Management of Biological Invasions (2014) Volume 5, Issue 4: 377–393 doi: http://dx.doi.org/10.3391/mbi.2014.5.4.09 Open Access © 2014 The Author(s). Journal compilation © 2014 REABIC

Review

Chromolaena odorata invasion in Nigeria: A case for coordinated biological control

Osariyekemwen O. Uyi1,5*, Frank Ekhator2, Celestine E. Ikuenobe2, Temitope I. Borokini3, Emmanuel I. Aigbokhan4, Ikponmwosa N. Egbon5, Abiodun R. Adebayo6, Igho B. Igbinosa7, Celestina O. Okeke2, Etinosa O. Igbinosa8 and Gift A. Omokhua5,9 1Department of Zoology and Entomology, Rhodes University, P. O. Box 94, Grahamstown 6140, South ; 2Agronomy Division, Nigerian Institute for Oil Palm Research, P. M. B. 1030, Benin City, Nigeria; 3National Centre for Genetic Resources and Biotechnology, P. M. B 5382, Moor Plantation, Ibadan, Nigeria; 4Department of Biology and Biotechnology, University of Benin, P. M. B. 1154, Benin City, Nigeria; 5Department of and Environmental Biology, University of Benin, P. M. B. 1154, Benin City, Nigeria; 6Department of Crop, Soil and Pest Management, Federal University of Technology, Akure, Nigeria; 7Department of Zoology, Ambrose Alli University, P. M. B. 14, Ekpoma, Nigeria; 8Dept. of Microbiology, University of Benin, P. M. B. 1154, Benin City, Nigeria; 9Research Centre for Plant Growth and Development, School of Life Sciences, University of KwaZulu-Natal, Pietermaritzburg, Private Bag X01, Scottsville 3209, South Africa *Corresponding author E-mail: [email protected]

Received: 8 February 2014 / Accepted: 23 May 2014 / Published online: 4 August 2014

Handling editor: Vadim Panov

Abstract

Chromolaena odorata (L.) King and Robinson (: ) is an invasive perennial weedy scrambling of neotropical origin, widely acknowledged as a major economic and ecological burden to many tropical and subtropical regions of the world including Nigeria. Here, we examine the invasion and management of C. odorata in Nigeria over the last seven decades using historical records and field surveys and ask: (i) Does the usefulness of C. odorata influence its invasion success? (ii) Is a coordinated control approach against C. odorata needed in the face of its usefulness or do we need to develop strategies for its adaptive management? We searched major institutional libraries in Nigeria and carried out extensive research of historical records using different data base platforms, including Google Scholar, Science Direct, ISI web of Science, SciFinders and Scopus. Apart from the biological invasive characteristics of C. odorata and the increased anthropogenic disturbances occurring over the time period, the records indicate that the ethno-pharmacological, funcigicidal, nematicidal importance of the plant and its use as a fallow and as a soil fertility improvement plant in the slash and burn rotation system of agriculture is partly responsible for the invasion success of the weed. The current distribution and infestation levels of this invasive weed in Nigeria are mapped. The current methods of control and the failed attempt made by the Nigerian government to eradicate the weed between the late 1960s and 1970s are discussed. We argue that even in the face of the usefulness of C. odorata, it is reasonable to implement a nationwide coordinated control programme against it with biological control as a core component, because weed biological control does not eliminate the target species, instead it aims to establish an equilibrium which maintains the weed’s population below the level where it causes significant harm to natural and semi-natural ecosystems. Key words: invasive alien weed, spread and distribution, weed status, conflict of interest, biological control, Nigeria

natural and semi-natural ecosystems in most parts Introduction of its introduced ranges (see Zacharides et al. 2009) thereby compromising ecosystems integrity. This Invasive alien plant species impact negatively on invasive alien shrub which smothers existing agriculture, livelihoods and the conservation of native plant communities also attracts significant biodiversity (Mack et al. 2000; Rejmánek et al. attention because of the threat it poses to 2005; Pejchar and Mooney 2009) worldwide, agriculture and human livelihoods. Chromolaena causing significant economic losses (Pimentel 2002; odorata, known in Nigeria as Awolowo, Akintola Perrings et al. 2010). As is common with other or Queen Elizabeth weed, is a perennial weedy invasive alien plant species, Chromolaena odorata shrub native to the from southern Florida King and Robinson, 1970 (= odoratum) to northern Argentina including the (Asteraceae) is and remains a huge threat to islands (McFadyen 1988).

377 O.O. Uyi et al.

Following its introduction from Sri Lanka into understanding of its invasion and management southern Nigeria in 1937 (Ivens 1974), it has history. Here, we examine the invasion (spread and reached alarming proportions in Nigeria (Lucas distribution) and management of C. odorata in 1989; Uyi et al. 2013; Uyi and Igbinosa 2013), Nigeria over the last seven decades using historical Cameroon, Ghana, and other parts of Africa records and field surveys. We ask: (i) How (Zachariades et al. 2009; 2013), and is now one rapidly did C. odorata spread and why? (ii) What of the worst weeds in Nigeria and West Africa. is the current extent of spread and impact? (iii) The biotype of C. odorata found in West and What attempts were made to control C. odorata Central Africa differs from the invasive form and were they successful? (iv) Do the positive attributes of C. odorata influence the continuous found in South Africa, in both morphology and spread of the weed? (v) Is a coordinated control aspects of its ecology (Zachariades et al. 2009; approach against C. odorata needed in the face Paterson and Zachariades 2013) and is thought to of its usefulness or do we need to develop strategies originate from Trinidad, Tobago and adjacent areas for its adaptive management? To answer these in the West Indies. The southern African C. odorata questions, we undertook a thorough literature biotype is not the subject of this paper. The search using the internet and major institutional biology and ecology of both biotypes of C. odorata libraries in Nigeria. has been well documented (see Holm et al. 1977; Gautier 1992; Witkowski and Wilson 2001; Methods Rambuda and Johnson, 2004) and reviewed in Zachariades et al. (2009). We systematically surveyed between November Because of its presence over large areas and 2011 and December 2013 reports in University its invasive nature, the application of chemical of Benin and Nigerian Institute for Oil Palm and mechanical control methods is not sustainable (NIFOR) libraries in Benin City, Nigeria, published in terms of cost and practicability, hence by Federal Ministry of Agriculture and Rural biological control of the weed was attempted in Development and in national and international Nigeria in the 1970s (Cock and Holloway 1982), scientific journals from 1960s until the present but this effort was not successful (Julien and day. Information gathering also involved the use Griffiths 1998). Following the unsuccessful control of different data base platforms, including Google attempts, biologists, ecologists, conservationists, Scholar, Science Direct, ISI web of Science agriculturists and non-professionals in the country SciFinders and Scopus. The eligibility criteria have continuously differed on the best way to were deliberately broad in order to ensure that we respond to the C. odorata invasion, partly because included all relevant materials. All reports and the weed is thought to offer a variety of benefits. papers that mention C. odorata and its control in For example, many publications describe the any capacity (for example spread, status, control importance of C. odorata as a fallow species in measures) were included in the selection process. slash and burn fallow rotations practiced by farmers Over one hundred records were identified. A in the country (e.g. Akobundu and Ekeleme 1996; thorough search of these records was carried out Tian et al. 1998; Akobundu et al. 1999; Tian et to examine the narrative surrounding C. odorata al. 2005) and there are also many publications on in each record. These records were used to answer its medicinal uses in several parts of the country the questions raised earlier. (e.g. Odugbemi et al. 2007; Ajao et al. 2011; To examine the extent of spread of C. odorata Alisi et al. 2011). Furthermore, the importance in Nigeria, opportunistic surveys were conducted of the weed in livestock nutrition, improvement by the individual authors between 2003 and 2013 of soil fertility and its potential use as a pesticide in different parts of the country; results were has been reported (see references in Table 1). used to map the current distribution of the weed. At present, there are no control or management efforts in place to check the spread of the weed in Nigeria. With the exception of the earlier Results and discussion publications by Ivens (1974) and Lucas (1989), History and current distribution of Chromolaena we are not aware of any later attempt to review odorata in Nigeria and/or assess the invasiveness and status of C. odorata in Nigeria. Due to the perceived usefulness The first collection of C. odorata in Nigeria was of C. odorata, the initiation of a control or in 1942 from a forestry plantation near Enugu, in management programme would require a proper south-eastern Nigeria and is thought to have resulted

378 Seven decades of Chromolaena odorata invasion in Nigeria

Table 1. The status of Chromolaena odorata as a weed versus its usefulness in Nigeria.

References Weed Beneficial Author’s submissions Adebayo (2013) * Threat to biodiversity and agriculture Adebayo and Uyi (2010) * - Adetoro et al. (1998) * Improvement of soil fertility Adeyemi (1989) * Weed of plantation crops Afolayan (1988) * Threat to agriculture Agamagu et al. (2008) * Threat to agriculture Agbim (1987) * Fallow species/improve soil fertility Agunbiade and Fawale (2009) * Biomarker and bioremediation Ajao et al. (2011) * Medicinal plant Akinmoladun et al. (2007) * - Akinyemiju and Alimi (1989) * Threat to agriculture Akobundu and Agyakwa (1998) * Akobundu and Ekeleme (1996) * Fallow species/improve soil fertility Akobundu et al. (1999) * - Alisi and Onyeze (2009) * Medicinal plant Alisi et al. (2011) * - Amiolemen et al. (2012) * Improvement soil fertility Anoliefo et al. 2003 * Phyto-remediation Aro and Fajemilehin (2005) * Livestock nutrition Aro et al. (2009) * Medicinal plant Aweto and Iyanda (2003) * Fallow species Borokini (2011) * Threat to biodiversity conservation Egbe and Oladokun (1987) * Threat to agriculture Ekeleme et al. (2004) * Fallow species/improve soil fertility Ekhator et al. (2013) * Threat to agriculture Ekpa (1996) * Medicinal plant Etejere (1980) * Agricultural weed Etejere (1982) * - Etejere (1983) * - Etuk (1973) * - Eze and Gill (1992) * - Fadiyimu et al. (2005) * Livestock nutrition Fasuyi et al. (2006) * - Gill et al. (1996) * Weed of plantation crops Hoevers and M’boob (1996) * Threat to biodiversity and agriculture Igboh et al. (2009) * Medicinal plant/livestock nutrition Ige et al. (2008) * Agricultural weed Iheagwam (1983) * - Ikuenobe (1992) * Weed of plantation and arable crops Ikuenobe and Anoliefo (2003) * Fallow species/improve soil fertility Ikuenobe and Ayeni (1998) * Weed of plantation and arable crops Ilondu (2011) * Fungicide Ilori et al. (2011) * Manure Ivens (1972) * Threat to agriculture Ivens (1973) * - Ivens (1974) * - Ivens (1975) * - Iwu (1993) * Medicinal plant Jibril and yahaya (2010) * Improvement of soil fertility Komolafe (1980) * Threat to agriculture Komolafe (1976) * - Lucas (1989) * - Nwokolo (1987) * Livestock nutition Obatolu and Agboola (1993) * Improvement of soil fertility Odeyemi (1981) * Biogas Odeyemi et al. (2011) * Nematicide Odugbemi (2006) * Medicinal plant Odugbemi et al. (2007) * -

379 O.O. Uyi et al.

Table 1 (continued).

References Weed Beneficial Author’s submissions Odukwe (1965) * Weed of agriculture and forestry Ogbe et al. 1994 * Weed: allelopathic effect Ogundola and Liasu (2007) * - Oigiangbe et al. (2007) * Host of important pests of crops Okeke and Omaliku (1992) * Soil fertility Okigba et al. (2010) * Fungicide Olaniyi et al. (2009) * Improvement of soil fertility Olaoye (1986) * Threat to agriculture and forestry Olaoye (1977) * - Olaoye (1976) * Improvement of soil fertility Olaoye and Egunjobi (1974) * Threat to agriculture and forestry Onwugbuta-Enyi (2001) * Allelopathic effects on crops Otoikhian and Oyefa (2010) * Medicinal plant Owolabi et al. (2010) * Medicinal plant/essential oil Riddock et al. (1991) * Weed: prevent tree seedling growing Sheldrick (1968a) * Weed of plantation crops Smith and Alli (2005) * Threat to agriculture Taiwo et al. (2000) * Medicinal plant Tian et al. (2005) * Fallow plant Tian et al. (1998) * Fallow plant Utulu (1996) * Weed of plantation crops Uyi and Igbinosa (2013) * Threat to biodiversity and agriculture Uyi et al. (2013) * - Uyi (2011) * Threat to biodiversity and agriculture Uyi et al. (2011) * Threat to biodiversity and livelihoods Uyi and Aisagbonhi (2009) * Threat to agriculture Uyi et al. (2008) * - Yeni et al. (2010) * Fungicide Total 45 41 Percent 52.32 47.68

from the importation of contaminated seeds of movement of people, troops and military hardware the forest tree Gmelina arborea Roxb., 1814 during and after the war. Disturbed soil in forest (Verbenaceae) from Sri Lanka in 1937 (Ivens 1974). clearing provides an ideal habitat for the plant Following its introduction, the weed quickly and the construction of new roads in the country spread through eastern Nigeria in the 1940s and through the rainforest zones appears to have greatly was first reported by Ivens (1974) to the west of influenced the distribution of the weed at the the river Niger in 1955 and from Lagos and its early stages of invasion. environs in 1960 (Odukwe 1965) from where it The introduction of C. odorata into Nigeria might have spread into Benin Republic and other instigated many local names tied to historical events countries in West Africa. By 1960, C. odorata at the time of its occurrence among the locals. had occupied the south-eastern states of Nigeria, For example, the inhabitants of mid-western from where it spread into Cameroon (Hoevers Nigeria called it “Awolowo” apparently after and M’boob 1996). Its rapid spread through the Chief Obafemi Awolowo, the mercurial politician entire southeast in the 1940s to reach the southwest of the 1950-60s who conducted his electioneering of the country in the 1950s may have been as a campaigns with helicopter flights into the remotest result of regional trade, and human and vehicular villages in Nigeria, a period which coincided movement especially by the colonial administration with the spread of C. odorata weed in the mid- and local politicians at the time. The civil war in western region. Other areas of the country have Nigeria between the late 1960s and early 1970s different names for it based on other happenstance may have also facilitated the spread of C. odorata that coincided with its appearance or mode of from the south-eastern region because of the spread. For example, in Warri area of the Niger

380 Seven decades of Chromolaena odorata invasion in Nigeria

Figure 1. Distribution and infestation levels of Chromolaena odorata in Nigeria.

Delta, it is called “Ogbeko” or “Shell-copy” (the many climatic zones (Timbilla and Braimah 1996; latter literally a corruption of Shell Petroleum Goodall and Erasmus 1996; Robertson et al. 2008). Development Company (SPDC) whose oil The results of the surveys conducted between prospecting activities in the Niger Delta Region 2003 and 2013 in the different regions of Nigeria coincided with the appearance of the weed). To indicate that C. odorata is now present in all the west, the weed is referred to by other names parts of Nigeria, except in the northeast and far such as “Akintola” or “Awolowo”. In eastern north (Figure 1) where the prevailing climatic Nigeria, it is called several names among which conditions are probably not suitable for its growth are “Obialofulu” and “Queen Elizabeth” indicating and establishment. Infestations of C. odorata that the spread of weed might have been widely were rated in three categories viz; (i) high, (ii) noticeable during the period of the queen’s visit medium and (iii) low (Figure 1). In category one to Nigeria in 1956. There is no known local name infestation, C. odorata was present and abundant for it in the Hausa language which probably is in all places suitable for its growth, completely due to its absence in the drier climes of northern smothering co-occurring vegetation, while in Nigeria which is predominantly populated by the categories two and three infestations, the weed Hausas. was less invasive. Infestations of the weed were Overall, the invasive success of C. odorata is observed in cocoa, rubber, oil palm and coconut thought to depend upon the combination of its plantations, arable crop farms (including ), high reproductive capacity, high growth rate and nursery gardens, secondary forests, forest margins, net assimilation rate (Ramakrishnan and Vitousek wastelands, abandoned plots, road sides and other 1999), its capacity to suppress native vegetation land use types. through light competition (Kushwaha et al. 1981; These surveys showed that the entire south- Honu and Dang 2000), its allelopathic properties eastern, south-western, Niger Delta and parts of (Gills et al. 1996; Onwugbuta-Enyi 2001) as well north-central regions have been colonized by as its ability to grow on many soil types and in C. odorata (Figure 1) and that the weed has

381 O.O. Uyi et al. successfully spread to over 23 states of the 36 and cocoa plantations in southern Nigeria. The states in Nigeria, and is present in a wide range fires may prevent the recruitment of native plant of vegetation zones including rainforest and species, leading to changes in the structure and fresh water swamp forest in the south (annual composition of native flora. For example, te rainfall > 1600 mm) and woodland and grassland Beest et al. (2012) showed how fire interacted savannah zones in the north central (where annual with the conventional clearing of C. odorata in rainfall ranges between 900 and 1600 mm). South Africa and induced an intense canopy fire Figure 2 shows the vegetation zones of Nigeria that caused a shift from woodland to grassland. with total annual rainfall. The rainforest, Also McFadyen (2004) reported considerable woodland savannah and fresh water swamp forest damage to surrounding native vegetation due to zones are particularly vulnerable and severely fire caused by dry stems of C. odorata. affected, with C. odorata achieving invasive Although the arrival and continuous spread of status. Chromolaena odorata is now present in the C. odorata is thought to pose a serious threat to guinea (woodland, grassland and tall grass) subsistence and commercial agriculture in Nigeria savannah states of Nasarawa, Benue, Kebbi, (Sheldrick 1968; Lucas 1989; and several Kwara, Kogi, Plateau, Niger, Taraba and the references in Table 1), very little has been done Federal Capital Territory in Abuja where it had to elucidate its full impact on agricultural crops not previously been reported. However, the (subsistence or commercial). Future research density of C. odorata infestations varies in these work should be carried out to support or refute locations, ranging from medium to low (Figure speculations regarding the negative impact of the 1). The situation today is dissimilar to that weed so as to guide stakeholder’s decisions when reported in the 1980s by Lucas (1989), in that the considering control measures against the weed. As weed has now spread to large parts of the north- with other invasive weed species elsewhere, C. central region and parts of the northwest in odorata is thought to be a problem in young tree Kebbi State. McFadyen (1989) predicted that the crop plantations (e.g. rubber, oil palm, cocoa and minimum annual rainfall requirement for fruit trees), cassava, yam, banana, plantain and C. odorata was 1200 mm, but a considerable other important agricultural crops in southern lower limit has been recorded in Chad, Ghana and central parts of the country. and South Africa (Goodall and Erasmus 1996; The problem of C. odorata in rubber, cocoa, Timbilla 1998; Kriticos et al. 2005). Because of coconut and oil palm plantations is pronounced the vast land area of the woodland and grassland in the early stages of crop establishment, where savannah zones in Nigeria, it is believed that its invasion can lead to the shading and smothering C. odorata is yet to achieve its maximum spread of young crops. Sheldrick (1968) reported that potential in the country. The weed range will severe infestation of oil palm plantations in the probably increase further with change in climate early stage of growth by C. odorata have been if rainfall increases in the savannah zone. found to delay fruiting in oil palms for two years. In arable crops, the yield of maize has been The problems of Chromolaena odorata in Nigeria found to be reduced by C. odorata infestations by as much as 17% while that of cassava was In Nigeria and most parts of West Africa, reduced by as much as 60–70% (Lucas 1989). C. odorata impacts on farming, pastoral agri- Cassava is the most widely grown staple crop in culture, and biodiversity and on human welfare. Nigeria (FAO 2000) providing the main staple Chromolaena odorata can easily invade open for most Nigerians especially the resource poor spaces and heavily disturbed environments such farmers and rural populations. Some local farmers as croplands and neglected pastures, forest margins interviewed during our survey are of the opinion and disturbed rainforests. It competes effectively that the invasiveness of the weed in rural areas with crops and other plant species and may become especially in cassava farms is thought to cause dominant, thus causing loss of ecosystem integrity. serious apprehension about food and livelihood Die-back of after flowering presents a fire security. Chromolaena odorata is thought to impacts risk during the intense dry season, causing extensive on crop establishment through competition and/or and frequent bushfires in southern Nigeria (Uyi its allelopathic effects (Gill et al. 1996; Onwugbuta- and Igbinosa 2013). These bushfires impact Enyi 2001). For example, Ogbe et al. (1994) negatively on human livelihoods and destroy reported a strong inhibiting effect of the leaf cultivated crops (e.g. cassava, yam, cocoyam, maize, extracts of C. odorata on the growth of maize ) and have resulted in the loss of plantain seedlings. The most important effect of the weed

382 Seven decades of Chromolaena odorata invasion in Nigeria

Figure 2. Vegetation types in Nigeria that are infested or have the potential to become infested by Chromolaena odorata. The total annual rainfall ranges in the different vegetation zones are shown on the map.

on crop production is probably its high cost of eggs from predators and parasitoids (Boppré control, especially on small holdings. In Ghana 1991) leading to increased fitness and population for example, management of C. odorata in young density of this polyphagous pest of crops (including infested plantation crops is known to contribute cassava). about a third of the cost of production (Timbilla In terms of the weed’s impact on biodiversity et al. 2003). It has been observed that farmers in in Nigeria, we did not fin