Harnessing Opportunities Provided by the Invasive Chromolaena odorata to Keep It under Control

: Invasive alien plants (IAPs) have been well-documented as socio-ecological change drivers in most countries globally. Billions of dollars have been spent worldwide on IAP management projects with varying degrees of success. Understanding the contribution of IAPs to human well-being and livelihoods could provide insights into potential sustainable incentives that could be used to achieve e ﬀ ective IAP management. A review was conducted to assess the beneﬁts of the invasive Chromolaena odorata on human well-being and livelihoods. Literature was gathered using keyword searches in electronic databases. The ﬁndings from this review showed that C. odorata is utilised in bioenergy production, crop production and protection, ethnopharmacology, human nutrition, and livestock production. However, most of these beneﬁts were reported on the Asian / West African biotype. There was only one ethnopharmacological beneﬁt record on the southern African biotype. This shows that, although C. odorata has signiﬁcant negative impacts on the environment and livelihoods, its beneﬁts have been integrated into human well-being and livelihoods. Therefore, C. odorata utilisation in bioenergy production, crop and livestock production, crop protection, and ethnopharmacology could create an economic incentive for species control in invaded sites. However, for utilisation to be e ﬀ ective, it should be used as a complementary control strategy. The following keywords used search relevant literature: “ Chromolaena odorata ”, “ Eupatorium odoratum ”, and “siam in combination with “animal production”, “beneﬁts”, “bioenergy”, “biogas”, “control methods”, “crop production”, “disbeneﬁts”, “disservices”, “ecosystem services”, “ethnopharmacological use”, “human well-being”, “livelihood impacts”, “impacts”, “medicinal use”, and “socio-economic beneﬁts”.


Introduction
Invasive alien plants (IAPs) are now well recognised as one of the key drivers of global socio-ecological change. This is because they affect biodiversity and ecosystem services [1,2], thus in turn affecting human well-being and livelihoods. The IAPs invade both human-modified and natural ecosystems [3], thus reducing their biodiversity and ability to deliver ecosystem services needed to maintain and enhance human well-being and livelihoods [4]. To counteract biodiversity and ecosystem services loss, millions of dollars are spent around the globe annually to manage IAPs [5]. For example, South Africa is currently spending more than US$101 million per year in the management of IAPs [6].
IAPs can have both negative and positive impacts on human well-being and livelihoods [4]. Human well-being is comprised of security, access to basic material to sustain good life, health, personal freedom, and good social relations [7]. Livelihood includes capabilities, assets, and activities needed to earn a living [8]. IAPs' negative impacts pose significant threats to human well-being and livelihoods in many parts of the world, but the impacts are severe in developing countries where most people (especially in rural areas) are more dependent on ecosystem services [9][10][11]. Most research has been focused on IAPs' ecological impacts [9,10,12], but currently the focus is also shifting towards IAPs' impacts on human well-being and livelihoods [4][5][6][7][8][9][10][11][12][13].
Environmental managers are often faced with a challenge of limited resources to manage IAPs, thus necessitating the need for alternative economic incentives that could be used to augment IAP use", and "socio-economic benefits". A literature search was conducted between August 2019 and February 2020, and only literature published in the English language was considered. Books, proceedings papers, reports, research papers, review papers, and theses (referred to as papers in this review) that mentioned C. odorata, E. odoratum, or siam weed invasion status, distribution, human well-being, and livelihood benefits (e.g., crop and livestock production, and insecticidal or medicinal potential), negative and positive impacts on society and the environment, and species management strategies, were selected. The search yielded more than 1000 articles that were screened to identify relevant papers. After screening, 728 papers were found relevant. All 728 papers were read in detail to identify papers that investigated the potential benefits of C. odorata on human well-being and livelihoods. Furthermore, papers on C. odorata's negative impacts and control methods were also considered to inform an effective utilisation strategy that will help keep the species under control. Based on the review of papers that investigated C. odorata's potential benefits, six categories were developed; namely, (1) animal production, (2) bioenergy, (3) crop production, (4) crop protection, (5) ethnopharmacology, and (6) food source.

Results and Discussion
Out of 728 papers, 54 papers investigated the potential benefits of C. odorata on human wellbeing and livelihoods. Out of 54 papers, 17 papers investigated ethnopharmacological benefits, followed by crop production, animal production, crop protection, bioenergy, and then food source ( Figure 1). Fifty-three out of 54 studies were from the countries where the Asian/West African biotype is invasive, and one study was from the countries where the southern African biotype is invasive.

Ethnopharmacological Uses
Despite C. odorata's invasive status in Asia and West Africa, it has been integrated into traditional medicine. Chromolaena odorata aqueous extract and decoction from the leaves are widely used to treat wounds, burns, and diseases such as diabetes and eye problems, in countries such as Vietnam, Malaysia, Thailand, Nigeria, and Ivory Coast [43][44][45][46]. A considerable number of scientific studies have confirmed the pharmacological efficacies of C. odorata. Chromolaena odorata contains anticancer, antidiabetic, antifungal, anti-hepatotoxic, anti-inflammatory, antimalarial, antimicrobial, and antioxidant properties [43][44][45][46][47][48][49][50][51][52][53][54][55]. In Vietnam, formulations prepared from leaf aqueous extracts and decoctions are licensed for clinical use [56]. Ethnopharmacological uses of C. odorata in humans from different countries are reported in Table 1. Given C. odorata's traditional utilisation in Asia and West Africa, information on C. odorata utilisation in traditional medicine is very limited in eastern and

Ethnopharmacological Uses
Despite C. odorata's invasive status in Asia and West Africa, it has been integrated into traditional medicine. Chromolaena odorata aqueous extract and decoction from the leaves are widely used to treat wounds, burns, and diseases such as diabetes and eye problems, in countries such as Vietnam, Malaysia, Thailand, Nigeria, and Ivory Coast [43][44][45][46]. A considerable number of scientific studies have confirmed the pharmacological efficacies of C. odorata. Chromolaena odorata contains anticancer, antidiabetic, antifungal, anti-hepatotoxic, anti-inflammatory, antimalarial, antimicrobial, and antioxidant properties [43][44][45][46][47][48][49][50][51][52][53][54][55]. In Vietnam, formulations prepared from leaf aqueous extracts and decoctions are licensed for clinical use [56]. Ethnopharmacological uses of C. odorata in humans from different countries are reported in Table 1. Given C. odorata's traditional utilisation in Asia and West Africa, information on C. odorata utilisation in traditional medicine is very limited in eastern and southern Africa [41], except one record from Shackleton et al. [13]. According to Omokhua et al. [41], the non-utilisation of C. odorata in eastern and southern Africa can be partly explained by four hypotheses. Firstly, the locals might be still trying to fully comprehend C. odorata's benefits as the species' introduction is recent. Although one can argue that the species was introduced more than seven decades ago in South Africa [38], its spread and a substantial increase in density occurred between the 1950s and 1980s [33]. Secondly, traditional medicine practitioners may be lacking ethnopharmacological knowledge of the plant because it is only found in the eastern parts of the country. Thirdly, studies on traditional usage of the plant are still lacking. Lastly, the southern African biotype might be lacking medicinal properties that are contained in the Asian/West African biotype [41]. However, Naidoo et al. [57] showed that the southern African biotype has potential use in traditional medicine. Their findings showed that leaf methanol extract inhibited Bacillus cereus, Bacillus subtilis, Staphylococcus aereus, and Staphylococcus epidermidis (Gram-positive bacteria), and Escherichia coli (Gram-negative bacterium).
Apart from ethnopharmacological uses, in India, C. odorata leaves are used to treat wounds in livestock [58].

Crop Production
The application of organic mulching is effective in soil physicochemical properties enhancement, weed growth control, soil temperature reduction, soil moisture conservation, and soil erosion reduction, thus increasing crop yield and quality [69][70][71][72]. Chromolaena odorata fallow crops and mulch increase soil macro-invertebrates (e.g., earthworms) and nutrients (e.g., nitrogen, phosphorus, potassium, magnesium, and calcium) [73][74][75][76][77][78]. As a result, C. odorata is widely used as a fallow crop and mulch for soil fertility and crop yield improvement in countries where it is invasive ( Table 2). For example, in Nigeria, Agbede et al. [78] found that C. odorata mulch (5 t ha −1 ) produced an average of 35.4 t ha −1 of Dioscorea rotundata Poir. over two seasons compared to control (23.2 t ha −1 ). In Ghana, Fening et al. [79] reported higher Zea mays L. yield under C. odorata mulch (3 t ha −1 ) compared with control (2.23 t ha −1 ). These findings show that C. odorata can be used as an alternative source of fertilizer by impoverished farmers who cannot afford inorganic fertilizer.

Animal Production
Livestock such as goats and cattle avoid foraging on C. odorata in its natural state (i.e., fresh leaves) , and this is attributed to the strong odour of essential oils in the leaves [40]. Furthermore, there have been reports of cattle that died after consuming C. odorata fresh leaves [4,40]. The strong odour is greatly reduced when the leaves are sun-dried [92]. As a result, C. odorata leaf meal is used as a feed additive. This is because C. odorata is rich in crude protein, amino acids (e.g., arginine, histidine, leucine, lysine, and methionine) [92][93][94], and minerals such calcium, phosphorus, magnesium, potassium, zinc, and iron [95].
A considerable number of studies have reported on C. odorata utilisation as a feed additive in livestock diets, while some studies showed that C. odorata leaf meal has the potential to be used as a feed additive (Table 3). In Nigeria, Fasuyi et al. [96] assessed the effect of C. odorata leaf meal-based diets (0, 2.5, 5, and 7.5%) on layer chickens' feed intake, body weight, and total egg production, weight, and yolk colour over eight weeks. The highest feed intake, body weight, and total egg production were achieved under the 5% of C. odorata leaf meal inclusion, while the highest egg weight and yolk colour were achieved under 5% and 7.5%, respectively [96]. Furthermore, in Nigeria, Aro et al. [40] also recorded the highest total egg production under the 5% C. odorata leaf meal inclusion over eight weeks.
In Nigeria, Jiwuba et al. [97] assessed the effect of C. odorata leaf meal-based diets (0, 4, 8, and 12%) on broiler chickens' carcass weight over 49 days. The highest weight (2952 g) was achieved by broilers that were fed a 4% C. odorata leaf meal-based diet, followed by broilers (2771 g) that were not fed a C. odorata leaf meal-based diet [97]. Contrary to Jiwuba et al. [97]'s findings, Donkoh et al. [98] in Ghana, Enkenyem et al. [99] in Nigeria, and Bonsu et al. [100] in Ghana found that broilers that were fed a 0% C. odorata leaf meal-based diet gained more weight than broilers fed with (1% to 7.5%) C. odorata leaf meal-based diets, although there were no significant differences. Nevertheless, Donkoh et al. [98] concluded that the weight of C. odorata leaf meal-fed broilers might be increased if tannins in C. odorata leaves could be eliminated or neutralised. Enkenyem et al. [99] recommended that C. odorata leaf meal (5%) could be used as a cheaper ingredient in broiler diets, while Bonsu et al. [100] recommended that only 3% should be included in broiler finisher diets.
The overall findings suggest that to achieve the highest egg and meat production, the optimal level of C. odorata leaf meal inclusion in chicken (broilers and layers) and goat diets should be between 4% and 5%. However, C. odorata leaf meal should be prepared before plant maturity (i.e., seed set) to obtain higher nutritive value and to avoid the dispersal of the weed to uninvaded areas [101,103].

Crop Protection
Due to negative environmental impacts associated with synthetic insecticides, botanical insecticides are regarded as the best alternatives owing to their environmental-friendly pest management [105]. However, impoverished small-holder farmers cannot afford commercially available botanical insecticides such as Pyrethrum and azadirachtin [103]. Chromolaena odorata is regarded as a cheaper and effective botanical insecticide against pests of various crops. This is because it is readily available and doesn't require organic solvents, and complex apparatus to extract the insecticide [79,103]. In countries where C. odorata is invasive, impoverished small-holder farmers are using C. odorata leaves and leaf extract to control pests in the field and during harvest storage (Table 4).

Bioenergy
With the ever-increasing demand for energy coupled with the emission of greenhouse gases and the declining supply of fossil fuels, alternative renewable energy sources are becoming more imperative [113,114]. Although IAPs present more disservices than services, research is evolving on the bioenergy potential of IAPs that are already present in the environment [115][116][117][118][119][120]. In Nigeria, Dahunsi et al. [121] found that C. odorata has the potential to be used for biogas production, because they obtained a gas yield of more than 49.2%. In South Africa, Melane [120] found that C. odorata is the best species to be utilised as feedstock for combustion in low-technology reactors to produce heat and electricity via steam turbines owing to its physical, chemical, and economic viability.

Food Source
Some IAPs are utilised as traditional leafy vegetables owing to their nutritional value, thus making a significant contribution to human well-being [122][123][124]. In southern parts of Nigeria, C. odorata leaves are consumed as a vegetable, and this is largely attributed to high nutritional content in the leaves [41].

Chromolaena Odorata Management
Although C. odorata contributes to human well-being and livelihoods, it is regarded as a destructive species. This is because it was found to have high negative impacts on society and the environment, and low benefits [19]. This is supported by Shackleton et al. [13], who found that in northern-central Tanzania, most research respondents reported significant negative impacts (e.g., loss of grazing land) associated with C. odorata, while a few respondents reported its benefits (e.g., medicinal use). The control or eradication (where possible) of destructive species causes little conflict between people who benefit from the species utilisation and those who are responsible for species control (e.g., environmental managers) [19]. All the benefits presented in this review are obtained through the harvest of the species' biomass (leaves and stems). Therefore, C. odorata utilisation can provide a win-win solution. However, it should be noted that utilisation alone cannot be effective; therefore, it should be used as a complementary control strategy.
Utilisation should entail repeated cutting of stems at 3 cm above ground at least four times per year, to exhaust plant reserves in the rootstock [125]. This method is effective in reducing the number of resprouts, which cause dense infestations, and also result in plant mortality, usually after the third cutting [125]. This harvesting strategy should also be adopted by people who only derive benefits from C. odorata leaves. Chromolaena odorata seeds are wind-dispersed, but not greater than 80 m from the source . Vehicles are largely responsible for long-distance dispersal [126]. Therefore, biomass harvesting should be done before flowering to combat species introduction into new areas as a result of seed dispersal. Vigilant monitoring should also be carried out in areas adjacent to the infested sites and on roadsides, to eradicate any seedlings present through uprooting. Development of C. odorata awareness programmes could also help improve the species' monitoring and control efforts in new areas when detected. In areas where there is no utilisation, C. odorata clearing should be integrated with chemical control (e.g., fluroxypyr and triclopyr/picloram herbicides), followed by biomass burning to reduce species densities [20][21][22][23][24][25][26][27][28][29][30][31][32][33][34][35][36]. However, in habitats where there are indigenous tree species (e.g., woodlands, riparian zones, and forests), controlled burning is recommended as C. odorata biomass can create high and intense flames that can end up killing trees [36]. Biomass burning is also effective in reducing reinvasion, because it kills C. odorata rootstock and the soil seed bank [23,35,36]. Furthermore, the use of biological control agents can be effective in reducing C. odorata spread and densification. For example, biological control agents such as Cecidochares connexa (Macquart) (Tephritidae), Pareuchaetes insulata (Walker) (Erebidae), and Pareuchaetes pseudoinsulata Rego Barros (Erebidae) have been reported to be effective in reducing C. odorata infestation densities in some parts of the Pacific, southern and western Africa, and South-East Asia . If C. odorata utilisation can be integrated with the other effective control methods, there will be a reduction in costs associated with mechanical and chemical control methods, and less burden on people responsible for IAP management.

Conclusions
Synthesising information on the contribution of IAPs to human well-being and livelihoods is a vital step in the planning of an effective IAP management plan that incorporates benefits associated with the species. This review showed that C. odorata provides benefits that enhance human well-being and livelihoods in countries where it is invasive, as a bioenergy crop, feed additive (leaf meal) in livestock production, organic fertilizer, and biopesticide in crop production and protection, and food (leafy vegetables). Therefore, C. odorata utilisation should be integrated with other control methods to achieve sustainable management of the species. Furthermore, people who are benefitting from species utilisation, and environmental managers responsible for species control, should co-develop the species management plan. This is because when all the stakeholders are involved in the co-development of the species management plan, the co-developed control strategies are equitable and non-controversial [19]. However, C. odorata utilisation is still limited to Asia and West Africa where the Asian/West Africa biotype is invasive. Therefore, there is a need for studies on the potential benefits of the southern African biotype on human well-being and livelihoods. Given the current rise in renewable energy research, more studies are needed to explore technologies that can optimise biogas extraction in C. odorata. Furthermore, there is also a need for studies on the cost-benefit analyses of different C. odorata utilisation categories (e.g., crop protection). This will help to identify a utilisation category that offers maximum return on investment.
Funding: This research received no external funding.