Crop Protection 87 (2016) 44e49

Contents lists available at ScienceDirect

Crop Protection
journal homepage: www.elsevier.com/locate/cropro

Bioherbicides: Dead in the water? A review of the existing products

for integrated weed management

phane Cordeau a, b, *, Marion Triolet a, Sandra Wayman b, Christian Steinberg a,
Ste
Jean-Philippe Guillemin a
a
Agro

ecologie, AgroSup Dijon, INRA, Univ. Bourgogne, Franche-Comt
e, 21000, Dijon, France
b
Cornell University, Soil and Crop Sciences Section, Ithaca, NY, 14853, USA

a r t i c l e i n f o a b s t r a c t

Article history: The intensive use of synthetic herbicides is questioned for many reasons. Bioherbicides, as integrated
Received 3 February 2016 weed management tools, however, have the potential to offer a number of benefits such as increased
Received in revised form target specificity and rapid degradation. Despite the efforts to identify effective bioherbicide agents in
13 April 2016
laboratory and field, only thirteen bioherbicides are currently available on the market. Since 1980, the
Accepted 22 April 2016
Available online 1 June 2016
number of biopesticides has increased around the world, while the market share of bioherbicides rep-
resents less than 10% of all biopesticides. Nevertheless, weed management implemented at the cropping
systems scale needs bioherbicides because of legislation to drive weed management away from heavy
Keywords:
Bioherbicides
reliance on chemicals, the global increase in organic agriculture, the need of both organic and conven-
Mycoherbicides tional agriculture to increase weed control efficiency, concerns about herbicide resistance, and concern
Micro-organisms from the public about environmental safety of herbicides. Consequently, we review here the existing
Natural substances products on the market and describe their history, mode of action, efficacy and target weeds. This review
Integrated weed management is unique because we also discuss the role of bioherbicides in integrated weed management: to manage
Agroecology soil weed seedbanks with seed-targeted agents in addition to primary tillage, to increase the efficacy of
mechanical weeding because bioherbicides are more effective on seedlings, to increase the suppression
effect of crop cultivars by first slowing weed growth, to terminate cover crops particularly in conser-
vation agriculture, and finally to manage herbicide resistant populations.
© 2016 Elsevier Ltd. All rights reserved.

1. Introduction
Crop losses due to weeds continue to reduce available produc-
tion of food and cash crops worldwide (Cramer, 1967; Oerke et al.,
1994; Oerke, 2006) even if weeds are known to support ecosystem
services in farming landscapes (Marshall et al., 2003). Strategies of
weed management can vary, but now mainly rely on the use of
synthetic herbicides (Thill et al., 1991). The intensive use of syn-
thetic herbicides in the last fifty years has considerably increased
productivity, but with striking environmental and ecological im-
pacts (Soule et al., 1990; Stoate et al., 2009), which have been
identified for many decades (Wauchope, 1978).
The heavy reliance on synthetic herbicides to control weeds has
been questioned for many decades, and is still being questioned, as
* Corresponding author. INRA, UMR1347, Agroe
cologie, 17 rue Sully, BP 86510, F-
21065, Dijon cedex, France.
E-mail address: stephane.cordeau@dijon.inra.fr (S. Cordeau).
the issues caused today are even more significant. Of the 15 mol-
ecules coming from plant protection products found in streams and
rivers in France in 2012, the most frequently found were herbicides
or their metabolites (French Ministry of Ecology Sustainable
Development and Energy, 2015). Consequently, the French and
European legislation has pulled many products or active in-
gredients from the market (Barzman and Dachbrodt-Saaydeh,
2011; Chauvel et al., 2012). Thus farmers have to manage weeds
with even fewer chemical tools that often contain only one active
ingredient (or one chemical family) and which favour the occur-
rence of phenological adaptations (Mortimer, 1997) and resistant
genotype selection (Chauvel et al., 2001). The emergence of resis-
tant individuals among weed populations is an increasingly
important issue worldwide (Heap, 1997) and weed management
strategies must change to face this issue (Colbach et al., 2016).
Weed management faces the same issues as in the two past
decades, i.e. yield losses (Oerke, 2006), reliance on synthetic her-
bicides (Chauvel et al., 2012), herbicide resistance (Chauvel et al.,

http://dx.doi.org/10.1016/j.cropro.2016.04.016
0261-2194/© 2016 Elsevier Ltd. All rights reserved.
 S. Cordeau et al. / Crop Protection 87 (2016) 44e49
2001), etc. Weed management also faces new challenges, particu-
larly because agriculture worldwide faces increasing economic,
environmental and social pressures (Lechenet et al., 2014; Petit
et al., 2015). Sustainable weed management is especially impor-
tant in the context of these pressures because ideal cropping sys-
tems could: allow farmers to be economically sustainable, decrease
agriculture's environmental impact, and respond to the social
pressures from the public about food safety and security.
Sustainable weed management is one of the main challenges for
both organic agriculture and conventional agriculture. Future weed
management has to consider new tools, in addition to those
existing, as a part of integrated weed management. Bioherbicides
are currently underused for many reasons (Ash, 2010; Auld and
Morin, 1995), although we will not detail them here. Even though
research has long been conducted on weed biocontrol, few
biocontrol products have actually been launched on the market.
Bioherbicides should be reconsidered as a tool for integrated weed
management because: (i) legislation will drive a move from
chemical weed management to new options; (ii) the extent of
organic agriculture is increasing throughout the world and needs
new tools to diversify the selection pressure on weeds and increase
in weed control efficiency; (iii) both certified organic agriculture
and conventional conservation agriculture need tools to manage
weeds and reduce their reliance on synthetic herbicides; (iv) her-
bicide resistance will be one of the biggest challenges in the next
decades; (v) finally, public concern about environmental safety of
herbicides has increased interest in developing effective
nonchemical weed management methods. Consequently, we pro-
vide here a short review of the existing bioherbicides on the market
and perspectives on the integration of bioherbicides in cropping
systems for integrated weed management.
2. Biocontrol
Using biocontrol for pest management consists of applying the
natural interactions that drive inter-species relationships to the
control of the balance of pest populations, rather than on their
eradication (Herth, 2011). Biocontrol products represent an array of
tools to be used alone or in association with other plant protection
methods (Herth, 2011). We consider biocontrol agents to be cate-
gorized into four groups: macro-organisms (e.g. predators, para-
sitoid insects, nematodes), micro-organisms (e.g. bacteria, fungi,
viruses), chemical mediators (e.g. pheromones) and natural sub-
stances (originated from plant or animal). Among these four cate-
gories, the last three belong to plant protection products, which fall
under the 1107/2009/CEE European regulation (Villaverde et al.,
2014).
Micro-organisms, macro-organisms, and natural substances are
the most investigated biocontrol agents for weed control (Hinz
et al., 2014; Zimdahl, 2011). In our review, only micro-organisms
and natural substances will be considered. Micro-organisms can
be fungi, bacteria or viruses, whereas natural substances are
derived from plants, animals or minerals. A review of the scientific
literature on the existing products on the market reveal that
biocontrol agents targeting weeds are weakly developed compared
with biocontrol agents targeting other pests and diseases.
3. Bioherbicides
Bioherbicide products are adapted from natural substances
already present in the environment, so they are expected to be
more environment-friendly. The half-life of bioherbicides is usually
shorter than that of chemicals (Duke et al., 2000). However, that a
product is naturally derived does not mean it is actually harmless.
Certain natural toxins produced by plants or micro-organisms are
45
present in the environment and can be a danger to animals,
including mammals. The activity spectrum of natural toxins should
be carefully evaluated (Duke et al., 2000).
3.1. Definition
In 1971 bioherbicides were defined as substances intended to
reduce weed populations without degrading the environment
(Conseil International de la Langue Française, 1971). Since then
their definition has evolved. According to Bailey (2014), bio-
herbicides are products of natural origin for weed control. Bio-
herbicide products can be either living organisms, and more
specifically micro-organisms, or products derived from living or-
ganisms, including the natural metabolites produced by these or-
ganisms in the course of their growth and development.
3.2. Modes of action
The mode of action of bioherbicides is similar to plant-pathogen
interaction mechanisms and allelopathy (Harding and Raizada,
2015). In the case of plant-pathogen interactions, the biocontrol
agent has to circumvent the weed's defense reactions. The rela-
tionship between the two individuals has to be compatible for the
pathogen (i.e., the biocontrol agent) to be able to infect the target
plant (Andanson, 2010). Different virulence factors are directly or
indirectly involved in this infection process. Firstly, the agents could
be enzymes that degrade plant cell walls (pectinases, cellulases,
ligninases, etc.), proteins and lipid membranes (proteases, pepti-
dases, amylases, phospholipases, etc.). They make it easier for the
biocontrol agents to get into and/or spread onto the host plant
(Ghorbani et al., 2005). Secondly, the agents could be phytotoxic
secondary metabolites and peptides that act as toxins that interfere
with plant metabolism (Stergiopoulos et al., 2013). The mecha-
nisms behind this metabolism interference have mainly been
demonstrated in crops, rather than weeds, because too few studies
have been devoted to weed-pathogen interactions including para-
sitic plants (Vurro et al., 2009). These toxins directly or indirectly
modify the expression of one or more genes which then lead to
plant death (Vincent et al., 2012; Torres et al., 2016). Toxins inter-
fere with a specific compound in the plant (an enzyme, a receptor,
etc.), so if this compound is missing or altered there is no toxic
effect (Xie et al., 2013). Therefore toxins and/or their molecular
targets are key determinants to characterize a host/pathogen range
(Hoagland et al., 2007; Daguerre et al., 2014). In the case of alle-
lopathy, only molecules extracted from plants or micro-organisms
are involved. This type of control corresponds to growth inhibi-
tion events that occur in certain agriculture fields. Allelopathy is
defined as “a negative or positive effect of chemical compounds
produced by the secondary metabolism of plants or micro-
organisms, and that have an influence on the growth and devel-
opment of biological and agricultural ecosystems (except mam-
mals)” (de Albuquerque et al., 2011). A well-known example is
hydroxamic acid, produced by maize (Collantes et al., 1998).
These different modes of action of microbial and plant origin
provide an outstanding diversity of biochemical compounds that
make it possible to target a large number of molecular sites in
weeds (Duke et al., 2000). Thus the possibilities for bioherbicide
use are wide and should be taken advantage of. Depending on the
biological origin of the bioherbicide, its efficiency will be influenced
by the specificity and virulence of its biocontrol agent, or on the
specificity of the natural substance. Moreover, for the bioherbicide
to be stored, marketed, handled and applied, it has to be formulated
with co-formulants, the compositions of which are not systemati-
cally made public, but which ensure that the product will have an
effective mode of action. Additional factors that bioherbicide action
46 S. Cordeau et al. / Crop Protection 87 (2016) 44e49
depends on include dose, phenological stage of the target, and
environmental conditions, including hygrometry (Ghorbani et al.,
2006; Hallett, 2005). Recently, natural molecules such as phos-
phinothricin, a biosynthetic version of glufosinate, and bialophos, a
microbial phytotoxic product, have made it possible to design
commercial bioherbicides (Duke et al., 2000). Leptospermone,
identified in 1977 for its herbicide properties, is a tricetone that has
been used to create numerous highly active chemical analogs such
as Sulcotrione® (Duke et al., 2001) and Mesotrione® (Mitchell et al.,
2001). These products are not bioherbicides per se, but they were
synthesized and produced based on natural molecules. They
represent only a small share of marketed herbicides, but they act on
different molecular targets. Pure natural tricetones can be easily
extracted from plant essential oils, simply using sodium hydroxyde.
However, synthetic products have been more common thus far
because they are chemically more stable and less volatile.
Although a growing number of authors have reviewed bio-
herbicides (Bajwa et al., 2015; Harding and Raizada, 2015), unfor-
tunately most studies do not attempt to understand the modes of
action that drive the interactions between micro-organism or
molecule and target plants; these studies also fail to address the
ecotoxicological impact of the bioherbicide (Fumagalli et al., 2013).
Yet such information would allow us to optimize the conditions of
bioherbicide application and encourage bioherbicide use. From a
regulatory point of view, it is preferable although not required, to
explain the mode of action of a bioherbicide for it to be authorized.
4. Currently marketed products
On a global scale, only thirteen bioherbicides derived from
micro-organisms or natural molecules are currently available on
the market. The first bioherbicides were marketed in the 1980s.
Since 1980, the number of biopesticides has increased around the
world, while the market share of bioherbicides represents less than
10% of all biopesticides (i.e. biofungicides, biobactericides, bio-
insecticides, and bionematicides) (Charudattan, 2001). Only a few
countries like the USA (n ¼ 4 bioherbicides available), Canada
(n ¼ 3), and the Ukraine (n ¼ 1) have bioherbicides on their markets
(Bailey, 2014). Since 2015, following the authorization of the new
herbicide Beloukha® in Europe, France is now part of the countries
that have at least one bioherbicide on their market. Among the
thirteen authorized bioherbicides, nine are based on fungal micro-
organisms, three on bacterial micro-organisms, and one contains
an active substance that is a natural plant extract.
Devine™ (1981) was produced by Abott Laboratories in the USA
(Kenney, 1986). It contains strain MVW of the oomycete Phytoph-
thora palmivora Butler. This bioherbicide was authorized to control
the weed Morrenia odorata (Hook. & Arn.) Lindl. in citrus crops.
However, since 2006 it is no longer available on the market.
Collego™ (1982) is produced in the USA by Upjohn Co (Bowers,
1986). Its activity results from spores of the ATCC (American Type
Culture Collection) 20358 strain of Colletotrichum gloeosporioides
f.sp. aeschynomene. This bioherbicide targets Aeschynomene vir-
ginica (L.) B.S.P. In 1997, the Environment Protection Agency (EPA)
re-evaluated Colletotrichum gloeosporioides f.sp. aeschynomene,
strain ATCC 20358, according to more recent standards. In 2006,
Collego™ became LockDown®.
BioMal® is a bioherbicide whose active agent is Colletotrichum
gloeosporioides f.sp. malvae (c.g.m.) ATCC 20767 (Boyetchko et al.,
2007). This biocontrol agent was registered as a bioherbicide in
Canada by Philom Bios Inc. in 1992. This bioherbicide is used to
control Malva pusilla Sm.in crops. In 1994, production and sales
were interrupted due to production and marketing costs. The
evolution of market conditions and the introduction of three new,
less costly, chemical herbicides put an end to the marketing of
BioMal®. In 2006, the Pest Management Regulatory Agency (PMRA)
re-evaluated the bioherbicide on the basis of new applicable
standards. However, in the absence of an industrial partner, the
registration validity period has expired.
Woad Warrior®, designed by Dr. Sherman Tomson in the USA,
was authorized in 2002. The active agent of this bioherbicide is the
fungus Puccinia thlaspeos C. Shub., that controls the weed Isatis
tinctoria L. This product is not available on the market, except to the
laboratory of the University of Utah by request only.
The bioherbicides Mycotech™ and Chontrol® Pastes were
derived from the fungus Chondrostereum purpureum (Fr.) Pouz.
These products were launched to control shoots from Prunus
serotine Ehrh. stumps and Populus euramericana Guinier in the
sandy soils of conifer forests. Myco-Forestis Corporation registered
Chondrostereum purpureum strain HQ1 under the name of Myco-
tech™ in 2002 in Canada and in 2005 in the USA. Chontrol® Pastes
was elaborated from strain PFC 2139 of the fungus C. purpureum
isolated from apple tree in 2004 (Hintz, 2007). The registration
period of Mycotech™ expired in 2008 and is therefore no longer
available on the market in France. However, Chontrol® Pastes is still
available in the USA and Canada.
The active principle of Smoulder® is the fungus Alternaria des-
truens L. Simmons, strain 059. This fungus is a pathogen of plants of
the Cuscuta genus. It controls several species of dodders that infest
different crops such as alfalfa, carrot, cranberry, sweet pepper, to-
mato, eggplant, cornflower, and ornamental ligneous plants. This
bioherbicide was discovered and developed by Dr. Tom Bewick at
the Cranberry Experimental Station of the University of Massa-
chusetts. It was produced and registered by Loveland Products Inc.,
Greely CO, and Sylvan Bio Inc., Kittanning, PA, and authorized by
the EPA in 2005 (Bailey, 2014). This biocontrol agent is sold in solid
granular form (Smoulder G) and wettable powder form (Smoulder
WP).
The bioherbicide Sarritor® is composed of the fungus Sclerotinia
minor Jagger, strain IMI 344141 and controls dicot weeds in turf. The
fungus was discovered by Dr Alan Watson in Quebec (Steward-
Wade et al., 2002). The product was first registered in 2007 with
proviso and after supplementary studies it was finally fully
authorized in 2010. However, that same year a new bioherbicide
produced from chelated iron (hydroxy ethylenediamine triacetic
acid, FeHEDTA) was launched and as a result Sarritor® sales fell.
Phoma was granted provisional registration for use on golf
courses in Canada in 2011. In the USA, the product was fully
registered for the same use in 2012. This bioherbicide was initially
developed to control dicots in golf courses, agriculture and agro-
forestry. The product contains the fungus Phoma macrostoma, strain
94-44B (Bailey and Falk, 2011). It was discovered by Karen Bailey
and Jo-Anne Derby, from Agriculture and Agri-Food Canada, and
developed by The Scotts Company, USA.
The active principle ingredient of MBI-000 EP is thaxtomin A, a
compound that is produced by fermentation from the bacterium
Streptomyces acidiscabies, strain RL-110. MBI-005 EP is the com-
mercial product used to manage Taraxacum officinale F.H.Wigg. in
turf rolls composed of Poa pratensis L. and Festuca sp. (Pest
Management Regulatory Agency, 2013). It can also be used in
agriculture, nurseries, and golf courses. Streptomyces acidiscabies
has a broad pre-emergence activity spectrumdit kills adventitious
plants when they germinatedand selective post-emergence ac-
tivity on lawns and certain crops. MBI-005 was discovered and
developed by Marrone Bio Innovations Inc. A commercial product
based on MBI-005, Opportune®, is in the process of being marketed
following a favourable notice for registration in April 2012.
Camperico® was designed to control Poa annua L. in turf. Its
active agent is the bacterial strain Xanthomonas campestris JTP482
(Imaizumi et al., 1997). This bioherbicide was developed under the
 S. Cordeau et al. / Crop Protection 87 (2016) 44e49
commercial name Camperico® by Japan Tobacco Inc (Tateno, 2000).
although the firm has not launched it for sale so far.
Organo-Sol® is a mixture of several lactic acid bacteria involved
in the fermentation of dairy products (i.e. Lactoserum), which
produce citric acid and lactic acid. These bacteria are: Lactobacillus
casei, strain LTP-111, Lactobacillus rhamnous, strain LTP-21, Lacto-
bacillus lactis ssp. Lactis, strain LL64/CSL, Lactobacillus lactis ssp.
Lactis, strain LL102/CSL, Lactobacillus lactis ssp. Cremoris, strain
M11/CSL. Organo-Sol® controls Trifolium repens L. and Trifolium
pretense L., Lotus corniculatus L., Medicago lupulina L. and Oxalis
acetosella L. established in lawns. Organo-Sol® was authorized in
Canada in 2010 and is currently marketed under the name Kona™
by AEF Global. In 2014, AEF Global launched Bioprotec Herbicide™
(www.aefglobal.com). Bioprotec Herbicide™ is the same product as
Kona™, but is formulated differently for domestic use.
In 2015, a new bioherbicide, Beloukha®, was authorized as a
plant protection product to be placed on the market in Europe.
Beloukha® can be used on grapevine to kill suckers and control
weeds, and on potatoes to kill stems and leaves. In 2016/2017,
Beloukha® will be on the European market and then should be
authorized for markets in the USA and Japan. Beloukha® is derived
from rapeseed oil, using a natural extraction process. The extracted
molecules are nonanoic acid and pelargonic acid. Beloukha® is
distributed by Jade Co., a subsidiary of ALIDAD’Invest Group
(Nguyen et al., 2013). Applications are currently under study to
authorize its use in arboriculture and market gardening; Beloukha®
should be authorized soon. Finally, Katoun® (pelargonic acid),
intended for non-agricultural lands (weeding of green spaces: park
paths, public gardens, sidewalks), will be distributed by Syngenta
Co.
5. Bioherbicides as a tool for integrated weed management
Integrated Weed Management (IWM) is the control of weeds
through a long-term management approach by combining physical,
genetic, biological, cultural and chemical weed management
techniques (Swanton and Weise, 1991). Although none of the in-
dividual techniques on their own can be expected to provide
acceptable levels of weed control, if they are implemented in a
systemic manner, significant weed management results can be
achieved. Over the past decades, IWM researches have focused on
how to reduce the reliance on synthetic herbicides in cropping
systems. Combining several techniquesdsuch as the diversification
of crops, soil tillage before sowing, and mechanical in-crop wee-
dingdcould lead to a decrease in herbicide use while maintaining
acceptable weed management (Chikowo et al., 2009). Bioherbicides
could help increase both the efficacy of individual weed control
techniques and the overall efficacy of the IWM systems to manage
weeds.
5.1. Managing soil seed banks
Some soil micro-organisms target weed seeds (Davis et al.,
2006; Kremer and Kennedy, 1996); mortality of weed seeds in
soil could be increased by enhancing the soil biological activity
through improving soil quality (Gallandt et al., 1999). Persistence of
weed seeds in the soil seed bank could also be decreased by the use
of bioherbicides with seed-targeting agents (see the review of
Wagner and Mitschunas (2008)). Isolates of Fusarium solani were
identified to inhibit germination of Striga (Ahmed et al., 2001),
which is a noxious and economically important parasitic weed in
cereal crops (Bebawi and Eplee, 1986). Motlagh (2011) isolated
Epicoccum purpurascens Ehrenb from Echinochloa spp. and then
demonstrated a significant reduction of seed germination of this
noxious weed which emerges in summer cash crops like maize and
47
soybean. In conservation agriculture, where the use of tillage is
reduced, weed seeds are concentrated in the upper soil layer
(Clements et al., 1996; Yenish et al., 1992), which allows surface
applications of bioherbicide agents to be in close proximity to weed
seeds. Consequently, the potential for enhancing weed seed decay
may be much greater in no-till. In addition, the higher moisture
rates (Blevins et al., 1971) and more stable temperatures (Stoller
and Wax, 1973; Hatfield and Prueger, 1996) of no-till soil surfaces
are more conducive to the survival of applied bioherbicide agents.
5.2. Increasing the efficacy of mechanical weeding
Bioherbicide agents such as ‘deleterious rhizobacteria’ (DRB)
have typically been applied directly to soil or vegetative residues to
attack germinating seeds and emerging seedlings and to eventually
suppress weed growth (Kremer and Kennedy, 1996). Consequently,
these bioherbicide agents could help improve weed control in the
early growth stages of the cash crop, when in-crop mechanical
weeding is too risky. Second applications of bioherbicide agents
just after mechanical weeding could control later emerging co-
horts, which often emerge after the pass of a rotary hoe or a tine
weeder (Melander et al., 2005). Mechanical weeding is most
effective when weeds are at the cotyledon or seedling stage.
Consequently, to achieve successful biocontrol of weed seedlings,
mechanical weeding should occur at the time when environmental
factors are conducive to bacterial growth before bioherbicides
should be sprayed on the soil surface. Ideally, the critical period for
weed control should overlap both with the critical period for
implementing mechanical weeding and with the critical period for
the environmental application requirements for the bioherbicide
agent.
5.3. Increasing the suppression effect of crop cultivars
The choice of crop varieties can be an IWM tool to compete with
weeds (Andrew et al., 2015). In both conventional and organic
agriculture farmers tend to choose cultivars by their weed sup-
pression potential. Bioherbicides could be considered an additive
tool to slow down the growth of weeds and increase weed:crop
competition in favour of the crop. Indeed, bioherbicide agents show
increasing efficacy for weed control when weeds suffer from crop
competition (Ditommaso et al., 1996; Kremer and Kennedy, 1996).
5.4. Terminating of cover crops
Cover crops could be used as a tool to suppress weeds (Teasdale,
1996) because they decrease weed emergence and reduce weed
growth (Cordeau et al., 2015). However, even if mechanical termi-
nation of cover crops is effective (Mirsky et al., 2013), chemical
herbicides (e.g. glyphosate)deither alone at full dose or at low dose
in addition to mechanical terminationdare often implemented.
Moreover, in continuous no-till systems, weed management is
reliant only on the use of chemical herbicides. In no-till cover crop
based systems (e.g. conservation agriculture, Bajwa (2014)), bio-
herbicides could be a tool for in-crop integrated weed management
as well as for cover crop termination, which would reduce the
reliance of these systems on the use of synthetic chemicals.
5.5. Managing herbicide resistant populations
Finally, integrated weed management is often utilized in the
management of herbicide resistant plant populations (Chauvel
et al., 2009; Owen et al., 2015). Herbicide resistance is now wide-
spread in many problematic weed species in crop production (Moss
et al., 2011), encouraged by the increasing dependence on a limited
48 S. Cordeau et al. / Crop Protection 87 (2016) 44e49
number of active ingredients (Chauvel et al., 2012). Bioherbicides
should be considered as a tool to diversify the selection pressure on
weeds, particularly when chemicals are not effective due to
resistance.
6. Conclusions
Despite the promise shown by many bioherbicides, however,
few have achieved long-term commercial success, in part due to
inconsistent performance in field conditions. Research, develop-
ment, and regulation are necessary to improve the number of
effective solutions on the bioherbicide world market. Given the
range of bioherbicide products presented in this review and the
opportunities to combine with other weed management tools, we
believe the use of bioherbicides should be an important step to-
wards sustainability in agriculture. Additionally, to increase the role
of bioherbicides in IWM, more assessments of the efficacy of bio-
herbicides in the field are necessary. Organic and integrated weed
management do not rely on any single weed management tech-
niques, unlike synthetic herbicides in conventional agriculture;
consequently, bioherbicides should be assessed concurrently with
other weed management techniques in cropping systems
experiments.
Acknowledgments
The literature and market review was financially supported by
INRA (French National Institute for Agricultural Research), Agrosup
(F-21000 Dijon, France) and De Sangosse (47480 Pont du Casse,
France). The authors are grateful to Annie Buchwalter, science ed-
itor and writer, for reviewing the manuscript.
References
Ahmed, N.E., Sugimoto, Y., Babiker, A.G.T., Mohamed, O.E., Ma, Y., Inanaga, S.,
Nakajima, H., 2001. Effects of Fusarium solani isolates and metabolites on Striga
germination. Weed Sci. 49, 354e358.
Andanson, A., 2010. Evolution de l'agressivite
des champignons phytopathoge nes,
couplage des approches the
orique et empirique (PhD). Universite
Nancy I.
Andrew, I., Storkey, J., Sparkes, D., 2015. A review of the potential for competitive
cereal cultivars as a tool in integrated weed management. Weed Res. 55,
239e248.
Ash, G.J., 2010. The science, art and business of successful bioherbicides. Biol.
Control 52, 230e240.
Auld, B.A., Morin, L., 1995. Constraints in the development of bioherbicides. Weed
Technol. 9, 638e652.
Bailey, K.L., 2014. In: Abrol, Dharam P. (Ed.), The Bioherbicide Approach to Weed
Control Using Plant Pathogens, Integrated Pest Management: Current Concepts
and Ecological Perspective. Elsevier (Academic Press), pp. 245e266.
Bailey, K.L., Falk, S., 2011. Turning research on microbial bioherbicides into com-
mercial products - a Phoma story. Pestic. Technol. 5, 73e79.
Bajwa, A.A., 2014. Sustainable weed management in conservation agriculture. Crop
Prot. 65, 105e113.
Bajwa, A.A., Mahajan, G., Chauhan, B.S., 2015. Nonconventional weed management
strategies for modern agriculture. Weed Sci. 63, 723e747.
Barzman, M., Dachbrodt-Saaydeh, S., 2011. Comparative analysis of pesticide action
plans in five European countries. Pest Manag. Sci. 67, 1481e1485.
Bebawi, F.F., Eplee, R.E., 1986. Efficacy of ethylene as a germination stimulant of
Striga hermonthica. Weed Sci. 34, 694e698.
Blevins, R., Cook, D., Phillips, S., Phillips, R., 1971. Influence of no-tillage on soil
moisture. Agron. J. 63, 593e596.
Bowers, R.C., 1986. Commercialization of COLLEGO - an industrialist view. Weed Sci.
34, 24e25.
Boyetchko, S., Bailey, K., Hynes, R., Peng, G., Vincent, C., Goettel, M., Lazarovits, G.,
2007. Development of the mycoherbicide, BioMal®. Biol. control a Glob. Per-
spect. 274e283.
Charudattan, R., 2001. Biological control of weeds by means of plant pathogens:
significance for integrated weed management in modern agro-ecology.
BioControl 46, 229e260.
Chauvel, B., Guillemin, J.-P., Gasquez, J., Gauvrit, C., 2012. History of chemical
weeding from 1944 to 2011 in France: changes and evolution of herbicide
molecules. Crop Prot. 42, 320e326.
Chauvel, B., Guillemin, J., Colbach, N., Gasquez, J., 2001. Evaluation of cropping
systems for management of herbicide-resistant populations of blackgrass
(Alopecurus myosuroides Huds.). Crop Prot. 20, 127e137.
Chauvel, B., Guillemin, J.P., Colbach, N., 2009. Evolution of an herbicide-resistant
population of Alopecurus myosuroides Huds. in a long term cropping system
experiment. Crop Prot. 28 (4), 343e349.
Chikowo, R., Faloya, V., Petit, S., Munier-Jolain, N.M., 2009. Integrated Weed Man-
agement systems allow reduced reliance on herbicides and long-term weed
control. Agric. Ecosyst. Environ. 132, 237e242.
Clements, D.R., Benott, D.L., Murphy, S.D., Swanton, C.J., 1996. Tillage effects on
weed seed return and seedbank composition. Weed Sci. 314e322.
Colbach, N., Chauvel, B., Darmency, H., De
lye, C., Corre, V.L., 2016. Choosing the best
cropping systems to target pleiotropic effects when managing single-gene
herbicide resistance in grass weeds. A blackgrass simulation study. Pest
Manag. Sci. http://dx.doi.org/10.1002/ps.4230.
Collantes, H.G., Gianoli, E., Niemeyer, H.M., 1998. Changes in growth and chemical
defenses upon defoliation maize. Phytochemistry 49, 1921e1923.
Conseil International de la Langue Française, 1971. In: La banque des mots : revue
semestrielle de terminologie française. Presses universitaires de France, Paris.
Cordeau, S., Guillemin, J.-P., Reibel, C., Chauvel, B., 2015. Weed species differ in their
ability to emerge in no-till systems that include cover crops. Ann. Appl. Biol.
166, 444e455.
Cramer, H.H., 1967. Plant Protection and World Crop Production. Bayer Pflanzen-
schutz-Nachrichten.
Daguerre, Y., Siegel, K., Edel-Hermann, V., Steinberg, C., 2014. Fungal proteins and
genes associated with biocontrol mechanisms of soil-borne pathogens: a re-
view. Fungal Biol. Rev. 28 (4), 97e125.
Davis, A.S., Anderson, K.I., Hallett, S.G., Renner, K.A., 2006. Weed seed mortality in
soils with contrasting agricultural management histories. Weed Sci. 54,
291e297.
de Albuquerque, M.B., dos Santos, R.C., Lima, L.M., Melo, P.D., Nogueira, R., da
Camara, C.A.G., Ramos, A.D., 2011. Allelopathy, an alternative tool to improve
cropping systems. A review. Agron. Sustain. Dev. 31, 379e395.
Ditommaso, A., Watson, A.K., Hallett, S.G., 1996. Infection by the fungal pathogen
Colletotrichum coccodes affects velvetleaf (Abutilon theophrasti)-soybean
competition in the field. Weed Sci. 924e933.
Duke, S., Dayan, F., Romagni, J., Rimando, A., 2000. Natural products as sources of
herbicides: current status and future trends. Weed Res. 40, 99e111.
Duke, S.O., Baerson, S.R., Dayon, F.E., Kagan, I.A., 2001. Biocontrol of weeds without
the biocontrol. In: Vurro, M. (Ed.), Enhancing Biocontrol Agents and Handling
Risks. IOS Press., p. 96
French Ministry of Ecology Sustainable Development and Energy, 2015. The Most
Quantified Pesticides in Rivers. French Ministry of Ecology Sustainable Devel-
opment and Energy.
Fumagalli, P., Andolfi, A., Avolio, F., Boari, A., Cimmino, A., Finizio, A., 2013. Eco-
toxicological characterisation of a mycoherbicide mixture isolated from the
fungus Ascochyta caulina. Pest Manag. Sci. 69, 850e856.
Gallandt, E.R., Liebman, M., Huggins, D.R., 1999. Improving soil quality: implications
for weed management. J. crop Prod. 2, 95e121.
Ghorbani, R., Leifert, C., Seel, W., 2005. Biological control of weeds with antagonistic
plant pathogens. Adv. Agron. 86, 191e225.
Ghorbani, R., Seel, W., Rashed, M.H., Leifert, C., 2006. Effect of plant age, tempera-
ture and humidity on virulence of Ascochyta caulina on common lambsquarters
(Chenopodium album). Weed Sci. 54, 526e531.
Hallett, S.G., 2005. Where are the bioherbicides? Weed Sci. 53, 404e415.
Harding, D.P., Raizada, M.N., 2015. Controlling weeds with fungi, bacteria and vi-
ruses: a review. Front. Plant Sci. 6, 659.
Hatfield, J.L., Prueger, J.H., 1996. Microclimate effects of crop residues on biological
processes. Theor. Appl. Climatol. 54, 47e59.
Heap, I.M., 1997. The occurrence of herbicide-resistant weeds worldwide. Pestic. Sci.
51, 235e243.
Herth, A., 2011. In: le bio-contro ^le pour la protection des cultures 15 recomman-
dations pour soutenir les technologies vertes. Ministe re de l’Agriculture, d.l.A.,
de la Pe^che, de la Ruralite
et de l’Ame
nagement du territoire, 156 pp.
Hintz, W., 2007. Development of Chondrostereum purpureum as a mycoherbicide
for deciduous brush control. In: Vincent, C., Goettel, M.S., Lazarovits, G. (Eds.),
Biological Control a Global Perspective. CAB Intern ed, pp. 284e290.
Hinz, H.L., Schwarzl€ander, M., Gassmann, A., Bourchier, R.S., 2014. Successes we may
not have had: a retrospective analysis of selected weed biological control agents
in the United States. Invasive Plant Sci. Manag. 7, 565e579.
Hoagland, R.E., Boyette, C.D., Weaver, M.A., Abbas, H.K., 2007. Bioherbicides:
research and risks. Toxin Rev. 26, 313e342.
Imaizumi, S., Nishino, T., Miyabe, K., Fujimori, T., Yamada, M., 1997. Biological con-
trol of annual bluegrass ( Poa annua L.) with a Japanese isolate of Xanthomonas
campestris pv. poae ( JT-P482 ). Biol. Control 14, 7e14.
Kenney, D.S., 1986. DEVINE - the way it was developed - an industrialists view.
Weed Sci. 34, 15e16.
Kremer, R.J., Kennedy, A.C., 1996. Rhizobacteria as biocontrol agents of weeds. Weed
Technol. 10, 601e609.
Lechenet, M., Bretagnolle, V., Bockstaller, C., Boissinot, F., Petit, M.-S., Petit, S.,
Munier-Jolain, N., 2014. Reconciling pesticide reduction with economic and
environmental sustainability in arable farming. PlosOne 9, e97922.
Marshall, E.J.P., Brown, V.K., Boatman, N.D., Lutman, P.J.W., Squire, G.R., Ward, L.K.,
2003. The role of weeds in supporting biological diversity within crop fields.
Weed Res. 43, 77e89.
Melander, B., Rasmussen, I.A., Ba rberi, P., 2005. Integrating physical and cultural
methods of weed control-examples from European research. Weed Sci. 53,
 S. Cordeau et al. / Crop Protection 87 (2016) 44e49
369e381.
Mirsky, S.B., Ryan, M.R., Teasdale, J.R., Curran, W.S., Reberg-Horton, C.S., Spargo, J.T.,
Wells, M.S., Keene, C.L., Moyer, J.W., 2013. Overcoming weed management
challenges in cover crop-based organic rotational No-Till soybean production in
the Eastern United States. Weed Technol. 27, 193e203.
Mitchell, G., Bartlett, D.W., Fraser, T.E.M., Hawkes, T.R., Holt, D.C., Townson, J.K.,
Wichert, R.A., 2001. Mesotrione: a new selective herbicide for use in maize. Pest
Manag. Sci. 57, 120e128.
Mortimer, A.M., 1997. Phenological adaptation in weedsdan evolutionary response
to the use of herbicides? Pestic. Sci. 51, 299e304.
Moss, S., Marshall, R., Hull, R., Alarcon-Reverte, R., Orson, J., Bush, M., Cook, S.,
Boys, E., Cussans, J., 2011. Current status of herbicide-resistant weeds in the
United Kingdom. Asp. Appl. Biol. 1e10.
Motlagh, M.R.S., 2011. Evaluation of Epicoccum purpurascens as biological control
agent of Echinochloa spp. in rice fields. J. Food, Agric. Environ. 9, 394e397.
Nguyen, C., Chemin, A., Vincent, G., 2013. VVH 86 086, nouveau de
fanant, desiccant
naturel a  effet herbicide, 22e me Confe
rence du COLUMA. Journe
es Inter-
nationales sur la lutte contre les Mauvaises Herbes. AFPP, Dijon, France,
pp. 953e962.
Oerke, E.-C., 2006. Crop losses to pests. J. Agric. Sci. 144, 31e43.
Oerke, E.C., Dehne, H.W., Schonbeack, F., Weber, A., 1994. Crop Production and Crop
Protection. Elsevier Science, Amsterdam, Netherlands.
Owen, M.D., Beckie, H.J., Leeson, J.Y., Norsworthy, J.K., Steckel, L.E., 2015. Integrated
pest management and weed management in the United States and Canada. Pest
Manag. Sci. 71, 357e376.
Pest Management Regulatory Agency, 2013. Registration Decision for Streptomyces
Acidiscabies Strain RL-110 T and Thaxtomin a. RD2014-14, p. 7p.
Petit, S., Munier-Jolain, N., Bretagnolle, V., Bockstaller, C., Gaba, S., Cordeau, S.,
Lechenet, M., Me
zie
re, D., Colbach, N., 2015. Ecological intensification through
pesticide reduction: weed control, weed biodiversity and sustainability in
arable farming. Environ. Manag. 56, 1078e1090.

, D., Jackson, W., Carroll, C., Vandermeer, J., Rosset, P., 1990. Ecological
Soule, J., Carre
impact of modern agriculture. Agroecology 165e188.
Stergiopoulos, I., Collemare, J., Mehrabi, R., De Wit, P., 2013. Phytotoxic secondary
metabolites and peptides produced by plant pathogenic Dothideomycete fungi.
Fems Microbiol. Rev. 37 (1), 67e93.
Steward-Wade, S.M., Green, S., Boland, G.J., Teshler, M.P., Teshler, I.B., Watson, A.K.,
Sampson, M.G., Patterson, K., Di Tommaso, A., Dupont, S., 2002. Taraxacum
officinale (Weber), Dandelion (Asteraceae). In: Mason, P.G., Huber, J.T. (Eds.),
Biological Control Programms in Canada, 1981-2000. CAB International,
49
Wallingford, UK, pp. 427e436.
Stoate, C., Baldi, A., Beja, P., Boatman, N.D., Herzon, I., van Doorn, A., de Snoo, G.R.,
Rakosy, L., Ramwell, C., 2009. Ecological impacts of early 21st century agricul-
tural change in Europe - a review. J. Environ. Manag. 91, 22e46.
Stoller, E.W., Wax, L.M., 1973. Temperature variations in the surface layers of an
agricultural soil. Weed Res. 13, 273e282.
Swanton, C.J., Weise, S.F., 1991. Integrated weed management - the rationale and
approach. Weed Technol. 5, 657e663.
Tateno, A., 2000. Herbicidal Composition for the Control of Annual Bluegrass. U.S.
Patent No 6162763. Patent and Trademark Office, Washington, DC, USA.
Teasdale, J.R., 1996. Contribution of cover crops to weed management in sustainable
agricultural systems. J. Prod. Agric. 9, 475e479.
Thill, D.C., Lish, J.M., Callihan, R.H., Bechinski, E.J., 1991. Integrated weed manage-
ment: a component of integrated pest management: a critical review. Weed
Technol. 648e656.
Torres, M.F., Ghaffari, N., Buiate, E.A.S., Moore, N., Schwartz, S., Johnson, C.D.,
Vaillancourt, L.J., 2016. A Colletotrichum graminicola mutant deficient in the
establishment of biotrophy reveals early transcriptional events in the maize
anthracnose disease interaction. BMC Genomics 17.
Villaverde, J.J., Sevilla-Mora
n, B., Sandín-Espan ~ a, P., Lo

pez-Goti, C., Alonso-
Prados, J.L., 2014. Biopesticides in the framework of the European pesticide
regulation (EC) No. 1107/2009. Pest Manag. Sci. 70, 2e5.
Vincent, D., Du Fall, L.A., Livk, A., Mathesius, U., Lipscombe, R.J., Oliver, R.P.,
Friesen, T.L., Solomon, P.S., 2012. A functional genomics approach to dissect the
mode of action of the Stagonospora nodorum effector protein SnToxA in wheat.
Mol. Plant Pathol. 13 (5), 467e482.
Vurro, M., Boari, A., Evidente, A., Andolfi, A., Zermane, N., 2009. Natural metabolites
for parasitic weed management. Pest Manag. Sci. 65 (5), 566e571.
Wagner, M., Mitschunas, N., 2008. Fungal effects on seed bank persistence and
potential applications in weed biocontrol: a review. Basic Appl. Ecol. 9,
191e203.
Wauchope, R., 1978. The pesticide content of surface water draining from agricul-
tural fieldsda review. J. Environ. Qual. 7, 459e472.
Xie, C.J., Wang, C.Y., Wang, X.K., Yang, X.Y., 2013. Proteomics-based analysis reveals
that Verticillium dahliae toxin induces cell death by modifying the synthesis of
host proteins. J. General Plant Pathol. 79 (5), 335e345.
Yenish, J.P., Doll, J.D., Buhler, D.D., 1992. Effects of tillage on vertical-distribution and
viability of weed seed in soil. Weed Sci. 40, 429e433.
Zimdahl, R.L., 2011. Biological weed control. Fundam. Weed Sci. 327e355.