(Asteraceae) and Its Biological Control in West Africa: the Story So Far

Biocontrol Science and Technology

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Eight decades of invasion by Chromolaena odorata (Asteraceae) and its biological control in West Africa: the story so far

Pascal Osa Aigbedion-Atalor, Medetissi Adom, Michael D. Day, Osariyekemwen Uyi, Ikponmwosa N. Egbon, Itohan Idemudia, Igho B. Igbinosa, Iain D. Paterson, Haruna Braimah, David D. Wilson & Costas Zachariades

To cite this article: Pascal Osa Aigbedion-Atalor, Medetissi Adom, Michael D. Day, Osariyekemwen Uyi, Ikponmwosa N. Egbon, Itohan Idemudia, Igho B. Igbinosa, Iain D. Paterson, Haruna Braimah, David D. Wilson & Costas Zachariades (2019) Eight decades of invasion by Chromolaenaodorata (Asteraceae) and its biological control in West Africa: the story so far, Biocontrol Science and Technology, 29:12, 1215-1233, DOI: 10.1080/09583157.2019.1670782 To link to this article: https://doi.org/10.1080/09583157.2019.1670782

Published online: 24 Sep 2019.

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Full Terms & Conditions of access and use can be found at https://www.tandfonline.com/action/journalInformation?journalCode=cbst20 BIOCONTROL SCIENCE AND TECHNOLOGY 2019, VOL. 29, NO. 12, 1215–1233 https://doi.org/10.1080/09583157.2019.1670782

REVIEW ARTICLE Eight decades of invasion by Chromolaena odorata (Asteraceae) and its biological control in West Africa: the story so far Pascal Osa Aigbedion-Atalora,b, Medetissi Adomc, Michael D. Dayd, Osariyekemwen Uyie, Ikponmwosa N. Egbone, Itohan Idemudiae, Igho B. Igbinosaf, Iain D. Patersonb, Haruna Braimahg, David D. Wilsonc and Costas Zachariadesh,i aInternational Centre of Insect Physiology and Ecology, Nairobi, Kenya; bCentre for Biological Control, Department of Zoology and Entomology, Rhodes University, Grahamstown, South Africa; cAfrican Regional Postgraduate Programme in Insect Science, University of Ghana, Legon, Ghana; dBiosecurity Queensland, Department of Agriculture and Fisheries, Ecosciences Precinct, Brisbane, Australia; eDepartment of Animal and Environmental Biology, University of Benin, Benin City, Nigeria; fDepartment of Zoology, Ambrose Alli University, Ekpoma, Nigeria; gBiological Control Unit, Crops Research Institute, Kumasi, Ghana; hAgricultural Research Council, Plant Health and Protection, Hilton, South Africa; iSchool of Life Sciences, University of KwaZulu-Natal, Scottsville, South Africa

ABSTRACT ARTICLE HISTORY Chromolaena odorata (L.) R.M. King and H. Robinson (Asteraceae) is a Received 23 June 2019 perennial weedy shrub of neotropical origin and a serious biotic Accepted 14 September 2019 threat in its invasive range. The Asian-West Africa (AWA) biotype KEYWORDS of C. odorata present in West Africa is both morphologically and Invasive alien plant; weed genetically different from the southern African (SA) biotype. The fi biocontrol; introduction and AWA biotype was rst introduced into Nigeria in the late 1930s impact; management and rapidly spread across West Africa. Currently, 12 of the 16 strategies; Pareuchaetes countries in West Africa have been invaded, with significant pseudoinsulata; Cecidochares negative effects on indigenous flora and fauna. However, locals in connexa West Africa have found several uses for the weed. As chemical, physical and other conventional methods were unsustainable, costly and largely ineffective, three biological control agents, Apion brunneonigrum (Coleoptera: Brentidae), Pareuchaetes pseudoinsulata (Lepidoptera: Erebidae) and Cecidochares connexa (Diptera: Tephritidae), have been released in West Africa between the 1970s and the early 2000s. However, only C. connexa and P. pseudoinsulata established, contributing to the control of the weed, in six and four countries in West Africa respectively. Limited research funding, the absence of post-release evaluations of the established agents, and the ‘conflict of interest’ status of C. odorata (i.e. being beneficial for local use but damaging to ecosystem services and agriculture), are serious factors deterring the overall biological control effort. Here, using historical records and field surveys, we examine the invasion history, spread, impacts, and management of C. odorata in West Africa and make recommendations for the sustainable management of C. odorata in the region.

CONTACT Pascal Osa Aigbedion-Atalor [email protected] International Centre of Insect Physiology and Ecology, P.O. Box 30772-00100, Nairobi, Kenya; Centre for Biological Control, Department of Zoology and Entomology, Rhodes University, P.O. Box 94, Grahamstown, South Africa © 2019 Informa UK Limited, trading as Taylor & Francis Group 1216 P. O. AIGBEDION-ATALOR ET AL.

1. Introduction The neotropical shrub Chromolaena odorata (L.) R.M. King and H Robinson (Astera- ceae) is invasive in Africa, Asia and the Pacific(Zachariades,Day,Muniappan,& Reddy, 2009). Two biotypes of C. odorata occur in Africa, the more widespread Asian- West African (AWA) biotype, which probably originated from Trinidad and Tobago, and the southern African (SA) biotype of Cuban or Jamaican origin (Paterson & Zachar- iades, 2013; Shao, Li, Lin, & He, 2018). These two biotypes are known to be morphologically and genetically different but display high within-biotype homogeneity (Paterson & Zachariades, 2013; Zachariades et al., 2009). They also exhibit some dissimilarities in aspects of their phytochemistry (Omokhua, McGaw, Finnie, & Van Staden, 2016). The subject of this review is the AWA biotype, which is the only biotype of the plant present in West Africa. The AWA C. odorata biotype was introduced into Nigeria in the late 1930s (Ivens, 1974) and is now widespread in 12 of the 16 countries in West Africa. It has negatively impacted agriculture, biodiversity conservation, and sustainable livelihoods since its introduction and spread (Braimah & Timbilla, 2002;Braimah, Ekyem, Isah, & Mochiah, 2013; Cock & Holloway, 1982; Hoevers & M’Boob, 1996; Tim- billa & Braimah, 1996). However, it also provides some local agricultural and medicinal benefits (Timbilla & Braimah, 1996;Uyi&Igbinosa,2013). Several aspects of the population dynamics and the drivers of the invasion of C. odorata in West Africa have been studied (e.g. Braimah & Timbilla, 2002; Castel, 2012; Hall, Kumar, & Enti, 1972; Timbilla & Braimah, 1996, 2000). These studies have resulted in a better understanding of the biology and ecology of the plant in the region, which is crucial for managing the species. However, ‘the conflict of interest’ status of C. odorata (i.e. being both beneficial for local purposes but damaging to ecosystem services and agriculture) has been the subject of debate and has been detrimental to biological control efforts. The benefits versus deleterious disposition of C. odorata and the lack of funding for research on invasive weeds in West Africa are longstanding and have been ascribed as the two most significant constraints to the success of biological control of C. odorata in West Africa (Uyi & Igbinosa, 2013 and references therein). This paper, therefore, presents a chronological review of the invasion history, distribution, and impact of C. odorata and the management initiatives undertaken since the weed’s introduction over 70 years ago. We discuss the consequences of the constraints of earlier perceptions of the weed’s status, provide insight into current perceptions and offer recommendations for the future management of C. odorata in the region.

2. Materials and methods We reviewed the literature by searching both academic and grey literature in Google Scholar and ISI Web of Science. Published papers, conference proceedings, and disser- tations, some of which are not available online, were also assessed. Prior to a systematic review of the reference lists in the acquired papers, we sorted all data sources and included only articles relevant to the history, impact, and biology of C. odorata in West Africa, as well as the released biological control agents. This was supported by discussions with members of the International Organisation of Biological Control (IOBC), who were BIOCONTROL SCIENCE AND TECHNOLOGY 1217 cited as experts on certain species in the region and authors of the world catalogue of biological control agents for weeds (Winston et al., 2014).

3. Description, biology and ecology of chromolaena odorata The AWA C. odorata can grow up to about 3 m high under open-field conditions in West Africa but can achieve heights of over 5 m when supported by other vegetation (Zachar- iades et al., 2009). Morphological characteristics of the AWA C. odorata consist of pale blue-lilac flowers, moderately hairy pale-green leaves, and scrambling stems which branch extensively, especially when surrounded by vegetation (McFadyen, 1988). The leaves are opposite, have tooth-like margins and three conspicuous veins. When crushed or damaged, the leaves emit volatiles with pungent odours (Waterhouse, 1994). The roots are fibrous, and flowers occur in clusters of 20 to 60 at stem tips (Waterhouse, 1994; Zachariades et al., 2009). Five-millimetre long seeds with hooks and a pappus (5 mm long white bristles) constitute the achenes (Waterhouse, 1994). The achenes can spread over long distances by wind and the seed hooks cling to machinery, clothing, and animal hair (McFadyen, 1988; Waterhouse, 1994). The production of seed is prolific. Climatically, it thrives in West Africa, albeit maladapted to extremely dry areas, such as parts of northern Nigeria, and in the dry arid regions east of Lake Volta in Ghana (e.g. Castel, 2012; Uyi et al., 2014). Chromolaena odorata plants growing in different sunlight conditions exhibit a degree of phenotypic and phytochemical variation (Uyi, Uwagiaha- nor, & Ejomah, 2017). It performs best under open sunny conditions, such as along road- sides, open farmlands, and abandoned plots (Timbilla & Braimah, 1996; Zachariades et al., 2009). Under shade conditions, its vegetative and reproductive performance is significantly reduced. However, it demonstrates a high degree of plasticity in semi-shaded environments, such as in the gaps of disturbed forests (Zachariades et al., 2009). It also shows a preference for soils which are well-drained, and seldom survives under water- logged conditions (Cruttwell, 1972). Flowering occurs in the dry season (Gautier, 1992; Sajise, Palis, Norcio, & Lales, 1974). Both in the native and invasive ranges, flower heads are produced in abundance and the plant is apomictic (Coleman, 1989). The start of the rainy season induces the germination of seeds in the soil as well as the growth of shoots either from undamaged axillary buds or from the crown (McFadyen, 1988, 1989). Several thousand seeds may germinate, albeit with high seedling mortality (Epp, 1987; Yadav & Tripathi, 1981). However, the viability of seeds buried in soils decline over time (Yadav & Tripathi, 1981).

4. Introduction and distribution of C. odorata in West Africa Outside of its native range, C. odorata was introduced ﬁrst as an ornamental plant in the north-eastern part of India in the mid-nineteenth century (Zachariades et al., 2009). It was detected in Sri Lanka and later throughout southeast Asia and Oceania in the late-nineteenth century (McFadyen, 1989; Muniappan & Marutani, 1988; Waterhouse, 1994). In Africa, C. odorata was ﬁrst reported in West Africa in 1942, around Enugu state, south-eastern Nigeria (Ivens, 1974). However, it is believed that it was introduced with the importation of seeds of the forest tree Gmelina arborea Roxb. (Verbenaceae) from Sri Lanka around 1937 (Ivens, 1974). 1218 P. O. AIGBEDION-ATALOR ET AL.

About eight years after its detection in Nigeria, C. odorata was reported in Côte d’Ivoire in 1950 (Hoevers & M’Boob, 1996; Zebeyou, 1991), over 900 km from Nigeria. First records of its presence in other parts of West and Central Africa include: Ghana (1969) (Hall et al., 1972), Benin, Guinea, Liberia, Sierra Leone, The Gambia and Togo (1970s) (Hoevers & M’Boob, 1996; Timbilla, 1998; Timbilla, Zachariades, & Braimah, 2003; Zachariades, Janse Van Rensburg, & Witt, 2013; Zebeyou, 1991). Chromolaena odorata has also been reported present in Burkina Faso (1990s) (Hoevers & M’Boob, 1996). His- torical records of surveys of C. odorata show the weed is now present in 12 of the 16 countries in West Africa (e.g. Uyi & Igbinosa, 2013; Zachariades et al., 2009, 2013) (Figure 1), with the latest record coming from Guinea-Bissau (Catarino, Indjai, Duarte, & Monteiro, 2019). So far, there are no records of C. odorata being in Cape Verde, Mali, Mauritania or Niger. However, new surveys are warranted to determine if C. odorata is present in any of these countries. It is uncertain whether the introduction of C. odorata into Côte d’Ivoire in 1950 was a separate introduction or whether it spread from Nigeria undetected through Benin, Togo and Ghana. There are two prominent theories that tend to support the deliberate introduction of the weed into Ghana (Timbilla & Braimah, 1996, 2000). The ﬁrst was that it was

Figure 1. Map showing the current distribution (as of 2019) of C. odorata in West Africa, and the distribution (as of 2018) of the two established biological control agents, Cecidochares connexa and Par- euchaetes pseudoinsulata. This map was generated based on various reports (published and unpublished data) (Ivens, 1974; Hoevers & M’Boob, 1996; Yehouenou, 1996; Timbilla & Braimah, 1996, 2000; R. Desmier de Chenon personal communication to C. Zachariades, 2009; Timbilla et al., 2003; Castel, 2012; Uyi et al., 2014; Zachariades et al., 2013; Aigbedion-Atalor et al., 2018a, 2018b; M. Adom personal communication to P. Aigbedion-Atalor, April 26, 2018; Catarino et al., 2019). Countries with C. odorata indicated by grey-shaded colour. BIOCONTROL SCIENCE AND TECHNOLOGY 1219 introduced between 1962 and 1966, with the intention of suppressing some noxious plant species around the electricity grids in the relatively small town of Akosombo, in the Greater Accra region of Ghana. The second theory suggests that the plant was introduced by Ghanaians who were resident in Nigeria, for its medicinal attributes (Timbilla & Braimah, 1996). However, there are no empirical validations for either theory. Anthropogenic inﬂuences, such as the movement of humans and machinery, trade, infrastructure development – such as road construction – and tourism across the ‘open borders’ in the sub-region, as well as medicinal and agricultural values attributed to the plant, have been suggested as the fundamental drivers that have facilitated the widespread invasion of C. odorata in West Africa (Braimah & Timbilla, 2002; Timbilla & Braimah, 1996; Uyi & Igbinosa, 2013). In addition, the high reproductive capacity of the weed, readily dispersed propagules, its ability to outcompete other plant species for both light and space, adaptation for growth in a range of soil types and climatic conditions, and its allelopathic properties, are aspects associated with its overall invasion success in new areas (Zachariades et al., 2009).

5. Impact of Chromolaena odorata 5.1. Inimical attributes Following the introduction of C. odorata into West Africa, the weed has been implicated in the transformation of the integrity of many natural and manipulated ecosystems, leading to a decline in biodiversity, agricultural production, and biodiversity conservation efforts in West Africa (Braimah et al., 2013; Timbilla & Braimah, 1996, 2000; Uyi & Igbinosa, 2013). Chromolaena odorata outcompetes and prevents the natural reseeding of indigenous tree species and other vegetation (Honu & Dang, 2000; Timbilla & Braimah, 2000). The weed rapidly invades new areas, smothers nearby vegetation, and induces significant losses in the diversity of indigenous plant species such as Aspilia africana Adams and Mel- anthera scandens Schumach (both Asteraceae) (Braimah & Timbilla, 2002). Chromolaena odorata thickets interfere with the communities of natural and agricultural ecosystems (Holm, Pucknett, Pancho, & Herberger, 1991; Zachariades et al., 2013) and constrain the movement of wildlife and livestock (Hoevers & M’Boob, 1996; Shack- leton, Witt, Nunda, & Richardson, 2017). Yeboah (1998) reported the decline of small mammal diversity in vegetation dominated by C. odorata thickets. Before the biological control interventions against the weed in Ghana, the biomass of grasses and broad- leaved species in the forest regions of the country were reported to have declined, to about 2% and 13% respectively, due to the smothering effects of C. odorata (Timbilla & Braimah, 1996). Consequently, there was a reduction in animal nutrition and a loss of livestock and game animals due to fodder shortage (Braimah & Timbilla, 2002). Indeed, this was one of the most devastating impacts of C. odorata in West Africa, with serious consequences to livestock ranching, and urgent sustainable control strategies were warranted (Timbilla & Braimah, 2000). The impact of C. odorata on agriculture in West Africa has been devastating (Hoevers &M’Boob, 1996; Timbilla et al., 2003; Timbilla & Braimah, 1996). In Ghana, for example, Timbilla and Braimah (1996) reported reductions in yield of numerous staple crops such as cocoa, oil palm, and citrus. Indeed, an increase in management costs of both subsistence 1220 P. O. AIGBEDION-ATALOR ET AL. and commercial agricultural systems has been associated with the abundance of C. odorata (Prasad, Muniappan, Ferrar, Aeschliman, & deForesta, 1996; Timbilla & Braimah, 1996, 2000). Losses incurred by farmers due to the suppression of staple crops by C. odorata in the early years of its invasion, was overwhelming and forced numerous farmers to abandon their plantations (Timbilla & Braimah, 1996). Chromolaena odorata contains allelopathic chemicals, with deleterious effects on crop production. Onwugbuta-Enyi (2001) showed that the aqueous leaf extracts of C. odorata significantly affected the dry weight of tomato and that the addition of 2 g of C. odorata leaf residue to 80 g of soil, significantly reduced the dry weight of tomato due to the inhi- bition of both the root and shoot growth of the crop. Under open-field conditions, C. odorata can induce the accumulation of toxic residues or leachates in crops, especially tomato, thus resulting in significant yield reductions (Onwugbuta-Enyi, 2001). In the dry season in West Africa, commonly referred to as ‘harmattan season’, charac- terised by the dry, dusty north-eastern trade winds, C. odorata constitutes a fire risk in many ecosystems, due to its flammable chemical composition and habit of forming dense dry thickets. Fires induced or increased in intensity by C. odorata, result in damage to agricultural lands, wildlife, human lives and property (Cock & Holloway, 1982; Timbilla & Braimah, 1996).

5.2. Beneficial attributes Chromolaena odorata has been reported by local people in West Africa to have several beneficial attributes (Timbilla & Braimah, 1996). First, and widespread, is that the plant is deemed to have pharmalogical potential (Omokhua et al., 2016). The leaf extract of C. odorata serves as first aid treatment of fresh wounds, as it is believed to facilitate blood clotting (Timbilla & Braimah, 1996). Omokhua et al. (2016) attested that the wide range of ethnopharmacological uses of the plant is probably because of the presence of flavonoids, essential oils, phenolics, tannins, and saponins. The plant is reported to have antibacterial, anti-inflammatory, antioxidant, anthelminthic, antifungal, cytotoxic, antic- onvulsant, antiprotozoal, antispasmodic, antipyretic and analgesic properties. Also, in some villages, notably in the northern region of Ghana, the weed is used for embalming cadavers, and for the treatment of a range of fever conditions such as malaria (Timbilla & Braimah, 1996). Secondly, there is widespread belief that C. odorata provides some useful agricultural benefits (Prasad et al., 1996). In Nigeria, for example, a mixture of C. odorata biomass plus urea fertiliser has been recommended to increase maize and yam production respectively (Agbede, Adekiya, & Ogeh, 2013; Ogundare, Babatunde, & Aduloju, 2014). Although the weed is generally considered poisonous to animals, and not recommended as livestock feed (e.g. Shackleton et al., 2017), some studies have shown that it is beneficial in low con- centrations (no more than 5%) to egg-laying poultry without any haematologically or bio- chemically negative consequences (e.g. Fasuyi, Fajemilehin, & Omojola, 2005). Recent studies have demonstrated that processed powders of the root and shoot systems of C. odorata, showed some repellent and insecticidal potency against pests of stored pro- ducts such as Callosobruchus maculatus (Fab) (Coleoptera: Chrysomelidae) (Uyi & Obi, 2017), and against vectors of economic importance such as Periplaneta americana L. (Blattodea: Blattidae) (Udebuani, Abara, Obasi, & Okuh, 2015). BIOCONTROL SCIENCE AND TECHNOLOGY 1221

The most important albeit controversial benefit is that provided by the ‘slash and burn’ of C. odorata in shifting agriculture system, which is largely practised by small-scale resource-poor subsistence farmers (Timbilla & Braimah, 1996). Tropical soils that have been under forest (usually in high rainfall regions) are quickly depleted of nutrients once the forest is cleared and used to grow crops. Therefore, it is necessary to abandon these fields after a few years and clear further forested areas. The abandoned areas have historically reverted to secondary forest, and the soil becomes replenished over time (the fallow period). However, with increased pressure on the land for crops, this fallow period has decreased, resulting in lower soil fertility and more forest cleared (Braimah et al., 2013). Invasion by C. odorata has offered a partial solution to this. Chromolaena odorata has a rapid growth rate and is excellent at turnover and production of biomass, resulting in increased soil fertility over a shorter period of time. This allows fields to be re-utilised suc- cessfully after a shorter fallow period. As C. odorata self-propagates at high densities, there is no need for farmers to cultivate it, as is the case with other cover crops. Therefore, it was deemed inappropriate from the perspective of these farmers, to release biological control agents to help control the weed. These concerns were articulated in Prasad et al. (1996), De Foresta and Schwartz (1991), Herren-Gemmill (1991) and Weise, Hauser, Koutika, and Tchamou (2002). However, in the two decades since, this controversy appears to have abated, probably because there is not enough land to practice slash and burn agriculture – land has to be used throughout the year and every year – hence the current seldom practice of shifting cultivation. Clearly, there is a need for cost-benefit analyses of C. odorata (the inimical vs beneficial attributes) in West Africa. Such analyses could investigate the cost of the human health vulnerabilities – injuries incurred by slashing the plants and other health complications due to the exposure to dangerous chemicals (Timbilla et al., 2003), versus the local usefulness of the weed (enumerated above) in the region. It is prudent to note that none of the current control methods (conventional and biological control) against C. odorata in West Africa would reduce the density of the weed to the point that it becomes non-existent in the region. This suggests that the reduction of C. odorata density below thresholds of ecological significance would not necessarily deter its local benefits.

6. Management strategies 6.1. Conventional control Many people, including governments, were of the opinion that the adverse eﬀects of the weed superseded the known beneﬁts (Uyi & Igbinosa, 2013). This led to the development of various management strategies against the weed across the sub-region (Ivens, 1974; Timbilla & Braimah, 1996). Several conventional methods were adopted (Figure 2) and are still being used in managing C. odorata in West Africa. Notably, the use of physical means, such as weeding with crude implements – shovels, hoes, and cutlasses have been widely adopted in managing C. odorata. Another widely adopted control method is ‘slash and burn’ (Timbilla & Braimah, 1996). Here, the scrambling stems of C. odorata are severed and subsequently burned after stem wilting. To prevent regrowth, most farmers in Nigeria and Ghana go a step further to uproot the stumps with harvesters, hoes or other mechanical equipment. This method is however, laborious and expensive. 1222 P. O. AIGBEDION-ATALOR ET AL.

Figure 2. The invasion history and control of Chromolaena odorata in West Africa. Besides physical control, the use of herbicides, albeit rarely, has been documented (Tim- billa & Braimah, 1996). Some farmers across the sub-region use several herbicides such as glufosinate-ammonium, glyphosate-isopropylamine, glyphosate-trimesium and triclopyr and hexazinone for the control of C. odorata (Ikuenobe & Ayeni, 1998). However, due to the high purchasing cost and associated human health challenges such as respiratory ailments induced by these chemicals, herbicides are seldom used (Uyi & Igbinosa, 2013).

6.2. Biological control The widespread impact of C. odorata and the decrial of the conventional means of managing the weed in West Africa started a new era (biological control) of its management in West Africa and beyond (Ivens, 1974). In the late 1960s, the Nigerian government com- missioned two scientific task forces with the mandate of finding sustainable means of managing the weed in West Africa (Ivens, 1974, Lucas, 1989). In their assessments, biological control was identified as the most suitable strategy. Subsequently, two biological control agents, the weevil Apion brunneonigrum Béguin-Billecocq (Coleoptera: Brentidae) and the folivore Pareuchaetes pseudoinsulata Rego Barros (Lepidoptera: Erebidae) were identified in the native range of the weed, and then introduced into West Africa following testing to ensure host specificity (Figure 2) (Cock & Holloway, 1982; Cruttwell, 1972). This was the first attempt at biological control of C. odorata worldwide and was funded by the Nigerian government, through the Nigerian Institute for Oil Palm Research (NIFOR). Chronologically, we enumerate the three classical biological control programmes undertaken in West Africa and their respective outcomes from the 1970s to date.

6.2.1. Introduction of Apion brunneonigrum and Pareuchaetes pseudoinsulata (the 1970s) With the intention of ﬁnding potential biocontrol agents of C. odorata in its native range for release in West Africa, surveys and host-range trials were conducted in Trinidad in the BIOCONTROL SCIENCE AND TECHNOLOGY 1223 late 1960s and early 1970s (Cruttwell, 1972, 1974). Host-speciﬁcity trials showed that A. brunneonigrum, Acalitus adoratus Keifer (Acarina: Eriophyidae), Phestinia costella (Solis, Metz and Zachariades) (=Mescinia sp. nr. parvula) (Zeller) (Lepidoptera: Pyralidae) and P. pseudoinsulata were potential candidates for release (Bennett & Crutt- well, 1973; Cruttwell, 1977) in West Africa. However, only A. brunneonigrum and P. pseudoinsulata were introduced into Ghana and Nigeria, in the early 1970s. Unfortu- nately, neither agent was thought to have established in either Ghana or Nigeria, probably due to predation (Cock & Holloway, 1982).

6.2.2. Re-introduction of Pareuchaetes pseudoinsulata (1991-1996) In 1991, a renewed collaborative effort between the Crop Research Institute (CRI) of Ghana and the University of Guam led to the successful re-introduction of P. pseudoinsulata into Ghana, between 1991 and 1996 (Timbilla & Braimah, 2000). Par- euchaetes pseudoinsulata spread widely across the southern part of the country, inflicting varying levels of damage to C. odorata (Braimah et al., 2013; Timbilla & Braimah, 2000) (see. Figure 3). At a similar time (1991), P. pseudoinsulata was also released in Côte d’Ivoire but failed to establish (Timbilla et al., 2003). About 18 years later (2009), P. pseudoinsulata was detected at two villages, Evbuabogun (6°15’53.5’’N, 5°39’53.7’’E) and Uson (6°14’10.9’’N, 6°04’29.4’’E), in Edo state, south- western Nigeria (Uyi, Egbon, & Igbinosa, 2011). In elucidating the presence of the moth in Nigeria, Uyi et al. (2011) hypothesised that either some populations of the moth had established in the first releases made in the country in the 1970s or that it spread from established sites in Ghana. In another instance, in Edo State, three separate clusters of several tens of larvae of P. pseudoinsulata were seen defoliating C. odorata in a locality at a boundary plot (6°21’12.8 ’’N, 5°53’39.4’’E) between the two villages, Iguoghae and Ebueneki, about 50 km north of Evbuabogun, in the months of May and June 2018. An attempt to further quantify its persistence yielded none of the agent’s life stages in that locality. Although the moth is present in four countries in West Africa, its population level is generally low in the field, albeit with periodic outbreaks (Aigbedion-Atalor, Idemudia, Adom, & Day, 2018a; Uyi, 2008; Uyi et al., 2017). Several studies (e.g. in Ghana) have shown that P. pseudoinsulata significantly decreased the cover of C. odorata plants from 80% cover to 30% (Braimah et al., 2013; Timbilla et al., 2003). However, in a re- evaluation study, Uyi, Wilson, and Zachariades (2009) reported a decline in the density of the moth and concluded that the moth was incapable of providing further significant control of C. odorata. Braimah et al. (2013) attested that the low in densities of P. pseudoinsulata was resultant of the significant reduction in densities of the weed. To validate the report by Braimah et al. (2013), Aigbedion-Atalor (2016) conducted surveys of C. odorata and P. pseudoinsulata in the southern part of Ghana in 2015 and 2016. Results showed that along a 100 m line transect, indices (e.g. larvae, frass, exuviae, and defoliated C. odorata leaves – specific to the herbivory by the moth) indicated the presence of the moth. However, the moth was difficult to detect in the majority of sites, occurring mostly in locations with high (∼ 81%) abundance of C. odorata in the Ashanti, Central, Eastern, and Greater Accra regions of Ghana. In landscapes where the weed was in low (11%) abundance, the moth was not recorded. Indeed, P. pseudoinsulata demonstrates a preference for landscapes with dense thickets of C. odorata, and the frequencies 1224 P. O. AIGBEDION-ATALOR ET AL.

Figure 3. Pareuchaetes pseudoinsulata (A) Eggs, (B) Larva, and (C) Adult on C. odorata. Photo credits: (A) W. Orapa (B) M. D. Day, (C) W. Orapa. of the moth settle to a low-density equilibrium when C. odorata thickets are reduced or occur in fragmented patches (Zachariades et al., 2009), as that which currently occurs across several parts of West Africa. Currently, despite the generally low densities of P. pseudoinsulata in West Africa, the moth has continued to expand its range in the sub-region (Aigbedion-Atalor et al., 2018a). In April 2018, P. pseudoinsulata was detected in Togo for the first time (Aigbe- dion-Atalor, Idemudia, Witt, & Day, 2019a), indicating a likely spread of the moth from established populations in Ghana. Pareuchaetes pseudoinsulata is now reported to be established in Benin, Ghana, Nigeria, and Togo (Figure 2) and it is possible that it could be found in countries further west such as Liberia and further east, into Central Africa. Compared with prior densities, in the early period of its establishment, the current low abundance of P. pseudoinsulata in West Africa suggests it to be less effective (e.g. Aigbe- dion-Atalor, 2016; Aigbedion-Atalor, Day, Idemudia, Wilson, & Paterson, 2019b but see Timbilla & Braimah, 2000). However, equating its low density to current low effectiveness BIOCONTROL SCIENCE AND TECHNOLOGY 1225 could be erroneous, given that the moth has provided, and still provides somewhat significant control of C. odorata in West Africa (Braimah et al., 2013; Timbilla & Braimah, 2000), and probably beyond. Indeed, the case of P. pseudoinsulata in West Africa is not peculiar. It has been asserted that wherever the moth had established, C. odorata cover has been reduced to about 30 percent. However, the moth appears unable to reduce it any further because it does not perform well on isolated patches of C. odorata plants (R. McFa- dyen personal communication to C. Zachariades, 2009).

6.2.3. Introduction of Cecidochares connexa (2003) Although P. pseudoinsulata has established in West Africa and there is some evidence that it is contributing towards the control of the weed, the continual pervasive impact of C. odorata in West Africa resulted in a proposal to introduce another biological control agent to help complement the herbivory of P. pseudoinsulata (Zachariades et al., 2009). Host-specificity testing of the stem galling fly Cecidochares connexa (Macquart) (Diptera: Tephritidae) (Figure 4), in numerous countries against over 136 different plant species, indicated that the gall fly is host specifictoC. odorata (Day, Riding, & Senar- atne, 2016; McFadyen, Desmier de Chenon, & Sipayung, 2003). Cecidochares connexa induces galls on C. odorata stems (McFadyen et al., 2003) and the development of galls, results in a reduction in both the vegetative and reproductive performances of the plant

Figure 4. Cecidochares connexa (A) larvae in a dissected gall, (B) galls on C. odorata stems, and (C) Adult. Photo credits: C. Wilson. 1226 P. O. AIGBEDION-ATALOR ET AL.

(Aigbedion-Atalor et al., 2019b Cruz, Muniappan, & Reddy, 2006; Soekisman, 1999). The reduction in the plant’s performance is due to the diversion of the plant’s mineral nutrients into galls housing the juvenile life-stages of the gall fly. The formation of galls act as a nutrient sink and consequently deprives the plant of a significant amount of its nutrients for growth and reproduction (Cruz et al., 2006; McFadyen et al., 2003). In 2003, many years after the gall fly was successful in other parts of the world such as Indonesia and Papua New Guinea (Day, Bofeng, & Nabo, 2013b; McFadyen et al., 2003), it was introduced into West Africa (Côte d’Ivoire) (R. Desmier de Chenon, personal communication to C. Zachariades, 2009). In April 2014, C. connexa was detected at high densities to the west of Lake Volta in Ghana (Paterson & Akpabey, 2014). Surveys conducted across the southern part of Ghana in 2015, revealed the presence of the gall fly, albeit in low density close to the Togo border, east of Lake Volta. Surveys in 2016, confirmed its presence in Togo (Aigbedion-Atalor et al., 2019a). This finding indicated that between 2003 and 2016 (13 years), it had spread over 1000 km from the release sites of Soubre and Okrouyo in Côte d’Ivoire (Aigbedion-Atalor et al., 2019a). The gall fly is now present in six West African countries (see Figure 1), and significantly reducing the performance of the weed in Ghana (Aigbedion-Atalor et al., 2019b). Monitoring the effectiveness of the gall flyonC. odorata in other countries in West Africa has not been conducted. In a recent study, the stem-galling effect of C. connexa was shown to have significantly reduced the vegetative and reproductive performance of the plant in Ghana (Aigbedion- Atalor et al., 2019b). This was the first formal post-release study assessing the impact of C. connexa on C. odorata in West Africa, 16 years after its release. In a related study, 16% parasitism of C. connexa by a chalcid larval ectoparasitoid Ormyrus sp. Westwood (Hymenoptera: Chalcidoidea: Ormyridae) in Ghana was documented (Aigbedion- Atalor et al., 2019a). This finding raised concern because C. connexa is one of only two highly effective biological agents of the weed currently in West Africa, and parasitism is often considered a factor that could reduce the effectiveness of biological control agents (e.g. McFadyen et al., 2003). Although Ormyrus sp. has been reported present in three regions (Central, Eastern and Greater Accra) in the southern part of Ghana, its country-wide and sub-regional distribution is however, unknown.

7. Breaking free from past constraints: future outlook of the management of chromolaena 7.1. Constraints of the biological control of C. odorata Historically, two major factors have constrained the biological control efforts of C. odorata in West Africa. The conflict of interest in the status of C. odorata (weed vs medicinal/ fallow shrub) and funding for original research in weed biological control is generally not prioritised by many institutions and governments in West Africa (Uyi & Igbinosa, 2013; Uyi et al., 2014). For example, in the 1990s, a proposal submitted to the Food and Agriculture Organisation (FAO) of the United Nations (UN), to fund a biological control programme against C. odorata in West Africa, was not successful due to this conflict of interest (Agbim, 1987; Akobundu, Ekeleme, & Chikoye, 1999; De Rouw, 1991, 1995; McFadyen, 1996; Prasad et al., 1996). We cannot dispute that there is substan- tial scientific evidence supporting the local usefulness of C. odorata both in medicine and BIOCONTROL SCIENCE AND TECHNOLOGY 1227 agriculture in West Africa. However, fortunately, over the past decade, there has been an increase through published articles, in the acknowledgment of C. odorata as a highly invasive weed in West Africa causing significant impacts to agriculture and the environment (Uyi et al., 2014). This, therefore, serves as a positive beacon for the future outlook of the biological control of C. odorata in West Africa.

7.2. Future outlook Current data show that C. connexa is highly effective at controlling populations of C. odorata in Ghana (Aigbedion-Atalor et al., 2019b), which suggests that the gall fly could also perform well in other countries in West Africa. Therefore, assessing the performances of both C. connexa and P. pseudoinsulata, against C. odorata in West Africa is needed. In this evaluation programme, and in a stepwise manner, the following should be considered: (1) Surveys should be conducted across the sub-region with the intention of determining the distribution of C. odorata, especially in the countries where the weed is currently reported absent (see Figure 2). Notably, surveys for C. connexa are warranted in the south-western part of Nigeria due to the recent (October 2018) detection of C. connexa in Abomey-Calavi, (6°24’52.0’’N, 2°20’35.2’’E) in Cotonou, Benin Republic (P. Neuenschwander personal communication to M. Day 2018; M. Adom personal communication to P. Aigbedion-Atalor, April 26, 2018). (2) Cost: benefit study, assessing the socio-ecological assessments of the impact of C. odorata, notably on the livelihoods of the indigenous people and the local benefits of the weed. 1. (3) Long-term evaluations of the distribution, spread, and abundance of C. connexa and P. pseudoinsulata in West Africa. For example, since the first record of C. connexa in Togo (Aigbedion-Atalor et al., 2019a), no further study has been conducted to determine the distribution and abundance of the fly in the country. Similarly, prior to the re-evaluation of the impact of P. pseudoinsulata in Ghana by Uyi (2008), no study on the moth have been conducted in the country for almost a decade after its establishment was confirmed (Timbilla & Braimah, 2000). This trend of discontinuance of further studies of the gall fly, following first records of establishment or detection, has been observed also in Côte d’Ivoire, Guinea, and Liberia. Such studies undertaken on an ongoing basis would help in the detection of potential threats such as Ormyrus sp. (Aigbedion-Atalor et al., 2019a). For example, in Indonesia, an estimated 15% parasitism by Ormyrus sp. has been document (McFadyen et al., 2003). Alas, no solutions can be provided against Ormyrus sp. because it occurs naturally in Africa. (4) Evaluation of the impact of both C. connexa and P. pseudoinsulata, and the outcome of their interactions in countries where both agents are present. Here, results obtained would help unravel the need (if required) for considerations for the addition of other agents, such as the neotropical stem-galling weevil, Conotrachelus reticulatus Champion (Coleoptera: Curculionidae) to help complement the impact of C. connexa and P. pseudoinsulata. This is because, both C. connexa and P. pseudoinsulata are thought to be less effective/slower in drier regions; as is the case to the east of Lake Volta in Ghana (Aigbedion-Atalor, Wilson, Eziah, Day, & Paterson, 2018b). For a long time, the importance of the social dimensions of biological invasions such as impacts on livelihoods has been underrated (Shackleton, Shackleton, & Kull, 2019). 1228 P. O. AIGBEDION-ATALOR ET AL.

However, recent studies indicate that such social dimensions are as fundamental as the ecological consequences of invasions (Shackleton et al., 2019 and references therein). Con- sidering that C. connexa is regarded as the most successful biological control agent of C. odorata worldwide (Cruz et al., 2006; Day, Bofeng, & Nabo, 2013a, 2013b; Day et al., 2013c; McFadyen et al., 2003; Zachariades et al., 2009), the need for major actors such as Governments, Institutions, funding bodies, and scientists in West Africa and beyond, to participate in a concerted regional alliance aimed towards addressing the management of C. odorata in the region has been reiterated (Aigbedion-Atalor et al., 2018a, 2018b). However, with or without the realisation of the recommended regional alliances, we antici- pate the agents to remain active in the landscapes of West Africa.

8. Summary points

. Chromolaena odorata was introduced into West Africa in the late 1930s in Ghana. It is now present in 12 of the 16 countries in West Africa. New surveys are warranted in the four countries in the region where it has not been recorded. . Chromolaena odorata is a threat to the diversity of extant vegetation and impacts negatively on agriculture. It is considered one of the worst invasive species in West Africa. . Control strategies have historically relied on conventional means such as slash and burn, and the seldom use of chemical herbicides. These methods are, however, laborious and costly in the long-term and are not sustainable. . Biological control of C. odorata worldwide first began in West Africa in the 1970s. Although this first attempt failed, the second attempt in 1991 was successful. In this attempt, P. pseudoinsulata established and significantly reduced densities of the weed in the 1990s. However, its effectiveness at controlling the weed was limited. . Another biological control agent C. connexa was introduced into West Africa in 2003. Cecidochares connexa is established in six countries in West Africa and reducing populations of C. odorata where monitoring has been conducted. . A conflict of interest in the status of the plant has been the key factor hampering the biological control efforts of C. odorata in West Africa. . Benefit-cost studies are needed throughout the region to determine the current view of C. odorata and to try to clarify any current conflicts of interest. . Long-term studies, through a new biological control programme against C. odorata is warranted to understand the population dynamics and effectiveness of C. connexa and P. pseudoinsulata in the West and Central Africa sub-regions and to determine if additional biological control agents are warranted.

Acknowledgements We thank Nana Aidoo Akotsen-Mensah for assisting with the acquisition of literature for this paper. Aigbedion-Atalor and Paterson were supported by the Working for Water Programme (WfW) of the Department of Environment Forestry and Fisheries: Natural Resource Management Programmes (DEFF: NRM), as well as by the South African Research Chairs Initiative (SARChI) of the Department of Science and Technology (DST) and the National Research Foundation (NRF). BIOCONTROL SCIENCE AND TECHNOLOGY 1229

Disclosure statement No potential conﬂict of interest was reported by the authors.

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