Integrated Pest Management Reviews 2, 71–76 (1997)

Biological control of the annual weed Chenopodium album, with

emphasis on the application of Ascochyta caulina as a microbial
herbicide
P. C . S C H E E P E N S 1 , C . K E M P E NA A R 1 , C . A N D R E A S E N 2, T H . E G G E R S 3 , J. N E T L A N D 4 and
M. VURRO 5
1
DLO-Institute for Agrobiology and Soil Fertility (AB-DLO), PO Box 14, NL-6700 AA Wageningen, The Netherlands
2
Department of Agricultural Sciences, Royal Veterinary and Agricultural University, Thorvaldsenvej 40, DK-1871 Frederiksberg C, Copenhagen, Denmark
3
Federal Biological Research Centre for Agriculture and Forestry, Messeweg 11=12, D-38104 Braunschweig, Germany
4
Norwegian Crop Research Institute, Fellesbygget, N-1432 Ås, Norway
5
Institute of Toxins and Mycotoxins from Plant Parasites, Viale Einaudi 51, I-70125 Bari, Italy

Chenopodium album is a worldwide-distributed plant species growing in disturbed habitats. It

is an abundant and very competitive weed in spring-sown crops, particularly if they retain an
open structure for a relatively long period. In most crops it is currently controlled by
herbicides. In some crops, such as maize, chemical control is difficult, because C. album has
become resistant to these herbicides. In other crops, such as sugar beet, the use of herbicides
could be reduced considerably if selective control of C. album were possible. Recent
experiments using the fungus Ascochyta caulina as a microbial herbicide to control C. album
are encouraging (up to 70% control under field conditions). Within the framework of a
COST action on ‘Biological Control of Weeds in Europe’, five countries have cooperated in
developing a biological control method for C. album. To integrate the biological control of C.
album in existing weed management systems is one of the remaining challenges.
Keywords: Chenopodium album; Ascochyta caulina; biological control; microbial herbicide.

The weed problem caused by Chenopodium album
Description of the weed, its distribution and habitats
Chenopodium album L. (Chenopodiaceae) is an erect, pale-
green annual plant, varying in height from a few
centimetres to 2 m and sometimes even up to 3 m. It is
strongly taprooted. The stems are smooth, often having
ascending, angular or ridged branches. The leaves are
simple, alternate, ovate to lanceolate, regularly dented, 1.5–
8 cm in length and 0.5–3 cm broad. The inflorescence is a
spiked panicle in the leaf axils or at the termini of stems
and branches, with small dense flower clusters crowded on
the branches. The seeds are lens-shaped, black or light
brown in colour and approximately 2 mm in diameter. The
taxonomic features in this polymorphic species could be
correlated to its physiological properties such as herbicide
resistance (e.g. Arlt and Jüttersonke, 1990).
There is no specific system of seed dispersal, so most
seeds fall on the soil next to the mother plant. The black
seeds but not the brown are dormant. Seeds that mature
under long-day conditions are far more dormant than the
seeds collected from plants grown under short-day
conditions (Gutterman, 1985). Low temperatures or alter-
nating high and low temperatures will break the dormancy.
Germination usually occurs in spring. A short photoperiod
hastens flowering and maturity. Germination in summer
may result in tiny plants that flower and produce a few
seeds.
1353–5226 # 1997 Chapman & Hall
Chenopodium album is reported to be one of the 12
most successful colonizing species (Allard, 1965). It is
found from 70 8N to more than 50 8S and from sea level
up to 3600 m (Holm et al., 1977). It grows in all inhabited
areas except in extreme desert climates. It thrives on all
soil types and over a wide range of pH values (Andreasen
et al., 1991). It occurs in habitats that have been opened
up by disturbances. These include crop land, set-aside land
and ruderal vegetations. It is rated as one of the most
abundant species in a number of spring-sown crops in
Europe (Schroeder et al., 1993).
Chenopodium album as a weed in crops: an opportunity for
biological control
Chenopodium album has frequently been reported to be
troublesome in sugar beets, potatoes, maize, cereals and
vegetables all over the world (Holm et al., 1977). These are
sensitive to competition from a few weeks after sowing until
closing of the canopy. In most crops it is currently controlled
by herbicides. In maize and some vegetable crops C. album
is relatively insensitive or has become resistant to the triazine
herbicides that are often used in these crops (e.g. Solymosi et
al., 1986; Kees and Lutz, 1991; Myers and Harvey, 1993). A
selective biological control method comes to view as a
possible solution to the problem caused by this weed. In
other crops the availability of selective control of C. album
would reduce the use of herbicides considerably. An example
72
is sugar beet. The current practice is to control the weeds
shortly after the emergence of the crop with a mixture of a
soil herbicide (metamitron) and a foliar herbicide (phenme-
dipham). Depending on the weed density, the foliar
application is repeated once or twice. These herbicide
treatments may be omitted and replaced by one mechanical
cleaning. However, C. album is then often the only emerging
weed. Thus, a selective control method that reduces or
prevents competition of C. album with the crop and that can
be implemented in integrated pest management (IPM) is
required for adequate weed control. Biological control could
provide such a selective control. Because the time that is
available to prevent competition is short, inundative use of
the biocontrol agent will probably be needed. A plant
pathogen used as a microbial herbicide will provide a good
opportunity. Alternatively, an isolated phytotoxin from a
plant pathogen might be used as a selective herbicide
(Strobel et al., 1991).
Within the framework of an action of the European
Cooperation in the field of Scientific and Technical
Research (COST) on ‘Biological Control of Weeds in
Europe’ (Anonymous, 1992), five countries cooperated in
developing a biological control method for C. album.
Weed–Pathogen interactions
Focus on Ascochyta caulina
During a limited survey in The Netherlands, three
pathogens from C. album were identified (Scheepens,
1979): Ascochyta atriplicis (renamed Ascochyta caulina
by Van der Aa and Van Kesteren (1979)), Cercospora
chenopodii (Ellis, 1976) (synonym of Cercospora dubia, cf.
Brandenburger, 1985) and Peronospora farinosa f. sp.
chenopodii. The latter was never regarded as a serious
candidate for biological control, because downy mildew
fungi can thus far only be grown on living host plants or
tissue cultures and no methods are available to store the
spores for a prolonged time. Cercospora dubia was able to
reduce the plant dry weight of C. album by 20% at the most
4 weeks after inoculation (P.C. Scheepens, unpublished
data). After inoculation with a mixture of spores and
mycelium, the plants had formed new leaves before necrosis
developed. In the USA, similar results were obtained with a
local strain of this fungus (Winder and Van Dyke, 1985). A
larger potential as a biochemical agent was attributed to A.
caulina, because it could kill its host within 1 week under
appropriate conditions (Scheepens, 1979). Due to the
encouraging results, later efforts on the biological control
of C. album were focused on this pathogen.
Ascochyta caulina is described on Chenopodium and
Atriplex species in many countries in Europe and Asia
(Van der Aa and Van Kesteren, 1979). In North America, a
closely related pathogen, Ascochyta hyalospora, was found
(Allan et al., 1986). Knowledge of the life cycle of A.
caulina is incomplete. The natural occurrence of necrotic
Scheepens et al.
spots is not frequently observed until late summer. Under
moist conditions pycnidia develop on these necrotic spots.
If the conditions remain wet, a slimy mass containing two-
celled conidia is secreted from the pycnidia. Like all fungi
producing pycnidia, the conidia are dispersed by splashing
water droplets. The conidia may infect the leaves and
stems and give rise to new necrotic lesions. A teleomorph
of the fungus has not been found. The fungus may
overwinter as pycnidia or mycelia on decaying plant
residues (not observed yet) or as mycelia in seeds
(Kempenaar et al., 1995).
Factors that influence disease development by A. caulina
The natural build up of inoculum by A. caulina is too slow
to result in substantial growth reduction or even the
mortality of C. album as is needed for control of the weed.
To estimate the potential of this fungus as a mycoherbicide
the factors that may influence infection and disease
development have to be elucidated. According to Holcomb
(1982), such factors may be related to the pathogen, to the
host or the interaction between the host and pathogen. The
pathogen-related factors that have been studied for A.
caulina are the inoculum production, host range and
virulence. The host-related factors are the susceptibility of
C. album and other species, the degree of susceptibility of
the plant stages and the host genotypes of C. album. The
influence of spore density, additives to spore suspension and
the environmental factors temperature and wetness duration
on the host–pathogen interaction have been investigated
(Kempenaar et al., 1996a).
The lack of availability of the inoculum at the time that
weed control is needed is easily overcome by artificial
inoculation. The conidia of A. caulina are readily
produced in the pycnidia on artificial substrates
(Kempenaar, 1995). By drying cultures on a wheat bran
medium and subsequent storage of the dried cultures at
5 8C, spores remained viable for at least 1 year. This
method ensured the availability of spores for inoculum
experiments throughout the year. Fermentation in a liquid
medium, which would be more attractive for production on
a much larger scale, has not yet been investigated.
The germination of the conidia and infection of C.
album leaves and stems take place only if certain moisture
requirements are met. At temperatures between 18 and
30 8C during the light period and 12 8C during the dark
period, a minimum wetness period of at least 8 h is
necessary for the conidia to germinate and to penetrate the
host tissue. Under these temperature regimes, a wetness
period of more than 24 h was needed to obtain the
maximum degree of necrosis (Kempenaar et al., 1996a).
At 6 8C during the dark period, the maximum rate of spore
germination was not reached even after 32 h. Disintegrat-
ing cells in the leaf tissue become visible after 48 h and
at 72 h necrosis can be observed macroscopically
(Kempenaar et al., 1996a). Eggers and Thun (1988) found
Biological control of C. album 73

a similar moisture requirement for another isolate of A. Phytotoxins produced by A. caulina

caulina and they even doubted whether this requirement
would be met under field conditions.
At a conidia density of 107 mÿ2 or less, necrotic spots
of only a few millimetres in diameter developed. Fungal
growth was restricted to the necrotic areas. In contrast, on
detached leaves the fungus grows rapidly without obvious
limitations. At densities of a magnitude higher, large areas
of the leaves and stems become necrotic. As a result of
inoculation, the plants either died or resumed to develop
healthy new leaves after several days. The degree of
necrosis was also increased by the interaction betweeen the
conidia density and added surfactant (Sylgard 309) and
nutrients (Czapek broth supplemented with yeast extract)
to conidia suspensions. The effect on the plant depends on
the growth stage, the smallest plants being the most
vulnerable (Eggers and Thun, 1988; Kempenaar et al.
1996a). The results of Eggers and Thun (1988) suggest
that older leaves become resistant to infection. According
to Kempenaar et al. (1995), the fungus can infect the
leaves and flowers of C. album during the flowering stage.
Infection during early flowering resulted in complete death
of the plant. Their observations, together with findings for
other Ascochyta species (Maden et al., 1975; Hagedorn,
1984; Gossen and Morrall, 1986), indicate that at this
stage the fungus infects the flowers and the scars left by
the flower leaves.
Ascochyta is a well-known toxin-producing genus. Members
of this genus produce a range of phytotoxin compounds,
such as cytochalasins (Vurro et al., 1992), pinolidoxins
(Evidente et al., 1993) and solanopyrones (Alam et al.,
1989), that are chemically diverse and possess a broad
range of biological activities. Phytotoxins might well be
responsible for the necrosis development of C. album plants
by A. caulina.
Culture filtrates, obtained from growing A. caulina on a
semi-synthetic liquid medium, were assayed for their
phytotoxic properties using leaf and seedling assays. In
the leaf assay, large necrotic spots similar to those caused
by the pathogen appeared after 2–3 days. In the seedling
assay, necrosis developed after 2 days, mainly on the edges
of the leaves. The stems were not affected, indicating
translocation and accumulation of the compounds in the
leaves. Analysis of partially purified culture filtrate
indicates the presence of at least one toxic compound
with a hydrophilic nature and a molecular weight less than
3500 kDa. The chemical and biological characterization of
the phytotoxin(s) is in progress.
Host range of A. caulina
The host range of A. caulina appears to be more or less
confined to Chenopodium and Atriplex species (Table 1).

Table 1. Development of necrosis on plants of different taxa 1 week after the

application of spores of A. caulina (after Kempenaar et al., 1996a)
Plant taxon Cultivar Necrosisa
Atriplex patula L. ‡
Atriplex prostrata Boucher ex DC. ‡
B. vulgaris spp. vulgaris Carla ÿ
Lucy ÿ
Univers ÿ
Kyros ÿ
Egyptische platte ronde ÿ
Brassica oleracea L. sp. capitata ÿ
C. album ‡
Chenopodium ficifolium Sm. ‡
Chenopodium glaucum L. ‡
Chenopodium polyspermum L. 6
C. quinoa Elsevier ‡
Wild type 6
Chenopodium rubrum L. ÿ
Corispermum marschallii Stev. ÿ
Pisum sativum L. Eminent ÿ
S. oleracea Amsterdams reuzenblad ÿ
Martine 6
Triticum aestivum L. Arminda ÿ
Zea mays L. Brazil ÿ
Mandigo ÿ
a
ÿ, no necrosis; 6, less then 10% of the leaf area; ‡, between 10 and 35%.
74 Scheepens et al.

Beyond plants of these two genera, a small degree of
susceptibility was found on one cultivar of Spinacea
oleracea L. Another cultivar of S. oleracea, some other
species of Chenopodiaceae including several cultivars of
Beta vulgaris L. and species belonging to other families
were resistant to the isolate of A. caulina tested by
Kempenaar et al. (1996a).
Status of biological control of C. album by A. caulina
Three strategies to control C. album by A. caulina related
to the growth stage of the weed can be envisaged: control of
seedlings before emergence, control of juvenile plants and
control of flowering plants (Kempenaar, 1995).
From a practical point of view, the post-emergence
application of the biocontrol agent before the onset of
weed competition with the crop is the most attractive
strategy. Several field experiments to control C. album in a
sugar beet and a maize crop were conducted by
Kempenaar et al. (1996b). The application of A. caulina
on C. album plants planted in crop rows resulted in the
necrosis of C. album, but not of the respective crop. The
mean fractions of necrosis 1 week after application varied
from 0.35 and 0.75. The mortality after 3 weeks, relative
weed dry weight at harvest of the crop and yield reduction
of the crop are shown in Table 2. In the weed-free control,
the crop yields were 2021 g mÿ2 in 1992 (maize, above-
from the day on which the fungus was no longer active
(Kempenaar et al., 1996b). In a sugar beet crop, some C.
album plants became higher than the sugar beet plants,
resulting in severe competition for light and a yield
reduction of the crop plants.
The control of mature plants of C. album by A. caulina
was investigated in the same fields as the control of
juvenile plants in the previous paragraph. Control of the
mature plants may be useful both in preventing inter-
ference with harvesting of the crop and seed setting.
Alternatively, it may be used in long-term control
strategies of C. album, as well as on temporary set-aside
land or in field margins. The reduction or prevention of
the seed production of C. album by A. caulina in the
experiments of Kempenaar et al. (1996b) was influenced
by the weather conditions, growth stage of the weed and
the presence of a maize crop. The seed production in a
maize crop is shown in Fig. 1. Application at the
beginning of the flowering period resulted in abortion,
whereas application at the end of the flowering period had
no effect on the seed production.
12000
107 spores ml21
Untreated

ground biomass) and 1609 g mÿ2 (maize) and 2422 g mÿ2

Seeds per 4 plants

9000
in 1993 (sugar beet, aboveground plus storage organs). The
aboveground biomasses of C. album in the untreated
6000
controls in these experiments were 190, 264 and
1072 g mÿ2 , respectively. The mortality of C. album was
influenced by the experiment and by extension of the leaf 3000
wetness period in one of the three experiments. After 3
weeks, visible symptoms of the disease had disappeared.
The weed plants that survived the attack were reduced in 0
A B C
biomass. Crop yield reductions occurred in a sugar beet
Plant stage at inoculation
crop, but not in a maize crop. Comparing the growth rates
of the weed and crop at different dates between the Fig. 1. Seed production of C. album plants after treatment with A.
application of the fungus and the final yield date indicates caulina at (A) the beginning, (B) the mid-flowering or (C) the end
that the maize crop suppresses the weed to a large extent of the flowering period (Kempenaar et al., 1995).

Table 2. Results of field experiments to control C. album with A. caulina (after Kempenaar, 1995)
Mortality of C. album (growth Yield reduction of crop (potential
Crop and year Weather shortly after applicationc reduction)a (%) yield reduction)b (%)
Maize 1992 Cloudy,
showery 30 (79) 0 (19)
showery (‡24 h)
Cloudy, 50 (95) 0 (19)
Sugar beet 1993 Cloudy,
one shower 5 (43) 50 (73)
one shower (‡16 h)
Cloudy, 30 (66) 30 (73)
one shower (‡28 h)
Cloudy, 50 (80) 19 (73)
Maize 1993 Cloudy,
showery 70 (90) 0 (20)
a
Reduction in C. album dry weight mÿ2 , expressed as percentage of untreated controls.
b
Yield reduction on untreated controls, expressed as a percentage of weed-free controls.
c
Extension of wetness period (number of hours in parentheses).
Biological control of C. album
The control of C. album by pre-emergence application
of A. caulina has the advantage that it is less dependent
on the high humidity of the atmosphere. It was
investigated in pot experiments in the greenhouse
(Kempenaar et al., 1996c). Conidia suspensions were
either mixed through the top layer of the soil or sprayed
on the soil. Non-sterile soils were used in the experiments.
Ascochyta caulina had no effect on the emergence rate of
C. album, but it caused disease and mortality of the
seedlings shortly after emergence. The disease incidence
and severity and mortality were influenced by the conidia
density, soil type and soil moisture content. We estimated
that 109 –1010 conidia mÿ2 were required for 50%
mortality of emerged C. album.
Outlook
The market for a microbial herbicide to control C. album
The biological control of weeds by applying indigenous
plant pathogens as microbial herbicides may become an
important component of IPM, resulting in less use of
chemical herbicides. So far, the commitment of private
industry in the development of microbial herbicides has
been limited. Potential manufacturers mostly mention
commercial factors as limiting, not the lack of efficacy of
the control agents (Greaves and McQueen, 1991; Rodgers,
1993). The microbial herbicides available supply only
small, regional markets. A microbial herbicide against C.
album based on A. caulina would have a much larger
market. Chenopodium album is a widely distributed,
noxious weed in field crops such as maize, potatoes, sugar
beets and vegetables and ornamentals such as tulips and
other flower bulbs. It is a noxious weed in these crops
because the existing weed control strategies have a
weakness against C. album. Regarding the limited host
range of A. caulina, it will be safe to use in all crops except
S. oleracea and Chenopodium quinoa Willd.
Liquid culture filtrates and chromatographic fractions of
A. caulina showed toxic effects similar to the symptoms
caused by the pathogen itself, suggesting the involvement
of toxins in disease development. The fast appearance of
large necrotic spots on the host leaves justifies further
investigations on the possible practical use of these
metabolites alone or as synergists together with the
pathogen against C. album.
Critical issues for the further development of A. caulina as
a microbial herbicide
Under field conditions, a mortality rate of 70% of C. album
plants and a substantial growth reduction of the surviving
plants have been achieved by one application of A. caulina
(Kempenaar et al., 1996b). This level of control appears to
be sufficient in competitive crops such as maize, but a
higher efficacy will be necessary in less competitive crops.
The results in the field were achieved with only one isolate
75
of A. caulina. A small test in the laboratory with two
additional isolates suggests the existence of considerable
variation in virulence between the isolates. The first option
to increase the efficacy will be a survey for more virulent
isolates in the whole distribution range of the fungus. An
alternative approach would be the addition of synergists that
decrease resistance in the host plant (Sharon et al., 1992).
The variability in the environmental conditions is too
great to ensure enough efficacy at any time. In particular,
the need of A. caulina and most other fungi for a
prolonged period of high humidity shortly after application
is very critical. The selection of fungal strains that are
adapted to adverse weather conditions might be an option
to overcome the environmental constraints. The correct
timing of application is primarily determined by the need
to reduce the competitiveness of the weed and it might be
difficult to obtain the right weather for application in that
period. As irrigation of the crop is not possible or not
realistic in many cases, formulation will be the option to
create the right environment in which spores of the agent
organism can germinate and infect the host plant (e.g.
Womack et al., 1996).
Biological control of C. album and IPM
In most situations, C. album is not the only non-crop
species present. If C. album is controlled selectively, plants
of other species may replace it. Although they will in
general not be as competitive as C. album, in large numbers
they can be damaging to the crop. Biological control as a
single measure is not meaningful to farmers; instead an
integrated approach to control all the weeds in a given crop
should be used. Such an approach may include mechanical
control and chemical control of other species. In both sugar
beet and maize, mechanical weed control (harrowing) up to
the two-leaf stage of the crop could replace the application
of a soil herbicide. Massive emergence of C. album is
expected after that time. A microbial herbicide based on A.
caulina could be used to control this weed. If seeds of other
weeds germinate as well, the fungus may be tank mixed
with half the regular dose of a sulphonyl ureum herbicide.
It should be ensured that the biological control is
compatible with other measures in a cropping system. For
instance, in a potato crop the application of fungicides
could interfere with the control of C. album by A. caulina.
In that case, the timing of the fungicide application or the
use of selective fungicides that do not inhibit A. caulina
could solve the incompatibility problem.
In maize and sugar beet crops, no fungicides are usually
applied at all, so no compatibility problems with myco-
herbicides will arise.
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