamut region (Ghazvin Province), northwest, Iran. The botanical name, family name, vernacular name, part used, and the application of the plants have been provided in this paper. Alamut region was divided into different villages with the aid of maps. We recorded traditional knowledge and use of medicinal plants from herbal practitioners and village seniors in Alamut. The plants were gathered from different sites. The fully dried specimens were then mounted on herbarium sheets. We found 16 medicinal plants belonging to 11 families which were traditionally used in Alamut. Finally, we describe traditional usages by the native people in the Alamut region. The obtained results were compared with data on the herb’s clinical effects. A set of voucher specimens were deposited to the Institute of Medicinal Plants Herbarium (IMPH).

Introduction

Before the introduction of chemical medicines, man relied on the healing properties of medicinal plants. Some people value these plants due to the ancient belief which says plants are created to supply man with food, medical treatment, and other effects. It is thought that about 80% of the 5.2 billion people of the world live in the less developed countries and the World Health Organization estimates that about 80% of these people rely almost exclusively on traditional medicine for their primary healthcare needs. Medicinal plants are the “backbone” of traditional medicine, which means more than 3.3 billion people in the less developed countries utilize medicinal plants on a regular basis ( 1 ). There are nearly 2000 ethnic groups in the world, and almost every group has its own traditional medical knowledge and experiences ( 2 , 3 ). Iran is home to several indigenous tribes with a rich heritage of knowledge on the uses of medicinal plants. Iran has varied climates and geographical regions that have caused a wide distribution of individual medicinal plant species such that each tribe has its own plants and customs. Alamut is one of the most important geographic regions in Iran because of its ancient history of cultivating traditional medicinal plants. Alamut region and the several villages it encompasses are secluded from other cities in Iran, which is why the people living in this region have relied on indigenous medical knowledge and medicinal plants. In this study, we analyzed the medicinal plants with most therapeutic usage in the region.

Experimental

Geographic and climatic overview

Alamut mountainous region is situated in the central Alborz Mountains, between 36˚24´ and 36˚46´ northern latitudes and 50˚30´ and 50˚51´ eastern longitudes with an altitude ranging from 2140 to 4175 m. The region is located on the northeast of Ghazvin Province and is bounded to the north by the Mazandaran Province in Tonekabon and bounded on the east by Tehran Province in the Taleghan mountains. Annually, it rains 368.03 mm and the average temperature is 14°C. Topography is distinctly marked with several mountains, springs, rivulets, and rivers. This area is geographically located in the Irano-Turanian region ( Figure 1 ).

Study area: Iran map and Alamut in Ghazvin Province

The ethnic composition of the region is quite diverse and almost 90% of its population resides in rural areas. The language of the inhabitants is known as Deylamite. People of Alamut have a long history of exporting medicinal plants to other regions of Iran. Roadways have increased communication among the rural natives in Alamut and have also increased tourism to the region because of its several ancient castles. Because of good quality of medicinal plants in this region and more immethodical pick of them, some of species have become extinct. For this reason, an important aim of this study is to protect the preservation of the region’s plants. Other aims include:

Documenting the traditional knowledge of medicinal plants from the natives.

Assessing the most commonly used local medicinal plants.

Promoting the potential benefits of medicinal plants.

Data collection

We first prepared a map with a scale of 1:25,000 from the region to identify the number of villages, roads, and vegetations. We visited the region and spoke to herbal practitioners and village seniors. A questionnaire was used to obtain information on the types of ailments treated using traditional medicinal plant species. Sometimes informants were asked to come to the field and introduce us to the plants. When this was not possible, plants were collected around the villages of the informants and were shown to them to confirm the plant names. This investigation took over 2 years and information was collected 1-2 days per week. Voucher samples were also collected for each plant and were identified using floristic, taxonomic references. Flora Iranica and a dictionary of Iranian plant names were used for identification purposes ( 4 , 5 ). Plants were deposited at the herbarium of Institute of Medicinal Plants (IMPH).

Although ancient sages through trial and error methods have developed herbal medicines, the reported uses of plant species do not certify their efficacy ( 6 ). Reports on ethnomedicinal uses of plant species require pharmacological screenings, chemical analyses, and tests for their bioactive activities. Pharmacological screening of plant extracts provides insight to both their therapeutic and toxic properties as well as helps in eliminating the medicinal plants or practices that may be harmful ( 7 ).

This study provides information on 16 medicinal plants belonging to 12 families that are most commonly used for traditional medicine in Alamut region. Botanical names of plants were sorted alphabetically, and for each species and the following information was hence represented: family, vernacular name, part used ( Table 1 ). Traditional use and preparation was compared with other references ( Table 2 ).

Medicinal plants collected from Alamut region

Comparison of problems due to hot flash in studied groups during the study base on HFQ.

Among these medicinal plants, Apiaceae, Lamiaceae , and Boraginaceae were the most dominant families with 4, 2, 2 species belonging to 4, 2, 2 genera of medicinal plants, respectively.

Of the 16 medicinal plants, 8 species had similar effects in traditional and medicinal uses when comparing Alamut with other references. Achillea millefolium had antibacterial effects; Capparis spinosa is used for headache, renal complaints and stimulating tonic; Echium amoenum is used for common cold and had sedative effects; Ferula persica is used for gout; Juglans regia is used for diabetes; Smyrnium cordifolium is edible and used as tonic; Viola odorata is used for fever and migraine; Ziziphora clinopodioides is used for cold, infections and stomachache.

Some effects which are mentioned in traditional medicine of Alamut region were important with no scientific information about them. For example, Berberis integerrima and Hippophae rhamnoides had good effect on lowering of serum lipids and blood sugar and hypertension. Malva neglecta is used for mouth fungal infection in children and Stachys lavandulifolia is used for headache and renal calculus. Other researches can perform experiments to discover their components and effects.

All of the medicinal plants were collected from the wild or in the native people’s gardens. Some medicinal plants can no longer be found in the region and are only cultivated in the native people’s gardens. For example, Echium amoenum is an endemic plants in Iran with historically wide spread in the region, but because of frequent picking, the species is now just cultivated in the native people’s gardens.

Different parts of medicinal plants were used by the inhabitants of Alamut region as medicine for treating ailments. The most common parts used were flowers (25%). The use of aerial parts, leaves, fruits and roots were the same (15%). Use of the stems (7%), seeds, and blooms (4%) were lower than the others ( Figure 2 ). The 16 medicinal plant species were used in treating 27 different types of ailment ( Table 3 ).

Plants part use and their percentage

Medicinal plant species were used in treating different types of ailment

Acknowledgment

This work was supported by grants from Institute of Medicinal Plants and the Iranian Academic Center for Education, Culture, and Research (ACECR). The authors would like to thank Ghazvin Research Institute of Forests and Rangelands for their sincere cooperation.