TRANSGENIC HERBICIDE RESISTANT PLANTS

Transcription

TRANSGENIC HERBICIDE RESISTANT PLANTS
II MODIFICATION RELATED CONCERNS
TRANSGENIC HERBICIDE RESISTANT PLANTS
G. SCHÜTTE
FSP BIOGUM
University of Hamburg
Research Center for Biotechnology, Society and the Environment
Ohnhorststr. 18
22609 Hamburg
agbiosich@botanik.uni-hamburg.de
February 2000
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HERBICIDE RESISTANT PLANTS
About FSP BIOGUM
Our research center for Biotechnology, Society and the Environment (head of FSP BIOGUM: Prof.
Dr. Beusmann) was established at the University of Hamburg in 1993 parallel to the research centers
for applied molecular biology at the Institute for Botany and molecular neurobiology at the Medical
University Clinic. The task of FSP BIOGUM is research, teaching and communication in technology
assessment of modern biotechnologies. Risks to society and the environment in comparison to
technical and institutional alternatives shall be discussed.
II MODIFICATION RELATED CONCERNS
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GENERAL AND MODIFICATION RELATED ECOLOGICAL RISKS OF TRANSGENIC PLANTS
AND REGULATION CRITERIA
Years of field experience with transgenic plants have shown that they are able to deliver
ecological and economic benefits. To keep risks of transgenic cultivars below acceptable limits is
the challenge for science and regulation. A comprehensive and thorough assessment is a
prerequisite for the responsible development of the potentials of green biotechnology.
The reports are based on a broad review by SCHÜTTE et al. (1998) for the German Federal
Environmental Agency (Umweltbundesamt) and on experiences gained by conducting biosafety
workshops for African countries in South-Africa and Zimbabwe (1997 & 1998). Dr. K.-H. Wolpers,
GTZ (Gesellschaft für Technische Zusammenarbeit) encouraged us to publish summaries of the
main risk themes in English for use in developing countries. It turned out that risk discussion and
regulation developed so fast that a substantial update was necessary. In order to make the
material available as soon as possible, it was decided to publish the chapters step by step as
contributions to a series. Meanwhile, at GTZ Dr. W. Kasten took over the work of Dr. Wolpers,
who retired. We thank both of them for their cooperation and the GTZ for financial support.
The different reports will focus on several general and modification-related scopes of the risk
discussion. A coherent description and interpretation of the risk research and discussion, tables
with summarized facts, recommendations and a list of selected literature on special subtopics are
and will be presented.
I General concerns
Unexpected effects
Gene transfer and invasiveness of transgenic plants or their hybrid progeny
II Modification related concerns
Herbicide resistant plants
(this issue)
Varieties resistant against invertebrate pests
(published)
Virus resistant plants
Disease resistant plants
Plants tolerant against abiotic stress
(published)
Plants with changed compounds
Plant varieties producing pharmaceuticals
Antibiotic resistance and horizontal gene transfer
(published)
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HERBICIDE RESISTANT PLANTS
CONTENT
INTRODUCTION................................................................................................................... 5
SYNOPSIS ............................................................................................................................ 6
MAMMALIAN TOXICITY OF HERBICIDES ....................................................................... 6
ECOTOXICITY OF HERBICIDES ...................................................................................... 8
Effects on microorganisms ............................................................................................. 8
Effects on agricultural flora ............................................................................................12
Direct effects on agricultural fauna ................................................................................14
EROSION EFFECTS OF THE USE OF BROAD SPECTRUM HERBICIDES ......................
AND TRANSGENIC RESISTANT PLANTS ......................................................................15
RISING NEW WEED PROBLEMS ...................................................................................16
Resistance to herbicides in weeds ................................................................................16
Herbicide resistant volunteers, interfertile weeds and weedy crops ...............................19
CONCLUSIONS ...................................................................................................................20
STATE OF KNOWLEDGE ................................................................................................23
CRITERIA FOR RISK ASSESSMENT ..............................................................................24
RECOMMENDATIONS FOR RISK ASSESSMENT AND MONITORING..........................25
RECOMMENDATIONS FOR THE APPROVAL AND USE OF HERBICIDE ........................
RESISTANT VARIETIES ..................................................................................................26
LITERATURE .......................................................................................................................27
II MODIFICATION RELATED CONCERNS
INTRODUCTION
Herbicide resistance is the most often field tested transgenic trait category worldwide
(USDA-APHIS 1999, JAMES 1999). Worldwide 71% of the acreage of GM (genetically
modified) plants were herbicide resistant in 1998 (BARBER 1999). Over 50 different
transgenic plant species resistant to one of at least nine different herbicides have been field
tested so far. The herbicides used most often are the two non selective herbicides
glyphosate and glufosinate (over 75% of field tests worldwide).
In the USA, herbicide resistant corn, oilseed rape, soybean and cotton have been
commercialized for 3-5 years now. Transgenic herbicide resistant varieties are already
planted on 20-40% of the soybean acreage (glyphosate resistance) in the USA and the
canola acreage (glufosinate resistance) in Canada (ANONYMOUS 1998). Many other plants
like wheat, barley, rice and poplar have been commercialized since 1996 (USDA-APHIS
1999, JAMES & KRATTIGER 1996). Glyphosate and glufosinate resistant soybean, corn,
sugar beet and canola varieties are available in the USA or Canada. Cotton and oilseed rape
varieties resistant to three different herbicides (glyphosate, sulfonylurea and bromoxynil
respectively imidazolinones) are on the USA market as well (DOWNEY 1999). Thus, it is
possible to spray non-selective herbicides in rotation with or without crop rotation for several
years on one field.
In Europe, two or three applications of glufosinate per season in sugar beet and corn, and
sometimes in oilseed rape when problem weeds occur or when glyphosate is used (AMMAN
1998), may become reality (PETERSON & HURLE 1998, CREMER 1996). In Europe,
oilseed rape, corn and sugar beet are the main herbicide resistant crops tested.
In Latin America the most often field tested herbicide resistant species are oilseed rape, corn
and cotton, soybean and sugar beet. A high percentage of the soybean acreage is planted
with transgenic varieties in Argentina (ANONYMOUS 1998). In Africa in addition to corn,
cotton and oilseed rape also forage grasses, alfalfa and strawberry lines have been tested
(JAMES & KRATTIGER 1996).
In Germany and other European countries herbicides are used on a very high percentage of
crops and fields, and feral land is rare compared to the USA (OSTEEN 1993, PIMENTEL et
al. 1993, PALLUTT & BURTH 1994). This might be one of the reasons for the different
perspectives in these countries. Also, the percentage of fields on which post ermergence
herbicides are used in combination with economic threshold determinations are small,
although post emergence herbicides are already available in most cases in Germany
(different sources in SCHÜTTE 1998b, p.385).
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Using the above background, the risk discussion in Germany on transgenic herbicide
resistance focussed on following issues:
•
mammalian toxicity
•
ecotoxicity (side effects on soil microorganisms and agricultural flora or fauna)
•
erosion effects,
•
raising herbicide resistant weeds and volunteers
Hazards of the new herbicide resistance technology have sometimes been compared to
hazards of other currently used herbicides or alternative weed control measures. It has to be
mentioned that application rates (active compounds per hectare and year) and eceological
side effects are different for each herbicide. Thus, comparisons solely based on quantities
are of no relevance for an assessment (WALTER 1998). An extreme example are
sulfonylurea herbicides of which only a few gram are needed on one hectare compared to
0,5 to 3 kg for other herbicides. But in assessing the toxicological effects, side effects on
organisms and effects on soil degradation in agricultural practice,
it is of importance,
whether one or more applications per season are necessary, when and how the herbicide is
applied (pre- or postemergence, only on rows, patchy weed control, in combination with
cover crops). The possible misuse by application of higher dosages than necessary without
negative effects to the resistant crop plant was another aspect of concern (WALTER 1998).
SYNOPSIS
MAMMALIAN TOXICITY OF HERBICIDES
The accessible information on toxicological behavior of many herbicides is very limited. The
US National Research Council (GOLDBURG 1992) estimated that herbicides account for
31% of the oncogenic risks of pesticides on fresh food. The following table reflects the state
of public knowledge on toxicological data of some herbicides used in herbicide resistant
plants.
II MODIFICATION RELATED CONCERNS
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Table 1: Published knowledge on toxicity of active compounds
and
metabolites
Glyphosate
Glufosinate
Bromoxynil
Atrazine
Sulfonylurea
Metabolic
Pathway
partly known,
missing data
quite well
known
partly known
quite well
known
quite well
known
Persistence +
Solubility
low persist..
except in
3
plants ,
soluble, but
persistent
quite persistent
in soil
very low risk of
water
contamination
low risk of
water
contamination
high risk of
water
contamination
high risk of
water
contamination
Persistence +
Solubility
major
metabolite low
persistence +
insoluble
four
metabolites
stable, one
4
soluble
insoluble
metabolite
insoluble and
soluble
metabolites
Bioavailability
some data
known
no data
in animals
known, in
plants not
known
Bioavailability
open questions partly known
no data
in animals
known, in
plants not
not known
Mammalian
toxicity/
mutagenicity
effects,
oncogenicity in
1
one case ,
commercial
formulation:
teragenicity
effects –
possibly
3
carcinogenous
“harmful”,
other data ?
?
?
stimulation of
hormone prod.
2
in beans
Mammalian
Toxicity
only partly
known
no dangerous
effects so long
but missing
data for two
4
metabolites
?
?
?
Regulation
of residues
yes
yes
regulation not
practical
yes
too high
maximum
accepted
Regulation
of residues
no
yes
no
no
no
Compiled from reviews of SANDERMANN (1994), OHNESORGE (1994), BÖGER (1994), KLEIN
2
1,
3
(1994), SANDERMANN & WELLMANN (1988) , HARDELL & ERIKSON (1999) GOLDBURG (1992) ,
4
4,
METZ et al. 1998 EBERT et al.1990 cited in METZ et al. 1998
Information about herbicides are written in white background and about herbicide metabolites in grey
background. The question mark signifies that it is not published, whether and which findings are known
but confident. Missing data means that data are not “only” unpublished but really missing. The category
“Mammalian Toxicity” includes mutagenicity, teragenicity and oncogenicity.
Obviously, some data is missing on the question of synergistic effects of two or more
pesticides used together in a crop have not been adressed too. Glyphosate deserves further
epidemiological studies according to HARDELL and ERIKSON (1999). When assessing
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mammalian toxicity, one is faced with the problem of missing information. According to
SANDERMANN (1994) and OHNESORGE (1994) the knowledge is not sufficient for a
scientifically based comparison or judgement. Nevertheless, the common opinion based on
the few pieces of information published is that the toxicity of both broad spectrum herbicides
(glyphosate, glufosinate) for mammalians is seemingly lower compared with other
herbicides. The LD50 for glufosinate is higher than for alachlor and metribuzin and only a
tenth of the LD50 for bromoxynil. The LD50 for glyphosate is even higher than for glufosinate
(SANDERMANN 1994, OHNESORGE 1994). Scientists still recommend further pre-market
testing and state that the toxicological impact of actually sprayed plants is not sufficiently
clear (for Glufosinate see METZ et al. 1998). The authors also stated that crop or speciesspecific metabolites could occur (METZ et al. 1998).
ECOTOXICITY OF HERBICIDES
Effects on microorganisms
The effects on microorganisms can be indirectly measured by biomass indicators like
dehydrogenase activity (also indicating soil fertility) and short term respiration (12 hours) or
organic carbon content. On the other hand, turnover indicators such as long term respiration,
nitrogen mineralization, oxygen uptake (GERBER et al. 1989), straw degradation and
substrate utilization (AUGUSTIN et al. 1998) can also be used.
The influence on microbial populations is also tested through germination of culturable
microorganisms. The comparison of germination rates is limited by the estimated portion of
0,1 to 12,5% culturable microorganisms (PICKUP 1991 cited in BENDE & LOPEZ-PILA
1993). Other measures to compare masses of culturable and non-culturable microorganisms
are the use of fluorescent markers and direct counting, the T-RFLP approach and the
determination of fatty acid patterns (LUKOW & LIESACK 1999, ERNST et al. 1998)
Species or special taxa can be detected and counted using PCR and marker techniques and
„enzyme-linked immunosorbent assay“ (ELISA) (BENDE & LOPEZ-PILA 1993, PICKUP
1991 in BENDE & LOPEZ-PILA 1993), no matter if they are culturable or not. But the
absorption of microorganisms to soil particles makes detection difficult (depending on soil
type), and humic acids or salt are a hindrance for PCR and the inadequate specificity of
primers sometimes impedes an interpretation.
Of the herbicides listed above in table 1, glufosinate and glyphosate are known to exhibit
antibiotic activities (OHNESORGE 1994). Experimental results on glyphosate and
glufosinate effects are summarized here:
II MODIFICATION RELATED CONCERNS
Biomass indicators
Short time respiration and dehydrogenase activity were either not affected by herbicides or
slightly increased during the first week but decreased from the second week to at least 16
weeks after application of both herbicides. The results from pure soils and soils amended by
lucerne-meal did not differ much (MALKOMES 1988). An increase of microorganism
biomass was also detected by AUGUSTIN et al. (1998) for the first weeks after glufosinate
application when compared to the two control soils (1: transgenic variety without herbicide
application, 2: conventional variety with application of the herbicide butisan).
Turnover indicators
Long term respiration and nitrogen mineralization slightly increased for at least 16 weeks
after application of both herbicides in pure soils and soils amended by lucerne-meal. Only
direct contamination of higher dosages inhibited straw degradation (MALKOMES 1988).
Similar results were published by AUGUSTIN et al. (1998) who also showed differing
substrate utilization depending on the application of herbicides and on the herbicide choice
(butisan, gufosinate).
Populations
The results summarized in table 2 show a reduction of bacteria and fungi populations after
one application of the two herbicides (glyphosate & glufosinate), which can be reversed after
one week or not reversed even after two months depending on the temperature. The
absence (almost) of herbicide sensitive bacteria after a few seasons of application (see
BARTSCH & TEBBE 1989 and ERNST et al. 1998) seems to be due to the elimination of
sensitive bacteria and to resistance developments (AHMAD & MALLOCH 1995, ERNST et
al. 1998). ERNST et al. (1998) did not present their data, and therefore they are not
mentioned in the table 2. They found „no essential differences“ for glufosinate and controls
without herbicide use.
The effects on microorganisms other than bacteria and fungi are almost not investigated,
contrasting the fact that especially cyanobacteria and algae are sensitive indicators
(MALKOMES 1994). The suppression of algae by glufosinate was investigated by DORN
(1992), who found an effect on algae at a dosage of 2,5 mg active compound per liter. A
maximum of 4 mg active compound per kg soil is expected by DORN et al. (1992) to be
found after glufosinate application. The level of no observed effect (NOEL) of glyphosate on
algae is 0,23 mg per liter according to OHNESORGE (1994). Thus soil algae can be harmed
by a normal application of glufosinate.
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Table 2: Germination of culturable microorganisms after one application:
Herbicide
Conditions
Glyphosate
Glufosinate
always typical dosages
used
decrease to 53% and
69% of control
(bacteria)
decrease to 58% and
82% of control
(bacteria)
20°C, 2 different soils,
decrease to 52% and
68% of control (fungi)
decrease to 71% and
8% of control (fungi)
20°C, 2 different soils,
MALKOMES 1988
results after 8 weeks
far under 20°C,
significant decrease of
fungi
far under 20°C,
results after 2 months
results after 2 months
decrease to 80% of
control (fungi)
MALKOMES 1988
results after 8 weeks
significant decrease of
bacteria
decrease to 60% of
control (bacteria)
Author
20°C, 12 different soils
results after 2 weeks
20°C, 15 different soils
results after 2 weeks
CHAKRAVARTY &
CHATARPAUL 1990
CHAKRAVARTY &
CHATARPAUL 1990
AHMAD & MALLOCH
1995
AHMAD & MALLOCH
1995
significant reduction of
microorganisms,
reversed after 7 days
27°C, 2 different soils,
results after one week
ISMAIL et al. 1995
5% of 300 bacteria
isolates tested were
sensitive
soil after 3 years of
glufosinate application
BARTSCH & TEBBE
1989
Special taxa
AHMAD and MALLOCH (1995) investigated the effect of different dosages on various fungal
species. They found a strong negative effect on some beneficial mycoparasitic Trichoderma
species and a high tolerance of Verticillium species, a genus representing some serious
plant pathogens. These findings indicate a negative effect on the antagonistic potential of
soils (AHMAD & MALLOCH 1995). A decrease in pathogen populations of the
Gaeumannomyces-Philapora complex after glufosinate application compared to controls and
an increase after 40 days were also measured.
Also affected by the herbicide were some saprophytic molds (Aspergillus spec.), which could
lead to a disruption of the microbial nutrient cycle. Rhizobia were also decreased by
glufosinate (BROER 1995). The herbicide led to a decrease in population of Rhizobium
leguminosarium in approximately 10 days as compared to the control (Butisan and
conventional variety). The population structure also changed (AUGUSTIN at al. 1998). Some
mycorrhiza species were sensitive, but only to multiple dosages (CHAKRAVARTY &
CHATARPAUL 1990).
II MODIFICATION RELATED CONCERNS
Ecological significance of results
The question of whether an impact exists and to what degree of it is of importance from the
ecological point of view is open. GERBER et al. (1989) published recommendations for
laboratory tests and a statement regarding the critical time span for a recovery of microbial
populations. A recovery after 31 to 60 days was considered „maybe critical“, after taking into
account that short time reductions of up to 50% do also occur in nature. Furthermore they
underlined the necessity of testing effects on: plant pathogens, beneficial (e.g.
entomophagous) microorganisms, nodulation of legumes, and on mycorrhizal associations.
In assessing side effects, the interactions between microflora and microfauna should also be
investigated (GERBER et al. 1989). Especially species with low population densities are
possibly reduced.
Other possible useful indicators are the diversity of soil enzymes and typical functional
organic groups of molecules (FRIELINGHAUS pers. Communication) that might be used in
future.
We know from test results that the two main herbicides have an impact and supress soil
microorganisms and that the suppression can last at least 60 days at temperatures below
20°C. A reduction of bacteria and fungi of approximately 40% or greater (sometimes less,
see Table 2) for more than 8 weeks cannot be without impact on the microfauna feeding on
it and on the whole food chain (invertebrate fauna and vertebrate fauna) because the
relevant (growing) season for many invertebrates does not last more than 18 to 25 weeks in
northern Europe. This has to be evaluated with the fact that mostly two and sometimes three
herbicide applications will be needed (CREMER 1996, HARMS et al. 1998).
Also some beneficial microorganisms are negatively affected by one application unlike some
plant pathogens (AHMAD and MALLOCH 1995). According to AHMAD and MALLOCH
(1995), the dominance identity of the soil biocoenosis and proportions of species in the soil
are changed by the herbicide. They conclude from their study that changes in composition of
soil microflora may be an inevitable consequence of using glufosinate for weed control.
MALKOMES (1994) added in his discussion that effects of herbicides on microorganisms are
stronger on sandy soils than on other types of soil.
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HERBICIDE RESISTANT PLANTS
Effects on the agricultural flora
The abundance of associated flora in agriculture is important for: integrated plant production
(plants supporting beneficial fauna), the prevention of soil erosion and in regions with high
input agriculture for the conservation of species.
Conservation of species
In Germany for example, where fallow land makes up much less than 10% of the national
area, 30-50% of the floral species (HANF 1985 cited in KÖRNER 1990) and 45-85% of the
associated arthropod fauna species (HEYDEMANN 1983 cited in RASKIN et al. 1992) have
been forced back by intensified agriculture since the fifties. Density reductions of the
individuals of arthropods - which depend on the flora - have even been higher (up to 99%
according to KOCH & KUNISCH 1998). Also, the reduction of the density of individuals of
soil invertebrates was estimated to reach 99%.
About a quarter of the floral species of Germany is endangered (KORNECK & SUKOPP
1988), and of these, 10% belong to the associated agricultural flora (EGGERS & ZWERGER
1998). According to HEYDEMANN (1983 cited in RASKIN et al. 1992) each plant species is
essential for an average of 10-12 insect species in northern Europe. About 68% of the
reduction of individual abundance of the flora (CALLAUCH 1981) and the decrease of 3,515% of the endangered floral species was estimated to be due to herbicide use (4 different
estimations reviewed in SCHÜTTE 1998b). Drainage, cultivation of special natural habitats
and the reduction of crop rotation also contributed to the loss of diversity and abundance of
the agricultural flora (KÖRNER 1990, HAUG 1990).
Another effect of clean weeding and herbicide use are alterations of the dominance order of
the associated flora and the development of problem weeds (see below). Mechanical
weeding does not reduce the density of the weed flora and associated flora as compared to
herbicides (BÖHRNSEN & BRÄUTIGAM 1990, KORR et al. 1996, ALBRECHT & MATTHEIS
1998). The more difficult task in this context is to find a way to increase not only the
abundance of the associated flora, but also their diversity and to support the non-target and
endangered species. ALBRECHT and MATHEIS (1996) for example, found an increased
species diversity after changing the farming system to biological (no herbicides used) but not
to integrated (economic threshold models applied) control. But, endangered species did not
reappear. When discussed, this result was found to be due to the use of herbicides for
decades on the investigated area in the past. We know from the studies of FRIEBEN
(1990)*, CALLAUCH (1981)*, PLAKOLM (1989)*, WOLF-STRAUB (1989)*, van ELSEN
(1994)*, JÜTTERSÖNKE and ARLT (1998), BECKER and HURLE (1998, eight years of
II MODIFICATION RELATED CONCERNS
monitoring) and of WITTMANN and HINTZSCHE (1998) that extensification or organic
farming can lead to an increase in endangered species but it sometimes takes many years
and also depends on the soil (history of pesticide use, nutrition, soil type). DUBOIS et al.
(1998, five years of monitoring) could only find a significant increase of seeds in the soil
when crop rotation was mainly based on cereals (60%) in integrated and biological farming.
MAYER and ALBRECHT (1998) came to the conclusion that the kind of organic fertilizer and
especially the combination and diversity of seeds in manure, is a more important factor than
the actual farming system. Therefore it is important to manage the seed bank in soil.
Sowing and conserving special flora species, increasing crop rotation, increasing the use of
strips without herbicide spraying and setting land aside for periods of about three years
(when special plants are sown to prevent weed infestation) can help to increase the diversity
of the associated flora (OESAU 1998, RASKIN et al. 1992, ALTIERI & WITHCOMB 1979,
BOSCH 1987, ALBRECHT et al. 1998).*
Non-target plants and integrated plant production
Over 95% weed control is achieved by non selective herbicides like glyphosate and
glufosinate (WESTWOOD 1997). But a 95% control of weeds is not necessary for the
exclusion of competitive effects of weeds and associated flora to crops (PALLUT et al. 1997,
KORR et al. 1996, WERNER & GARBE 1998). WERNER and GARBE (1998) for example,
showed that 23-74% of the area of monitored oilseed rape fields in Germany were not
infested enough by weeds to reach the economic injury level. These and many other authors
therefore plead for patchy weed control for the future (PLUSHKELL & PALLUTT 1996,
WERNER & GARBE 1998, HÄUSLER et al. 1998, SCHWARZ et al 1998)
A degree of coverage of associated flora of about 15% of weeds between rows of sugar beet
did not influence yields (SCHÄUFELE 1991) and can even lead to a 7% higher productivity
(HÄNI et al. 1990). The experiments of KORR et al. (1996) with potato and wheat (three
years of investigation), showed that mechanical weeding led to 38-60% higher associated
species diversity as compared to herbicide use without significant yield reduction in potato
and – except under high infestation - in wheat too. All these findings are of agricultural
relevance because many of the pest antagonists such as predators (Coccinellidae,
Syrphidae) and parasitic wasps (Ichneumoidea), depend on pollen feeding on early flowering
plants - parasitic wasps especially on umbellifers (Apiaceae=Compositae) (ALTIERI &
WITHCOMB 1979). A coverage of 15-20% of associated flora led to a doubled or multiple
*
cited in ALBRECHT & MATHEIS 1996
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density activities of ground beetles and increased abundance of many other arthropods in
sugar beet (BOSCH 1987).
We also know (from newest assessments), that predators were able to control aphids below
the economic threshold in nine of twelve cereal fields in Germany (FREIER et al. 1999).
Assessments
Assessments of the effect of herbicide resistance in combination with non selective
herbicides on species diversity have been carried out in Europe. The conclusion of these ex
ante assessments were that the herbicide resistance in connection with non-selective
herbicides might reduce species diversity and abundance further when it is applied more
often than every third year (HEITEFUSS et al. 1994, HURLE 1994). According to MAHN
(1994) the planting of oilseed rape resistant to non selective herbicides will generally
endanger special groups of floral species. Important winter-adapted floral species will be
reduced due to late applications in autumn and plants emerging in warmer periods will be
shadowed and forced back by faster growing oilseed rape plants.
The use of glyphosate will further reduce the range of perennial species according to
HURLE (1994). Currently different practical investigations addressing these questions are
performed (MAHN 1996, PALLUT & HOMMEL 1998, AUGUSTIN et al. 1998 p. 30, TURNER
in press).
Direct effects on the agricultural fauna
The indirect effects of herbicide use on the fauna due to the loss of microorganism and floral
abundance were discussed above. Information published on direct toxic impacts of
herbicides to animals is very rare. Mostly, the original reports are considered confidential.
Furthermore, officially requested toxicity tests in Germany and in other countries include only
a few (mostly epigeal) predators as indicator species. Therefore, the effect on other aphid
predators (Coccinellidae, Syrphidae), parasitic wasps (Ichneumoidea), or other non target
pests is not known (FORSTER 1995). An alternative for testing the side effects to a broader
range of invertebrates was described and recommended by BODE (1988).
The study of VOLKMAR et al. (1998) which was partly financed by AgrEvo should be
mentioned in this context although their results cannot be interpreted in the way they did.
They compared the density activity of quite mobile arthropods (Staphilinidae, Carabidae,
Aranae) on small test plots (total test site was „a few hectares“) with standard herbicide
application, with glufosinate in combination with resistant varieties, and without herbicide use
over a period of three years. A significant difference of activity density was not found. These
results are typical for test areas small enough to let species move from one plot to the other
II MODIFICATION RELATED CONCERNS
and stand in contradiction to many other studies (e.g. KULA 1994, BOSCH 1987, for a
compilation and profound discussion see SCHÜTTE 1998b, p. 425-430). SCHÜTTE (1990)
found an up to 260% higher arthropod biomass in integrated farming systems (less
herbicides used) compared to conventional farming (5 years, plots of more than 100
hectares compared, use of pitfall traps like VOLKMAR et al. 1998).
Knowledge on ecotoxicity of glufosinate available to the public
Glufosinate is known to be slightly toxic to fish (LC50 for formulation: 14-56mg/l, to species
tested, DORN et al. 1992) and aquatic invertebrates (EC50 for formulation: 0,5-42mg/l,
OHNESORGE 1994, or 15-78mg/l, DORN et al. 1992). The pure phosphinotricin (without
formulation) is not toxic to aquatic organisms (LC50:710-1000mg/l depending on the
species) (DORN et al. 1992, METZ et al. 1998). The highest concentration expected after
applications in agriculture is 0,25mg/l in small lakes (formulation).
Glufosinate was classified as toxic for the aquatic fauna and for fish (OHNESORGE 1994).
BOCK (1991 unpublished in DORN et al. 1992) detected harmful effects of glufosinate to
arachnids (Arachnidae), but not to some other (unknown) tested species. No mortality could
be observed in earthworms and honey bees (METZ et al. 1998). The maximum tolerable
intake for birds is 13mg/kg/d according to LEIST and EBERT (1988a in DORN et al. 1992).
The toxicity of the metabolite acetyl-phosphinotricin (which remains stable in plants) to nonmammalians has not yet been tested (METZ et al. 1998).
Knowledge on ecotoxicity of glyphosate available to the public
Glyphosate was classified as toxic to fish and aquatic invertebrates (OHNESORGE 1994). It
also is known to harm ground beetles (genus Bembidion) (DIERCKS & HEITEFUSS 1990).
Glyphosate reduced the growth rate of the earthworm Aporrectodea caliginosa at all rates of
application (SPRINGETT & GRAY 1992).
EROSION EFFECTS OF THE USE OF BROAD SPECTRUM HERBICIDES
AND TRANSGENIC RESISTANT PLANTS
Non-selective herbicides often lead to a percentage of weed control greater than 95%
(WESTWOOD 1997) and a low degree of soil coverage. When the herbicides are applied
within periods of high rainfall, the level of erosion can increase (AUERSWALD 1994). A postemergance application in sugar beet will coincide with high rainfall in Germany. A reduced
frequency of pesticide application per season and thereby lowered ground pressure could be
favorable. In North America, most researchers recommended two herbicide applications at
the 1997 meeting of the Weed Science Society of America (WESTWOOD 1997).
15
16
HERBICIDE RESISTANT PLANTS
Presentations for European regions showed, that sometimes three applications will be
necessary, depending on the crop and on the amount of precipitation (CREMER 1996,
HARMS et al. 1998). Ground pressure will therefore not decrease. In Europe, ground
pressure might be increased in corn and decreased in sugar beet.
Cover crops and no-till agriculture are known to prevent soil erosion, and it is often argued,
that herbicide resistant crops make it easier to control weeds in such systems
(WESTWOOD 1997). Other authors state that no-till agriculture does not necessarily
depend on herbicide resistance, and cover crops with a high competitive ability like rye can
suppress weeds (HEITEFUSS et al. 1994, KEES 1990).
RISING NEW WEED PROBLEMS
Resistance to herbicides in weeds
The number of herbicide resistant weeds has dramatically increased since the end of the
1980´s when only about 12 resistant species were known. Currently about 216 resistant
species (53 to ALS inhibitors, 26 to sulfonylurea and imidazolinone classes, 19 to ACC
inhibitors) have become a problem on more than 6 million hectares of arable land (BARBER
1999). More or less, half of the resistant biotypes are multiple-resistant to different
herbicides (WESTWOOD 1997, GRESSEL 1996, GOLDBURG 1992, LeBARON 1991). One
can find resistances due to target site mutations or to detoxification and degradation of the
active compounds (e.g. by cytochrome P450). Recent findings also demonstrate, that
herbicide resistance does not always decline in absence of the herbicide. This was shown
for a triazine resistant weed under low stress and cold, moist situations (PLOWMANN et al.
1999). It was also shown that glufosinate resistance in Brassica rapa after introgression from
oilseed rape did not decrease fitness after backcrossing (SNOW et al. 1999 cited in
J∅RGENSON 1999).
Most resistances are found in regions with high input agriculture such as in the middle of
Europe, Canada and parts of the USA and Australia.
Different classes of herbicides have been used for a long time until resistances developed
on weeds. 2,4 D (auxinic herbicide) or paraquat and dinitroanilines were quite safe because
of, either low selection pressure or multiple target sites and the lack of cross resistance. It
took two decades until triazine resistances were found, but resistances to newer classes like
the ALS (acetolactate synthase) inhibitors, AHAS (acetohydroxy acid synthase) inhibitors
(sulfonylurea, imidazolinones...), ACC (acetic coenzyme A carboxylase) inhibitors and to
carbamates or amides have evolved faster and are steadily increasing in number (RUBIN
1996).
II MODIFICATION RELATED CONCERNS
Although glyphosate is a herbicide which acts against different enzymes, one resistant
biotype (Lolium rigidum) has developed and been recorded (ANONYMOUS 1996).
PETERSON and HURLE (1998) estimated, that the use of glufosinate or glyphosate could
make up 25-30% of the total amount of herbicide use in German agriculture when 50% of
oilseed rape, corn and sugar beet fields are controlled by one of the herbicides. Such a
concentration on special herbicides would be higher than ever reached by atrazine or the
current main herbicide in Germany. This leads to a very high selection pressure. Herbicide
resistance is therefore discussed to further decrease weed diversity and enhance problems
with difficult weeds, a problem which exists in high input agriculture. 10 of the 20 most
relevant weeds in sugar beet, corn and oilseed rape are relevant in all three crops in
Germany, which shows the concentration of a few weeds, which are very difficult to control
(PETERSEN & HURLE 1998). Such a concentration provides a high likelihood of emerging
resistances but other criteria have to be taken into account as well; such as:
Conditions leading to a fast development of resistance
high persistence of the herbicide
low herbicide and crop rotation
high initial frequency of herbicide resistance gene
high mutation frequency of the resistance gene
high selection pressure of the herbicide
single mode of action
gene flow from herbicide resistant crops to weedy relatives
Conditions under which the portion of resistant biotypes quickly increases
short-living seeds, few seeds in soil
high amounts of pollen distribution over long distances
(sources: BÖGER 1994, THILL 1996, HURLE 1994)
Precautionary resistance management necessary?
The gene flow in selfing plants was estimated to be as low as mutation rates, but this has
turned out to be an underestimation. Especially in selfing plants (cross pollination under 20%
according to HERMANUTZ 1991) recessive alleles can be distributed quite quickly. Isolation
distances of 100m are too small (JASENIUK et al. 1996). The number of resistant plants in a
field can increase from 1 to 100000 during four years (DARMENCY in press). Nevertheless,
gene flow is too low to use refuges as for management of insect resistance (JASENIUK et al
1996).
17
18
HERBICIDE RESISTANT PLANTS
Recommendations to prevent or manage resistance in weeds are published by RUBIN
(1996, different citations there) but practical attempts have failed to date (RUBIN 1996).
Herbicide rotation (different modes of action and different crop selectivities), crop rotation,
rotation of weed control measures (mechanical weeding, bioherbicides, cover plants, the use
of clean seeds and lowering selection pressure, are the main preventative measures
recommended. Lowering selection pressure by application of lower amounts of herbicides
could facilitate the development of non-target resistance, which is often a multiple resistance
in contrast to target-site resistance (GRESSEL 1995). This happened in India with
isoproturon in wheat and it was shown for glyphosate in laboratory selections (different
sources cited in GRESSEL 1995). GRESSEL (1995) discussed the danger of this sort of
“creeping” resistance, with different minor mutations (leading to a polygenic resistances or
gene amplifications) especially when the dose is gradually increased. He recommended to
use a sequence of low doses followed by a moderate dose. The moderate dose should be
sufficient to control individuals with a low resistance. Models show that this approach delays
resistance better than a consistant use of high or low doses. Patchy weed control will also be
a helpful tool to decrease selection pressure.
It is also of importance to recognize the mode of action and resistance in order to be able to
choose an adequate management option and also to monitor resistance (SHANER 1995,
JUTSUM et al. 1998). According to SHANER (1995) it is partly possible to predict the mode
and the time of developing resistance including the genetic attributes by analyzing
laboratory-generated resistant biotypes and the mechanism of crop selectivity.
The potential of parasitic weeds to develop resistance
Parasitic weeds like Striga spp. and Orobanche spp. are more sensitive to the herbicides
glyphosate and glufosinate than other weeds and therefore suffer a higher selection
pressure from the same dosage (GRESSEL 1996). The high selection pressure and the
extremely high reproductive potential (1000 seeds per plant for Orobanche) of the parasitic
weeds will favor a quick resistance development. Some resistance management tactics have
been discussed in the past and it was recommended to use smaller dosages and to
eradicate resistant biotypes by manual hoeing, but the concepts have to be better
developed.
It is important to assess alternative control methods such as the use of resistant varieties,
trap crops which trigger germination of the weed but which are no host plants (like corn,
pepper and alfalfa), special mycoherbicides or antagonistic diptera against Orobanche
(LINKE et al. 1995, SANDS et al. 1995). Some sorghum, millet, corn and cowpea varieties
are resistant or partially resistant to Striga (TRIBE 1994). A new approach to breed for
II MODIFICATION RELATED CONCERNS
resistance is to delete the plant gene coding for the substance which triggers the weeds´
germination (ANONYMOUS 1997).
Herbicide resistant volunteers, interfertile weeds and weedy crops
Herbicide resistance can create problem in three groups of crops: volunteers in following
crops, high competitive ability and weedy characteristics, and interfertile with weedy species.
Volunteers
At least for oilseed rape the volunteer/multiple resistance problem and intraspecific crosses
between varieties (with different herbicide resistances) might be a bigger problem as
compared to introgression of herbicide resistance genes into cross compatible weeds in the
short term, just because of the small amount of fertile offspring of the latter or of missing
abundance in Europe (J∅RGENSON 1999, CHAMPOLIVIER et al. 1999). Especially the
hybrid varieties (Triolo, Synergy) which are easier pollinated by alien pollen because lower
pollen competition could lead to a wide spread of transgenes. The dimension of farm to farm
cross pollination when emasculated bait plants are used were examined by THOMPSON et
al. (1999), SIMPSON et al. (1999) and TIMMONS et al. (1995). Cross pollination occured
depending on the distance from the source at 5% (4000m), 18% (2000m), 61% (100m) and
88% (1m) in an area of 70 square kilometers where oilseed rape was common (THOMPSON
et al. 1999).
The first oilseed rape volunteer monitoring project from the UK was performed on eight
different sites with different crop rotation monitored for two years was presented by NORRIS
et al. (1999). Different proportions of herbicide resistant volunteers and seeds in the
transgenic crop field, the adjacent field and outside the field/area were determined (0-42%
resistant volunteers in the GM crop field post harvest [4 sites], 0-40% resistant volunteers in
the adjacent (non-transgenic ) fields [2 sites]).
ORSON and OLDFIELD (1999) underlined the potential problem of double-resistant
volunteers mentioning the relative high costs of potato and sugar beet volunteer control.
For the USA, corn volunteers are known to appear in soybean and wheat, wheat in oilseed
rape, and oilseed rape in wheat. Oats and oilseed rape can cause problems in corn and
sugar beet and wheat in sugar beet in Europe (PETERSEN & HURLE 1998). According to
SCHLINK (1998) 4.7% of buried seeds of oilseed rape could still germinate after 10 years.
Barley can become a volunteer and is interfertile with feral species too (MAHN 1994). Crops
and volunteers resistant to the same herbicide class will cause problems (WESTWOOD
1997).
19
20
HERBICIDE RESISTANT PLANTS
Interfertile weeds
The abundance of interfertile weeds might become a problem in oilseed rape because of its
many feral interfertile species. In Europe, the weeds Sinapsis arvensis and Raphanus
raphanistrum are of presumably less relevance on the short term (see above) than oilseed
rape and Brassica rapa, sugar beet and weed beets (Beta maritima which can become a
„bridge“ to other Beta forms).
Gene flow between Johnsongrass (Sorghum halepense) and Sorghum bicolor, oats and
Avena sativa, wheat and Aegilops cylindrica (SEEFELDT et al. 1998, SEEFELDT et al.
1999), many vegetables and their relatives (radish, squash, carrots..) or rice and Oryza
sativa will be assessed where herbicide resistant varieties of these plants are planned to
grow and the corresponding weeds occur (WILCUT et al. 1996, THILL 1996, SCHÜTTE
1998a).
The expression of resistance genes in chloroplasts is one possible way to mitigate
outcrossing (DANIELI et al. 1998, ROTINO et al. 1997), although they will not be totally
contained (GRAY & RAYBOULD 1998). (see also Chapter 2). SEEFELDT et al. (1999) and
PINDER et al. (1999) proposed to locate the resistance gene on the A or B genome in wheat
and on the C-genome in oilseed rape to decrease the chance of gene flow into Aegilops
cylindrica respectively into Brassica. rapa or B. juncea.
Weedy crops
Alfalfa, Sorghum and sunflower can create weed problems in the USA, and herbicide
resistant varieties of these species should thoroughly be assessed (THILL 1996).
CONCLUSIONS
A deliberate use of herbicide resistance could help to solve special problems of modern
agriculture such as the control of multiple resistant gras weeds (e.g. isoproturon resistance
in India or ALS and ACC resistance in the USA, GRESSEL 1996, RUBIN 1996) of
troublesome weeds (e.g. in the USA quackgrass in corn, sicklepod in soybean) and
perennials (e.g. in oilseed rape; WILCUT et al. 1996). Some toxicologically worse herbicides
such as triazine and MCPA in corn and cereals could possibly be exchanged. The new
varieties could be used in no-tillage agriculture and even limit the use of plastic in vegetables
(WILCUT 1996)
Furthermore, it will be easier to control weeds post emergence in some additional crops (e.g.
rice, potato, oilseed rape in areas for drinking water conservation) and to use economic
threshold models. But for most of the crops in Germany, post emergence herbicides are
available and therefore herbicide resistance does not provide a new option. Furthermore,
II MODIFICATION RELATED CONCERNS
late post-emergence applications are sometimes not feasible due to the application
technique (WALTER 1998).
Oilseed rape is sensitive to many herbicides and thus sometimes not planted. Herbicide
resistance can solve this problem and thereby elevate crop rotation.
Sometimes it is argued that fast degrading herbicides like glufosinate and glyphosate also
lead to conservation of flora because they only function for a short time, but these herbicides
are often sprayed a second or third time depending on the climate (CREMER 1996,
LECHNER et al. 1996, WESTWOOD 1997).
First management guidelines
This year the first detailed managment recommendations or proposals for growing herbicide
resistant oilseed rape in Canada and wheat in the USA were published. Both
recommendations are developed for current varieties without containment mechanisms (see
above) for the resistance genes.
Oilseed rape in Canada
•
It was recommended to avoid planting oilseed rape with resistance to different
herbicides in the same or adjacent fields (DOWNEY 1999).
•
The seed bank could be decreased by tilling with a chisel instead of a moldboard
plough (COLBACH et al. 1999).
•
Delaying sowing and the use of large sowing rates could decrease volunteer
abundance by reduction of viable seed bank and by competition (COLBACH et al.
1999).
•
The spread of transgenes to farms not using herbicide resistant varieties or using
different herbicide resistances and to weeds should be prevented by seperate storage,
cleaning seed drills and other equipment, avoiding leakage during seed transport,
adopting practices for volunteer control in subsequent crops (ORSON & OLDFIELD
1999).
•
Providing information on all management aspects (ORSON & OLDFIELD 1999).
21
22
HERBICIDE RESISTANT PLANTS
Wheat in the USA
•
Preplant
consider a one-time burn on non-highly erosive land when Aegilops cylindrica infestation
is heavy - on erosive land use of chisel plow
•
Crop year
Aegilops cylindrica should not be abundant within half a mile of the field, a herbicide
resistant variety should be competitive against Aegilops cylindrica, high seeding rates
and narrow rows should be used, herbicide should additionally be applicated to the field
borders
•
Harvest
remove most seed from the field (wheat and Aegilops cylindrica), use grain trucks
hauling seeds to prevent seeds from being blown off the truck, clean machinery
•
Following years
plant a non winter crop in order to use alternative control methods for Aegilops cylindrica,
hand-weed and destroy F1 hybrids (easy to detect because of its big size), add another
spring crop in the following year, do not use herbicide resistant varieties in the next
winter crop (wheat or others), eradicate small Aegilops cylindrica infestations
(SEEFELDT et al. 1999)
A list of assessment needs for the use of transgenic rice varieties was presented by COHEN
et al. (1999).
The potential benefits of the new technology can only be achieved when herbicide resistance
is one of multiple control measures which are chosen in awareness of potential negative
effects. It seems to be necessary to develop and implement weed control decision models
which take into account the various large-scale and long-term implications (poorly
considered by single farmers) and the aims of sustainable production (prevention of erosion
and resistance, conservation of non-target species) mentioned and summarized below.
II MODIFICATION RELATED CONCERNS
STATE OF KNOWLEDGE
•
Data on mammalian toxicity metabolic pathways, solubility and ecotoxicity of herbicides
and the knowledge on their metabolites are not sufficient for a thorough assessment.
•
Bromoxynil causes deformities in unborn children.
•
Application of non-selective herbicides in periods of high rainfall may cause erosion.
•
Glufosinate and glyphosate have an impact on soil microorganisms and the
suppression can last at least 60 days at temperatures lower than 20°C. A reduction of
bacteria and fungi of about 40% and more for more than 8 weeks cannot be without
impact on the microfauna feeding on them.
•
Science–based limits and criteria are missing which classify microbial population
decreases as acceptable or harmful.
•
Some beneficial microorganisms are negatively affected by the two herbicides
gluphostae and glufosinate in contrary to some plant pathogens. The dominance
identity of the soil biocoenosis and proportions of species are changed by the
herbicides.
•
A 95% control of weeds is not necessary for the exclusion of competitive effects of
weeds and associated flora to crops as shown in many studied cases in Europe. A
certain ground coverage of flora and density microorganisms supports (through the
completion of the food chain) beneficial antagonists lowering the need of pesticide
applications. The abundance of associated flora in agriculture is relevant for integrated
plant production (plants supporting beneficial fauna), the prevention of soil erosion and
in high input agriculture regions also for the conservation of species.
•
Practical attempts to delay the development of herbicide resistance in weeds have
failed to date, but models exist.
•
It would be helpful to develop additional selective herbicides or bioherbicides against
prevailing weeds with low economic threshold levels (Galium aparine e.g.) in order to
reduce the need to apply herbicides.
•
The possibly negative effect of non-selective herbicides on the associated non-target
flora is currently investigated in Germany and in Great Britain.
23
24
HERBICIDE RESISTANT PLANTS
CRITERIA FOR RISK ASSESSMENT
•
In general erosion effects, mammalian toxicity, ecotoxicity and the adequacy for
integrated plant production are the main criteria for an assessment of herbicide
resistant plants.
•
The presence of weeds cross pollinating with the herbicide resistant crop and the
potential of volunteer occurrance are important aspects (high impact plants).
•
The occurrence of resistant biotypes to any herbicide in a region indicates the
possibility of a new resistance development. Weeds with high reproductivity are most
problematic ones.
II MODIFICATION RELATED CONCERNS
RECOMMENDATIONS FOR RISK ASSESSMENT AND MONITORING
•
The toxicity of herbicides to cyanobacteria, algae, typical plant pathogens, symbiotic
microorganisms rare microorganisms as well as to a random selection of soil
invertebrates should be tested further.
•
The influence of glufosinate and glyphosate on soil microorganisms should be
assessed in a long term investigation, when these two herbicides, alternative
herbicides and weed control measures are used on different test plots for years. The
effects on rare and stenoecious species as well as biocoenosis changes should be
investigated.
•
Science–based limits which classify a microbial population decrease as harmful or
acceptable through the criteria time-span, quantity and quality (ecological functions of
species, diversity) should be established.
•
Integrated control methods for weeds, soil-borne diseases and insects should not be
studied in isolation but using a multidisciplinary approach.
•
Mammalian toxicity metabolic pathways, solubility and ecotoxicity of herbicides and
their metabolites should further be assessed.
•
Generally the effects of herbicides on insects other than some epigeal arthropods
should be tested.
•
Resistance management strategies should be developed by experts (plant pathology,
population dynamics, farming, industry).
•
Measures for early detection of resistant weeds and genetics of resistance and
prediction of mode and development of resistance should be developed. Also models
describing changes in the seed bank should be used and validated for better
predictions of weed and volunteer problems.
•
The proposals to prevent resistance in weeds should be validated in experiments
(sequence of low doses followed by a moderate dose).
•
Breeding approaches to prevent outcrossing of herbicide resistance genes should
further be developed where necessary. Also, isolation distances for large sources and
large sinks of genes (farm to farm pollination) should be established on the basis of
seed production experiences and knowledge on gene flow (depending on: crop,
pollinator abundance, hybrid variety use).
25
26
HERBICIDE RESISTANT PLANTS
RECOMMENDATIONS FOR THE APPROVAL AND USE OF HERBICIDE
RESISTANT VARIETIES
•
Data an toxicity and ecotoxicity of herbicides should be made availiable for the public.
•
Regulation should support modes of herbicide application which conserve non-target
plants.
•
The implementation of measures like rotating and mixing different weed control
methods in order to prevent erosion (mulch, no-till agriculture), to conserve non-target
associated flora and to prevent the selection of resistant and difficult weeds (economic
threshold determination, row fertilization and application, precision agriculture/patchy
weed control, mechanic weeding, selective herbicides and bioherbicides, crop rotation)
by farmers should be honored and encouraged or made obligatory.
•
For high input agriculture in Europe it is recommended to use herbicide resistance (to
non-selective herbicides) only once in crop rotation.
•
It is recommend to plant strips with beneficial flora species, to plant and conserve field
margin ecosystems including wooden plants and managed set-aside lands in order to
balance side effects in regions of high input agriculture.
•
When crops are interfertile to weeds or weeds are present which are known to quickly
develop resistance, it might be favorable only to use one of the non-selectve herbicides
in a region.
•
It may be useful to establish local advisory centres and boards where independent
experts recommend farming measures and develop obligatory guidelines.
•
A maximum daily intake should be established not only for the pesticides but for their
metabolites as well.
•
An early detection of resistant biotypes and genetics of resistance might be provided
and the occurrence of resistant weed biotypes documented.
•
Herbicides with the same mode of action and crop specificity mechanism should be
labeled and not used in rotation.
•
Parasitic weeds are very sensitive to the herbicides glufosinate and glyphosate. A
dosage adequate for other weeds could easily lead to resistance because of the high
selection pressure and the enormous reproductive potential. Existing alternative control
measures should be taken into account (e.g. prevention of germination).
II MODIFICATION RELATED CONCERNS
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