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Journal of Resources and Ecology >

2023 , Vol. 14 >Issue 3: 533 - 541

DOI: https://doi.org/10.5814/j.issn.1674-764x.2023.03.009

Resource Economy

Biological Characteristics and Resource Utilization of Tagetes minuta L.

  • WANG Jingsheng , 1, * ,
  • CAO Kaili 1, 2 ,
  • LIU Jie 1 ,
  • ZHAO Yanzhe 1, 2
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  • 1. Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing 100101, China
  • 2. University of Chinese Academy of Sciences, Beijing 100049, China
*WANG Jingsheng, E-mail:

Received date: 2022-02-14

  Accepted date: 2022-09-19

  Online published: 2023-04-21

Supported by

The Survey, Collection and Monitoring of Agricultural Wild Plant Resources in Tibet Autonomous Region(13200357)

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Abstract

Tagetes minuta L. is native to the temperate grasslands and relatively high-altitude areas of South America. In 1990, it was first discovered in the Beijing Botanical Garden in China. In 1994, Pema Dawa introduced the species as a Tibetan medicine from the mountains of northern India to his courtyard in Gangjiang Village, Wolong Town, Milin County. Around 2010, scholars discovered that Tagetes minuta L. was widely invasive, which aroused extensive social concern. Featuring small weight, large number, and awns, Tagetes minuta L., is easy to spread and has a high seed germination rate, with 20% of the reproductive investment. The plant is tolerant of barrenness and drought and adapts to climates with large diurnal temperature differences and strong light conditions. Rich in aromatic substances and essential oils, the leaves and flowers serve medicinal, food, flavoring, health care and cosmetic purposes. Thiophene in the roots and bioactive components in the essential oil have anti-inflammatory, sterilizing, insect-repellent, and fly control effects, with significant allelopathy on native species. The biological and ecological characteristics of Tagetes minuta L. lay the material basis for its population spread. According to Tibetan folklore, we suggest using physical methods or biological control techniques for ecological control and strengthening the research of development and application to guide its economic benefits in Tibetan Buddhist supplies.

Key words： Tagetes minuta L.; biological invasion; population expansion; ecological control; resource utilization

Cite this article

WANG Jingsheng , CAO Kaili , LIU Jie , ZHAO Yanzhe . Biological Characteristics and Resource Utilization of Tagetes minuta L.[J]. Journal of Resources and Ecology, 2023 , 14(3) : 533 -541 . DOI: 10.5814/j.issn.1674-764x.2023.03.009

1 Introduction

Biological invasion refers to the invasion of species from their original habitat to a new environment by natural or artificial means, which affects the production of agriculture, forestry, livestock and fishery and biodiversity in the invaded area, causing economic losses, ecological disasters, and human health risks. China is seriously affected by biological invasion, with more than 660 invasive alien species identified (Ministry of Ecology and Environment, 2020), including as many as 515 invasive plant species (Xinhua News Agency, 2014). Although means of controlling biological invasions are becoming increasingly diverse, they are mainly traditional physical removals, with little progress in resource utilization. With diverse landforms, climate patterns and biodiversity, the ecological environment of the Tibetan plateau is extremely fragile. The Tibetan plateau is often considered a low-risk area for plant invasion due to its habitat characteristics of high altitude, low temperature, drought and barrenness (Pathak et al., 2019). Nevertheless, according to incomplete statistics, as many as 146 invasive plants exist in the Tibet Autonomous Region, including 14 malignant invasive plants. Tagetes minuta L., currently in a relatively serious invasive expansion, is in the third class—locally invasive status (Xu, 2021).
As an economic species, Tagetes minuta L. is widely cultivated and applied in many countries worldwide. However, due to its short naturalization time, harmfulness and invasiveness, it has been classified as an invasive species in China. Moreover, the research on its invasion mechanism and ecological hazards is at an early stage, with less than 10 publications. Therefore, this paper focuses on reviewing the biological characteristics contributing to the invasion, tracing the introduction, escape, settlement and expansion process of the plant in the Tibet Autonomous Region, and theoretically analyzing the mechanism of its expansion in the region. Additionally, we anticipate the possible expansion of this species based on the context of global climate change and the unique habitat of the Tibetan plateau. Since there are no comprehensive anti-invasive measures, this paper reviews foreign research results on the utilization of this plant and analyzes the possibility of its transformation from an “invasive species” to an “economic species” in China, aiming to provide theoretical and technical support for the control of this species.

2 Study area and research methods

The main study area is located in Milin County, Nyingchi City, Tibet Autonomous Region, where Tagetes minuta L. was first discovered. It is between 28°39´-29°50´N and 93°07´-95°12´E, and the topography is high in the west and low in the east, with an average altitude of 3700 m (Fig. 1). The area features a temperate semi-humid monsoon climate, with an average annual temperature of 8.2 ℃, annual precipitation of 641 mm and abundant sunshine. The research method is mainly a walking survey to understand the invasion history of the plant and to investigate its biological characteristics favorable to invasion through fieldwork and experiments.

3 Morphological features

Tagetes minuta L., Marigold, family Asteraceae, is an annual herb with a strong aroma (Zhang et al., 2019). The plant is 10-250 cm tall, with smooth, glabrous, longitudinally ribbed, multi-branched stems (especially in larger plants or after cutting) and an almost lignified base. Usually, leaves are opposite; upper leaves are alternate, dark green, and 3-30 cm long and 0.7-8 cm wide. It is pinnately compound, with deeply lobed blades and long elliptic lobes, 1-11 cm long and 0.7-8 cm wide, and has margins with cuspidate teeth. Leaf margins and backs have clear yellow oil glands; leaf rachis has narrow wings containing 9-17 leaflets, which are linear-lanceolate, up to 2-4 cm long, with serrulate margins and orange glands. Additionally, pseudo-stipules are linear. Heads are crowded, 3-4 mm in diameter, and arranged corymbosely at the top of the stem, solitary or organized into racemes. Involucral bracts are 8-12 mm, narrowly terete, and yellow-green; there are 3-4 1-layered leafy bracts in 8-12 mm length that connate to be tubular; apiculus has 3-4 teeth, glabrous, covered with linear brown or orange oil gland dots. There are 2-3 ligulate flowers, yellowish to creamy, in 2-3.5 mm length; there are 4-7 tubular flowers, yellow to dark yellow, in 4-5 mm length. The achenes are black, linear-oblong, 6-7 mm long, covered with short hairs, angular, and narrowed at the base. Crown hairs are scale-like, and 1-2 are long awn-like, about 3 mm long; the rest are short and obtuse, about 1 mm long. The flowering and fruiting period is from October to November (Dong et al., 2013; Zhang et al., 2014). Details are shown in Fig. 2.
Fig. 2 Pictures of roots, stems, leaves, flowers and fruits of Tagetes minuta L.

4 Origin and naturalization in China

Tagetes minuta L. is native to South America and distributed in temperate grasslands and relatively high altitudes in countries such as Argentina, Peru, Bolivia, Chile, and Paraguay (McVaugh, 1943; Naghinezhad and Shahriar, 2007; Walia and Kumar, 2020). It was introduced to Europe, Asia and Africa during the Spanish colonization of South America. With the intensification of agricultural activities, the species has now been widely introduced to or invaded many countries in North America, Europe, Africa, Asia and Oceania (Australia) (Stadler et al., 1998; Ireri et al., 2010; Walia and Kumar, 2020).
The invasion of Tagetes minuta L. in East and Southeast Asia began in Japan, where it was reported as a naturalized weed in 1972. In China, it was first discovered at the Beijing Botanical Garden in October 1990, and a naturalized species was discovered in the central alpine region of Taichung, Taiwan, in 2006 (Wang and Chen, 2006). Its first collection in the southeastern Tibet Autonomous Region was conducted as early as 2009 at Milin County, Nyingchi Region (now Nyingchi City) (Xu and Tashi, 2015); and authors’ retrospective survey in 2019 revealed that the species was artificially introduced from mountains in northern India to Wolong Town, Milin County, in 1994 before escaping and settling in the wild. It has now expanded rapidly and become a danger.
Around 2010, the invasion and naturalization of this species in China gradually caught the attention of scholars, and a series of reports and literature emerged. For example, its large populations were found in Huilongguan and Xingshou Towns, Changping District, Beijing, in 2011 (Zhang et al., 2014); The species was found settled in Houtai Mountain, Lianyungang, Jiangsu, in 2013 (Dong et al., 2013); Large naturally colonized populations of this species were found in Shijiazhuang, Hebei Province, Jinan and Qingdao, Shandong Province, and showed a population expansion trend into endangered status (Zhang et al., 2019). A coordination meeting of Tagetes minuta L. prevention and control lawsuit case was held in Pingding County, Yangquan City, Shanxi Province in 2021 (Shanxi People’s Procuratorate, 2021), which was the first time for inspection authorities to intervene in the defense and control of invasive species in China, pioneering the legal control of invasive species.

5 Introduction and escape in the southeast Tibet Autonomous Region

Pema Dawa, Menba nationality, was born on 1918 in Bema Gang Village, Medog Town, Medog County, Nyingchi District, Tibet Autonomous Region, and was said to have grown up in Bema Gang Temple. Around 1980, he moved to Gangjiang Village, Wolong Township, Milin County. In 1994, he asked monks from the temple to plant Tagetes minuta L. from northern India in his own courtyard as “Tibetan medicine”. In 1996, the plant was found to escape to the roadside, riverside, wasteland and abandoned courtyard areas of Gangjiang and Ri Village of Wolong Township, where it thrived. In the following years, villagers kept telling him about this herb that cattle and sheep do not eat. Red spots and itching appear on the skin after touching its leaves. A long time to smell its flowers will cause dizziness, nausea and even vomiting, so some villagers called it poisonous grass, indicating ominousness.
A few months before Pema Dawa passed away in 2005, he felt he had done something wrong and told villagers that this herb must be completely cleared. In 2008, when the Gangjiang village committee was changed, Qiga was elected as the village chief. After that, under the guidance of agricultural and rural departments at the township, county, city and autonomous region levels, Qiga started to organize villagers to remove the plant manually in late June and early July every year. Around 2012-2013, the plant around Gangjiang and Ri Villages was basically cleared. Little did we know that at that time, the species had crept out eastward along Lilong Township-Milin County-Bayi District-Nyingchi County and westward along Dongga Township-Lang County-Shannan City-Lhasa City-Shigatse City, forming a stable population of considerable size with an obvious trend of expansion.

6 Analysis of rapid expansion mechanism in Tibet Autonomous Region

6.1 Biological characteristics of seed are conducive to dispersal and settlement

The pollen of Tagetes minuta L. is spherical, and spheres are densely covered with spines, as shown in Fig. 3a (Tu et al., 2019), which facilitates dispersal carried by insects and improves pollination efficiency for fruit set. The seeds are black or brown achene, see Figs. 3(b-c), which is linear-oblong, angular, narrowed at the base, covered with short bristles throughout, 4-7 mm long and 0.3-1 mm wide. Crown hairs are scale-like, with 1-2 long awn-like spines at the tip, around 3 mm long, and 2-3 remaining awn spines, short and blunt, about 1 mm long, see Fig. 3b. Long awn of seeds makes them easier to carry and spread by cattle, sheep, wildlife and humans, thus providing further opportunities for population expansion. Short bristles increase the surface area and roughness of seeds, see Fig. 3d, creating favorable conditions for floating on the water surface and spreading downstream.
Fig. 3 External morphological characteristics of pollen and seeds of Tagetes minuta L.

6.2 Reproductive investment strategy preferences

Ecological responses are strategies that an organism has developed during evolution to adapt to other living and abiotic environments, which outline morphological and functional characteristics organisms have adopted to adapt, survive and reproduce in habitats (Bao et al., 2013; Yao et al., 2022). Reproductive strategy is a crucial aspect of plant life history and plays an important role in ecological processes, including plant population growth and dispersal, community structure and ecosystem function (Barrett et al., 2008; Brown and Eckert, 2005). A major determinant of the rapid invasion and expansion of Tagetes minuta L. worldwide, especially its settlement and explosive spread in the southeastern Tibet Autonomous Region, is its adoption of the R response life history strategy. R response, also known as R selection, refers to the life history response adopted by species with a short lifespan, small individuals, and high dispersal ability. “R” comes from “reproduction”, indicating high fecundity (MacArthur, 1962).
Phenotypic plasticity refers to the characteristics of the same genotypic species that produce different phenotypes in heterogeneous habitats (Lu et al., 2007) and is positively correlated with ecological amplitude and environmental adaptability as an important predictor of plant invasiveness (Liu et al., 2010). As one of the main manifestations of phenotypic plasticity in plants, the ability to regulate the biomass of population components is also an important factor for the successful invasion of exotic plants (Qi et al., 2006; Zhou et al., 2015). The coefficient of variation for the biomass of each component of Tagetes minuta L. reaches 105.49%-149.08%, showing strong phenotypic plasticity (Chou et al., 2020) and high reproductive investment (flowers and seeds account for 19.75% of biomass). Single plants have 6000-9000 seeds, up to 29000 seeds (Hulina, 2008), which are light and small, with a thousand seed weight of only 0.96-1.65 g, and do not require dormancy. The germination rate can reach 100% in a greenhouse at 25 ℃ under normal light conditions within a week (Zhang et al., 2019). The coefficient of variation in flower biomass is 38.30%, remarkably higher than that in roots, stems and leaves (Chou et al., 2020). The above characteristics create favorable conditions for its rapid population expansion in invaded areas.

6.3 Human activities facilitate spread

Tagetes minuta L. prefers to settle on human-disturbed soils, such as gardens, roadsides, and abandoned sites (Hulina, 2008; Meshkatalsadat et al., 2010). During the investigation in the southeastern Tibet Autonomous Region, we found that the distribution is mainly behind houses, around cattle, sheep and pig sheds, abandoned villages and courtyards, roadsides, freight yards, river banks, cattle, sheep and pig slaughterhouses (woolen mills), orchards, farmlands, green areas and sandy wastelands, as shown in Fig. 4. Human activities provide advantageous facilities for the plant to spread and settle. Firstly, seed awns easily stick to human clothes or fur of pigs, cattle, sheep and other livestock and can be carried to farther areas. Furthermore, seeds of this species are likely to germinate and settle in soil that has been turned or trampled on roadsides, house surroundings, farmlands, orchards and livestock activity sites.
Fig. 4 Distribution and habitats of Tagetes minuta L. in the southeastern Tibet Autonomous Region

6.4 Global climate change provides opportunities for the invasion of higher elevations

In India, Tagetes minuta L. is mainly introduced in the northern plains and hilly mountainous regions at 1000-2500 m altitude (Moghaddam et al., 2007). Its seeds sprout and establish in acidic (pH is 4.3-6.6) soils such as sandy loam and clay loam (Schmid et al., 1998), while plant growth and flowering prefer a temperate and cool climate with a large difference in diurnal temperature. The quality of essential oil is optimal when the average daily temperature during the growing season is between 12 ℃ and 30 ℃, and precipitation should be guaranteed to be at least 50 mm (Singh et al., 2003), which indicates that Tagetes minuta L. is extremely drought tolerant.
Affected by the global warming environment, the average annual temperature in agricultural areas (Lhasa, Shannan, Shigatse, etc.) and forest areas (Nyingchi, Chamdo) in the Tibet Autonomous Region ranges from 5.6 ℃ to 18.4 ℃, with annual precipitation of 335-850 mm (the average annual precipitation in Medog County is as high as 2330 mm). Most of the growing season is between May and October, with the average daily temperature above 10 ℃. Most areas are suitable for Tagetes minuta L., and its distribution altitude can extend to about 3800 m, which is 1300 m higher than that of India (2500 m). Detailed data are shown in Table 1.
Table 1 Temperature and precipitation in distribution areas of Tagetes minuta L. in Tibet Autonomous Region
Location Shigatse Shannan Lhasa Milin Nang Nyingchi Bayi Bomi Zayu Medog Kongbo
ALT (m) 3800 3500 3650 2950 3100 3100 3000 2700 2400 1200 3600
MAT (℃) 5.6 8.2 8.1 8.2 11.0 8.7 8.1 8.5 12.0 18.4 8.3
MAP (mm) 426 335 426 641 475 665 660 850 801 2330 808

Note: ALT = altitude; MAT = annual air temperature; MAP = mean annual precipitation.

Moreover, we previously simulated and predicted the distribution of potential fitness zones in the Tibet Autonomous Region for Tagetes minuta L. between 2050 and 2070 under two climate change scenarios using a maximum entropy (MaxEnt) model combined with BCC-CSM1.1 climate model data. The result shows that the species will further occupy the southeastern Tibet Autonomous Region and spread to the northeastern region. In short, in terms of the spatial scale, the species will expand to higher elevations and latitudes (Xu et al., 2021).

7 Resource utilization

Tagetes minuta L. has been used as a beverage, condiment, ornamental, or tonic since ancient times (Walia and Kumar, 2020). It is also often used in religious ceremonies and folklore, depending on its geographical distribution and ethnic background (Hamayun et al., 2005). The leaves and flowers of this herb are rich in essential oils and can be used in medicines, condiments, foods, cosmetics, and biocides.

7.1 Medicinal functions

After boiling and consuming as a soup, Tagetes minuta L. can treat common colds, digestive disorders, gastrointestinal distress, diarrhea, and liver disorders (Neher, 1968). Essential oils contain bioactive substances with bronchodilating, sedative, hypotensive, anti-spasmodic and anti-inflammatory effects and promote external wound healing (Maity et al., 2011). Moreover, plant extracts show antibacterial, anticancer (essential oil concentrations over 200 µg mL‒1), antioxidant, and free radical scavenging properties (Karimian et al., 2014; Shirazi et al., 2014) and are widely used in industrial pharmaceuticals.
The essential oil and plant extracts of Tagetes minuta L. have been found to have anticancer activity against leukemia cells (Mahmoud, 2013; Salehi et al., 2018) and be effective against human nasopharyngeal and hepatocellular carcinoma cells (Shirazi et al., 2014). Additionally, it also has a strong inhibitory effect on breast tumors (Ali et al., 2014).

7.2 Food, condiments and health products

According to an encyclopedia published in the United Kingdom, the leaves, stems, and flowers of Tagetes minuta L. were cooked as herbal medicine in the early nineteenth century in parts of South America, including Peru, Ecuador, Chile, and Bolivia. There is also a folk history of using its aqueous infusion as a medicinal tea and flavoring (Singh et al., 2003). Furthermore, the USA Food and Drug Administration (FDA) allows the use of Marigold plant extracts in human foods and has determined that Tagetes minuta L. extracts are safe (GRAS) when used in specific foods and beverages (Walia and Kumar, 2020). However, for the use of natural flavoring, the dosage must be limited according to GMP (FDA, 2016). Orange carotenoids extracted from herbs are widely used as food colorants in human foods, such as pasta, baked goods, confectionery, dairy products, beverages, and poultry feed (Timberlake and Henry, 1986; Zhang et al., 2009; Nerio et al., 2010). The health function of its essential oil, specifically in the extensive use of aromatherapy, has also been documented in the history of Kenya and England (Qureshi, 2006).

7.3 Disinfection and deworming

The extracted essential oil shows a 95%-100% inhibitory effect on Gram bacteria due to the content of thiophene and acyclic monoterpene ketones (Chan et al., 1975; Héthélyi et al., 1986; Lima et al., 1993). For example, the minimum inhibitory concentrations are 150 µg mL‒1, 165 µg mL‒1, 67 µg mL‒1 and 75 µg mL‒1 for Salmonella typhi, Escherichia coli, Staphylococcus aureus and Bacillus subtilis, respectively; 135 µg mL‒1 and 115 µg mL‒1 for Aspergillus niger and Candida albicans (Shirazi et al., 2014). Its volatile oil component affects its antibacterial activity mainly by inhibiting the synthesis of peptidoglycan, disrupting the microbial membrane structure and improving the hydrophobicity of the bacterial membrane surface (Kwamboka et al., 2016). In addition, the (E)-ocimenone component of oil has an insecticidal effect on mosquito larvae (Wells et al., 1992); the rich terpenoids and sterones in oil can repel ticks and inhibit their development (Nchu et al., 2012); monoterpenes, sesquiterpenes and phenylpropanoids of oil have larvicidal, anti-feeding and tropism effects (Reddy et al., 2016).

7.4 Cosmetics

Tagetes minuta L. is grown commercially for its rich essential oil content and is widely traded in the flavor field with the reputation of “marigold oil” (Babu and Kaul, 2007). The essential oil extracted from flowers by steam distillation can be used to produce perfumes; if mixed with sandalwood oil, it can be formulated to the aroma of rose oil (Rahman, 2013). Industry assessment concluded that its extracts and essential oils are phototoxic and therefore recommended against their use in cosmetics. However, the safety assessment report from the International Fragrance Association (IFRA) proved that its essential oils are safe when used as a fragrance in cosmetic leave-on products at concentrations of no higher than 0.01% and thiophene contents of no more than 0.35%, while emphasizing that they should not be added to sunscreen products (Coenraads, 2016).

8 Discussion and conclusions

This paper briefly describes the botanical characteristics, origin and distribution of Tagetes minuta L. and discusses the findings on the reasons for the development and naturalization of the plant in the Southeast Tibet Autonomous Region. From the perspective of invasion ecology, the invasion mechanism that enables its rapid expansion is analyzed by exploring its unique biological characteristics. Based on previous studies and using the MaxEnt model to simulate the potential future distribution of this plant in the Tibet Autonomous Region, it can be found that this species can further expand its distribution under the influence of climate change. Such an invasive species may threaten the security of the plateau ecosystem in the future. However, the basic situation investigation on the biological and physiological-ecological characteristics of the invasion of Tagetes minuta L., whether it causes an ecological disturbance, and its harm in China is far from adequate. Relevant prevention and management strategies are lacking. Whether the invasion of exotic plants can be successful depends largely on the degree of attention and the prevention and control measures taken. Research on Tagetes minuta L. should be started as soon as possible.
Since Tagetes minuta L. has a long history of research abroad and is considered a resourceful cash crop by many countries, this paper reviews its rich economic value. Therefore, the resource utilization of this plant in China is a natural and effective prevention and management measure. At present, for the prevention and control of this plant, the Tibet Autonomous Region mainly adopts administrative measures to mobilize villagers to manage the plant by physical elimination methods such as excision. Experimental studies conducted in China have not proposed systematic and effective chemical and biological prevention and control methods. Therefore, considering the economic characteristics of this species and foreign experience, we suggest adding this herb to the production of Tibetan incense as an aromatic plant, which can not only solve the problem of insufficient supply of raw materials for Tibetan incense but also control the disorderly expansion of plant populations.

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