prospects for the management of invasive alien weeds using co
TRANSCRIPT
Biological Invasions 6: 23–45, 2004.© 2004 Kluwer Academic Publishers. Printed in the Netherlands.
Prospects for the management of invasive alien weeds usingco-evolved fungal pathogens: a Latin American perspective
Carol A. Ellison1,∗ & Robert W. Barreto2
1CABI Bioscience UK Centre (Ascot), Silwood Park, Ascot, Berks SL5 7TA, UK;2Departamento de Fitopatologia, Universidade de Vicosa, 36.570 Vicosa, MG, Brazil;∗Author for correspondence (e-mail: [email protected]; fax: +44-1491-829123)
Received 13 February 2002; accepted in revised form 21 May 2003
Key words: Caribbean Islands, classical biological control, fungal pathogen, Galapagos 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 constraintto agricultural production worldwide. The use of co-evolved natural enemies, a strategy referred to as classicalbiological control (CBC), has proven to be a potentially efficacious, cost-effective, and safe option for the manage-ment of alien weeds. An analysis of CBC of invasive weeds in Latin America is presented, which shows that only5% of the worldwide releases of agents, overwhelmingly arthropod, have been in this region. Fungal pathogensare increasingly being considered in CBC programmes, and there are now 11 examples of Latin American fungihaving been released as biocontrol agents in other regions of the world. In contrast, only three weed pathogens havebeen deliberately released in the region. Possible reasons for the paucity of CBC programmes in Latin America arepresented, despite the presence of a significant number of alien weed species (60 are listed). An analysis of theseweeds reveals that many of them could be amenable to control using natural enemies, including nine weed speciesfor which CBC programmes have been successfully implemented elsewhere in the world. In addition, for many ofthese 60 species, a co-evolved and damaging mycobiota has already been recorded. The prospects for managementof invasive alien weeds in Latin America, using co-evolved fungal pathogens, are assessed with particular referenceto 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 tothe preservation of global biodiversity after habitatdestruction, as well as imposing an increasing financialburden on agriculture (Kaiser 1999; Mack et al. 2000;Mooney 2001). Weeds form a significant part of thisinvasion (McWhorter and Chandler 1982; Cronk andFuller 1995). There has been an extensive movementof plant species around the world by humans, as aconsequence of trading activities. This has resulted inexotic species forming a significant part of the agricul-tural 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% ofthe world’s agricultural output. Although it is difficultto translate this into actual monetary value, for CentralAmerica and the Southern Cone (Argentina, Bolivia,Brazil, Chile, Paraguay and Uruguay), in maize alone,actual losses due to weeds from 1997 to 1999 were esti-mated at US$1.7 billion. Without crop protection, thisfigure would have risen to nearly US$5.4 billion (FAOdata, http://apps1.fao.org/servlet/). In natural ecosys-tems, it is impossible to put a price on the cost of theloss of biodiversity and the implications for society.
24
Weeds contribute to the destruction of global bio-diversity by altering habitat structure via a number ofdifferent processes. For example, direct competitionwith the native flora can result in monocultures of analien weed, such as by Psidium cattleianum Sabine(strawberry guava) in Mauritius. In addition, directcompetition can be aided by alleopathic effect pro-duced by the weed, such as Parthenium hysterophorusL. (white top) in Australia and India (Evans 1997).More insidious effects can also be caused, such as thealteration of the hydrology of a region, that result ina fundamental change in the type of habitat that canbe supported, for example the effects of Andropogonvirginicus L. (broom sedge) on tropical rainforest inHawaii (Cronk and Fuller 1995).
In the majority of agroecosystems, weeds are con-trolled using cultural and chemical methods (Hanceand Holly 1990). However, in natural ecosystemsand rangelands, such conventional control methodstend to be impractical, uneconomic, and environmen-tally undesirable (McFadyen 1998). Concern is nowgrowing throughout the world about the environmen-tal impact and toxic effects of the widespread use ofchemical methods of pest control, and Latin Americais no exception (Bennett 1984; FAO 1990). This con-cern has, in part, fuelled the current global upsurgein interest in biological control of weeds as a sustain-able, environmentally benign, and potentially effectivemethod of weed control. The Global Invasive SpeciesProgramme helps countries to catalyse action againstinvasive alien species by developing national andregional control and prevention strategies. Under thisprogramme the first global best practise guidelines havebeen produced, and this champions classical biologicalcontrol (CBC) as one of the main control strategies forinvasive weeds (Wittenberg and Cock 2001).
CBC targets alien weeds and is based on the enemyrelease hypothesis (ERH). This hypothesis assumesthat plant populations, once freed of their naturalenemy complexes, can expand rapidly and, therefore,become more competitive than those subject to natu-ral control (Wilson 1969; Mitchell and Power 2003).Most introduced plant species do not become weedyonce established in a new region. However, if cli-matic factors are favourable then there are few barriersto regulate growth, and this may result in populationexplosions with the subsequent development of weedinvasions (Mack et al. 2000).
Alien plant species are usually introduced, eitherdeliberately or accidentally, into a new geographic
area without any or most of their co-evolved naturalenemies: CBC aims to redress this imbalance. Co-evolved natural enemies (plant pathogens and arthro-pods) are collected from the centre of origin of thetarget weed; selecting those that appear to have themost impact on the target species. After passing acomprehensive evaluation and screening programmethe best agent(s) are introduced and released in theexotic target area (FAO 1996). This approach fits wellinto an integrated, biologically-based approach to pestmanagement in agroecosystems (Charudattan 2001).Increasingly, it is the only viable long-term option forthe control of invasive, alien weeds in rangeland andnatural environments (McFadyen 1998).
CBC has been successfully employed for over acentury utilising arthropods, and there have beensome spectacular success stories (Julien and Griffiths1998). For example, control of the South Americanaquatic plant Salvinia molesta D.S. Mitchell (waterfern) in Asia, Africa, and Australasia was achievedwith the weevil Cyrtobagous salviniae Calder & Sands(Thomas and Room 1986). However, the exploitationof fungal pathogens is a relatively new, but growingapproach. The first release of a pathogen was made in1972 in Australia, when the rust Puccinia chondrillinaBubak & Sydow was introduced from Europe to con-trol Chondrilla juncea L. (skeleton weed) (Hasan andWapshere 1973). The total estimated saving due toincreased crop yields and reduced herbicide usagevaries. However, the cost : benefit ratio has been put at112 : 1 (Marsden et al. 1980). Mortensen (1986) cred-ited this pathogen with an annual saving of over US$ 12million, and Marsden et al. (1980) estimated a savingof AU$ 260 million, projected up to the year 2000.
Since 1972, over 25 introductions of fungalpathogens to control alien weeds have been madeworldwide, and a significant number of these eitherhave been successful in reducing the impact of anexotic weed or are looking highly promising (Evans2002). For example, the gall-forming rust fungus,Uromycladium tepperianum (Sacc.) McAlpine wasintroduced into South Africa from Australia to controlAcacia saligna (Labill.) Wendl. (Port Jackson willow),an invasive and damaging weed of the unique Fynbosecosystem. After an 8–10 year lag phase, the rust is nowresponsible for a 90–95% reduction in the weed popu-lations 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, have77% fewer fungal and viral diseases than in their nativerange. This provides compelling support to the growinginterest in pathogens as CBC agents, as an acceptabletool to help combat the increasing global problem ofinvasive weeds (Mack et al. 2000; Evans 2000).
This review focuses on some existing examplesof CBC, and on future prospects for extending thisapproach to other invasive weed species in LatinAmerica. For the purposes of this assessment, LatinAmerica will include the Caribbean and GalapagosIslands.
CBC of weeds and Latin America:the significance of pathogens
The majority of CBC implementation programmes ofweeds have been in the USA, Australia, South Africa,Canada, and New Zealand. There is also an increasingnumber of programmes in several Asian and Africancountries. However, there is a dearth of examples inLatin America (Julien and Griffiths 1998). Worldwidethere have been 949 recorded releases of exotic agentsfor the control of weeds over the last 100 years. LatinAmerica provides only about 5% of this figure: 19 weedspecies have been targeted and 51 deliberate introduc-tions of natural enemies have been made, the majorityof them were arthropods. Just over half of the targetedweed species are on mainland Latin America and 43%of the releases have been made there. The exploitationof pathogens forms only a small part of this, as it doesworldwide, but it is becoming increasingly consideredin current and future programmes (McFadyen 1998).Pathogens have been introduced and released againstfour weed species in Latin America, three in Chile,and one in Argentina. These programmes are discussedbelow, together with one that is currently at the releasestage for Costa Rica.
Current status of programmes in Latin Americafor the CBC of weeds with pathogens
Chondrilla junceaSkeleton weed is an important weed of pasture andwheat in Argentina. Following on from successful bio-logical control programmes in Australia and USA, therust P. chondrillina was subsequently introduced intoArgentina (Deloach et al. 1989). The first strain of therust tested in 1982 (ex Italy via USA) proved not to
be pathogenic to the local biotype of the weed, sinceonly a hypersensitive response was elicited in the targetplants (Sanson and Rodriguez 1984). Subsequently, acompatible strain of the rust was imported from Italyand released in 1984. This strain became establishedbut at very low densities. Isoenzyme analysis has sinceshown that the weed infestation in Argentina was likelyto have been from a single introduction, as there was lit-tle genetic variation between populations (Sacco 1989).Hence, resistance of part of the weed population tothe rust was unlikely to be the reason for poor estab-lishment. It is probable that environmental conditionsin Argentina do not encourage the build-up of rustepiphytotics.
Galega officinalis L. (goat’s rue)Goat’s rue is an annual herbaceous plant of Eurasianorigin. It was introduced into the Americas as a forageplant (Williams 1980), but developed into a seriousweed of crops and pasture in many regions, includingChile. It was of some value as an ornamental, due toits showy flowers, and there are reports of its use as amedicinal plant. However, these were not consideredto be significant benefits and the weed was targeted forCBC. The rust Uromyces galegae (Opiz) Saccardo, exFrance, was released in Chile in 1973 and has success-fully established (Oehrens and Gonzalez 1975). How-ever, it does not reduce seed production (Norambuenaand Ormeno 1991). The rust has now been recordedin Argentina (Kiehr-Delhey and Delhey 1988), but norecently published data can be found on its impact onthe 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 19thcentury. They became naturalised and spread over vastareas; by 1973 it was estimated that 5 million ha werecovered by the 2 species. R. constrictus, a shrub ofcentral European origin, is present in southern Chilegrowing along river banks, roadsides, and invadingsignificant areas of arable and grazing land. R. ulmi-folius has a Mediterranean centre of origin, and infestsroadsides and the edge of irrigation canals in centralChile. An isolate of the rust Phragmidium violaceum(Schults) Winter was introduced into Chile from Ger-many in 1973 as a potential control agent of the weeds.The isolate was originally from R. sulcatus but wasfound to attack R. constrictus severely (Oehrens 1977).
26
Limited host range screening revealed that neither ofthe two commercial species of Rubus, R. idaeus L.(raspberry), and R. loganobaccus L.H. Bailey (logan-berry), was susceptible to the rust (Oehrens andGonzalez 1977).
Phragmidium violaceum was released by inoculat-ing the underside of young leaves of plants in the field.The rust established quickly and spread rapidly overthe weed-infested areas (70 km after 20 months), andin less than three years the rust had covered south-ern Chile (from the Itata River to south of Chonchi).R. constrictus was found to be considerably more sus-ceptible to the rust than R. ulmifolius; fortunately theformer is the more troublesome of the two species.The rust hastens normal defoliation and infected stemsdo not lignify properly, thereby facilitating invasionby secondary, opportunistic pathogens and increas-ing their susceptibility to frost damage (Oehrens andGonzalez 1977). After three seasons, the stature ofinfected plants was visibly reduced (2.5–1 m) andthe remaining plants are now being displaced bynative species, such as Cytisus monspessulanus L. andAristotelia chilensis (Mol.) Stuntz, as weed vigour, andhence competitiveness, is reduced (Oehrens 1977).
Rottboellia cochinchinensis (Lour.)W.D. Clayton (itch grass)Itch grass is an Old World annual grass, with seedsas the only means of propagation. It is a pantropi-cal agricultural weed, but is particularly aggressivein Latin America and the Caribbean Islands where itcauses serious yield reduction in both perennial andannual crops. For example, in Costa Rica crop lossesof 45–64% have been recorded in maize (Rojas et al.1993). An Afro-Asian co-evolved, host-specific headsmut, Sporisorium ophiuri (P. Henn.) Vanky does notoccur in the New World and thus has the potentialfor introduction as a CBC agent. The smut is a soil-borne pathogen, infecting itch grass seedlings beforethey emerge from the soil via germinating teliospores.The infection is systemic, and the fungus is able toinvade the flower primordia resulting in virtually noseed set. The seed heads are converted into columns ofpowdery black teliospores which are shed into the soilto infect the next generation of seedlings (Ellison andEvans 1995).
The potential efficacy of this pathogen as a classicalagent lies in the short-lived nature of the weed–seed bank (three to four years) and the aggressive-ness of the smut. Pot-based experiments have shown
that 80% infection of plants is consistently achievable(Ellison and Evans 1995). Small-plot field trials havedemonstrated that infected plants compete equally withnon-infected plants and consequently, the seed inputinto the seed bank is reduced in direct relation to thelevel of smut infection (Reeder et al. 1996). Smith et al.(1997) modelled this plant–pathogen system, and con-cluded that the smut, as the sole control agent, couldreduce the population level of R. cochinchinensis by90% over 20 seasons, with an annual infection rateof 85%. This high level of infection is unlikely to beachieved consistently and over an entire population.However, further modelling of the system by Smith andHolt (1996) showed that the smut could be more effec-tive 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, thesmut could have a significant impact with only 50%infection of a weed population.
It can be concluded that the smut offers a safe, lowlabour (self-perpetuating) addition to the current con-trol measures employed by farmers in the developingworld. If its full potential is reached then it may elim-inate the need for other control methods. Nonetheless,it is likely to have most benefit in areas, such as fallowfields, headlands, and areas of waste ground, whereweeds are generally not controlled, but can signifi-cantly contribute to the seed bank of the cultivated land.
Reeder and Ellison (1999) proposed the intro-duction of the smut into Costa Rica following thesuccessful completion of a DFID-UK (Departmentfor International Development) funded, collaborativeprogramme, between Centro Agronominico Tropicalde Investigacion y Ensenanza (CATIE), Costa Rica,CABI Bioscience, UK and Natural Resources Insti-tute, UK (Sanchez Garita 1999). The Costa Ricanplant health authorities (Sanidad Vegetal) approvedthe introduction of the smut in December 1999 intoquarantine at CATIE for additional host range screen-ing, prior to field release. Funding is currently beingsought to undertake the implementation phase of thisprogramme.
Pathogens from Latin America exploited asweed CBC agents in other regions of the world
Whilst there have been relatively few introductions ofweed pathogens into Latin America to date, a signifi-cant number have been exported from Latin Americain 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. Kingand H. Robinson (Asteraceae)
Phaeoramularia eupatorii-odorati(J.M. Yen) X.J. Liu and Y.L. Guo(Hyphomycetes)
Mexico South Africa (1987)
Ageratina riparia (Regel) R.M. King andH. Robinson (Asteraceae)
Entyloma ageratinae R.W. Barreto andH.C. Evans (Ustilaginales: Tilletiaceae)
Mexico Hawaii (1975)New Zealand (1998)South Africa (1989)
Clidemia hirta (L.) D. Don(Melastomataceae)
Colletotrichum gloeosporioides (Penz.)Sacc. f.sp. clidemiae (Coelomycete)
Panama Hawaii (1986)
Lantana camara L. (Verbenaceae) Septoria sp. (Coelomycete) Ecuador Hawaii (1997)Lantana camara Prospodium tuberculatum (Speg.)
Arthur (Uredinales: Uropyxidaceae)Brazil Australia (2001)
Miconia calvescens D.C. (Melastomataceae) Colletotrichum gloeosporioides f.sp. miconiae Brazil Hawaii (1997)
Mimosa pigra L. (Mimosaceae) Diabole cubensis (Arthur and J.R. Johnst.)Arthur (Uredinales: Raveneliaceae)
Mexico Australia (1996)
Mimosa pigra Phloeospora mimosae-pigrae H.C. Evansand G. Carrion (Coelomycete)
Mexico Australia (1994)
Parthenium hysterophorus L. (Asteraceae) Puccinia abrupta Dietel and Holw. var.partheniicola (Uredinales: Pucciniaceae)
Mexico Australia (1991)
Parthenium hysterophorus Puccinia melampodii Dietel and Holw. Mexico Australia (1999)Passiflora tripartita Breit. (Passifloraceae) Septoria passiflorae Louw. Colombia Hawaii (1996)∗Updated from Evans 2002; Julien and Griffiths 1998.
their exotic ranges (Table 1) (Evans 2002; Julien andGriffiths 1998). This list accounts for at least 44% ofall the examples of pathogens that have been used inCBC programmes against weeds worldwide. In addi-tion, a number of other weed–pathogen systems arecurrently being investigated, and some are near to therelease phase of the programmes. For example, permis-sion has been granted by the South African QuarantineAuthorities to introduce the fungus, Mycovellosiellalantanae (Chupp) Deighton (ex Brazil), for the controlof Lantana camara (lantana) (A. Urban, pers. comm.[2001]). In addition, in 2002 Indian Quarantine Author-ities issued an import permit for the introduction, intoquarantine in Delhi, of the rust Puccinia spegazz-inii de Toni (ex Trinidad) for release against Mikaniamicrantha Kunth. ex H.B.K. (mile-a-minute weed).
Analysis of the paucity of programmes inLatin America for the CBC of weeds
It is clear that the developing world is lagging behindin implementing CBC of weeds, despite the obvi-ous benefits of this cost effective and safe strategy(Auld et al. 1987; Baretto and Evans 1997; McFadyen1998). Cock et al. (2000) discussed this issue, andconcluded that donors have a poor record in providinglong-term funding for CBC programmes aimed at the
developing world, with the exception of South Africa.Almost all successful CBC programmes in the develop-ing world have ‘piggy-backed’ on research undertakenfor weed problems in the developed world. Researchprojects specifically aimed at weeds that have not yetinvaded 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 waitingto be investigated. For example, Liothrips mikaniae(Priesner) was introduced into the Solomon Islandsin 1988 and Malaysia in 1990 for CBC of mile-a-minute weed but failed to establish and, consequently,funding was not continued until a new initiative withpathogens was initiated in 1996 (Cock et al. 2000).However, in Latin America, it does not appear thatthe paucity of programmes can solely be attributed tounder-investment.
An analysis of the literature would suggest an appar-ent low number of exotic invasive weeds in LatinAmerica when compared with other regions of theworld. Cronk and Fuller (1995) attributed this largelyto, ‘the early withdrawal of Portugal and Spain and theminor involvement of Britain (by far the most activepower in plant transport)’. Certainly, plant trade wassignificantly biased towards movement from the Newto the Old World. In addition, many weed scientistsbelieve that exotic species have failed to invade tropicalLatin America because introduced species have been
28
unable to compete with the native flora (Mack et al.2000). Indeed, intact tropical ecosystems are gener-ally quite robust in deflecting attempts at exotic plantinvasions; unfortunately intact ecosystems are on thedecline.
A deeper analysis, however, reveals that there hasbeen little recognition of actual invasions, many ofwhich occurred centuries ago. The species are now nat-uralised and considered to be part of the natural flora,although in reality they have replaced the endemicspecies. Brazil for example, is often regarded as nothaving spectacular examples of exotic plant invasions,where the whole landscape or ecosystem may be mod-ified, such as has happened in Australia. However,grass species originating from Africa (e.g. Panicummaximum Jacq. (Guinea grass) and Brachiaria spp.)now dominate vast areas of Brazil. The Brazilian pub-lic and even Brazilian weed scientists appear to beunaware of the significance of this problem. Thesegrasses, many introduced for fodder, have escapedfrom the grazing lands carved into the natural forests.They are now dominant in parts of South America,especially Amazonian Brazil, permanently changingthe landscape and preventing regeneration of the nativeflora (Williams and Baruch 2000).
In agricultural ecosystems, particularly arable crops,the weed flora in Latin America is less disparate thanthat of the rest of the world. Plant species especiallyadapted to flourish in disturbed habitats have been liber-ally distributed between continents. Sometimes this hasbeen done intentionally, for example Cynodon dactylon(L.) Pers. (Bermuda grass) was introduced into a num-ber 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 shipmentsfor breeding programmes (Huelma et al. 1996). Thegrass weed R. cochinchinensis, discussed above, is aprime example of this.
Evaluation of potential invasive alienweed targets for CBC in Latin America
Problematic weed species in Latin America can bebroadly divided into two categories: alien species thathave invaded natural ecosystems (Table 2), and weedsof agricultural importance, which can be either nativeor exotic in origin (Table 3). None of these constitutesan exhaustive list, but they do represent the range ofimportant weed species present in this region. Alien
weeds within these two categories are at various stagesof invasion, from those that have only recently becomeinvasive, and for which a distinct front can be defined,such as Commelina benghalensis (wandering Jew – anative from the Indian Subcontinent) in Brazil, to thosespecies that have been present in this region for manydecades, such as Calotropis procera (rubber bush – anative from the Old World tropics) in Brazil, and havebecome naturalised.
Invasive plants of natural ecosystems
Cronk and Fuller (1995) define an invasive plant as,‘an alien plant spreading naturally (without the directassistance of people) in natural or seminatural habitats,to produce a significant change in terms of composi-tion, structure, or ecosystem processes’. There are 38invasive species listed in Table 2, and these can beconsidered under the following subsections.
Distribution of speciesNearly a third of the species listed (12) are exclusivelyinvading the Galapagos Archipelago, and demonstratethe vulnerability of island ecosystems to plant inva-sions (Mauchamp 1997). The islands of the Galapagosstand apart from the rest of Latin America and, tosome extent, so do the Caribbean Islands. The floraand fauna are distinct from mainland America on theGalapagos Islands; there is 32% endemism and half ofthe invasive weeds listed originate from the mainland.A significant number of crop plants have also becomeinvasive there (Tye 2001). Many of the weed specieswould be extremely amenable to CBC, which histor-ically has been more successful when implementedon islands (Julien and Griffiths 1998; Wittenberg andCock 2001). The Caribbean islands have been sub-jected to more intense human disturbance and trafficfrom mainland Latin America than the Galapagos and,consequently, the weed invasions are more similar tothose that have occurred on the mainland. However,five plant species became ecosystem invaders on one(or a few) of the Caribbean Islands. These biolog-ical invasions may represent situations where CBCcould again be a particularly appropriate method ofcontrol.
Plants with potential economic valueGraminaceous species, that have some value as fodderor as pasture grasses, represent a total of six species.
29
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sive
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iden
tified
(9,a
)
Cas
uari
naeq
uise
tifo
lia
J.R
.&G
.For
st.
(Cas
uari
nace
ae),
com
mon
iron
woo
d,tr
eeB
aham
asM
ales
ia,A
ustr
alas
iaU
sed
for
fuel
woo
d,an
dsh
elte
ron
sand
ysh
ores
.Sev
eral
inse
ctpe
sts
have
been
reco
rded
from
the
nativ
era
nge,
buta
ppea
rto
have
are
lativ
ely
broa
dho
stra
nge
(10)
.C
edre
laod
orat
aA
.Jus
s.(M
elia
ceae
),W
estI
ndia
nce
dar,
tree
Gal
apag
osC
entr
alM
exic
oto
Bra
zil
Still
has
valu
eas
timbe
rsp
ecie
s,m
aybe
confl
icts
ofin
tere
st(1
1)C
inch
ona
succ
irub
raPa
v.ex
Klo
tsch
(Rub
iace
ae),
red
quin
ine
tree
,tre
eG
alap
agos
Mai
nlan
dE
cuad
orN
otco
nsid
ered
asi
gnifi
cant
sour
ceof
quin
ine,
wor
thco
nsid
erin
gfo
rC
BC
(11)
Cit
rus
lim
etta
Ris
so(R
utac
eae)
,sw
eetl
ime,
tree
Gal
apag
osE
uras
ia,N
orth
Afr
ica
Cro
psp
ecie
s,m
aybe
confl
icts
ofin
tere
st(1
1)C
rypt
oste
gia
gran
diflo
ra(R
oxbu
rgh)
R.B
row
n,(A
scle
piad
acea
e),r
ubbe
rvi
ne,w
oody
clim
ber
Som
eM
embe
rsof
the
Les
ser
Ant
illes
(Cur
acao
,Vir
gin
Isla
nds)
Mad
agas
car
Goo
dpo
tent
ialf
orsu
cces
sful
CB
C.O
rigi
nally
intr
oduc
edto
Neo
trop
ics
aspo
tent
ials
ourc
eof
rubb
erdu
ring
seco
ndW
orld
War
.Bio
cont
rol
agen
tsfr
omM
adag
asca
rha
vebe
enre
leas
edin
Aus
tral
ia(i
nsec
tin
1988
,rus
tpat
hoge
nin
1994
)an
dar
eca
usin
gex
tens
ive
dam
age
thro
ugho
utra
nge
(12)
Dig
itar
iade
cum
bens
Sten
t.(P
oace
ae)p
ango
lagr
ass,
herb
Gal
apag
osSo
uth
Afr
ica
Impo
rtan
tpas
ture
gras
s,he
nce
pote
ntia
lcon
flict
sof
inte
rest
with
CB
C(1
3)E
ichh
orni
acr
assi
pes
(Mar
t.)So
lms-
Lau
b.(P
onte
deri
acea
e),w
ater
hyac
inth
,fr
eeflo
atin
g,pe
renn
ialh
erb
Cen
tral
Am
eric
aN
eotr
opic
al(u
pper
Am
azon
)G
ood
pote
ntia
lfor
succ
essf
ulC
BC
.Ins
ects
(ex
Sout
hA
mer
ica)
have
been
rele
ased
innu
mer
ous
coun
trie
ssi
nce
1970
with
som
elo
calis
edsu
cces
s.In
Hon
dura
san
dPa
nam
are
leas
escu
rren
tlyun
der
eval
uatio
n.Pa
thog
en(C
erco
spor
api
arop
iTha
rp)
rele
ased
inSo
uth
Afr
ica,
othe
rsun
der
eval
uatio
n(2
,14)
Eug
enia
jam
bos
L.(
Myr
tace
ae),
rose
appl
e,sh
rub
Gal
apag
osSo
uthe
astA
sia
Frui
thas
min
orva
lue
(11)
Fur
crae
acu
bens
is(J
acq.
)V
ent(
Aga
vace
ae),
Cub
anhe
mp,
shru
bG
alap
agos
Cen
tral
Am
eric
a,So
uth
Am
eric
aM
inor
valu
efo
rfib
re(1
1)
Hed
ychi
umco
rona
rium
(Zin
gibe
race
ae),
whi
tegi
nger
,rhi
zom
atou
she
rbB
razi
l,Pa
nam
a,G
alap
agos
Indi
aSo
urce
ofce
llulo
sefo
rpa
per
man
ufac
ture
,fibr
esfo
rte
xtile
s,ed
ible
star
ch,
anim
alfe
ed,f
ungi
cida
lpro
pert
ies,
orna
men
tal,
arom
atic
flow
ers
used
inth
epe
rfum
ein
dust
ryan
dm
edic
inal
valu
e(1
5)
30
Hyd
rill
ave
rtic
illa
ta(L
.f.)
Roy
le(H
ydro
char
itace
ae),
hydr
illa,
aqua
tic,p
eren
nial
herb
Pana
ma
Aus
tral
asia
,Sou
thA
sia,
Afr
ica
Goo
dpo
tent
ialf
orsu
cces
sful
CB
C.I
nsec
t(ex
Indi
a)re
leas
edin
USA
in19
87,i
mpa
ctin
gon
plan
tden
sity
inm
any
wat
erbo
dies
(2,1
6)H
ypar
rhen
iaru
fa(N
ees)
Stap
f(P
oace
ae),
jara
gua
gras
s,he
rbV
enez
uela
Tro
pica
lAfr
ica
Impo
rtan
tpas
ture
gras
s,po
tent
ialc
onfli
cts
ofin
tere
stw
ithC
BC
(1)
Kal
anch
oepi
nnat
a(L
am.)
Pers
.(C
rass
ulac
eae)
,‘a
irpl
ant’
,suc
cule
nthe
rb/s
hrub
Gal
apag
osM
adag
asca
rC
omm
only
culti
vate
dor
nam
enta
lspe
cies
(11)
Lan
tana
cam
ara
L.(
Ver
bena
ceae
),la
ntan
a,w
hite
sage
,tic
kbe
rry,
scra
mbl
ing
shru
bG
alap
agos
Cen
tral
and
Sout
hA
mer
ica
Goo
dpo
tent
ialf
orsu
cces
sful
CB
C.E
xten
sive
CB
Cpr
ogra
mm
esim
plem
ente
dth
roug
hout
exot
icra
nge
sinc
e19
02,3
9ag
ents
rele
ased
(ex
Sout
hA
mer
ica)
,inc
ludi
ngtw
opa
thog
ens
(see
Tabl
e1)
.N
ine
inse
cts
have
had
sign
ifica
ntlo
cali
mpa
ct(1
1,12
,17,
18)
Leu
caen
ale
ucoc
epha
la(L
am.)
deW
it(L
egum
inos
ae),
wild
tam
arin
d,sh
rub/
tree
Wes
tInd
ies
Sout
hA
mer
ica
(Sou
thto
Bra
zil)
Cen
tral
Am
eric
a(S
outh
Mex
ico
toG
uate
mal
a)C
BC
diffi
cult
toim
plem
entd
ueto
itsec
onom
icim
port
ance
,spe
cies
still
bein
gde
liber
atel
ysp
read
.Dam
agin
gps
yllid
(cau
ses
defo
liatio
n)cu
rren
tlysp
read
ing
thro
ugh
rang
e(1
)L
igus
trum
luci
dum
Aito
n(O
leac
eae)
,gl
ossy
priv
et,s
hrub
orsm
allt
ree
Nor
thA
rgen
tina
Chi
na,K
orea
On-
goin
gC
BC
prog
ram
me
onot
her
Lig
ustr
umsp
.cou
ldbe
nefit
apr
ogra
mm
eag
ains
tthi
spo
tent
ialt
arge
t(19
)M
elin
ism
inut
iflor
aB
eauv
.(Po
acea
e),
mol
asse
sgr
ass,
pere
nnia
lher
bw
ithru
nner
sJa
mai
ca,V
enez
uela
Tro
pica
lAfr
ica
Intr
oduc
edas
past
ure
gras
s(a
lthou
ghco
nsid
ered
rela
tivel
yun
pala
tabl
eto
cert
ain
stoc
ksp
ecie
s)(1
3)N
icot
iana
glau
caG
rah.
(Sol
anac
eae)
,w
ildto
bacc
o,sh
rub
Mex
ico
Nor
thw
esta
ndC
entr
alA
rgen
tina,
Para
guay
and
Bol
ivia
Bio
logi
calc
ontr
olw
ithbe
etle
inSo
uth
Afr
ica
aspa
rtof
inte
grat
edco
ntro
lpro
gram
me
(1)
Pani
cum
max
imum
(Jac
q.)
(Poa
ceae
),G
uine
agr
ass,
herb
Ant
igua
,Bar
buda
,A
ngui
lla,V
enez
uela
Afr
ica
Oft
enre
gard
edas
the
mos
tdam
agin
gin
vasi
vew
eed
intr
opic
alec
osys
tem
sin
Bra
zil,
buti
ntro
duce
das
past
ure
gras
s,he
nce
pote
ntia
lcon
flict
sof
inte
rest
for
CB
C(1
3)Pe
nnis
etum
purp
ureu
mSc
hum
ach.
(Poa
ceae
),el
epha
ntgr
ass,
napi
ergr
ass,
pere
nnia
lher
bG
alap
agos
Tro
pica
lAfr
ica
Past
ure
gras
s,he
nce
pote
ntia
lcon
flict
sof
inte
rest
for
CB
C.N
umer
ous
natu
ral
enem
ies
reco
rded
from
Ken
ya,i
nclu
ding
pote
ntia
lco-
evol
ved
spec
ies
(13,
20)
Pers
eaam
eric
ana
Mill
er(L
aura
ceae
),av
ocad
ope
ar,s
hrub
Gal
apag
osC
entr
alA
mer
ica
Cro
psp
ecie
s,po
tent
ialc
onfli
cts
ofin
tere
stfo
rC
BC
Pit
tosp
orum
undu
latu
mV
ent.
(Pitt
ospo
race
ae),
chee
sew
ood,
shru
bor
tree
Jam
aica
Aus
tral
iaO
rnam
enta
land
seed
sm
ayha
veva
lue
for
oila
sa
fuel
.Po
tent
ialp
atho
gen
for
CB
Cid
entifi
ed(2
1,a)
Psi
dium
guaj
ava
L.(
Myr
tace
ae)
Gua
va,s
hrub
/tree
Gal
apag
osSo
uth
Am
eric
aC
rop
spec
ies,
buta
lso
high
lyin
vasi
vein
agro
ecos
yste
ms,
ther
efor
eam
enab
leto
CB
Cin
this
isla
ndsi
tuat
ion.
Des
truc
tive
rust
path
ogen
,Puc
cini
aps
idii
G.W
inte
r,pr
esen
tin
itsna
tive
rang
e,re
cord
edfr
oma
wid
era
nge
ofM
yrta
ceae
,but
spec
ies
spec
ific
path
otyp
esid
entifi
ed(2
2)R
icin
usco
mm
unis
L.(
Eup
horb
iace
ae),
cast
orbe
an,s
hrub
Ant
igua
Tro
pica
lAfr
ica
Cro
psp
ecie
s,po
ssib
leco
nflic
tsof
inte
rest
with
CB
C(1
)R
osa
rubi
gino
saL
.(R
osac
eae)
swee
t-br
iar,
shru
bA
rgen
tina
Eur
ope
Folia
gesc
ente
d,flo
wer
sm
edic
inal
(1)
Rub
usni
veus
Thu
nb.(
Ros
acea
e)H
illor
Mys
ore
rasp
berr
y,Sh
rub
Gal
apag
osA
sia
Pote
ntia
lpat
hoge
nfo
rC
BC
iden
tified
(11,
a)
Scae
vola
plum
ieri
L.V
ahl.
(Goo
deni
acea
e),s
hrub
Para
guay
,Ven
ezue
laA
ustr
alia
Use
dfo
rst
abili
satio
nof
sand
dune
s(1
)Ta
mar
indu
sin
dica
L.(
Leg
umin
osae
)ta
mar
ind,
tree
Ant
igua
Tro
pica
lAfr
ica,
Indi
aC
rop
spec
ies,
poss
ible
confl
icts
ofin
tere
stw
ithC
BC
(1)
Ule
xeu
ropa
eus
L.(
Leg
umin
osae
)go
rse,
shru
bB
razi
l,C
hile
Eur
ope
Goo
dpo
tent
ialf
orsu
cces
sful
CB
C.A
rthr
opod
s(e
xE
urop
e)re
leas
edin
Haw
aii,
Wes
tern
USA
and
New
Zea
land
(193
1–19
98)
with
sign
ifica
ntim
pact
.On-
goin
gpr
ogra
mm
esin
Aus
tral
iaan
dC
hile
.Myc
oher
bici
depr
ogra
mm
ein
New
Zea
land
(2,2
3,24
,25,
26,a
)
a=
see
Tabl
e4;
1=
Cro
nkan
dFu
ller
(199
5);
2=
Julie
nan
dG
riffi
ths
(199
8);
3=
Den
nill
and
Don
nelly
(199
1);
4=
Will
son
(198
5);
5=
Whi
ttake
ran
dW
arri
ngto
n(1
985)
;6
=D
ong
etal
.(1
993)
;7
=L
owry
etal
.(1
994)
;8
=M
ehro
tra
and
Ver
ma
(199
3);
9=
Bar
reto
etal
.(1
999)
;10
=H
assa
n(1
990)
;11
=Ty
e(2
001)
;12
=A
non
(200
2);
13=
Will
iam
san
dB
aruc
h(2
000)
;14
=C
haru
datta
net
al.
(199
6);
15=
Mac
edo
(199
7);
16=
Cen
ter
etal
.(1
997)
;17
=B
roug
hton
(200
0);
18=
Tho
mas
and
Elli
son
(200
0);
19=
R.H
.Sh
aw,
pers
.co
mm
.(2
000)
;20
=Fa
rrel
let
al.
(200
2);
21=
Cal
vin
(198
5);
22=
Ray
achh
etry
etal
.(20
01);
23=
Mar
kin
etal
.(19
96);
24=
Ree
set
al.(
1996
);25
=H
illet
al.(
2000
);26
=N
oram
buen
aan
dPi
per
(200
0).
31
Four of these species are particularly economicallyimportant, hence, their consideration for biologicalcontrol may be problematic, despite the habitat destruc-tion they are causing. Many of the other species listed,particularly on the Galapagos, are crop species or haveother important economic uses, including: Cedrelaodorata (Spanish cedar), Citrus limetta (sweet lime),Leucaena leucocephala (leucena), Persea americana(avocado), Psidium guajava (guava), Ricinus commu-nis (caster oil bean), and Tamarindus indica (tamarind).However, they are not all significantly exploited by thelocal populations and in some cases are also weedy inagroecosystems (e.g. P. guajava). Consequently, theirdetrimental effect as weeds may outweigh any ben-efits and, therefore, biological control could still beappropriate.
Classical biological controlCBC programmes have been successfully implementedin other parts of the world for seven of the invasivespecies identified: Acacia melanoxylon (Australianblackwood), Acacia nilotica (babul), Cryptostegiagrandiflora (rubber vine), Eichhornia crassipes (waterhyacinth), Hydrilla verticillata (hydrilla), Lantanacamara (lantana), and Ulex europaeus (gorse). Arthro-pod agents have, in all but one of these cases (rubbervine), been cited as the control factor, although insuf-ficient time has elapsed since release of the pathogenson water hyacinth and lantana to assess their efficacyfully. The impact of CBC on populations of rubber vinein Australia has been spectacular, and the Madagas-can rust Maravalia cryptostegiae (Cummins) Y. Onois the key agent in the suppression of this weed (Anon2002; Evans and Tomley 1994, 1996; McFadyen andMarohasy 1990).
In the above cases, it may be possible to use theresults from such successful programmes to ‘fast track’Latin American programmes. For example, L. camarahas a suite of natural enemies with a proven track recordthat could be immediately available for implementa-tion (Broughton 2000; see Table 2). In addition, a rustpathogen, Puccinia lantanae Farl., originally collectedin Peru (Thomas and Ellison 2000), and a highly host-specific strain of the leaf-spot pathogen Corynesporacassiicola (Berk. & Curt.) Wei, from Brazil have beenidentified (Pereira and Barreto 2000) that infect theonly biotype of the weed thought to be present in theGalapagos Islands (Pereira et al. 2003).
Many of the lessons learned could be harnessed toprovide more effective selection of agents and improve
release strategies. In addition, the results of rela-tively costly host range screening programmes couldbe incorporated and adapted to local Latin Americanspecies and crop varieties, reducing the number ofspecies that need to be screened and thus the cost. Afurther five species have had at least some degree ofstudy undertaken on their potential for CBC with fungalpathogens (Table 4), and an assessment of these is givenin the next section. Although some degree of successfulcontrol of U. europeaus has been achieved with arthro-pod agents, mainly in New Zealand and Hawaii, workhas also been undertaken on the potential of pathogensand so this also included in Table 4. For the major-ity of the weeds listed (26 species), there is little orno information published concerning their suitabilityfor CBC.
Weeds of agricultural importance
There are 22 species of agricultural importance listedin Table 3 (Holm et al. 1977; H.C. Evans andB.E. Valverde, pers. comm. [1999]), and these can beconsidered under the following subsections.
Origin of speciesThree of the 22 species are native, three have anunknown centre of origin, one is considered to be cos-mopolitan, and 15 are exotic, although many of themhave become naturalised.
Plants with potential economic valueFor 15 of the 22 species listed, some value to manhas been recorded, although less than half this numbercan be considered to have significant value, mainly asfodder.
Classical biological controlCBC programmes have been implemented in otherparts of the world for four of the species listed,using arthropod agents: Cyperus esculentus (yellownutsedge), Cyperus rotundus (purple nutsedge),Ambrosia artemisiifolia (common ragweed) andSonchus arvensis (perennial sowthistle). However, sig-nificant control, in some regions, was only achievedwith the latter two species. In addition, a pathogenis near release against a further weed, Rottboelliacochinchinensis (itch grass), in Latin America (seeprevious section). In the same way as discussedfor invasive plants of natural ecosystems, it may be
32
Tabl
e3.
Prob
lem
atic
wee
dsof
agri
cultu
rali
mpo
rtan
cein
Lat
inA
mer
ica
and
pros
pect
sfo
rth
eir
clas
sica
lbio
logi
calc
ontr
ol.
Wee
dsp
ecie
s,fa
mily
,com
mon
nam
e,an
dbo
tani
cald
etai
lR
egio
nsw
here
cons
ider
eda
prob
lem
(maj
orcr
ops
affe
cted
/neg
ativ
eim
pact
ofth
ew
eed)
Ori
gin
Ben
efits
(act
uala
ndpo
tent
ial)
CB
Cpo
tent
ial,
note
s,an
dre
fere
nces
Am
bros
iaar
tem
isii
foli
aL
.(C
ompo
sita
e),
annu
alra
gwee
d,an
nual
herb
Bra
zil(
past
ure
and
plan
tatio
n)So
uthe
rnN
orth
Am
eric
ato
Mex
ico
Non
ere
port
edG
ood
pote
ntia
lfor
succ
essf
ulC
BC
.Eff
ectiv
eco
ntro
lin
Aus
tral
iaw
ithin
sect
s(e
xM
exic
o)re
leas
edin
1980
and
1984
.Myc
oher
bici
des
unde
rin
vest
igat
ion.
Path
ogen
sid
entifi
ed,
spec
ifici
tyte
stin
gre
quir
ed(1
,2,a
)A
xono
pus
com
pres
sus
(Sw
.)B
eauv
.(Po
acea
e),
carp
etgr
ass,
stol
onif
erou
s,pe
renn
ialg
rass
.C
osta
Ric
a(c
offe
e),V
enez
uela
(cac
ao),
Tri
nida
d(s
ugar
cane
)T
ropi
calA
mer
ica
Can
mak
ea
good
fodd
ergr
ass.
Use
das
ala
wn
gras
sin
dry
area
s.
Impo
rtan
tben
efits
and
nativ
e,th
eref
ore
CB
Can
unlik
ely
optio
n
Bor
reri
ala
tifo
lia
(Aub
l.)K
.Sch
um.,
(Rub
iace
ae),
broa
dlea
fbu
ttonw
eed,
annu
alhe
rb,p
eren
natio
non
lyby
seed
Cos
taR
ica
(cof
fee)
,Bra
zil(
soyb
eans
,cot
ton,
cass
ava)
,Mex
ico
(mai
ze,u
plan
dri
ce),
Tri
nida
d(s
ugar
cane
)
Prob
ably
Neo
trop
ics
Non
ere
port
edN
ativ
e,th
eref
ore
CB
Can
unlik
ely
optio
n
Bra
chia
ria
mut
ica
(For
sk.)
Stap
f.(P
oace
ae),
Para
gras
s,st
olon
ifer
ous,
pere
nnia
lgra
ssJa
mai
ca,P
eru
and
Puer
toR
ico,
Bra
zil(
suga
rca
ne),
Tri
nida
d(c
itrus
,tob
acco
),C
olom
bia
(oil
palm
),Pe
ru(r
ice)
Clo
gsir
riga
tion
cana
lsan
dw
ater
way
s
Tro
pica
lAfr
ica
Fodd
erIm
port
antv
alue
asfo
dder
,the
refo
repo
tent
ial
confl
icts
ofin
tere
stw
ithC
BC
(3)
Bra
chia
ria
plan
tagi
nea
(Lin
ck)
Hitc
hc.
(Poa
ceae
),A
lexa
nder
gras
s,an
nual
gras
s,se
ed
Bra
zil(
arab
lecr
ops)
Afr
ica?
Not
used
asa
past
ure
spec
ies
inB
razi
lN
oda
taav
aila
ble
onco
-evo
lved
natu
ral
enem
ies,
butw
orth
yof
inve
stig
atio
nin
toC
BC
pote
ntia
l
Chl
oris
chlo
ride
a(P
resl
)H
itchc
.(Po
acea
e),
finge
rgr
ass,
unde
rgro
und
sexu
alse
eds
(cle
isto
gam
y)an
dae
rial
seed
s
Mex
ico,
ElS
alva
dor,
curr
ently
inva
ding
Hon
dura
san
dC
osta
Ric
a(r
ice)
.—
——
Com
mel
ina
beng
hale
nsis
L.(
Com
mel
inac
eae)
Wan
deri
ngJe
w,a
nnua
lor
pere
nnia
lher
b,se
eds
and
stol
ons
Bra
zil(
soyb
ean
and
annu
alcr
ops)
,Per
u(p
eren
nial
crop
s)O
ldW
orld
trop
ics
(pos
sibl
yIn
dia
orE
ast
Afr
ica)
Poor
fodd
erPo
tent
ialp
atho
gens
for
CB
Cid
entifi
ed(a
)
Cyn
odon
dact
ylon
(L.)
Pers
.(Po
acea
e),
Ber
mud
agr
ass,
pere
nnia
lrhi
zom
esgr
ass
Arg
entin
a(s
ugar
cane
,vin
eyar
ds,p
lant
atio
ncr
ops)
Col
ombi
a(v
eget
able
s,su
gar
cane
),B
razi
l(ri
ce,v
eget
able
s)Ja
mai
ca,T
rini
dad,
Peru
,Mex
ico
and
Puer
toR
ico
(sug
arca
ne),
Cen
tral
Am
eric
a(c
orn)
Tro
pica
lAfr
ica,
orIn
do-M
alay
sia
Use
fulp
astu
regr
ass,
prev
ents
soil
eros
ion,
used
asa
law
nan
dpl
ayin
gfie
ldgr
ass
Impo
rtan
tben
efits
,the
refo
repo
tent
ialc
onfli
cts
ofin
tere
stw
ithC
BC
Cyp
erus
escu
lent
usL
.(C
yper
acea
e),y
ello
wnu
tsed
ge,p
eren
nial
sedg
e,rh
izom
es,t
uber
s.Pe
ru(s
ugar
cane
,citr
us),
Chi
le(r
ice)
Cos
taR
ica
(sug
arca
ne)
Unk
now
nT
uber
sea
ten
byhu
man
san
dpi
gsC
BC
pote
ntia
lreq
uire
sfu
rthe
rin
vest
igat
ion.
Rus
t(P
ucci
nia
cana
licu
lata
)re
dist
ribu
ted
inU
SA,f
aile
dto
esta
blis
h(4
)C
yper
usro
tund
usL
.(C
yper
acea
e),p
urpl
enu
tsed
ge,p
eren
nial
sedg
e,rh
izom
es,t
uber
sA
llco
untr
ies
(pri
ncip
ally
annu
alcr
ops
espe
cial
lyri
ce,c
otto
n,ve
geta
bles
,and
corn
.A
lso
suga
rca
ne)
Old
Wor
ldPi
gsea
ttub
ers,
med
icin
alva
lue
(Chi
na),
soil
stab
ilise
r(I
ndia
);m
akes
apo
orfo
dder
plan
t
Pote
ntia
lpat
hoge
nsfo
rC
BC
iden
tified
.Ins
ect
agen
tsre
leas
edfo
rC
BC
wer
eno
tsuc
cess
ful.
Myc
oher
bici
des
unde
rst
udy
(a,4
)
Dic
hros
tach
ysci
nere
a(L
.)W
ight
.and
Arn
.(L
egum
inos
eae)
Mar
abu,
pere
nnia
lshr
ub/tr
eeC
uba
(ara
ble
and
past
ure)
NO
TE
:Thi
ssp
ecie
sis
also
inva
ding
natu
rale
cosy
stem
sA
fric
a,A
sia
Aus
tral
iaO
rnam
enta
lPo
tent
ialp
atho
gens
for
CB
Cid
entifi
ed(a
)
Ech
inoc
hloa
crus
-gal
li(L
)B
eauv
.(Po
acea
e),
barn
yard
gras
s,an
nual
gras
s,se
edB
razi
l,C
hile
,Arg
entin
a,C
olom
bia,
Peru
,C
osta
Ric
a(r
ice)
Can
beto
xic
toca
ttle
(acc
umul
ates
nitr
ates
intis
sues
)
Eur
ope
and
Indi
aN
one
repo
rted
Pote
ntia
lpat
hoge
nsfo
rC
BC
iden
tified
.M
ycoh
erbi
cide
sun
der
stud
y(a
)
33
Isch
aem
umru
gosu
mSa
lisb.
(Poa
ceae
),w
rink
led
gras
s,an
nual
gras
s,se
edB
razi
l,Pe
ru,C
olom
bia,
Guy
ana,
Suri
nam
,T
rini
dad,
Cos
taR
ica
(ric
ean
dsu
gar
cane
)T
ropi
calA
sia
Cat
tlefo
dder
Impo
rtan
tval
ueas
fodd
er,t
here
fore
pote
ntia
lco
nflic
tsof
inte
rest
with
CB
CPa
nicu
mm
axim
umJa
cq.(
Poac
eae)
,Gui
nea
gras
s,tu
fted
pere
nnia
lgra
ssC
uba,
Mex
ico,
Cos
taR
ica,
Bra
zil(
suga
rca
ne),
Cos
taR
ica
(oil
palm
),C
olom
bia
(cor
n),
Ecu
ador
(cac
ao)
NO
TE
:Thi
ssp
ecie
sis
also
inva
ding
natu
rale
cosy
stem
s
Afr
ica
Past
ure,
hay
and
sila
gegr
ass
Impo
rtan
tval
ueas
anim
alfe
edm
akes
ita
diffi
cult
targ
etfo
rC
BC
.Als
o,co
nsid
ered
bym
any
tobe
the
mos
tim
port
ante
nvir
onm
enta
lw
eed
inB
razi
l,so
this
may
outw
eigh
itsbe
nefit
s(3
)Pa
spal
umco
njug
atum
Ber
g(P
oace
ae),
sour
gras
s,pe
renn
ial,
stol
onif
erou
sgr
ass
Cos
taR
ica
(cof
fee,
oilp
alm
),M
exic
o(c
offe
e),
Tri
nida
d(s
ugar
cane
,cac
ao)
Tro
pica
lAm
eric
aPo
orfo
dder
valu
eN
ativ
e.H
owev
er,p
atho
gens
reco
rded
from
outs
ide
ofna
tive
rang
eth
atco
uld
bein
vest
igat
ed(5
)Pe
nnis
etum
clan
dest
inum
Hoc
hst(
Poac
eae)
,K
ikuy
ugr
ass,
pere
nnia
l,rh
izom
atou
sgr
ass
Ecu
ador
(pas
ture
gras
s),C
osta
Ric
a(r
owcr
ops,
tea)
,Col
ombi
a(i
rrig
ated
crop
s),P
eru
(per
enni
alcr
ops)
Tro
pica
leas
tern
Afr
ica
Past
ure
gras
s,so
ilbi
nder
Sign
ifica
ntbe
nefic
ialv
alue
s,th
eref
ore
pote
ntia
lco
nflic
tsof
inte
rest
with
CB
C(3
)
Pte
ridi
umaq
uili
num
(L.)
Kuh
n(D
enns
taed
itiac
eae)
,bra
cken
,per
enni
al,
rhiz
omat
ous
fern
Col
ombi
a(c
assa
va),
Hon
dura
s(m
aize
),C
entr
alA
mer
ica,
Ecu
ador
,Bra
zil,
Col
ombi
a,(e
ncro
ache
son
graz
ing,
pois
ons
stoc
k);C
osta
Ric
a(g
astr
icca
ncer
inhu
man
sfr
omdr
inki
ngco
ntam
inat
edm
ilk)
Cos
mop
olita
nsp
ecie
sA
esth
etic
valu
e,so
ilst
abili
satio
nM
ycoh
erbi
cide
sin
vest
igat
ed.S
uppo
rts
adi
ffer
ents
uite
ofna
tura
lene
mie
sin
diff
eren
tre
gion
s,bu
tdam
age
isra
rely
seve
re.
Wor
thw
hile
inve
stig
atin
gth
epo
tent
ialo
fta
king
diff
eren
tnat
ural
enem
ies
into
Lat
inA
mer
ica
that
are
alre
ady
pres
ente
lsew
here
(6,
7,8,
9)R
ottb
oell
iaco
chin
chin
ensi
s(L
our.)
W.D
.C
layt
on(P
oace
ae)
Itch
gras
s,an
nual
gras
s,se
ed
Cen
tral
and
Sout
hA
mer
ica
–st
illad
vanc
ing
inne
wre
gion
s(n
umer
ous
annu
alan
dpe
renn
ial
crop
s,pa
rtic
ular
lym
aize
,upl
and
rice
and
suga
rca
ne)
Indi
a(p
ossi
bly
also
Eas
tAfr
ica)
Non
ere
cord
edC
BC
prog
ram
me
atim
plem
enta
tion
stag
e(s
eepr
evio
usse
ctio
n).M
ycoh
erbi
cide
sin
vest
igat
ed(1
0,11
,a)
Sacc
haru
msp
onta
neum
L.(
Poac
eae)
,pe
renn
ial,
rhiz
omat
ous
gras
sPa
nam
a,G
uyan
a,Pu
erto
Ric
o,in
vadi
ngC
osta
Ric
a(f
orag
es,p
astu
re,a
nnua
land
pere
nnia
lcr
ops,
e.g.
rice
,sug
arca
ne,t
ea,c
offe
e,ru
bber
)
Indi
aC
attle
fodd
er(p
oor)
;soi
lm
ulch
,roo
fth
atch
ing,
rope
and
mat
mak
ing
(Asi
a);
med
icin
alpr
oper
ties
(Phi
lippi
nes)
;you
ngsh
oots
eate
n(I
ndon
esia
);us
edin
bree
ding
prog
ram
mes
(bel
ieve
dto
bean
ance
stor
ofS.
offic
inar
um[c
omm
erci
alsu
gar
cane
])
Sign
ifica
nthu
man
valu
e,th
eref
ore
pote
ntia
lco
nflic
tsof
inte
rest
with
CB
C
Sorg
hum
hale
pens
eL
.(Pe
rs.)
(Poa
ceae
),Jo
hnso
ngr
ass,
pere
nnia
l,rh
izom
atou
sgr
ass
Mex
ico,
Ven
ezue
la,A
rgen
tina,
Chi
le,B
razi
l,Pe
ru,C
olom
bia
(cot
ton,
suga
rcan
e,m
aize
,ci
trus
,alf
alfa
,ric
e,ve
geta
bles
,bea
ns,
sorg
hum
).L
eave
san
dst
ems
can
accu
mul
ate
toxi
nsin
som
eco
nditi
ons
(hyd
rocy
anic
acid
)
Med
iterr
anea
nC
attle
fodd
er,s
econ
dary
host
ofcr
opdi
seas
esSi
gnifi
cant
valu
eas
fodd
er,t
here
fore
pote
ntia
lco
nflic
tsof
inte
rest
with
CB
C(3
)
Sonc
hus
arve
nsis
L.(
Ast
erac
eae)
,per
enni
also
wth
istle
,per
enni
alhe
rb,s
eed
Peru
(veg
etab
les)
,Bra
zil(
coff
ee),
Mex
ico
(sun
flow
ers)
,Gua
tem
ala
(whe
at)
Eur
ope
May
prov
ide
pote
ntia
lsou
rce
ofru
bber
,med
icin
alva
lue
(Chi
na),
sala
dhe
rb(E
urop
e)
Goo
dpo
tent
ialf
orsu
cces
sful
CB
C.I
nsec
tex
Aus
tria
rele
ased
inC
anad
ain
1981
and
can
redu
cew
eed
dens
ityby
50%
.Dam
agin
gm
ycob
iota
reco
rded
(12,
a)W
edel
iatr
ilob
ata
(L.)
Hitc
hc.(
Com
posi
tae)
,Si
ngap
ore
dais
yT
rini
dad,
Cos
taR
ica,
Puer
toR
ico,
Hon
dura
s,B
eliz
e(o
ilpa
lman
dci
trus
)—
——
Dat
ano
tava
ilabl
e;a
=se
eTa
ble
4;1
=B
rier
eet
al.(
1995
);2
=M
cFad
yen
(198
9);3
=W
illia
ms
and
Bar
uch
(200
0);4
=Ju
lien
and
Gri
ffith
s(1
998)
;5=
Wat
erho
use
(199
4);6
=V
illal
obos
Sala
zar
(198
7);
7=
Wom
ack
etal
.(19
96);
8=
Ras
hbro
oket
al(1
989)
;9=
Hol
met
al.(
1997
);10
=E
lliso
n(1
992)
;11
=Sa
nche
z-G
arita
and
Zun
iga
(199
9);1
2=
Schr
oede
r(1
973)
.
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 xanthiiSchwein (Uredinales: Pucciniaceae)
Batra, 1981; Hartmann andWatson 1980
Broussonetia papyrifera Aecidium mori Barclay var. broussenetia(Uredinales: Incertae sedis), Cercospora sp.(Hyphomycete), Dendryphiella broussonetiaeY.L. Guo and Z.Y. Zhang (Hyphomycete),Mycovellosiella broussonetiae Goh andW.H. Hsieh (Hyphomycete), Uredo broussonetiaeSawada (Uredinales: Incertae sedis)
D. Jianqing, pers. comm.(2001); Guo and Zhang 1999;Herb. IMI
Calotropis procera Ascochyta tripolitana Sacc. and Trotter(Coelomycete), Gloeosporium calotropidisPat. and Har. (Coelomycete), Napicladiumcalotropidis Morstatt (Hyphomycete),Phoma calotropidis Speg. (Coelomycete)
Barreto et al. 1999
Commelina benghalensis Cercospora benghalensis Chidd. Cylindrosporiumkilimandscharicum Allesch. (Hyphomycete),Kordyana celebensis Gaum. (Exobasidiales:Brachybasidiaceae), Phakopsora tecta H.S. Jacksand Holw (Uredinales: Phakopsoraceae), Septoriacommelinae Canonaco (Coelomycete), Uromycescommelinae 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 Ravinder1988; H.C. Evans,pers. comm. (1998)
Echinochloa crus-galli Tolyposporium bullatum J. Schrot. (Ustilaginales:Cintractiaceae), Ustilago crus-galli Tracy andEarle (Ustilaginales: Ustilaginaceae), Ustilagotrichophora (Link) Kunze
Waterhouse 1994
Pittosporum undulatum Phomopsis pittospori (Cooke and Harkn),Grove (Coelomycete)
Herb. IMI
Rottboellia cochinchinensis Puccinia rottboelliae Syd. Sporisorium ophiuri(Henn.), Vanky (Ustilaginales: Ustilaginaceae)
Ellison 1993(see previous section)
Rubus niveus Phragmidium barclayi Dietel (Phragmidiaceae,Uredinales), Phragmidium himalense J.Y. ZhuangPhragmidium octoloculare Barclay, Phragmidiumshogranense Petr., Pseucercospora sp.(Hyphomycete)
Herb. IMI
Sonchus arvensis∗ Alternaria sonchi Davis (Hyphomycete),Coleosporium sonchi (Pers.) Lev. (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, MacDonaldSeptoria 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 mycobiotais also known, that could complement the current programmes.
35
possible to use the results from such successful pro-grammes to ‘fast track’ Latin American programmes.Mycoherbicide programmes are also being developedfor at least five of those listed, using indigenousfungal pathogens: annual ragweed, purple nutsedge,Echinochloa crus-gall (barnyard grass), Pteridiumaquilinum (bracken), and itch grass. Thirteen speciesare considered to have good potential for CBC withpathogens. For seven of these, there is some informa-tion concerning their mycobiota (see Table 4) and theseare discussed in the next section. Bracken is consideredto have good potential for CBC, although investiga-tions have not revealed an extensive mycobiota and,hence, arthropods are considered the most appropriatebiocontrol agents (Holm et al. 1997). Indeed, a mothConservula cinisigna de Joannis, from South Africawas fully screened for release against bracken in theUK (Fowler 1993), but a release programme was neverundertaken due to lack of governmental financial sup-port. In addition, attempts have been made to employmycoherbicides in the UK (Womack et al. 1996).
Future prospects for CBC of alien weedswith fungal pathogens in Latin America
Table 4 lists 12 alien weed species from LatinAmerica, together with their known co-evolved fun-gal pathogens, that can be considered good targetsfor CBC using the currently available knowledge. Thefungal records presented are based on searches under-taken in Herb. IMI (CABI Bioscience, Egham, UK),database searches (CAB Abstracts®, Wallingford,UK), and reviews (Evans 1987; Barreto and Evans1995; Waterhouse 1994). However, it is unlikely thatthese lists are definitive, since it is clear from the resultsof field surveys (Barreto et al. 1995; Evans and Reeder2001), that there is an enormous mycobiota waiting tobe discovered, even on well studied plant species.
There are a number of omissions of weeds fromTable 4 that would appear to be good targets basedon their morphology (e.g. broad-leaved), the habitatthey infest (e.g. those with high humidity), their levelof destruction (e.g. displaced native flora and faunain primary habitats) and have a known centre of ori-gin. For example, Hedychium spp. have many of thesecharacteristics, but there is no information availableconcerning their mycobiota. In addition, weeds arenot included that already have successful CBC pro-grammes in place, although for some the mycobiotais well documented. However, in the short-term it is
considered more profitable to implement known suc-cess stories than start from scratch with an unstudiedweed–pathogen system. There are more than enoughtargets that need control for which nothing is known! Abrief assessment of the selected targets is given below.
Ambrosia artemisiifoliaCommon ragweed is a weed of pasture and plantationsin subtropical habitats of Brazil. The centre of ori-gin of this species is probably southern USA throughto Mexico. It is, however, a major problem in cropsin northeastern USA. A number of pathogens havebeen recorded from this species throughout its range,although specificity still remains to be established inmost cases (Bohar and Vajna 1996). There is evidencethat the white blister ‘rust’, Albugo tragopogonis, andthe rust, Puccinia xanthii, occur as a number of for-mae speciales, with each pathotype infecting a relatedbut different plant host species (Batra 1981; Hartmannand Watson 1980). However, little is known about thepowdery mildew (Erysiphe cichoracearum), althoughhost-specific races of this cosmopolitan pathogen mayexist. On current evidence (H.C. Evans and M.K. Seier,unpublished data) the rust would appear to be the bestcandidate for initial study, since it is recorded fromMexico, where A. artemisiifolia is not a problem weed,and its range does not appear to extend down intoBrazil.
Broussonetia papyrifera (paper mulberry)Paper mulberry has been recorded as an invasive treein Peru, although published data on the impact ofthis species is lacking. It is also a weed in Pakistan,where it has colonised waste ground forming mono-culture forests, and is now invading reserves set asideto preserve the indigenous flora. There is also a healthissue; much of the population is at least slightly allergicto pollen from the tree (M.J.W. Cock, pers. comm.[1998]). The potential for CBC requires evaluation,although five potentially useful pathogens have alreadybeen recorded from its native range in China andJapan.
Calotropis proceraThis plant is a problem in the semi-arid, northeasternregions of Brazil. It was introduced at the beginningof the century, and has become a problem in pasturesand roadsides, and of unique natural ecosystems, suchas scrubland (‘Caatinga’) and savannah (‘Cerrado’)(Brandao 1995; Kissmann and Groth 1992). Within
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the exotic range of rubber bush a number of pathogenshave been recorded. For example, Phaeoramulariacalotropidis (Ellis & Everh.) Kamal, A.S. Moses &R. Chaudhary was probably introduced into Brazilwith its host; whereas the rust Puccinia obliqua Berk& M.A. Curtis is known to have a wide host rangewithin the neotropical Asclepiadaceae, and hence itscompatibility with rubber bush can be considered apredictable ‘new encounter’ (Barreto et al. 1999).However, although the rust does appear to be exert-ing some control in the more humid areas, none ofthe pathogens appear to be exerting sufficient pressureon the host to achieve adequate suppression. Fungalherbarium records and the literature suggest that theMiddle East and Northeast Africa may be the bestsources of exploitable co-evolved natural enemies andfour potential fungal agents are listed in Table 4.
Commelina benghalensisWandering Jew is a succulent, creeping, herbaceousplant that can be either annual or perennial dependingon the climatic conditions. It originates from the OldWorld and has only recently been recorded as a weed incropping systems in Latin America (Kissmann 1991).It is able to grow in wet conditions, rapidly formingdense, monocultures, and smothering crop plants, andpastures (Holm et al. 1977). From herbarium records,Evans (1987) documented a relatively rich mycobiotaon C. benghalensis and, hence, there would appear tobe good potential for CBC. Although some of the mostpromising pathogens (e.g. the rusts Phakopsora tectaand Uromyces commelinae) are already present in theNew World, they are restricted to certain regions, andcould be redistributed. In Brazil, for example, none ofthe two aforementioned rusts has been found, despite10 years of observations (R.W. Barreto, pers. obs.). Theother four pathogens listed appear to be restricted to theOld World and require basic investigations concerningtheir specificity and damage to their host.
Cyperus rotundusPurple nutsedge is considered to be one of the world’sworst weeds (Holm et al. 1977; Terry and Ritches2001). Hence, although a difficult target for CBC, dueto its effective methods of propagation and regener-ation, it warrants considerable effort. The taxonomicisolation of the species from crop plants of importancealso makes it an ideal target. Most of the biologicalcontrol work undertaken so far has involved insect
natural enemies and, although, there have been nosubstantial successes with CBC releases (Julien andGriffiths 1998), the early season augmentation of themoth Bactra verutana Zeller in the USA has beenpartially successful (Frick and Chandler 1978).
Others have investigated native pathogens as poten-tial mycoherbicides (Barreto and Evans 1995; Ingliset al. 2001; Kadir and Charudattan 2000; Dinoor et al.1999). A more novel approach could also be inves-tigated, using the same methods as that developedby Phatak (1992) for the control of C. esculentus inthe Southern USA. The indigenous rust fungus Puc-cinia canaliculata (Schw.) Lagerh. is bulked up in theglasshouse on its host during the winter months, andthen applied to weed populations in the field early in theseason. The spores are formulated, incorporating a lowdose herbicide, and sprayed on to the plants as a myco-herbicide. By applying the rust early in the season, epi-phytotics are produced much earlier than would occurnaturally, and the weed is rendered non-competitive.Unfortunately, the product Dr BiosedgeTM has not beenreleased on to the commercial market, purportedly dueto problems with the mass production of the rust spores.Callaway et al. (1985) considered developing, by sex-ual recombination, other strains of the rust virulent onboth C. rotundus and C. esculentus. In addition, it maybe possible to use other co-evolved pathogens listed inTable 4, in a similar manner, combining both classicaland inundative biological control.
Dichrostachys cinerea (marabu)This woody, leguminous shrub or small tree is believedto have an Afro-Asian native range (Mabberley 1997).In 1919 marabu was first reported as a weed in Cubaunder the name Dichrostachys nutans (Pers.) Benth.(Weir 1927). Since that time is has increased its rangeon the island, forming impenetrable, thorny thickets(M.K. Seier, pers. comm. [1998]). It is now a majorweed of agriculture, encroaching on grazing land, andalso in natural ecosystems, where it is replacing thenative scrub vegetation. Three pathogens have beenfound infecting D. cinerea in India (H.C. Evans, pers.comm. [1996]). Field observations suggest that the rustRavenelia sp. (Bagyanarayana and Ravinder 1988) isthe most promising of the three identified agents, sinceit attacks the growing points, inducing tissue malfunc-tion and results in the formation of spectacular witches’brooms. Funding is currently being sought to continuethe work.
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Echinochloa crus-galliThis noxious grassy weed is pantropical in distribu-tion. It is particularly important in rice and has beentargeted for inundative biological control in Europe byScheepens (1987) and in the Philippines by Zhang andWatson (1997). In the first case, Cochliobolus lunatusNelson & Haasis was used to control barnyard grassin combination with a sub-lethal dose of the chemi-cal herbicide atrazine. In the Philippines, the fungusExserohilum monoceras (Drechsler) K.J. Leonard &Suggs is being developed as a mycoherbicide for usein rice. The potential product is composed of a mixtureof pathogens, each specific to a different weed speciesor genus within the rice weed complex (Eusebio andWatson 2000). It should be feasible to investigate sim-ilar approaches using indigenous pathogens in LatinAmerica.
Barnyard grass is said to be native to Europe andIndia but very few natural enemies have been reportedattacking it in this vast region, and surveys are requiredto establish its CBC potential (Waterhouse 1994).There are three head smut species recorded from theweed and these may be worthy of further investigation,since it is an annual grass and seeds are the only meansof perennation.
Pittosporum undulatum (cheesewood)This Australian tree species was introduced intoJamaica in 1883, and has become a serious invasiveweed in the Blue Mountain forests (Healey et al. 1992).Cheesewood is still in its invasive phase and poses aserious threat to the biodiversity of the range. It isunusual in that it invades species-rich rainforest vegeta-tion, although the damage caused by hurricane Gilbertin 1988 has accelerated the invasion. An evaluation ofthe impact of the tree and potential control methodshas been undertaken by Healey et al. (1992). An addi-tional study was undertaken to investigate more fullythe control options (Goodland and Healey 1997). Itwas concluded that manual removal and application ofherbicides should be employed initially. However, itwas conceded, with some reservations, that CBC maybe the only long-term solution to the problem. Counterarguments to CBC were presented, based mainly ona perception of limited potential efficacy of agents. Itwas recommended that a full assessment of a biologicalsolution, including costs, should be made.
There is little information on natural enemies ofcheesewood and whether insects or pathogens shouldform the focus of effort. The tree does have some
value in Jamaica for firewood and, consequently, aseed-feeding insect may be the best option, since thishas the potential to reduce spread without impingingon the value of the wood. However, native speciescould be developed to fill this niche, in tandem witha concerted effort to reduce the impact of the weedby targeting a number of plant parts. In South Africa,where P. undulatum is also a problem weed, a diseasehas been reported causing severe destruction of plants(Goodland and Healey 1997). If it proved to be at leastgenus specific, it may be considered for introduction,since there are no native members of the Pittosporaceaein Jamaica. In Australia, there are some reports of habi-tats where cheesewood has become invasive (Mullettand Simmons 1995). This could be considered con-trary to the principle that plants are rarely invasive intheir native range. However, the reports discuss thatthe invasions tend to be in disturbed habitats that areusually distant from the native populations and, thus,support the supposition that the plant is effectivelycontrolled by natural enemies in its natural ecologicalrange. Data obtained from Herb. IMI suggested thatonly one pathogen, Phomopsis pittospori, was consid-ered worthy of investigation. Clearly, comprehensivesurveys in Australia are required.
Rottboellia cochinchinensisCBC of this serious invasive weed using a head smut(Sporisorium ophiuri) has been discussed in detailpreviously. However, there is also a rust pathogen(Puccinia rottboelliae) found in many parts of Africaattacking this grass, and preliminary investigations(C.A. Ellison, unpublished data) suggest it may alsobe of value in Latin America.
Rubus niveus (Mysore or hill raspberry)This thorny, perennial shrub is of Asiatic origin, but hasbecome a serious weed in the Galapagos Islands. Thisspecies only arrived there in the early 1980s and is stillin its invasive phase. Currently, expensive chemicalcontrol is being used, but at best this is only slowingthe invasion. Recent ad hoc surveys in China foundthe species is attacked by a number of natural enemies,including a damaging leaf spot that induces extensivenecrosis (Pseudocercospora sp.), and a stem-gallinginsect (H.C. Evans, pers. comm. [2000]). Mycolog-ical records (Herb. IMI) show that at least four rustspecies (Phragmidium spp.) have been recorded in itsHimalayan range, but whether they actually consti-tute four distinct taxa, or are conspecific synonyms,
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requires validation. Phragmidium violaceum (Schultz)G. Winter is proving to be successful as a CBC agentagainst Rubus spp. in Chile and Australia (Mahr et al.1998; Oehrens 1977), and so the prospects wouldappear to be excellent for CBC of R. niveus.
Sonchus arvensisThis composite of Eurasian origin can reach heights ofup to 1.5 m. It has been targeted for CBC in Canada andsome insect species have been released (ex Austria),although they have not been generally effective (Julienand Griffiths 1998). Other insect species are underevaluation. Perennial sowthistle is a relatively recentintroduction to Latin America but it is increasing inimportance, particularly in Peruvian vegetable crops(S. Helfgott, pers. comm. [1996]). There are a largenumber of potentially exploitable co-evolved naturalenemies recorded from the species in its native range,and five pathogens are listed in Table 4. A damag-ing and host specific rust, Puccinia suaveolens, hasbeen investigated in Russia and appears to have goodpotential for biological control (Holm et al. 1997).
Ulex europaeusThis fast-growing, spiny shrub has an European centreof origin. It can form impenetrable thickets, reachingheights of up to 4 m, with individual plants survivingfor nearly three decades. Although a highly invasive,noxious weed, some conflicts of interest were identifiedwhen this plant was targeted for biological control. InNew Zealand, it has value as a source of pollen forbees, a nurse-plant for native forest regeneration onabandoned agricultural land, fodder for goats, protec-tion against erosion, and shelter for grazing animals(Hill et al. 2000). However, analysis revealed thatthe economic benefits resulting from successful con-trol, far outweighed those resulting from the uses ofgorse, by a factor of more than 12 : 1. Equally, thenon-economic costs (e.g. impact on native vegetation)were in favour of implementing control (Hill 1989).Consequently, insect agents have been released and gosome way towards successful control.
Programmes currently underway in Chile have led-on from these successes in New Zealand (Norambuenaet al. 2000). The first agent Apion ulicis (Forester),released in 1976, was ineffective (Norambuenaand Piper 2000), but further agents have beenreleased (Tetranychus lintearius Dufour in 1997 andAgonopterix ulicetella (Stainton) in 1997–1998). It istoo early to assess efficacy of these biocontrol agents.
There are two particularly interesting pathogens thathave been recorded from gorse in its native range, therust Uromyces pisi f. sp. europaei and leaf spot Septoriaslaptoniensis. Both are damaging in the field, and theformer is currently under assessment in Hawaii andlikely to be released soon (Hill et al. 2000). A myco-herbicide is also being developed in New Zealand usingthe native pathogen Fusarium tumidum Sherb. (Morinet al. 1998).
Discussion and conclusions
CBC is an under-exploited approach to the control ofinvasive alien weeds in Latin America. This approachoffers a safe, sustainable, environmentally benign,practical, and economically feasible method for theirmanagement. The data presented in this review indicatethat there is a significant untapped resource waiting tobe exploited in the field of CBC of weeds with fungalpathogens. Unfortunately and unjustifiably, the intro-duction of natural enemies is still regarded with suspi-cion, despite the clean track record, and the growingsuccess stories (Marohasy 1996; McFadyen 1998).
Spurious arguments on the dangers of CBC, based onthe disastrous consequences of introducing generalistanimal predators to control a single pest species (e.g.the cane toad in Australia, the African snail, and themongoose 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). Thesecases and others were predictable outcomes and, hence,could have been avoided had those concerned with theintroduction followed the stringent scientific evaluationthat is required today (Thomas and Willis 1998; FAO1996).
Others, with more understandable concerns, con-sider the introduction of biological control agents tobe unsafe inherently due to potential expansion of thehost range, or ‘host shifts’. Evidence suggests that thisdoes not occur with biological control agents that haveco-evolved with their host plant species over millennia.McFadyen (1998) lists worldwide-recorded instancesof damage to non-target plants by biological controlagents. Of the eight examples listed (all insect) fivewere anticipated. For the other three, the damage wasminor and short-lived. Marohasy (1996) adds more evi-dence to the inherent safety of using CBC agents, basedon the evaluation of 600 species of arthropod agents thathad been moved between geographic regions. It was
39
concluded that there were few documented examplesof ‘host shifts’ and that all were, in fact, predictablebehavioural responses, and not the result of a geneticchange.
Pathogens have been exploited only as CBC agentsof weeds for three decades, in contrast to a centuryof arthropod exploitation. The modern screening pro-cedures originally developed by Wapshere (1974) forarthropods, have been adhered to in the majority ofpathogen releases, and are in fact now more stringentfor pathogens (Evans 2002). Consequently, pathogenshave an impeccable track record as CBC agents. Itcan be concluded that, when carried out using strictscreening protocols, CBC is inherently safe (Evans2000).
This approach to weed control is, nevertheless, bio-logically based and hence not 100% predictable. It isultimately the responsibility of the quarantine author-ities of the importing country to undertake a riskassessment based on ‘good science’ provided by theresearchers (FAO 1996). It is then possible to decidewhether any risks outweigh the often-catastrophic dam-age that invasive weeds can cause to natural ecosys-tems and/or agricultural production. Indeed, insectshave been released against invasive weeds in the pastthat also were known to attack a closely related nativespecies. Louda et al. (1997) reported that the weevilRhinocyllus conicus (Frolich), introduced into NorthAmerica to control alien thistles on rangeland, alsoattacked rare native thistles. This was known priorto release but the cost–benefit analysis still allowedrelease (Schroeder 1980). Such cases do not help thebiological control cause, and careful legislation shouldbe in place to prevent the release of agents that causeunacceptable non-target effects.
In natural ecosystems, a similar non-target effectmay not be such a cause for alarm since, without thecontrol of the weed, there may not be a habitat leftto support the native species. This was the case withthe release of the Madagascan rust in Australia againstrubber vine (see previous section). The rust was foundto cause limited infection (in the glasshouse) on a nativeAsclepiadaceae, which was itself at risk of extinctionby the rubber vine invasion.
The public and government authorities worldwideare becoming aware of the value and the need to pre-serve the biodiversity of ecosystems. This is beingreflected by the development of international agree-ments, such as the Convention on Biodiversity, and sup-ported by national legislation (http://www.biodiv.org/).
An unfortunate consequence of this upsurge due to theinterest in biodiversity is that exploration for classicalbiocontrol agents is often not being treated separatelyfrom profit-oriented bioprospection for new drugs orother compounds. Novel anti-biopiracy legislation isoften full of highly conservative safeguards. Seri-ous and unnecessary delays for important biologicalcontrol projects are a consequence.
A recent example is that of Psidium cattleianum(strawberry guava). A potentially effective biocontrolagent, a gall-forming wasp, was selected and compre-hensively studied by a team of entomologists based atthe Universidade Federal of Parana (Curitiba: Brazil),funded by the Research Corporation of the Universityof Hawaii. The insect was proven to be a safe bio-control agent for one of the worst invasive weeds inisland ecosystems, and all is ready for its introductioninto Hawaii. Unfortunately, it has been over two yearssince the proposal for the export permit was presentedto the Brazilian authorities. So far, no final permithas been granted (J. H. Pedrosa-Macedo, pers. comm.2003). Funding of future projects is jeopardised bysuch delays, and it is essential that an adequate systembe organised based on new legislation. Special treat-ment for such a socially and environmentally desirablestrategy of pest control as CBC is necessary, highlyjustifiable and a matter of survival for the discipline.
Requirements for introduction of classical biocon-trol agents vary among different LA countries. Pro-tocols have yet to be fully in place in many of thecountries, although Costa Rica has an effective pro-cedure, based on the FAO Code of Conduct, thatalso incorporates decision making by the authoritieswithin strict time scales (FAO 1996). It was success-fully utilised for obtaining an import permit for theRottboellia cochinchinensis (itch grass) head smut (seeprevious section). In such countries there are no bureau-cratic burdens for classical biocontrol. In other countrysuch as Brazil, introductions of arthropods to be usedas biocontrol for other arthropods are made routinely,and the process is protracted but effective. Whether thiswould hold true for weed biological control agents isas yet untested.
To date, the majority of CBC projects have targetednative ecosystem plant invaders on the premise thatnatural enemies (particularly arthropods) tend to bemore effective in stable environments (Reznik 1996).However, the analysis presented in this paper, indi-cates that a similar number of weeds from agriculturaland natural ecosystems are suitable future targets for
40
CBC. This apparent anomaly may in part be due tothe often better documentation of pathogens on agri-cultural weed than their counterparts invading nat-ural ecosystems, as would be expected due to thedirect economic importance of these plants. Despite thebias of past and current CBC programmes that targetweeds of natural ecosystems, there are several exam-ples of CBC with pathogens being used to control alienweeds in agricultural systems (Hasan and Wapshere,1973; Chippendale 1995; McFadyen 1998, Reeder andEllison 1999).
In developing countries, CBC may prove to be theonly sustainable method of controlling exotic agricul-tural weed flora, although more research is required torealise the full potential of this method as part of anIPM approach in cropping situations (Altieri and Doll1978; Labrada 1996; Smith et al. 2001). For example,even agents that provide only limited control of a weedwithin an annual crop can be useful in helping to controlweeds in the field margins and fallow areas. Seeds fromthese weeds are known to contribute significantly toinfestations in subsequent crops (Ellison 1993).
As expected, most of the problem weeds inLatin America are exotic. Grasses (including sedges)constitute a significant proportion of the weed species.Unfortunately, these weeds are also notoriously diffi-cult targets for CBC, due both to their habit (protectedmeristem and ability to outgrow infection) and evo-lutionary closeness to major graminaceous crops. InJulien and Griffiths (1998) there are no examples ofarthropod species having been released against grasstargets. Indeed, it is generally considered that arthro-pods do not tend to be specific to single grass species(Evans 1991). Conversely, many co-evolved pathogenshave a highly restricted host range, attacking a sin-gle grass species or even a biotype. For example,Ellison (1993) found a number of fungal pathogens(Colletotrichum sp. nov., Puccinia rottboelliae andSporisorium ophiuri) isolated from itch grass, whichdemonstrated intraspecies specificity. Not only thatthey did not attack other grass species but were onlyable to infect certain biotypes within the species. Thus,fungal pathogens would appear to be the most suitablenatural enemies to investigate for CBC of grassy weedtargets.
In addition, grasses are difficult targets because mostof them also have economic importance as forage.For example, many of the most troublesome speciesin Brazil were originally deliberately introduced fromAfrica 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 beserious conflicts of interest about introducing naturalenemies for their control. However, with some of thesespecies, their threat to the native flora is increasingand consequently the benefits of control may prove tooutweigh their economic value.
There are examples where conflicts of interest havearisen with the control of an invasive weed. One exam-ple is that of Echium plantagineum L. which is known inAustralia as Paterson’s curse to farmers and to beekeep-ers as Salvation Jane. Despite a High Court injunctionbeing placed to prevent the release of biological controlagents, subsequent Government inquiries found thatcontrol of the weed was in the national interest anda CBC programme was implemented (Delfosse andCullen 1981; Bruzzese et al. 1997). In some cases itmay be possible to exploit biological control withoutseriously affecting the economic uses of an invasiveplant. In South Africa, for example, seed-boring insectswere introduced from Australia, which have success-fully helped to reduce the spread of a number of alienAcacia species. Many of these wattle species have valuein South Africa for firewood, timber, pulp, and tannins,but it is still possible for these uses to continue sinceonly seed production is affected (Dennill et al. 1999).
As discussed earlier, there are at least nine species inLatin America for which successful CBC programmeshave been implemented in other parts of the world. Itwould seem logical that these weeds constitute the firsttargets in future weed CBC programmes in this region,since costs of implementation will be low and successlikely to be high. A number of the other species listedhave characteristics that make them suitable targets,some with a well documented arthropod fauna and/ormycobiota and should be evaluated as the next step infuture CBC programmes.
There is also an increasing research effort in improv-ing the establishment of agents and developing novelmethods of exploitation, which could be utilised forthese releases. With pathogens, for example, in orderto achieve control of a range of biotypes of a weed, orto achieve control under different climatic conditions,a number of different strains of a pathogen can bereleased. Also, for agents that can be mass-produced,inundative application can be used to help acceleratetheir spread (Hennecke and Seier 1998). CBC cantake up to 10 years for a significant impact to beobserved. However, in the initial years, agents could
41
be manipulated to create ‘biotic barriers’ at the invasivefront of the weed to help limit further spread.
No doubt, as world travel and trade increase fur-ther plant species will accidentally be introduced intoregions where they have the potential to become weedproblems (Groves et al. 2001). It is imperative thatthe public is made aware of the risks. Many coun-tries already restrict the movement of plant materialbetween regions, usually due to the risk of introducingspecific pests and diseases (Anon 1994). However, thepotential for an introduced species to become a weedin the new environment must also be assessed (Cronkand Fuller 1995; Wittenberg and Cock 2001). Researchorganisations may have been responsible for the acci-dental spread of many weed species, often betweencontinents (Huelma et al. 1996). Although a signifi-cant percentage of agriculturally important weeds arealready ubiquitous others, for example Striga spp., arenot yet present in Latin America (Parker and Riches1993). It is thus vital that the quarantine authoritiesof all countries fastidiously monitor the movement ofplant germplasm.
Nevertheless, Charudattan (2001) concluded in thefinal section of his recent paper on weed biologicalcontrol in modern agro-ecology that, ‘It is unimagin-able, both from economic and ecological standpoints,to think that invasive weeds can be managed by regula-tions (exclusion and quarantine) or physical and chem-ical controls. Biological control, in all of its aspects,should be the centrepiece of a global strategy to tackleinvasive weeds.’
Acknowledgements
The authors would like to thank Dr Harry C. Evans forthe significant improvements and advice offered on themanuscript. Also, we appreciated the constructive crit-icism, particularly on the contents, by Dr Matthew A.Thomas. Dr Andy C. Croxford kindly proof read themanuscript.
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