Sustainable management based on biological control and ecological restoration of an alien invasive weed, adenophora () in China

F. Zhang,1 W.-X. Liu,2 F.-H. Wan2 and C.A. Ellison3

Summary Crofton weed, (Sprengel) R. King and H. Robinson, originally from Central America, was introduced into China in the 1940s. The weed spreads rapidly and is seriously damag- ing grasslands and hindering livestock production in southwestern China. To tackle the weed problem and allow the sustainable use of pastures, an integrated strategy, based on biological control and habitat restoration, is being explored. In 1983, a gall utilis Stone, originating from Mexico, was introduced from Tibet into Yunnan Province for the control of crofton weed. The current efficacy of this agent was investigated, but no significant control effect was found due to more than 60% parasitism by native parasitoids. Surveys were undertaken to identify any indigenous fungal pathogens infecting the weed. At least six strains of Alternaria alternata (Fr.) Keissler and a Pestalotiopsis sp. were isolated from . One strain of Alt. alternata was selected for further study as a prospective mycoherbicide. Field trials on ecological restoration using competitive native and forages showed that A. adenophora was less interspecifically competitive thanSetaria sphacelata (Schum.) Stapf. ex Massey cv. Narok.

Keywords: crofton weed, natural enemies, competitive weed replacement, IPM.

Introduction adenophora is still continuing to spread with an aver- age expansion rate of 20 km/year throughout the south The crofton weed Ageratina adenophora (Sprengel) and middle subtropical zones, and 6.8 km/year in north R. King and H. Robinson (Asteraceae) (Synonym subtropical areas (Wang and Wang, 2006). It has in- adenophorum) from Central America was vaded meadow, forest and wetland, forming single introduced into China in the 1940s. The weed has dis- dominant communities over a short period of time and tributed rapidly and is seriously damaging grasslands thus has caused the decline and disappearance of the and livestock production in the southwestern China original community. It releases allelopathic sub- provinces of Yunnan, Guizhou, Sichuan, Guangxi and stances into the soil, via the roots, which can inhibit Tibet (Xiang, 1991; Qiang, 1998). Its successful inva- seed germination of neighbouring plant species (Tripa- sion can be attributed to its strong adaptability, com- thi et al., 1981; Baruah et al., 1994; Zheng and Feng, petitive ability in new invaded areas, abundant seed 2005). However, allelopathic effects on susceptible production and paucity of natural enemies, compared plants, such as Chromolaena odorata (L.) R.M. King with its native range (Qiang, 1998; Wang, 2005). A. and H. Robinson, Bidens pilosa L., conyzoi- des L. and Gynura sp., were not significant at the seed- ling stage of A. adenophora in shaded plots (Wang and 1 CABI South-East and Eastern Asia – China, 12 Zhongguancun Nanda- jie, Beijing 100081, China. Feng, 2006). This weed also exhausts arable soil fertility 2 Center for Management of Invasive Alien Species, Ministry of Agricul- due to its strong absorption of soil nutrients (Liu et al., ture, Institute of Plant Protection, Chinese Academy Agricultural Sci- 1989). Moreover, A. adenophora threatens the health ences, Beijing 100094, China. of livestock as the branches and leaves are poisonous 3 CABI Europe – Bakeham Lane, Egham, Surrey TW20 9TY, UK. Corresponding author: C. Ellison . to domestic , particularly horses (O’Sullivan, © CAB International 2008 1979; Kaushal et al., 2001; Wang, 2005).

699 XII International Symposium on Biological Control of Weeds

A. adenophora has become one of the worst invasive However, the dispersal of the gall fly has been lag- alien species (IAS) in China. In 2003, A. adenophora ging behind the spread of A. adenophora (Li et al., was one of 15 IAS listed in the ‘White Paper of Pri- 2006). In addition, the overall impact on the weed in mary IAS’, released by State Environmental Protection the field has been disappointing, and a number of con- Administration of China. Enormous efforts have been tributory factors have been investigated. made by Central Government (through the Ministry of • P. utilis shows highly selective oviposition behav- Agriculture) and local government, to control and/or iour, leading to a restricted population size in the eliminate A. adenophora in newly invaded areas, and field. The gall fly will only oviposit on the stem apex, control methods have been relying on chemical herbi- showing a preference for younger plant branches. cides and mechanical removal. However, A. adenophora This results in a reduction in eggs laid during the continues to spread, expanding its range principally to- flowering season of the plant, when only less opti- ward the vast area of southern and southcentral China mal oviposition sites are available (Wei et al., 1989; (Wang and Wang, 2006). This paper summarizes a Li et al., 2006). sustainable management approach, based on biologi- • Li et al. (2006) argued that P. utilis had no signifi- cal control and ecological restoration, currently being cant effects on the number of blossom branches, ca- developed for crofton weed in China. pitula and seeds produced by A. adenophora, which indicated limited impact on reproduction and spread Sustainable management measures of the weed. for Ageratina adenophora • Significant differences were found by Li et al. (2006) in the infestation rates based on individual Classical biological control with a gall fly, plants (71.7%) and plant branches (17.3%). Since Procecidochares utilis Stone A. adenophora produces a mean of 21 branches per plant, this suggests that P. utilis is unlikely to have a Procecidochares utilis, originating from Mexico, is significant impact on the whole weed population. a gall fly that forms galls in the stem ofA. adenophora. • Recent field surveys have also revealed thatP. utilis It lays eggs on the stem apex and on hatching the lar- is parasitized by indigenous parasitoids; Torymoi- vae tunnel into the stem. In response to larvae pres- des kiesenzuetteri (Mayr), Eupelmus urozonus Dal- ence, a gall forms in the stem, which may contain from man, Bracon sp., Eurytoma spp., Sphegigaster spp. 1 to 23 larvae (Bennett and Van Staden, 1986). Galls and Pteromalus spp., which might also explain its have been shown to cause severe stunting, a reduction lower-than-anticipated control effect. B.P. Li (2006, in flowering and seed set and may result in ultimate personal communication) observed heavy parasit- death of the plant when they occurred in large num- ism of more than 60% in the field. bers (Bennett and Van Staden, 1986). In 1984, P. utilis was introduced from Nienamu county Tibet into Kun- ming, Yunnan Province, for the control of crofton weed Biological control with fungal pathogens (Wei et al., 1989). Since its introduction, field popula- Fungal pathogens of A. adenophora have been stud- tions of P. utilis have been successfully established in ied since the first report of Phaeoramularia eupatorii- the introduced areas in Yunnan, Guizhou and Sichuan odorati (Yen) Liu and Guo (= Cercospora eupatorii provinces (Dai et al., 1991; Chen and Guan, 1994; Li Peck) in in 1954 (Auld, 1969). This fungus et al., 2006; Wang et al., 2006). The gall fly is multi- was accidentally introduced, probably carried by P. voltine with the number of generations varying across utilis adult when they were introduced from Ha- the weed’s invaded range in China (four in Kunming, waii. This -spot fungus is widespread and is respon- Yunnan Province; five in southwest Guizhou Prov- sible for significant premature leaf abscission, and is ince; and six generations in the warmer lowlands of particularly prevalent in cleared areas. It is believed Sichuan). that the impact of the weed in Australia is consider- A field study in 1990–1994 showed that infestation ably lessened by the pathogen (R.E. McFadyen, 2007, rate of P. utilis in the released area was approximately personal communication). It was released in South Af- 10–37% on average, but could reach up to 85–96%. The rica in 1987, but although it has established, its impact average annual dispersal rate of P. utilis was 20–25 km on weed populations is minimal (Julien and Griffiths, (max. 40 km) from original release sites, facilitated by 1998). the southwest monsoon (Chen and Guan, 1994). Infected In Yunnan province, P. eupatorii-odorati is a com- plants had a significantly decreased number, mon disease of A. adenophora and reaches epidemic as well as seed weight, size and percentage germina- levels during June and July. It causes reductions in the tion (Wang et al., 2006). It was concluded that the gall photosynthetic rate, transpiration rate and chlorophyll fly plays an important role in suppressing population content, thus reducing plant height and number of growth of crofton weed as well as reducing its rate of leaves and (Yang and Guo, 1991; Guo et al., spread (Chen and Guan, 1994; Wang et al., 2006). 1992). In laboratory studies, the optimal temperature for

700 Sustainable management based on biological control and ecological restoration of an alien invasive weed conidia germination of P. eupatorii-odorati was 25oC ex. Massey cv. Narok, Setaria viridis (L.) Beauv. and and the optimal pH was 5.0, and, like most pathogens, Trifolium repens L. it requires free water on the plant surface to develop In a greenhouse study using plants grown in pots, infection (Guo et al., 1992). This study recommended crofton weed was shown to be less interspecifically that the ideal time, considering temperature and water competitive than S. viridis and S. sphacelata, when requirements, to release this pathogen into the area comparing their shoot height and biomass at seedling where it does not occur in Yunnan province, was July stage (Jiang, 2007). The addition of nitrogen enhanced and August. the relative competitive ability of the forage species, In China, indigenous fungal pathogens infecting which indicated that improvement of fertilization could A. adenophora, which may have potential as mycoherbi- be of additional benefit to the restoration of the pasture. cides to control the weed (Qiang, 1998), have also been Field plots studies by Jiang (2007) confirmed that the investigated. At least six strains of Alternaria alternata growth (i.e. biomass) of A. adenophora was heavily (Fr.) Keissler and a Pestalotiopsis sp. were isolated suppressed by S. sphacelata, when both species were from leaves of A. adenophora (Wan et al., 2001; W.X. planted in a mixture at different densities, but no im- Liu, unpublished data). Necrotic leaf spots on A. ade- pacts were observed on the growth of S. sphacelata. nophora leaves were observed 24 hours after treatment Compared with the biomass produced in its monocul- with a toxin extract produced by Alt. alternata, at a dos- ture plots, the biomass of A. adenophora decreased by age of 50–300 mg/ml (Dai et al., 2004). Recent work by over 70% in the mixed plots. The relative competitive Qiang et al. (2006) has found that mycelial preparations ability of S. sphacelata was still higher than that of of Alt. alternata are more effective infection propagules A. adenophora after 16 months in the field. This ap- than conidia. The assessment of the potential of these proach has been widely used and recommended in the local fungal pathogens is at the early stages of labora- invaded areas for pastures and farming. tory research and small-scale field trials. Discussion Ecological restoration by competitive replacement with native plants and Field management of A. adenophora in China has been practised extensively using chemical and mechanical forage grasses control, and hand removal. However, these methods Ecological restoration involves the re-establishment are not sustainable, result in environmental problems, of the structure and function of an ecosystem, primar- are labour-intensive and expensive, and still fail to ily to achieve a pre-disturbance state. In China, studies contain the weed. Classical biological control was have focused on restoration of both natural habitats with not effective probably due to the impact of the indig- the native flora, and pastureland with forage grasses. enous parasitoids on P. utilis. Biological control us- The selection of alternative plants has been based on a ing fungal pathogens as mycoherbicides is still at the number of factors: research stage and it is too early to say how effective they will be in the field. Recently many efforts have • A. adenophora has a strong allelopathic effect on been made on ecological restoration of invaded pas- other plants, and degrades the soil; therefore, replace- tures by native plants and forage grasses. However, ment plants need to be tolerant of the prevailing soil ecological restoration itself is also not a sole solution conditions, as well as being strongly competitive. to resolve the weed problem since it would not be fea- • Seeds of crofton weed are very sensitive to sunlight sible to restore all of the vast areas already invaded during germination and demonstrate less interspe- by the weed. cific competitive ability at the seedling stage. There- Studies on the mechanisms involved in invasion fore, the chosen alternative plants should be easy to biology have also shed light on sustainable manage- grow, with a high rate of growth, and a canopy den- ment of A. adenophora. It appears that A. adenophora sity that can reach 70% within a short period. colonizes human-altered environments (i.e. roads and • In the pasturelands of southwestern China, it is also streams) to which it is better adapted than native spe- critical to consider field application and technology cies, rather than invading undisturbed habitats and dis- dissemination within the rural communities. There- placing locally adapted native species (Sax and Brown, fore, to enhance development in rural areas, it would 2000; Lu and Ma, 2006). Its invasion success is signifi- be favourable to choose alternative plants that have cantly negatively correlated with native plant diversity, a high economic value. and reduced native species cover appears to facilitate Following these criteria, the candidate species se- the invasion. Management to control A. adenophora in lected were Brachiaria subquadripara (Trin.) Hitchc, southwest China should also focus on habitats along Cajanus cajan (L.) Mjllspaugh, Lolium perenne L., roads and streams, which provide a significant source Pennisetum clandestinum Hochst. ex. Chiov., Pennise- of seed and facilitate the spread of the weed into other tum sinese Roxb., Setaria sphacelata (Schum.) Stapf. habitats. Increasing canopy cover of native species

701 XII International Symposium on Biological Control of Weeds could help control A. adenophora invasion in these Bennett, P.H. and Van Staden, J. (1986) Gall formation in area (Lu and Ma, 2006). crofton weed, Eupatorium adenophorum Spreng. (syn. The biological control programme against mist flower, Ageratina adenophora), by the Eupatorium gall flyProce - (Regel) R. King and H. Robinson cidochares utilis Stone (Diptera: Trypetidae). Australian (Asteraceae) in Hawaii is considered one of the most Journal of Botany 34, 473–480. Buriticá, P. and Hennen, J.F. (1980) Pucciniosireae (Ure- successful undertaken anywhere in the world (Morin dinales, Pucciniaceae). Flora Neotropica Monograph 24, et al., 1997). The most important control agent for 24–25. A. riparia in Hawaii appears to be the fungus Entyloma Chen, S.B. and Guan, D.S. 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