Biological Invasions 6: 23–45, 2004. © 2004 Kluwer Academic Publishers. Printed in the Netherlands. Prospects for the management of invasive alien weeds using co-evolved fungal pathogens: a Latin American perspective Carol A. Ellison1,∗ & Robert W. Barreto2 1 CABI Bioscience UK Centre (Ascot), Silwood Park, Ascot, Berks SL5 7TA, UK; Departamento de Fitopatologia, Universidade de Viçosa, 36.570 Viçosa, MG, Brazil; ∗ Author for correspondence (e-mail: c.ellison@cabi.org; fax: +44-1491-829123) 2 Received 13 February 2002; accepted in revised form 21 May 2003 Key words: Caribbean Islands, classical biological control, fungal pathogen, Galápagos Islands, invasive alien weed, Latin America, natural weed management Abstract Invasive alien weeds pose a serious threat to the biodiversity of natural ecosystems and a significant constraint to agricultural production worldwide. The use of co-evolved natural enemies, a strategy referred to as classical biological control (CBC), has proven to be a potentially efficacious, cost-effective, and safe option for the management of alien weeds. An analysis of CBC of invasive weeds in Latin America is presented, which shows that only 5% of the worldwide releases of agents, overwhelmingly arthropod, have been in this region. Fungal pathogens are increasingly being considered in CBC programmes, and there are now 11 examples of Latin American fungi having been released as biocontrol agents in other regions of the world. In contrast, only three weed pathogens have been deliberately released in the region. Possible reasons for the paucity of CBC programmes in Latin America are presented, despite the presence of a significant number of alien weed species (60 are listed). An analysis of these weeds reveals that many of them could be amenable to control using natural enemies, including nine weed species for which CBC programmes have been successfully implemented elsewhere in the world. In addition, for many of these 60 species, a co-evolved and damaging mycobiota has already been recorded. The prospects for management of invasive alien weeds in Latin America, using co-evolved fungal pathogens, are assessed with particular reference to selected species from the genera Ambrosia, Broussonetia, Calotropis, Commelina, Cyperus, Dichrostachys, Echinochloa, Pittosporum, Rottboellia, Rubus, Sonchus and Ulex. Introduction Invasive alien species represent the greatest threat to the preservation of global biodiversity after habitat destruction, as well as imposing an increasing financial burden on agriculture (Kaiser 1999; Mack et al. 2000; Mooney 2001). Weeds form a significant part of this invasion (McWhorter and Chandler 1982; Cronk and Fuller 1995). There has been an extensive movement of plant species around the world by humans, as a consequence of trading activities. This has resulted in exotic species forming a significant part of the agricultural weed flora, and in natural ecosystems, invasive weeds are almost exclusively alien (Groves et al. 2001). Oerke et al. (1994) calculated that losses due to weeds (based on eight major crops) average almost 13% of the world’s agricultural output. Although it is difficult to translate this into actual monetary value, for Central America and the Southern Cone (Argentina, Bolivia, Brazil, Chile, Paraguay and Uruguay), in maize alone, actual losses due to weeds from 1997 to 1999 were estimated at US$1.7 billion. Without crop protection, this figure would have risen to nearly US$5.4 billion (FAO data, http://apps1.fao.org/servlet/). In natural ecosystems, it is impossible to put a price on the cost of the loss of biodiversity and the implications for society. 24 Weeds contribute to the destruction of global biodiversity by altering habitat structure via a number of different processes. For example, direct competition with the native flora can result in monocultures of an alien weed, such as by Psidium cattleianum Sabine (strawberry guava) in Mauritius. In addition, direct competition can be aided by alleopathic effect produced by the weed, such as Parthenium hysterophorus L. (white top) in Australia and India (Evans 1997). More insidious effects can also be caused, such as the alteration of the hydrology of a region, that result in a fundamental change in the type of habitat that can be supported, for example the effects of Andropogon virginicus L. (broom sedge) on tropical rainforest in Hawaii (Cronk and Fuller 1995). In the majority of agroecosystems, weeds are controlled using cultural and chemical methods (Hance and Holly 1990). However, in natural ecosystems and rangelands, such conventional control methods tend to be impractical, uneconomic, and environmentally undesirable (McFadyen 1998). Concern is now growing throughout the world about the environmental impact and toxic effects of the widespread use of chemical methods of pest control, and Latin America is no exception (Bennett 1984; FAO 1990). This concern has, in part, fuelled the current global upsurge in interest in biological control of weeds as a sustainable, environmentally benign, and potentially effective method of weed control. The Global Invasive Species Programme helps countries to catalyse action against invasive alien species by developing national and regional control and prevention strategies. Under this programme the first global best practise guidelines have been produced, and this champions classical biological control (CBC) as one of the main control strategies for invasive weeds (Wittenberg and Cock 2001). CBC targets alien weeds and is based on the enemy release hypothesis (ERH). This hypothesis assumes that plant populations, once freed of their natural enemy complexes, can expand rapidly and, therefore, become more competitive than those subject to natural control (Wilson 1969; Mitchell and Power 2003). Most introduced plant species do not become weedy once established in a new region. However, if climatic factors are favourable then there are few barriers to regulate growth, and this may result in population explosions with the subsequent development of weed invasions (Mack et al. 2000). Alien plant species are usually introduced, either deliberately or accidentally, into a new geographic area without any or most of their co-evolved natural enemies: CBC aims to redress this imbalance. Coevolved natural enemies (plant pathogens and arthropods) are collected from the centre of origin of the target weed; selecting those that appear to have the most impact on the target species. After passing a comprehensive evaluation and screening programme the best agent(s) are introduced and released in the exotic target area (FAO 1996). This approach fits well into an integrated, biologically-based approach to pest management in agroecosystems (Charudattan 2001). Increasingly, it is the only viable long-term option for the control of invasive, alien weeds in rangeland and natural environments (McFadyen 1998). CBC has been successfully employed for over a century utilising arthropods, and there have been some spectacular success stories (Julien and Griffiths 1998). For example, control of the South American aquatic plant Salvinia molesta D.S. Mitchell (water fern) in Asia, Africa, and Australasia was achieved with the weevil Cyrtobagous salviniae Calder & Sands (Thomas and Room 1986). However, the exploitation of fungal pathogens is a relatively new, but growing approach. The first release of a pathogen was made in 1972 in Australia, when the rust Puccinia chondrillina Bubak & Sydow was introduced from Europe to control Chondrilla juncea L. (skeleton weed) (Hasan and Wapshere 1973). The total estimated saving due to increased crop yields and reduced herbicide usage varies. However, the cost : benefit ratio has been put at 112 : 1 (Marsden et al. 1980). Mortensen (1986) credited this pathogen with an annual saving of over US$ 12 million, and Marsden et al. (1980) estimated a saving of AU$ 260 million, projected up to the year 2000. Since 1972, over 25 introductions of fungal pathogens to control alien weeds have been made worldwide, and a significant number of these either have been successful in reducing the impact of an exotic weed or are looking highly promising (Evans 2002). For example, the gall-forming rust fungus, Uromycladium tepperianum (Sacc.) McAlpine was introduced into South Africa from Australia to control Acacia saligna (Labill.) Wendl. (Port Jackson willow), an invasive and damaging weed of the unique Fynbos ecosystem. After an 8–10 year lag phase, the rust is now responsible for a 90–95% reduction in the weed populations and the Fynbos is now in the process of recovery (Morris 1997). The recent study by Mitchell and Power (2003) provides strong evidence in support of the ERH, specifically for plant pathogens. They found that in the 25 USA, invasive plants originating from Europe, have 77% fewer fungal and viral diseases than in their native range. This provides compelling support to the growing interest in pathogens as CBC agents, as an acceptable tool to help combat the increasing global problem of invasive weeds (Mack et al. 2000; Evans 2000). This review focuses on some existing examples of CBC, and on future prospects for extending this approach to other invasive weed species in Latin America. For the purposes of this assessment, Latin America will include the Caribbean and Galápagos Islands. CBC of weeds and Latin America: the significance of pathogens The majority of CBC implementation programmes of weeds have been in the USA, Australia, South Africa, Canada, and New Zealand. There is also an increasing number of programmes in several Asian and African countries. However, there is a dearth of examples in Latin America (Julien and Griffiths 1998). Worldwide there have been 949 recorded releases of exotic agents for the control of weeds over the last 100 years. Latin America provides only about 5% of this figure: 19 weed species have been targeted and 51 deliberate introductions of natural enemies have been made, the majority of them were arthropods. Just over half of the targeted weed species are on mainland Latin America and 43% of the releases have been made there. The exploitation of pathogens forms only a small part of this, as it does worldwide, but it is becoming increasingly considered in current and future programmes (McFadyen 1998). Pathogens have been introduced and released against four weed species in Latin America, three in Chile, and one in Argentina. These programmes are discussed below, together with one that is currently at the release stage for Costa Rica. Current status of programmes in Latin America for the CBC of weeds with pathogens Chondrilla juncea Skeleton weed is an important weed of pasture and wheat in Argentina. Following on from successful biological control programmes in Australia and USA, the rust P. chondrillina was subsequently introduced into Argentina (Deloach et al. 1989). The first strain of the rust tested in 1982 (ex Italy via USA) proved not to be pathogenic to the local biotype of the weed, since only a hypersensitive response was elicited in the target plants (Sanson and Rodriguez 1984). Subsequently, a compatible strain of the rust was imported from Italy and released in 1984. This strain became established but at very low densities. Isoenzyme analysis has since shown that the weed infestation in Argentina was likely to have been from a single introduction, as there was little genetic variation between populations (Sacco 1989). Hence, resistance of part of the weed population to the rust was unlikely to be the reason for poor establishment. It is probable that environmental conditions in Argentina do not encourage the build-up of rust epiphytotics. Galega officinalis L. (goat’s rue) Goat’s rue is an annual herbaceous plant of Eurasian origin. It was introduced into the Americas as a forage plant (Williams 1980), but developed into a serious weed of crops and pasture in many regions, including Chile. It was of some value as an ornamental, due to its showy flowers, and there are reports of its use as a medicinal plant. However, these were not considered to be significant benefits and the weed was targeted for CBC. The rust Uromyces galegae (Opiz) Saccardo, ex France, was released in Chile in 1973 and has successfully established (Oehrens and Gonzalez 1975). However, it does not reduce seed production (Norambuena and Ormeño 1991). The rust has now been recorded in Argentina (Kiehr-Delhey and Delhey 1988), but no recently published data can be found on its impact on the weed populations. Rubus spp. (blackberry) There are two weedy species of blackberry in Chile: Rubus constrictus Lef. & M. and R. ulmifolius Schott, both introduced during the second half of the 19th century. They became naturalised and spread over vast areas; by 1973 it was estimated that 5 million ha were covered by the 2 species. R. constrictus, a shrub of central European origin, is present in southern Chile growing along river banks, roadsides, and invading significant areas of arable and grazing land. R. ulmifolius has a Mediterranean centre of origin, and infests roadsides and the edge of irrigation canals in central Chile. An isolate of the rust Phragmidium violaceum (Schults) Winter was introduced into Chile from Germany in 1973 as a potential control agent of the weeds. The isolate was originally from R. sulcatus but was found to attack R. constrictus severely (Oehrens 1977). 26 Limited host range screening revealed that neither of the two commercial species of Rubus, R. idaeus L. (raspberry), and R. loganobaccus L.H. Bailey (loganberry), was susceptible to the rust (Oehrens and Gonzalez 1977). Phragmidium violaceum was released by inoculating the underside of young leaves of plants in the field. The rust established quickly and spread rapidly over the weed-infested areas (70 km after 20 months), and in less than three years the rust had covered southern Chile (from the Itata River to south of Chonchi). R. constrictus was found to be considerably more susceptible to the rust than R. ulmifolius; fortunately the former is the more troublesome of the two species. The rust hastens normal defoliation and infected stems do not lignify properly, thereby facilitating invasion by secondary, opportunistic pathogens and increasing their susceptibility to frost damage (Oehrens and Gonzalez 1977). After three seasons, the stature of infected plants was visibly reduced (2.5–1 m) and the remaining plants are now being displaced by native species, such as Cytisus monspessulanus L. and Aristotelia chilensis (Mol.) Stuntz, as weed vigour, and hence competitiveness, is reduced (Oehrens 1977). Rottboellia cochinchinensis (Lour.) W.D. Clayton (itch grass) Itch grass is an Old World annual grass, with seeds as the only means of propagation. It is a pantropical agricultural weed, but is particularly aggressive in Latin America and the Caribbean Islands where it causes serious yield reduction in both perennial and annual crops. For example, in Costa Rica crop losses of 45–64% have been recorded in maize (Rojas et al. 1993). An Afro-Asian co-evolved, host-specific head smut, Sporisorium ophiuri (P. Henn.) Vánky does not occur in the New World and thus has the potential for introduction as a CBC agent. The smut is a soilborne pathogen, infecting itch grass seedlings before they emerge from the soil via germinating teliospores. The infection is systemic, and the fungus is able to invade the flower primordia resulting in virtually no seed set. The seed heads are converted into columns of powdery black teliospores which are shed into the soil to infect the next generation of seedlings (Ellison and Evans 1995). The potential efficacy of this pathogen as a classical agent lies in the short-lived nature of the weed– seed bank (three to four years) and the aggressiveness of the smut. Pot-based experiments have shown that 80% infection of plants is consistently achievable (Ellison and Evans 1995). Small-plot field trials have demonstrated that infected plants compete equally with non-infected plants and consequently, the seed input into the seed bank is reduced in direct relation to the level of smut infection (Reeder et al. 1996). Smith et al. (1997) modelled this plant–pathogen system, and concluded that the smut, as the sole control agent, could reduce the population level of R. cochinchinensis by 90% over 20 seasons, with an annual infection rate of 85%. This high level of infection is unlikely to be achieved consistently and over an entire population. However, further modelling of the system by Smith and Holt (1996) showed that the smut could be more effective as part of an integrated pest management (IPM) system, as is practised in the weedy range of the grass. Smith et al. (2001) demonstrated that, under IPM, the smut could have a significant impact with only 50% infection of a weed population. It can be concluded that the smut offers a safe, low labour (self-perpetuating) addition to the current control measures employed by farmers in the developing world. If its full potential is reached then it may eliminate the need for other control methods. Nonetheless, it is likely to have most benefit in areas, such as fallow fields, headlands, and areas of waste ground, where weeds are generally not controlled, but can significantly contribute to the seed bank of the cultivated land. Reeder and Ellison (1999) proposed the introduction of the smut into Costa Rica following the successful completion of a DFID-UK (Department for International Development) funded, collaborative programme, between Centro Agronóminico Tropical de Investigación y Enseñanza (CATIE), Costa Rica, CABI Bioscience, UK and Natural Resources Institute, UK (Sánchez Garita 1999). The Costa Rican plant health authorities (Sanidad Vegetal) approved the introduction of the smut in December 1999 into quarantine at CATIE for additional host range screening, prior to field release. Funding is currently being sought to undertake the implementation phase of this programme. Pathogens from Latin America exploited as weed CBC agents in other regions of the world Whilst there have been relatively few introductions of weed pathogens into Latin America to date, a significant number have been exported from Latin America in an attempt to control invasive plant species in 27 Table 1. Fungal pathogens from Latin America introduced as CBC Agents in to other regions of the world.∗ Weed species and family Pathogen Origin Released Ageratina adenophora (Spreng) R.M. King and H. Robinson (Asteraceae) Phaeoramularia eupatorii-odorati (J.M. Yen) X.J. Liu and Y.L. Guo (Hyphomycetes) Entyloma ageratinae R.W. Barreto and H.C. Evans (Ustilaginales: Tilletiaceae) Mexico South Africa (1987) Mexico Colletotrichum gloeosporioides (Penz.) Sacc. f.sp. clidemiae (Coelomycete) Septoria sp. (Coelomycete) Prospodium tuberculatum (Speg.) Arthur (Uredinales: Uropyxidaceae) Colletotrichum gloeosporioides f.sp. miconiae Diabole cubensis (Arthur and J.R. Johnst.) Arthur (Uredinales: Raveneliaceae) Phloeospora mimosae-pigrae H.C. Evans and G. Carrión (Coelomycete) Puccinia abrupta Dietel and Holw. var. partheniicola (Uredinales: Pucciniaceae) Puccinia melampodii Dietel and Holw. Septoria passiflorae Louw. Panama Hawaii (1975) New Zealand (1998) South Africa (1989) Hawaii (1986) Ecuador Brazil Hawaii (1997) Australia (2001) Brazil Mexico Hawaii (1997) Australia (1996) Mexico Australia (1994) Mexico Australia (1991) Mexico Colombia Australia (1999) Hawaii (1996) Ageratina riparia (Regel) R.M. King and H. Robinson (Asteraceae) Clidemia hirta (L.) D. Don (Melastomataceae) Lantana camara L. (Verbenaceae) Lantana camara Miconia calvescens D.C. (Melastomataceae) Mimosa pigra L. (Mimosaceae) Mimosa pigra Parthenium hysterophorus L. (Asteraceae) Parthenium hysterophorus Passiflora tripartita Breit. (Passifloraceae) ∗ Updated from Evans 2002; Julien and Griffiths 1998. their exotic ranges (Table 1) (Evans 2002; Julien and Griffiths 1998). This list accounts for at least 44% of all the examples of pathogens that have been used in CBC programmes against weeds worldwide. In addition, a number of other weed–pathogen systems are currently being investigated, and some are near to the release phase of the programmes. For example, permission has been granted by the South African Quarantine Authorities to introduce the fungus, Mycovellosiella lantanae (Chupp) Deighton (ex Brazil), for the control of Lantana camara (lantana) (A. Urban, pers. comm. [2001]). In addition, in 2002 Indian Quarantine Authorities issued an import permit for the introduction, into quarantine in Delhi, of the rust Puccinia spegazzinii de Toni (ex Trinidad) for release against Mikania micrantha Kunth. ex H.B.K. (mile-a-minute weed). Analysis of the paucity of programmes in Latin America for the CBC of weeds It is clear that the developing world is lagging behind in implementing CBC of weeds, despite the obvious benefits of this cost effective and safe strategy (Auld et al. 1987; Baretto and Evans 1997; McFadyen 1998). Cock et al. (2000) discussed this issue, and concluded that donors have a poor record in providing long-term funding for CBC programmes aimed at the developing world, with the exception of South Africa. Almost all successful CBC programmes in the developing world have ‘piggy-backed’ on research undertaken for weed problems in the developed world. Research projects specifically aimed at weeds that have not yet invaded developed countries are few and poorly funded. A single failure of an agent may stop the flow of funds, despite there often being promising agents still waiting to be investigated. For example, Liothrips mikaniae (Priesner) was introduced into the Solomon Islands in 1988 and Malaysia in 1990 for CBC of mile-aminute weed but failed to establish and, consequently, funding was not continued until a new initiative with pathogens was initiated in 1996 (Cock et al. 2000). However, in Latin America, it does not appear that the paucity of programmes can solely be attributed to under-investment. An analysis of the literature would suggest an apparent low number of exotic invasive weeds in Latin America when compared with other regions of the world. Cronk and Fuller (1995) attributed this largely to, ‘the early withdrawal of Portugal and Spain and the minor involvement of Britain (by far the most active power in plant transport)’. Certainly, plant trade was significantly biased towards movement from the New to the Old World. In addition, many weed scientists believe that exotic species have failed to invade tropical Latin America because introduced species have been 28 unable to compete with the native flora (Mack et al. 2000). Indeed, intact tropical ecosystems are generally quite robust in deflecting attempts at exotic plant invasions; unfortunately intact ecosystems are on the decline. A deeper analysis, however, reveals that there has been little recognition of actual invasions, many of which occurred centuries ago. The species are now naturalised and considered to be part of the natural flora, although in reality they have replaced the endemic species. Brazil for example, is often regarded as not having spectacular examples of exotic plant invasions, where the whole landscape or ecosystem may be modified, such as has happened in Australia. However, grass species originating from Africa (e.g. Panicum maximum Jacq. (Guinea grass) and Brachiaria spp.) now dominate vast areas of Brazil. The Brazilian public and even Brazilian weed scientists appear to be unaware of the significance of this problem. These grasses, many introduced for fodder, have escaped from the grazing lands carved into the natural forests. They are now dominant in parts of South America, especially Amazonian Brazil, permanently changing the landscape and preventing regeneration of the native flora (Williams and Baruch 2000). In agricultural ecosystems, particularly arable crops, the weed flora in Latin America is less disparate than that of the rest of the world. Plant species especially adapted to flourish in disturbed habitats have been liberally distributed between continents. Sometimes this has been done intentionally, for example Cynodon dactylon (L.) Pers. (Bermuda grass) was introduced into a number of Latin American countries for fodder (Holm et al. 1977). However, more often, weed seeds have been, and continue to be, passively carried in grain shipments for breeding programmes (Huelma et al. 1996). The grass weed R. cochinchinensis, discussed above, is a prime example of this. Evaluation of potential invasive alien weed targets for CBC in Latin America Problematic weed species in Latin America can be broadly divided into two categories: alien species that have invaded natural ecosystems (Table 2), and weeds of agricultural importance, which can be either native or exotic in origin (Table 3). None of these constitutes an exhaustive list, but they do represent the range of important weed species present in this region. Alien weeds within these two categories are at various stages of invasion, from those that have only recently become invasive, and for which a distinct front can be defined, such as Commelina benghalensis (wandering Jew – a native from the Indian Subcontinent) in Brazil, to those species that have been present in this region for many decades, such as Calotropis procera (rubber bush – a native from the Old World tropics) in Brazil, and have become naturalised. Invasive plants of natural ecosystems Cronk and Fuller (1995) define an invasive plant as, ‘an alien plant spreading naturally (without the direct assistance of people) in natural or seminatural habitats, to produce a significant change in terms of composition, structure, or ecosystem processes’. There are 38 invasive species listed in Table 2, and these can be considered under the following subsections. Distribution of species Nearly a third of the species listed (12) are exclusively invading the Galápagos Archipelago, and demonstrate the vulnerability of island ecosystems to plant invasions (Mauchamp 1997). The islands of the Galápagos stand apart from the rest of Latin America and, to some extent, so do the Caribbean Islands. The flora and fauna are distinct from mainland America on the Galápagos Islands; there is 32% endemism and half of the invasive weeds listed originate from the mainland. A significant number of crop plants have also become invasive there (Tye 2001). Many of the weed species would be extremely amenable to CBC, which historically has been more successful when implemented on islands (Julien and Griffiths 1998; Wittenberg and Cock 2001). The Caribbean islands have been subjected to more intense human disturbance and traffic from mainland Latin America than the Galápagos and, consequently, the weed invasions are more similar to those that have occurred on the mainland. However, five plant species became ecosystem invaders on one (or a few) of the Caribbean Islands. These biological invasions may represent situations where CBC could again be a particularly appropriate method of control. Plants with potential economic value Graminaceous species, that have some value as fodder or as pasture grasses, represent a total of six species. Table 2. Invasive plants of natural and semi-natural ecosystems in Latin America and prospects for their classical biological control (species selection based on 1). Weed species, family, common name, and botanical detail Region invaded Origin CBC potential, notes, and references Acacia melanoxylon R.Br., (Leguminosae), Australian blackwood, tree Acacia nilotica (L.) (Leguminosae), babul, shrub/tree Acer pseudoplatanus (L.) (Aceraceae), Sycamore, tree Ailanthus altissima (Miller) Swingle, (Simaroubaceae), tree of heaven Albizia lebbeck (L.) Benth. (Leguminosae), East Indian walnut, tree Albizia procera (Roxb.) Benth. (Leguminosae), tree Anthoxanthum odoratum L. (Poaceae), sweet vernal grass, herb Broussonetia papyrifera (L.) Vent. (Moraceae), paper mulberry, tree Calotropis procera (Ait.) R. Br (Asclepiadaceae), rubber bush, calotrope, shrub Casuarina equisetifolia J.R. & G. Forst. (Casuarinaceae), common ironwood, tree Argentina Australasia Antigua, Barbuda, Anguilla, Ecuador Chile Central America, South America Venezuela, Caribbean Venezuela, Puerto Rico Chile Arabian Peninsula, Pakistan, India, Myanmar Europe China Good potential for successful CBC. Insect (ex Australia) released in South Africa in 1986, established and spreading (2, 3) Good potential for successful CBC. Insect (ex Pakistan) released in Australia in 1982, established with up to 80% seed infestation (2, 4) Ecology of insect fauna extensively studied in Europe (5) Important ornamental/amenity, timber, medicinal tree in China, where arthropod ‘pest’ species have been recorded (6) Has value as fodder, ‘pests and diseases’ identified (7) Peru China and Japan Brazil Africa, Middle East Bahamas Malesia, Australasia Cedrela odorata A. Juss. (Meliaceae), West Indian cedar, tree Cinchona succirubra Pav. ex Klotsch (Rubiaceae), red quinine tree, tree Citrus limetta Risso (Rutaceae), sweet lime, tree Cryptostegia grandiflora (Roxburgh) R. Brown, (Asclepiadaceae), rubber vine, woody climber Galápagos Central Mexico to Brazil Galápagos Mainland Ecuador Galápagos Some Members of the Lesser Antilles (Curação, Virgin Islands) Eurasia, North Africa Madagascar Digitaria decumbens Stent. (Poaceae) pangola grass, herb Eichhornia crassipes (Mart.) Solms-Laub. (Pontederiaceae), water hyacinth, free floating, perennial herb Galápagos Central America South Africa Neotropical (upper Amazon) Eugenia jambos L. (Myrtaceae), rose apple, shrub Furcraea cubensis (Jacq.) Vent (Agavaceae), Cuban hemp, shrub Hedychium coronarium (Zingiberaceae), white ginger, rhizomatous herb Galápagos Galápagos Southeast Asia Central America, South America India Brazil, Panama, Galápagos Tropical Asia Northeast Africa Eurasia Has some value as fodder. Ravenelia clemensiae Syd. (Uredinales) has been recorded attacking the tree in India (8) Has some value as fodder (1) Inner bark used to make tapa or kapa cloth and paper. Potential pathogens for CBC identified (1, a) Ornamental. Potential pathogens for CBC identified (9, a) Used for fuel wood, and shelter on sandy shores. Several insect pests have been recorded from the native range, but appear to have a relatively broad host range (10). Still has value as timber species, may be conflicts of interest (11) Not considered a significant source of quinine, worth considering for CBC (11) Crop species, may be conflicts of interest (11) Good potential for successful CBC. Originally introduced to Neotropics as potential source of rubber during second World War. Biocontrol agents from Madagascar have been released in Australia (insect in 1988, rust pathogen in 1994) and are causing extensive damage throughout range (12) Important pasture grass, hence potential conflicts of interest with CBC (13) Good potential for successful CBC. Insects (ex South America) have been released in numerous countries since 1970 with some localised success. In Honduras and Panama releases currently under evaluation. Pathogen (Cercospora piaropi Tharp) released in South Africa, others under evaluation (2, 14) Fruit has minor value (11) Minor value for fibre (11) Source of cellulose for paper manufacture, fibres for textiles, edible starch, animal feed, fungicidal properties, ornamental, aromatic flowers used in the perfume industry and medicinal value (15) 29 30 Hydrilla verticillata (L.f.) Royle (Hydrocharitaceae), hydrilla, aquatic, perennial herb Hyparrhenia rufa (Nees) Stapf (Poaceae), jaragua grass, herb Kalanchoe pinnata (Lam.) Pers. (Crassulaceae), ‘air plant’, succulent herb/shrub Lantana camara L. (Verbenaceae), lantana, white sage, tick berry, scrambling shrub Panama Venezuela Australasia, South Asia, Africa Tropical Africa Good potential for successful CBC. Insect (ex India) released in USA in 1987, impacting on plant density in many water bodies (2, 16) Important pasture grass, potential conflicts of interest with CBC (1) Galápagos Madagascar Commonly cultivated ornamental species (11) Galápagos Central and South America Leucaena leucocephala (Lam.) de Wit (Leguminosae), wild tamarind, shrub/tree West Indies South America (South to Brazil) Central America (South Mexico to Guatemala) Ligustrum lucidum Aiton (Oleaceae), glossy privet, shrub or small tree Melinis minutiflora Beauv. (Poaceae), molasses grass, perennial herb with runners Nicotiana glauca Grah. (Solanaceae), wild tobacco, shrub North Argentina China, Korea Jamaica, Venezuela Tropical Africa Mexico Panicum maximum (Jacq.) (Poaceae), Guinea grass, herb Antigua, Barbuda, Anguilla, Venezuela Northwest and Central Argentina, Paraguay and Bolivia Africa Good potential for successful CBC. Extensive CBC programmes implemented throughout exotic range since 1902, 39 agents released (ex South America), including two pathogens (see Table 1). Nine insects have had significant local impact (11, 12, 17, 18) CBC difficult to implement due to its economic importance, species still being deliberately spread. Damaging psyllid (causes defoliation) currently spreading through range (1) On-going CBC programme on other Ligustrum sp. could benefit a programme against this potential target (19) Introduced as pasture grass (although considered relatively unpalatable to certain stock species) (13) Biological control with beetle in South Africa as part of integrated control programme (1) Pennisetum purpureum Schumach. (Poaceae), elephant grass, napier grass, perennial herb Persea americana Miller (Lauraceae), avocado pear, shrub Pittosporum undulatum Vent. (Pittosporaceae), cheesewood, shrub or tree Psidium guajava L. (Myrtaceae) Guava, shrub/tree Galápagos Tropical Africa Galápagos Central America Jamaica Australia Galápagos South America Ricinus communis L. (Euphorbiaceae), castor bean, shrub Rosa rubiginosa L. (Rosaceae) sweet-briar, shrub Rubus niveus Thunb. (Rosaceae) Hill or Mysore raspberry, Shrub Scaevola plumieri L. Vahl. (Goodeniaceae), shrub Tamarindus indica L. (Leguminosae) tamarind, tree Ulex europaeus L. (Leguminosae) gorse, shrub Antigua Argentina Galápagos Tropical Africa Europe Asia Paraguay, Venezuela Antigua Brazil, Chile Australia Tropical Africa, India Europe Often regarded as the most damaging invasive weed in tropical ecosystems in Brazil, but introduced as pasture grass, hence potential conflicts of interest for CBC (13) Pasture grass, hence potential conflicts of interest for CBC. Numerous natural enemies recorded from Kenya, including potential co-evolved species (13, 20) Crop species, potential conflicts of interest for CBC Ornamental and seeds may have value for oil as a fuel. Potential pathogen for CBC identified (21, a) Crop species, but also highly invasive in agroecosystems, therefore amenable to CBC in this island situation. Destructive rust pathogen, Puccinia psidii G. Winter, present in its native range, recorded from a wide range of Myrtaceae, but species specific pathotypes identified (22) Crop species, possible conflicts of interest with CBC (1) Foliage scented, flowers medicinal (1) Potential pathogen for CBC identified (11, a) Used for stabilisation of sand dunes (1) Crop species, possible conflicts of interest with CBC (1) Good potential for successful CBC. Arthropods (ex Europe) released in Hawaii, Western USA and New Zealand (1931–1998) with significant impact. On-going programmes in Australia and Chile. Mycoherbicide programme in New Zealand (2, 23, 24, 25, 26, a) a = see Table 4; 1 = Cronk and Fuller (1995); 2 = Julien and Griffiths (1998); 3 = Dennill and Donnelly (1991); 4 = Willson (1985); 5 = Whittaker and Warrington (1985); 6 = Dong et al. (1993); 7 = Lowry et al. (1994); 8 = Mehrotra and Verma (1993); 9 = Barreto et al. (1999); 10 = Hassan (1990); 11 = Tye (2001); 12 = Anon (2002); 13 = Williams and Baruch (2000); 14 = Charudattan et al. (1996); 15 = Macedo (1997); 16 = Center et al. (1997); 17 = Broughton (2000); 18 = Thomas and Ellison (2000); 19 = R.H. Shaw, pers. comm. (2000); 20 = Farrell et al. (2002); 21 = Calvin (1985); 22 = Rayachhetry et al. (2001); 23 = Markin et al. (1996); 24 = Rees et al. (1996); 25 = Hill et al. (2000); 26 = Norambuena and Piper (2000). 31 Four of these species are particularly economically important, hence, their consideration for biological control may be problematic, despite the habitat destruction they are causing. Many of the other species listed, particularly on the Galápagos, are crop species or have other important economic uses, including: Cedrela odorata (Spanish cedar), Citrus limetta (sweet lime), Leucaena leucocephala (leucena), Persea americana (avocado), Psidium guajava (guava), Ricinus communis (caster oil bean), and Tamarindus indica (tamarind). However, they are not all significantly exploited by the local populations and in some cases are also weedy in agroecosystems (e.g. P. guajava). Consequently, their detrimental effect as weeds may outweigh any benefits and, therefore, biological control could still be appropriate. release strategies. In addition, the results of relatively costly host range screening programmes could be incorporated and adapted to local Latin American species and crop varieties, reducing the number of species that need to be screened and thus the cost. A further five species have had at least some degree of study undertaken on their potential for CBC with fungal pathogens (Table 4), and an assessment of these is given in the next section. Although some degree of successful control of U. europeaus has been achieved with arthropod agents, mainly in New Zealand and Hawaii, work has also been undertaken on the potential of pathogens and so this also included in Table 4. For the majority of the weeds listed (26 species), there is little or no information published concerning their suitability for CBC. Classical biological control CBC programmes have been successfully implemented in other parts of the world for seven of the invasive species identified: Acacia melanoxylon (Australian blackwood), Acacia nilotica (babul), Cryptostegia grandiflora (rubber vine), Eichhornia crassipes (water hyacinth), Hydrilla verticillata (hydrilla), Lantana camara (lantana), and Ulex europaeus (gorse). Arthropod agents have, in all but one of these cases (rubber vine), been cited as the control factor, although insufficient time has elapsed since release of the pathogens on water hyacinth and lantana to assess their efficacy fully. The impact of CBC on populations of rubber vine in Australia has been spectacular, and the Madagascan rust Maravalia cryptostegiae (Cummins) Y. Ono is the key agent in the suppression of this weed (Anon 2002; Evans and Tomley 1994, 1996; McFadyen and Marohasy 1990). In the above cases, it may be possible to use the results from such successful programmes to ‘fast track’ Latin American programmes. For example, L. camara has a suite of natural enemies with a proven track record that could be immediately available for implementation (Broughton 2000; see Table 2). In addition, a rust pathogen, Puccinia lantanae Farl., originally collected in Peru (Thomas and Ellison 2000), and a highly hostspecific strain of the leaf-spot pathogen Corynespora cassiicola (Berk. & Curt.) Wei, from Brazil have been identified (Pereira and Barreto 2000) that infect the only biotype of the weed thought to be present in the Galápagos Islands (Pereira et al. 2003). Many of the lessons learned could be harnessed to provide more effective selection of agents and improve Weeds of agricultural importance There are 22 species of agricultural importance listed in Table 3 (Holm et al. 1977; H.C. Evans and B.E. Valverde, pers. comm. [1999]), and these can be considered under the following subsections. Origin of species Three of the 22 species are native, three have an unknown centre of origin, one is considered to be cosmopolitan, and 15 are exotic, although many of them have become naturalised. Plants with potential economic value For 15 of the 22 species listed, some value to man has been recorded, although less than half this number can be considered to have significant value, mainly as fodder. Classical biological control CBC programmes have been implemented in other parts of the world for four of the species listed, using arthropod agents: Cyperus esculentus (yellow nutsedge), Cyperus rotundus (purple nutsedge), Ambrosia artemisiifolia (common ragweed) and Sonchus arvensis (perennial sowthistle). However, significant control, in some regions, was only achieved with the latter two species. In addition, a pathogen is near release against a further weed, Rottboellia cochinchinensis (itch grass), in Latin America (see previous section). In the same way as discussed for invasive plants of natural ecosystems, it may be 32 Table 3. Problematic weeds of agricultural importance in Latin America and prospects for their classical biological control. Weed species, family, common name, and botanical detail Regions where considered a problem (major crops affected/negative impact of the weed) Origin Benefits (actual and potential) CBC potential, notes, and references Ambrosia artemisiifolia L. (Compositae), annual ragweed, annual herb Brazil (pasture and plantation) Southern North America to Mexico None reported Axonopus compressus (Sw.) Beauv. (Poaceae), carpet grass, stoloniferous, perennial grass. Costa Rica (coffee), Venezuela (cacao), Trinidad (sugar cane) Tropical America Borreria latifolia (Aubl.) K. Schum., (Rubiaceae), broadleaf buttonweed, annual herb, perennation only by seed Brachiaria mutica (Forsk.) Stapf. (Poaceae), Pará grass, stoloniferous, perennial grass Costa Rica (coffee), Brazil (soybeans, cotton, cassava), Mexico (maize, upland rice), Trinidad (sugar cane) Jamaica, Peru and Puerto Rico, Brazil (sugar cane), Trinidad (citrus, tobacco), Colombia (oil palm), Peru (rice) Clogs irrigation canals and waterways Brazil (arable crops) Probably Neotropics Can make a good fodder grass. Used as a lawn grass in dry areas. None reported Good potential for successful CBC. Effective control in Australia with insects (ex Mexico) released in 1980 and 1984. Mycoherbicides under investigation. Pathogens identified, specificity testing required (1, 2, a) Important benefits and native, therefore CBC an unlikely option Tropical Africa Fodder Important value as fodder, therefore potential conflicts of interest with CBC (3) Africa? Not used as a pasture species in Brazil No data available on co-evolved natural enemies, but worthy of investigation into CBC potential Mexico, El Salvador, currently invading Honduras and Costa Rica (rice). — — — Brazil (soybean and annual crops), Peru (perennial crops) Old World tropics (possibly India or East Africa) Tropical Africa, or Indo-Malaysia Poor fodder Potential pathogens for CBC identified (a) Useful pasture grass, prevents soil erosion, used as a lawn and playing field grass Important benefits, therefore potential conflicts of interest with CBC Unknown Tubers eaten by humans and pigs CBC potential requires further investigation. Rust (Puccinia canaliculata) redistributed in USA, failed to establish (4) Potential pathogens for CBC identified. Insect agents released for CBC were not successful. Mycoherbicides under study (a, 4) Brachiaria plantaginea (Linck) Hitchc. (Poaceae), Alexander grass, annual grass, seed Chloris chloridea (Presl) Hitchc. (Poaceae), finger grass, underground sexual seeds (cleistogamy) and aerial seeds Commelina benghalensis L. (Commelinaceae) Wandering Jew, annual or perennial herb, seeds and stolons Cynodon dactylon (L.) Pers. (Poaceae), Bermuda grass, perennial rhizomes grass Cyperus esculentus L. (Cyperaceae), yellow nutsedge, perennial sedge, rhizomes, tubers. Argentina (sugar cane, vineyards, plantation crops) Colombia (vegetables, sugar cane), Brazil (rice, vegetables) Jamaica, Trinidad, Peru, Mexico and Puerto Rico (sugar cane), Central America (corn) Peru (sugar cane, citrus), Chile (rice) Costa Rica (sugar cane) Cyperus rotundus L. (Cyperaceae), purple nutsedge, perennial sedge, rhizomes, tubers All countries (principally annual crops especially rice, cotton, vegetables, and corn. Also sugar cane) Old World Dichrostachys cinerea (L.) Wight. and Arn. (Leguminoseae) Marabu, perennial shrub/tree Echinochloa crus-galli (L) Beauv. (Poaceae), barnyard grass, annual grass, seed Cuba (arable and pasture) NOTE: This species is also invading natural ecosystems Brazil, Chile, Argentina, Colombia, Peru, Costa Rica (rice) Can be toxic to cattle (accumulates nitrates in tissues) Africa, Asia Australia Pigs eat tubers, medicinal value (China), soil stabiliser (India); makes a poor fodder plant Ornamental Europe and India None reported Native, therefore CBC an unlikely option Potential pathogens for CBC identified (a) Potential pathogens for CBC identified. Mycoherbicides under study (a) Ischaemum rugosum Salisb. (Poaceae), wrinkled grass, annual grass, seed Panicum maximum Jacq. (Poaceae), Guinea grass, tufted perennial grass Brazil, Peru, Colombia, Guyana, Surinam, Trinidad, Costa Rica (rice and sugar cane) Cuba, Mexico, Costa Rica, Brazil (sugar cane), Costa Rica (oil palm), Colombia (corn), Ecuador (cacao) NOTE: This species is also invading natural ecosystems Tropical Asia Cattle fodder Africa Pasture, hay and silage grass Paspalum conjugatum Berg (Poaceae), sour grass, perennial, stoloniferous grass Costa Rica (coffee, oil palm), Mexico (coffee), Trinidad (sugar cane, cacao) Tropical America Poor fodder value Pennisetum clandestinum Hochst (Poaceae), Kikuyu grass, perennial, rhizomatous grass Ecuador (pasture grass), Costa Rica (row crops, tea), Colombia (irrigated crops), Peru (perennial crops) Colombia (cassava), Honduras (maize), Central America, Ecuador, Brazil, Colombia, (encroaches on grazing, poisons stock); Costa Rica (gastric cancer in humans from drinking contaminated milk) Tropical eastern Africa Pasture grass, soil binder Cosmopolitan species Aesthetic value, soil stabilisation Central and South America – still advancing in new regions (numerous annual and perennial crops, particularly maize, upland rice and sugar cane) Panama, Guyana, Puerto Rico, invading Costa Rica (forages, pasture, annual and perennial crops, e.g. rice, sugar cane, tea, coffee, rubber) India (possibly also East Africa) None recorded India Significant human value, therefore potential conflicts of interest with CBC Mediterranean Sonchus arvensis L. (Asteraceae), perennial sowthistle, perennial herb, seed Mexico, Venezuela, Argentina, Chile, Brazil, Peru, Colombia (cotton, sugarcane, maize, citrus, alfalfa, rice, vegetables, beans, sorghum). Leaves and stems can accumulate toxins in some conditions (hydrocyanic acid) Peru (vegetables), Brazil (coffee), Mexico (sunflowers), Guatemala (wheat) Cattle fodder (poor); soil mulch, roof thatching, rope and mat making (Asia); medicinal properties (Philippines); young shoots eaten (Indonesia); used in breeding programmes (believed to be an ancestor of S. officinarum [commercial sugar cane]) Cattle fodder, secondary host of crop diseases Europe May provide potential source of rubber, medicinal value (China), salad herb (Europe) Wedelia trilobata (L.) Hitchc. (Compositae), Singapore daisy Trinidad, Costa Rica, Puerto Rico, Honduras, Belize (oil palm and citrus) — — Good potential for successful CBC. Insect ex Austria released in Canada in 1981 and can reduce weed density by 50%. Damaging mycobiota recorded (12, a) — Pteridium aquilinum (L.) Kuhn (Dennstaeditiaceae), bracken, perennial, rhizomatous fern Rottboellia cochinchinensis (Lour.) W.D. Clayton (Poaceae) Itch grass, annual grass, seed Saccharum spontaneum L. (Poaceae), perennial, rhizomatous grass Sorghum halepense L. (Pers.) (Poaceae), Johnson grass, perennial, rhizomatous grass Important value as fodder, therefore potential conflicts of interest with CBC Important value as animal feed makes it a difficult target for CBC. Also, considered by many to be the most important environmental weed in Brazil, so this may outweigh its benefits (3) Native. However, pathogens recorded from outside of native range that could be investigated (5) Significant beneficial values, therefore potential conflicts of interest with CBC (3) Mycoherbicides investigated. Supports a different suite of natural enemies in different regions, but damage is rarely severe. Worthwhile investigating the potential of taking different natural enemies into Latin America that are already present elsewhere (6, 7, 8, 9) CBC programme at implementation stage (see previous section). Mycoherbicides investigated (10, 11, a) Significant value as fodder, therefore potential conflicts of interest with CBC (3) Data not available; a = see Table 4; 1 = Briere et al. (1995); 2 = McFadyen (1989); 3 = Williams and Baruch (2000); 4 = Julien and Griffiths (1998); 5 = Waterhouse (1994); 6 = Villalobos Salazar (1987); 7 = Womack et al. (1996); 8 = Rashbrook et al (1989); 9 = Holm et al. (1997); 10 = Ellison (1992); 11 = Sánchez-Garita and Zúñiga (1999); 12 = Schroeder (1973). 33 34 Table 4. Selected weeds and their co-evolved fungal pathogens which could be exploited for CBC in Latin America. Weed species Recorded pathogens in native range References Ambrosia artemisiifolia∗ Albugo tragopogonis (Pers.) Gray (Peronosporales: Albuginaceae), Erysiphe cichoracearum DC (Erysiphales: Erysiphaceae), Puccinia xanthii Schwein (Uredinales: Pucciniaceae) Batra, 1981; Hartmann and Watson 1980 Broussonetia papyrifera Aecidium mori Barclay var. broussenetia (Uredinales: Incertae sedis), Cercospora sp. (Hyphomycete), Dendryphiella broussonetiae Y.L. Guo and Z.Y. Zhang (Hyphomycete), Mycovellosiella broussonetiae Goh and W.H. Hsieh (Hyphomycete), Uredo broussonetiae Sawada (Uredinales: Incertae sedis) D. Jianqing, pers. comm. (2001); Guo and Zhang 1999; Herb. IMI Calotropis procera Ascochyta tripolitana Sacc. and Trotter (Coelomycete), Gloeosporium calotropidis Pat. and Har. (Coelomycete), Napicladium calotropidis Morstatt (Hyphomycete), Phoma calotropidis Speg. (Coelomycete) Barreto et al. 1999 Commelina benghalensis Cercospora benghalensis Chidd. Cylindrosporium kilimandscharicum Allesch. (Hyphomycete), Kordyana celebensis Gäum. (Exobasidiales: Brachybasidiaceae), Phakopsora tecta H.S. Jacks and Holw (Uredinales: Phakopsoraceae), Septoria commelinae Canonaco (Coelomycete), Uromyces commelinae Cooke (Uredinales: Pucciniaceae) Evans 1987; Waterhouse 1994 Cyperus rotundus Entyloma cyperi S. Ahmad (Ustilaginales: Entylomataceae), Phytophthora cyperi-rotundati (Pythiales: Pythiaceae) Barreto and Evans 1995; Evans 1987 Dichrostachys cinerea Phloeospora sp. (Coelomycetes), Ravenelia sp. (Uredinales: Raveneliaceae), Stigmochora sp. (Phyllachorales: Phyllachoraceae) Bagyanarayana and Ravinder 1988; H.C. Evans, pers. comm. (1998) Echinochloa crus-galli Tolyposporium bullatum J. Schröt. (Ustilaginales: Cintractiaceae), Ustilago crus-galli Tracy and Earle (Ustilaginales: Ustilaginaceae), Ustilago trichophora (Link) Kunze Waterhouse 1994 Pittosporum undulatum Phomopsis pittospori (Cooke and Harkn), Grove (Coelomycete) Herb. IMI Rottboellia cochinchinensis Puccinia rottboelliae Syd. Sporisorium ophiuri (Henn.), Vánky (Ustilaginales: Ustilaginaceae) Ellison 1993 (see previous section) Rubus niveus Phragmidium barclayi Dietel (Phragmidiaceae, Uredinales), Phragmidium himalense J.Y. Zhuang Phragmidium octoloculare Barclay, Phragmidium shogranense Petr., Pseucercospora sp. (Hyphomycete) Herb. IMI Sonchus arvensis∗ Alternaria sonchi Davis (Hyphomycete), Coleosporium sonchi (Pers.) Lév. (Uredinales: Coleosporiaceae), Puccinia suaveolens (Pers.) Rostr., Puccinia sonchi Roberge ex Desm. Uromyces sonchi Oudem. Holm et al. 1997; Herb. IMI Ulex europaeus∗ Uromyces pisi f. sp. europaei, MacDonald Septoria slaptoniensis D. Hawksw and Punith Hill et al. 2000; Herb. IMI ∗ Species with successful CBC programmes using arthropods implemented in some regions/climatic zones, and for which a rich mycobiota is also known, that could complement the current programmes. 35 possible to use the results from such successful programmes to ‘fast track’ Latin American programmes. Mycoherbicide programmes are also being developed for at least five of those listed, using indigenous fungal pathogens: annual ragweed, purple nutsedge, Echinochloa crus-gall (barnyard grass), Pteridium aquilinum (bracken), and itch grass. Thirteen species are considered to have good potential for CBC with pathogens. For seven of these, there is some information concerning their mycobiota (see Table 4) and these are discussed in the next section. Bracken is considered to have good potential for CBC, although investigations have not revealed an extensive mycobiota and, hence, arthropods are considered the most appropriate biocontrol agents (Holm et al. 1997). Indeed, a moth Conservula cinisigna de Joannis, from South Africa was fully screened for release against bracken in the UK (Fowler 1993), but a release programme was never undertaken due to lack of governmental financial support. In addition, attempts have been made to employ mycoherbicides in the UK (Womack et al. 1996). Future prospects for CBC of alien weeds with fungal pathogens in Latin America Table 4 lists 12 alien weed species from Latin America, together with their known co-evolved fungal pathogens, that can be considered good targets for CBC using the currently available knowledge. The fungal records presented are based on searches undertaken in Herb. IMI (CABI Bioscience, Egham, UK), database searches (CAB Abstracts® , Wallingford, UK), and reviews (Evans 1987; Barreto and Evans 1995; Waterhouse 1994). However, it is unlikely that these lists are definitive, since it is clear from the results of field surveys (Barreto et al. 1995; Evans and Reeder 2001), that there is an enormous mycobiota waiting to be discovered, even on well studied plant species. There are a number of omissions of weeds from Table 4 that would appear to be good targets based on their morphology (e.g. broad-leaved), the habitat they infest (e.g. those with high humidity), their level of destruction (e.g. displaced native flora and fauna in primary habitats) and have a known centre of origin. For example, Hedychium spp. have many of these characteristics, but there is no information available concerning their mycobiota. In addition, weeds are not included that already have successful CBC programmes in place, although for some the mycobiota is well documented. However, in the short-term it is considered more profitable to implement known success stories than start from scratch with an unstudied weed–pathogen system. There are more than enough targets that need control for which nothing is known! A brief assessment of the selected targets is given below. Ambrosia artemisiifolia Common ragweed is a weed of pasture and plantations in subtropical habitats of Brazil. The centre of origin of this species is probably southern USA through to Mexico. It is, however, a major problem in crops in northeastern USA. A number of pathogens have been recorded from this species throughout its range, although specificity still remains to be established in most cases (Bohar and Vajna 1996). There is evidence that the white blister ‘rust’, Albugo tragopogonis, and the rust, Puccinia xanthii, occur as a number of formae speciales, with each pathotype infecting a related but different plant host species (Batra 1981; Hartmann and Watson 1980). However, little is known about the powdery mildew (Erysiphe cichoracearum), although host-specific races of this cosmopolitan pathogen may exist. On current evidence (H.C. Evans and M.K. Seier, unpublished data) the rust would appear to be the best candidate for initial study, since it is recorded from Mexico, where A. artemisiifolia is not a problem weed, and its range does not appear to extend down into Brazil. Broussonetia papyrifera (paper mulberry) Paper mulberry has been recorded as an invasive tree in Peru, although published data on the impact of this species is lacking. It is also a weed in Pakistan, where it has colonised waste ground forming monoculture forests, and is now invading reserves set aside to preserve the indigenous flora. There is also a health issue; much of the population is at least slightly allergic to pollen from the tree (M.J.W. Cock, pers. comm. [1998]). The potential for CBC requires evaluation, although five potentially useful pathogens have already been recorded from its native range in China and Japan. Calotropis procera This plant is a problem in the semi-arid, northeastern regions of Brazil. It was introduced at the beginning of the century, and has become a problem in pastures and roadsides, and of unique natural ecosystems, such as scrubland (‘Caatinga’) and savannah (‘Cerrado’) (Brandao 1995; Kissmann and Groth 1992). Within 36 the exotic range of rubber bush a number of pathogens have been recorded. For example, Phaeoramularia calotropidis (Ellis & Everh.) Kamal, A.S. Moses & R. Chaudhary was probably introduced into Brazil with its host; whereas the rust Puccinia obliqua Berk & M.A. Curtis is known to have a wide host range within the neotropical Asclepiadaceae, and hence its compatibility with rubber bush can be considered a predictable ‘new encounter’ (Barreto et al. 1999). However, although the rust does appear to be exerting some control in the more humid areas, none of the pathogens appear to be exerting sufficient pressure on the host to achieve adequate suppression. Fungal herbarium records and the literature suggest that the Middle East and Northeast Africa may be the best sources of exploitable co-evolved natural enemies and four potential fungal agents are listed in Table 4. Commelina benghalensis Wandering Jew is a succulent, creeping, herbaceous plant that can be either annual or perennial depending on the climatic conditions. It originates from the Old World and has only recently been recorded as a weed in cropping systems in Latin America (Kissmann 1991). It is able to grow in wet conditions, rapidly forming dense, monocultures, and smothering crop plants, and pastures (Holm et al. 1977). From herbarium records, Evans (1987) documented a relatively rich mycobiota on C. benghalensis and, hence, there would appear to be good potential for CBC. Although some of the most promising pathogens (e.g. the rusts Phakopsora tecta and Uromyces commelinae) are already present in the New World, they are restricted to certain regions, and could be redistributed. In Brazil, for example, none of the two aforementioned rusts has been found, despite 10 years of observations (R.W. Barreto, pers. obs.). The other four pathogens listed appear to be restricted to the Old World and require basic investigations concerning their specificity and damage to their host. Cyperus rotundus Purple nutsedge is considered to be one of the world’s worst weeds (Holm et al. 1977; Terry and Ritches 2001). Hence, although a difficult target for CBC, due to its effective methods of propagation and regeneration, it warrants considerable effort. The taxonomic isolation of the species from crop plants of importance also makes it an ideal target. Most of the biological control work undertaken so far has involved insect natural enemies and, although, there have been no substantial successes with CBC releases (Julien and Griffiths 1998), the early season augmentation of the moth Bactra verutana Zeller in the USA has been partially successful (Frick and Chandler 1978). Others have investigated native pathogens as potential mycoherbicides (Barreto and Evans 1995; Inglis et al. 2001; Kadir and Charudattan 2000; Dinoor et al. 1999). A more novel approach could also be investigated, using the same methods as that developed by Phatak (1992) for the control of C. esculentus in the Southern USA. The indigenous rust fungus Puccinia canaliculata (Schw.) Lagerh. is bulked up in the glasshouse on its host during the winter months, and then applied to weed populations in the field early in the season. The spores are formulated, incorporating a low dose herbicide, and sprayed on to the plants as a mycoherbicide. By applying the rust early in the season, epiphytotics are produced much earlier than would occur naturally, and the weed is rendered non-competitive. Unfortunately, the product Dr BiosedgeTM has not been released on to the commercial market, purportedly due to problems with the mass production of the rust spores. Callaway et al. (1985) considered developing, by sexual recombination, other strains of the rust virulent on both C. rotundus and C. esculentus. In addition, it may be possible to use other co-evolved pathogens listed in Table 4, in a similar manner, combining both classical and inundative biological control. Dichrostachys cinerea (marabu) This woody, leguminous shrub or small tree is believed to have an Afro-Asian native range (Mabberley 1997). In 1919 marabu was first reported as a weed in Cuba under the name Dichrostachys nutans (Pers.) Benth. (Weir 1927). Since that time is has increased its range on the island, forming impenetrable, thorny thickets (M.K. Seier, pers. comm. [1998]). It is now a major weed of agriculture, encroaching on grazing land, and also in natural ecosystems, where it is replacing the native scrub vegetation. Three pathogens have been found infecting D. cinerea in India (H.C. Evans, pers. comm. [1996]). Field observations suggest that the rust Ravenelia sp. (Bagyanarayana and Ravinder 1988) is the most promising of the three identified agents, since it attacks the growing points, inducing tissue malfunction and results in the formation of spectacular witches’ brooms. Funding is currently being sought to continue the work. 37 Echinochloa crus-galli This noxious grassy weed is pantropical in distribution. It is particularly important in rice and has been targeted for inundative biological control in Europe by Scheepens (1987) and in the Philippines by Zhang and Watson (1997). In the first case, Cochliobolus lunatus Nelson & Haasis was used to control barnyard grass in combination with a sub-lethal dose of the chemical herbicide atrazine. In the Philippines, the fungus Exserohilum monoceras (Drechsler) K.J. Leonard & Suggs is being developed as a mycoherbicide for use in rice. The potential product is composed of a mixture of pathogens, each specific to a different weed species or genus within the rice weed complex (Eusebio and Watson 2000). It should be feasible to investigate similar approaches using indigenous pathogens in Latin America. Barnyard grass is said to be native to Europe and India but very few natural enemies have been reported attacking it in this vast region, and surveys are required to establish its CBC potential (Waterhouse 1994). There are three head smut species recorded from the weed and these may be worthy of further investigation, since it is an annual grass and seeds are the only means of perennation. value in Jamaica for firewood and, consequently, a seed-feeding insect may be the best option, since this has the potential to reduce spread without impinging on the value of the wood. However, native species could be developed to fill this niche, in tandem with a concerted effort to reduce the impact of the weed by targeting a number of plant parts. In South Africa, where P. undulatum is also a problem weed, a disease has been reported causing severe destruction of plants (Goodland and Healey 1997). If it proved to be at least genus specific, it may be considered for introduction, since there are no native members of the Pittosporaceae in Jamaica. In Australia, there are some reports of habitats where cheesewood has become invasive (Mullett and Simmons 1995). This could be considered contrary to the principle that plants are rarely invasive in their native range. However, the reports discuss that the invasions tend to be in disturbed habitats that are usually distant from the native populations and, thus, support the supposition that the plant is effectively controlled by natural enemies in its natural ecological range. Data obtained from Herb. IMI suggested that only one pathogen, Phomopsis pittospori, was considered worthy of investigation. Clearly, comprehensive surveys in Australia are required. Pittosporum undulatum (cheesewood) This Australian tree species was introduced into Jamaica in 1883, and has become a serious invasive weed in the Blue Mountain forests (Healey et al. 1992). Cheesewood is still in its invasive phase and poses a serious threat to the biodiversity of the range. It is unusual in that it invades species-rich rainforest vegetation, although the damage caused by hurricane Gilbert in 1988 has accelerated the invasion. An evaluation of the impact of the tree and potential control methods has been undertaken by Healey et al. (1992). An additional study was undertaken to investigate more fully the control options (Goodland and Healey 1997). It was concluded that manual removal and application of herbicides should be employed initially. However, it was conceded, with some reservations, that CBC may be the only long-term solution to the problem. Counter arguments to CBC were presented, based mainly on a perception of limited potential efficacy of agents. It was recommended that a full assessment of a biological solution, including costs, should be made. There is little information on natural enemies of cheesewood and whether insects or pathogens should form the focus of effort. The tree does have some Rottboellia cochinchinensis CBC of this serious invasive weed using a head smut (Sporisorium ophiuri) has been discussed in detail previously. However, there is also a rust pathogen (Puccinia rottboelliae) found in many parts of Africa attacking this grass, and preliminary investigations (C.A. Ellison, unpublished data) suggest it may also be of value in Latin America. Rubus niveus (Mysore or hill raspberry) This thorny, perennial shrub is of Asiatic origin, but has become a serious weed in the Galápagos Islands. This species only arrived there in the early 1980s and is still in its invasive phase. Currently, expensive chemical control is being used, but at best this is only slowing the invasion. Recent ad hoc surveys in China found the species is attacked by a number of natural enemies, including a damaging leaf spot that induces extensive necrosis (Pseudocercospora sp.), and a stem-galling insect (H.C. Evans, pers. comm. [2000]). Mycological records (Herb. IMI) show that at least four rust species (Phragmidium spp.) have been recorded in its Himalayan range, but whether they actually constitute four distinct taxa, or are conspecific synonyms, 38 requires validation. Phragmidium violaceum (Schultz) G. Winter is proving to be successful as a CBC agent against Rubus spp. in Chile and Australia (Mahr et al. 1998; Oehrens 1977), and so the prospects would appear to be excellent for CBC of R. niveus. Sonchus arvensis This composite of Eurasian origin can reach heights of up to 1.5 m. It has been targeted for CBC in Canada and some insect species have been released (ex Austria), although they have not been generally effective (Julien and Griffiths 1998). Other insect species are under evaluation. Perennial sowthistle is a relatively recent introduction to Latin America but it is increasing in importance, particularly in Peruvian vegetable crops (S. Helfgott, pers. comm. [1996]). There are a large number of potentially exploitable co-evolved natural enemies recorded from the species in its native range, and five pathogens are listed in Table 4. A damaging and host specific rust, Puccinia suaveolens, has been investigated in Russia and appears to have good potential for biological control (Holm et al. 1997). Ulex europaeus This fast-growing, spiny shrub has an European centre of origin. It can form impenetrable thickets, reaching heights of up to 4 m, with individual plants surviving for nearly three decades. Although a highly invasive, noxious weed, some conflicts of interest were identified when this plant was targeted for biological control. In New Zealand, it has value as a source of pollen for bees, a nurse-plant for native forest regeneration on abandoned agricultural land, fodder for goats, protection against erosion, and shelter for grazing animals (Hill et al. 2000). However, analysis revealed that the economic benefits resulting from successful control, far outweighed those resulting from the uses of gorse, by a factor of more than 12 : 1. Equally, the non-economic costs (e.g. impact on native vegetation) were in favour of implementing control (Hill 1989). Consequently, insect agents have been released and go some way towards successful control. Programmes currently underway in Chile have ledon from these successes in New Zealand (Norambuena et al. 2000). The first agent Apion ulicis (Forester), released in 1976, was ineffective (Norambuena and Piper 2000), but further agents have been released (Tetranychus lintearius Dufour in 1997 and Agonopterix ulicetella (Stainton) in 1997–1998). It is too early to assess efficacy of these biocontrol agents. There are two particularly interesting pathogens that have been recorded from gorse in its native range, the rust Uromyces pisi f. sp. europaei and leaf spot Septoria slaptoniensis. Both are damaging in the field, and the former is currently under assessment in Hawaii and likely to be released soon (Hill et al. 2000). A mycoherbicide is also being developed in New Zealand using the native pathogen Fusarium tumidum Sherb. (Morin et al. 1998). Discussion and conclusions CBC is an under-exploited approach to the control of invasive alien weeds in Latin America. This approach offers a safe, sustainable, environmentally benign, practical, and economically feasible method for their management. The data presented in this review indicate that there is a significant untapped resource waiting to be exploited in the field of CBC of weeds with fungal pathogens. Unfortunately and unjustifiably, the introduction of natural enemies is still regarded with suspicion, despite the clean track record, and the growing success stories (Marohasy 1996; McFadyen 1998). Spurious arguments on the dangers of CBC, based on the disastrous consequences of introducing generalist animal predators to control a single pest species (e.g. the cane toad in Australia, the African snail, and the mongoose in Hawaii), are not relevant to the discussion (Thomas and Willis 1998). It is certainly not a case of, ‘When good bugs turn bad’ (Hamilton 2000). These cases and others were predictable outcomes and, hence, could have been avoided had those concerned with the introduction followed the stringent scientific evaluation that is required today (Thomas and Willis 1998; FAO 1996). Others, with more understandable concerns, consider the introduction of biological control agents to be unsafe inherently due to potential expansion of the host range, or ‘host shifts’. Evidence suggests that this does not occur with biological control agents that have co-evolved with their host plant species over millennia. McFadyen (1998) lists worldwide-recorded instances of damage to non-target plants by biological control agents. Of the eight examples listed (all insect) five were anticipated. For the other three, the damage was minor and short-lived. Marohasy (1996) adds more evidence to the inherent safety of using CBC agents, based on the evaluation of 600 species of arthropod agents that had been moved between geographic regions. It was 39 concluded that there were few documented examples of ‘host shifts’ and that all were, in fact, predictable behavioural responses, and not the result of a genetic change. Pathogens have been exploited only as CBC agents of weeds for three decades, in contrast to a century of arthropod exploitation. The modern screening procedures originally developed by Wapshere (1974) for arthropods, have been adhered to in the majority of pathogen releases, and are in fact now more stringent for pathogens (Evans 2002). Consequently, pathogens have an impeccable track record as CBC agents. It can be concluded that, when carried out using strict screening protocols, CBC is inherently safe (Evans 2000). This approach to weed control is, nevertheless, biologically based and hence not 100% predictable. It is ultimately the responsibility of the quarantine authorities of the importing country to undertake a risk assessment based on ‘good science’ provided by the researchers (FAO 1996). It is then possible to decide whether any risks outweigh the often-catastrophic damage that invasive weeds can cause to natural ecosystems and/or agricultural production. Indeed, insects have been released against invasive weeds in the past that also were known to attack a closely related native species. Louda et al. (1997) reported that the weevil Rhinocyllus conicus (Frölich), introduced into North America to control alien thistles on rangeland, also attacked rare native thistles. This was known prior to release but the cost–benefit analysis still allowed release (Schroeder 1980). Such cases do not help the biological control cause, and careful legislation should be in place to prevent the release of agents that cause unacceptable non-target effects. In natural ecosystems, a similar non-target effect may not be such a cause for alarm since, without the control of the weed, there may not be a habitat left to support the native species. This was the case with the release of the Madagascan rust in Australia against rubber vine (see previous section). The rust was found to cause limited infection (in the glasshouse) on a native Asclepiadaceae, which was itself at risk of extinction by the rubber vine invasion. The public and government authorities worldwide are becoming aware of the value and the need to preserve the biodiversity of ecosystems. This is being reflected by the development of international agreements, such as the Convention on Biodiversity, and supported by national legislation (http://www.biodiv.org/). An unfortunate consequence of this upsurge due to the interest in biodiversity is that exploration for classical biocontrol agents is often not being treated separately from profit-oriented bioprospection for new drugs or other compounds. Novel anti-biopiracy legislation is often full of highly conservative safeguards. Serious and unnecessary delays for important biological control projects are a consequence. A recent example is that of Psidium cattleianum (strawberry guava). A potentially effective biocontrol agent, a gall-forming wasp, was selected and comprehensively studied by a team of entomologists based at the Universidade Federal of Paraná (Curitiba: Brazil), funded by the Research Corporation of the University of Hawaii. The insect was proven to be a safe biocontrol agent for one of the worst invasive weeds in island ecosystems, and all is ready for its introduction into Hawaii. Unfortunately, it has been over two years since the proposal for the export permit was presented to the Brazilian authorities. So far, no final permit has been granted (J. H. Pedrosa-Macedo, pers. comm. 2003). Funding of future projects is jeopardised by such delays, and it is essential that an adequate system be organised based on new legislation. Special treatment for such a socially and environmentally desirable strategy of pest control as CBC is necessary, highly justifiable and a matter of survival for the discipline. Requirements for introduction of classical biocontrol agents vary among different LA countries. Protocols have yet to be fully in place in many of the countries, although Costa Rica has an effective procedure, based on the FAO Code of Conduct, that also incorporates decision making by the authorities within strict time scales (FAO 1996). It was successfully utilised for obtaining an import permit for the Rottboellia cochinchinensis (itch grass) head smut (see previous section). In such countries there are no bureaucratic burdens for classical biocontrol. In other country such as Brazil, introductions of arthropods to be used as biocontrol for other arthropods are made routinely, and the process is protracted but effective. Whether this would hold true for weed biological control agents is as yet untested. To date, the majority of CBC projects have targeted native ecosystem plant invaders on the premise that natural enemies (particularly arthropods) tend to be more effective in stable environments (Reznik 1996). However, the analysis presented in this paper, indicates that a similar number of weeds from agricultural and natural ecosystems are suitable future targets for 40 CBC. This apparent anomaly may in part be due to the often better documentation of pathogens on agricultural weed than their counterparts invading natural ecosystems, as would be expected due to the direct economic importance of these plants. Despite the bias of past and current CBC programmes that target weeds of natural ecosystems, there are several examples of CBC with pathogens being used to control alien weeds in agricultural systems (Hasan and Wapshere, 1973; Chippendale 1995; McFadyen 1998, Reeder and Ellison 1999). In developing countries, CBC may prove to be the only sustainable method of controlling exotic agricultural weed flora, although more research is required to realise the full potential of this method as part of an IPM approach in cropping situations (Altieri and Doll 1978; Labrada 1996; Smith et al. 2001). For example, even agents that provide only limited control of a weed within an annual crop can be useful in helping to control weeds in the field margins and fallow areas. Seeds from these weeds are known to contribute significantly to infestations in subsequent crops (Ellison 1993). As expected, most of the problem weeds in Latin America are exotic. Grasses (including sedges) constitute a significant proportion of the weed species. Unfortunately, these weeds are also notoriously difficult targets for CBC, due both to their habit (protected meristem and ability to outgrow infection) and evolutionary closeness to major graminaceous crops. In Julien and Griffiths (1998) there are no examples of arthropod species having been released against grass targets. Indeed, it is generally considered that arthropods do not tend to be specific to single grass species (Evans 1991). Conversely, many co-evolved pathogens have a highly restricted host range, attacking a single grass species or even a biotype. For example, Ellison (1993) found a number of fungal pathogens (Colletotrichum sp. nov., Puccinia rottboelliae and Sporisorium ophiuri) isolated from itch grass, which demonstrated intraspecies specificity. Not only that they did not attack other grass species but were only able to infect certain biotypes within the species. Thus, fungal pathogens would appear to be the most suitable natural enemies to investigate for CBC of grassy weed targets. In addition, grasses are difficult targets because most of them also have economic importance as forage. For example, many of the most troublesome species in Brazil were originally deliberately introduced from Africa as pasture grasses, and their value in this role still exists, e.g. Brachiaria spp., Panicum maximum, Melinis minutiflora, Pennisetum spp. (Kissman 1991; Williams and Baruch 2000). There is likely to be serious conflicts of interest about introducing natural enemies for their control. However, with some of these species, their threat to the native flora is increasing and consequently the benefits of control may prove to outweigh their economic value. There are examples where conflicts of interest have arisen with the control of an invasive weed. One example is that of Echium plantagineum L. which is known in Australia as Paterson’s curse to farmers and to beekeepers as Salvation Jane. Despite a High Court injunction being placed to prevent the release of biological control agents, subsequent Government inquiries found that control of the weed was in the national interest and a CBC programme was implemented (Delfosse and Cullen 1981; Bruzzese et al. 1997). In some cases it may be possible to exploit biological control without seriously affecting the economic uses of an invasive plant. In South Africa, for example, seed-boring insects were introduced from Australia, which have successfully helped to reduce the spread of a number of alien Acacia species. Many of these wattle species have value in South Africa for firewood, timber, pulp, and tannins, but it is still possible for these uses to continue since only seed production is affected (Dennill et al. 1999). As discussed earlier, there are at least nine species in Latin America for which successful CBC programmes have been implemented in other parts of the world. It would seem logical that these weeds constitute the first targets in future weed CBC programmes in this region, since costs of implementation will be low and success likely to be high. A number of the other species listed have characteristics that make them suitable targets, some with a well documented arthropod fauna and/or mycobiota and should be evaluated as the next step in future CBC programmes. There is also an increasing research effort in improving the establishment of agents and developing novel methods of exploitation, which could be utilised for these releases. With pathogens, for example, in order to achieve control of a range of biotypes of a weed, or to achieve control under different climatic conditions, a number of different strains of a pathogen can be released. Also, for agents that can be mass-produced, inundative application can be used to help accelerate their spread (Hennecke and Seier 1998). CBC can take up to 10 years for a significant impact to be observed. However, in the initial years, agents could 41 be manipulated to create ‘biotic barriers’ at the invasive front of the weed to help limit further spread. No doubt, as world travel and trade increase further plant species will accidentally be introduced into regions where they have the potential to become weed problems (Groves et al. 2001). It is imperative that the public is made aware of the risks. Many countries already restrict the movement of plant material between regions, usually due to the risk of introducing specific pests and diseases (Anon 1994). However, the potential for an introduced species to become a weed in the new environment must also be assessed (Cronk and Fuller 1995; Wittenberg and Cock 2001). Research organisations may have been responsible for the accidental spread of many weed species, often between continents (Huelma et al. 1996). Although a significant percentage of agriculturally important weeds are already ubiquitous others, for example Striga spp., are not yet present in Latin America (Parker and Riches 1993). It is thus vital that the quarantine authorities of all countries fastidiously monitor the movement of plant germplasm. Nevertheless, Charudattan (2001) concluded in the final section of his recent paper on weed biological control in modern agro-ecology that, ‘It is unimaginable, both from economic and ecological standpoints, to think that invasive weeds can be managed by regulations (exclusion and quarantine) or physical and chemical controls. Biological control, in all of its aspects, should be the centrepiece of a global strategy to tackle invasive weeds.’ Acknowledgements The authors would like to thank Dr Harry C. Evans for the significant improvements and advice offered on the manuscript. Also, we appreciated the constructive criticism, particularly on the contents, by Dr Matthew A. Thomas. 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