5 Direct and indirect effects on the agro-environment

The biological features, combined with the HR technology, as shown above, may entail direct, indirect, immediate, delayed and/or cumulative agro-environmental effects (Table 1 and 2).

Effects on the agro-environment may be induced by single or several different mechanisms; these may work singly or cumulatively (Graef, 2009*). The agro-environmental effects may be detected at a single scale or at multiple levels.

Section 6 discusses whether the effects are considered to be adverse, positive, not relevant or relevant for monitoring, whether they require further studies for the ERA or raise the concern of an environmental risk leading to deny approval, or whether they may constitute an environmental damage (Bartz et al., 2009*) that merits withdrawal of approval.

Effects directly or indirectly linked to sugar beet biology: Bolting, formation of groundkeepers, along with the high rate and distance of pollen spread and cross-pollination (Drießen et al., 2001; OECD, 2006) may trigger HR gene flow to neighbouring non-GM sugar beet, weed beets, wild beets and related wild species. The preconditions are spatial concurrence (Frese, 1998) and inefficient prevention of flowering by agricultural practice.

The potential increase of HR sugar beet in the seed banks, which may incorporate viable HR seeds over 10 years, may lead to persisting and invasive HR weed beets, wild beets and related wild species in fields and natural habitats. The preconditions: a selection advantage due to repeated glyphosate application, enhanced fitness parameters and genetic drift. Wilkinson et al. (2000) and Snow (2003) observed this for HR oilseed rape. Cultivated beet genes can persist in wild beet (Bartsch et al., 1999; Sukopp et al., 2005). If HR weed beets, wild beets and related wild species become invasive, this may variously impact habitats, food chains and biodiversity (Watkinson et al., 2000*; Züghart and Breckling, 2003*).

A horizontal gene transfer of HR from plant residues to soil microorganisms is rare but possible, irrespective of the HR trait (Heinemann and Traavik, 2004; Nielsen and Townsend, 2004), but its environmental implications are hard to determine. Another general ecological concern is the potential for a) adverse combinatory effects when GMHR sugar beet hybridises with weed beets, wild beets and related wild species that potentially affect the hybrid’s biology and/or herbivores and b) pleiotropic and epigenetic genome effects of the GM crop caused by the genetic modification procedure, as shown for instance with GM wheat (Zeller et al., 2010). These unintended and unanticipated effects, for instance on non-target organisms (NTOs), must be considered, especially when performing the ERA (GMO Panel, 2010*).

Effects directly or indirectly linked to the HR technology: More efficient weed suppression leads to less biomass, food and flowers for field organisms after spraying. This, in turn, entails lower abundances of various herbivores, pollinators and beneficial species (pest antagonists) (Bohan et al., 2005*; Heard et al., 2003b*), and may decrease agrobiodiversity (Watkinson et al., 2000*). A shift in weedy species (Heard et al., 2003b*,a*) and an increase of perennial weeds due to minimum-till practice is likely (Frick and Thomas, 1992*). Extending the HR technology may have various potential effects on field organisms and soil bio-geochemical cycles on the larger landscape scale (Benton et al., 2002*; Cerdeira and Duke, 2006*). Another ecological concern is possible adverse indirect effects on migratory and mobile species, leaf litter quality, crop competitiveness, and insect resistance (Squire et al., 2003*).

Applying glyphosate formulations compared to other herbicides has adverse effects on fields and neighbouring habitats. These include increased mortality of amphibians (Relyea, 2005a*,b*,c*) and mammals (Richard et al., 2005; Benachour and Séralini, 2009*) and, in combination with simultaneous exposure to parasites, reduced survival of freshwater fish (Kelly et al., 2010*). Adverse direct or indirect glyphosate effects were also reported for micronutrient uptake (Tesfamariam et al., 2009*), soil microflora and plant disease severity (Fernandez et al., 2009*; Heuer et al., 2002; Johal and Huber, 2009*; Kremer and Means, 2009*). This can hamper soil functions or bio-geochemical cycles (Züghart and Breckling, 2003*). Glyphosate formulations containing surfactants such as POEA (polyethoxylated tallow amine) are more toxic than the ai glyphosate alone (Benachour and Séralini, 2009*), in particular for aquatic organisms (Brausch and Smith, 2007). Some studies also indicate less herbicide toxicity and persistency than other herbicides (Agronomy Guide, 2010*; Cerdeira and Duke, 2006*; Squire et al., 2003*).

Until post-emergent spraying, more biomass is available for feeding organisms (Werner et al., 2000*; Strandberg et al., 2005*). After spraying, however, biomass drops compared to conventional spraying. Furthermore, spraying is usually done before weed seed development (Dewar et al., 2000), reducing the weed seed bank in the long term. Early band applications combined with late overall treatments may enhance biomass availability during the growing period (May et al., 2005). Nonetheless, seed development and abundance in arable flora are also reduced in the long run. Post-emergent spraying may increase herbicide drift into the agro-environment, for example due to increased spraying height (Johnson, 2001*). Post-emergent spraying also often entails a change in spray schedules of insecticides and fungicides, with potential implications for microbial and faunal activity (Champion et al., 2003*; Thorbek and Bilde, 2004*).

To control possible HR sugar beet volunteers in follow crops, modified crop rotations may be necessary. This may require farmers to change the tillage system (Schütte et al., 2004*), affecting field organisms and soil bio-geochemical cycles (McLaughlin and Mineau, 1995*; Orson, 2002). It may also require more ai, different types of herbicides or higher spraying frequency to control HR in weeds (Van Acker et al., 2003*). Again, this can impact agrobiodiversity. Coexistence measures to reduce gene flow may change agricultural practice and entail various environmentally relevant effects.

Table 2: Potential agro-enviromental effects across spatial scale levels linked to the HR technology and relevant to the ERA and PMEM (Graef, 2009*, modified).

Practice changes

Chain of potential agro-environmental effects





laboratory or greenhouse experiments

field trials or observations

landscape-scale experiments or observations


introduction of HR technology

increased weed suppression  less biomass, food, flowers and habitats for field organisms after spraying  lower abundance of various herbivores, pollinators and beneficial species (pest antagonists)  decrease in agrobiodiversity


20, 25

3, 6, 7, 9, 28, 33, 36, 37, 38



development of herbicide tolerance in weeds



3, 4, 9, 16, 35, 44



reduced crop rotation options



3, 9,



decrease and/or shift of weedy species and weed seedbank



4, 16, 28, 33, 35, 36, 37, 38, 44



little or no evidence: impact on migratory and mobile species, changed quality of plant parts, changed crop competitiveness, changed insect resistance, pleiotropic and epigenetic genome effects, impact on soil functions


20, 23

4, 21, 22, 36


 reduced herbicide ai amount, reduced no. of spray rounds, use of glyphosate only

less negative impacts on field organisms and/or soil compaction


1, 23, 25

2, 3, 12, 13


 higher herbicide & insecticide applications in formerly not cultivated areas

various adverse effects on field and aquatic organisms and/or soil bio-geochemical cycles



3, 22, 23, 29, 31


 glyphosate use instead of other more persistent or toxic herbicides

less residual activity to followcrops, less adverse effects on field organisms



2, 4, 8


 glyphosate use instead of other less toxic herbicides

adverse effects on field organisms and/or aquatic communities in cropped fields and neighbouring habitats, higher glyphosate concentrations in surface and ground waters

26, 40


4, 22, 36, 41



adverse effects on fungal communities, diseases and nutrient availability


10, 11, 15, 39

10, 45


 post-emergent spraying

more biomass for feeding organisms until spraying



5, 9, 28, 33, 36



less erosion due to more weed biomass and residues



4, 8



increased drift and pollution due to higher late-season wind speeds and/or increased spraying height


6, 27



 change in spray schedules of insecticides and fungicides due to modified herbicide spraying

positive or negative implications for microbial and/or fauna activities



9, 13, 22, 37


 minimum till associated with HR sugar beet cultivation

increased competitiveness of perennial weeds



14, 32



less soil compaction, higher soil biodiversity


24, 34

4, 8, 9


control of HR sugar beet volunteers in followcrops

reduced crop rotation options (e.g., wider rotations or crops with other HR traits)  various positive or negative implications for field organisms and soil bio-geochemical cycles



3, 32



changes in tillage system  positive or negative implications for soil degradation and erosion



3, 17, 32


control of increased HR in weeds

increased ai amount, different types of herbicides, higher spraying frequency



3, 12, 18, 22, 42



 various adverse effects on field organisms and/or soil bio-geochemical cycles



3, 17, 29, 32


in case of increased yield potential  increased fertiliser use

increased nutrient leaching





coexistence measures to reduce vertical gene flow

reduced crop rotation options, isolating fields of GMHR sugar beet



13, 19



 various positive or negative implications for field organisms and/or soil bio-geochemical cycles



22, 26, 32


1References legend (E: Expert opinions; M: Models; R: Review; O: Original data): 1 (Champion and May, 2004  O); 2 (Kleter et al., 2007  R); 3 (Schütte et al., 2004  E, R); 4 (Cerdeira and Duke, 2006  R); 5 (Bohan et al., 2005  O); 6 (Owen, 1999  E); 7 (Krebs et al., 1999  E, R); 8 (Agronomy Guide, 2010  E, O); 9 (Werner et al., 2000  E, M, R); 10 (Johal and Huber, 2009  R); 11 (Fernandez et al., 2009  O); 12 (Benbrook, 2009  R, O); 13 (Champion et al., 2003  O); 14 (Frick and Thomas, 1992  O); 15 (Tesfamariam et al., 2009  O); 16 (Beckie et al., 2006  R, O); 17 (Van Acker et al., 2003  E, R); 18 (Légère, 2005  E, R); 19 (Schiemann, 2003  E); 20 (Firbank and Forcella, 2000  E, R); 21 (Regal, 1994  E, R); 22 (Züghart and Breckling, 2003  R); 23 (Watkinson et al., 2000  M, E); 24 (Jordan et al., 2004  O); 25 (Strandberg et al., 2005  O); 26 (Relyea, 2005a,b,c  O); 27 (Johnson, 2001  E, O); 28 (Heard et al., 2003b  O); 29 (Robinson and Sutherland, 2002  R, O); 30 (Pacini et al., 2003  O); 31 (Benton et al., 2002  R, O); 32 (McLaughlin and Mineau, 1995); 33 (Heard et al., 2003a  O); 34 (Thorbek and Bilde, 2004  O); 35 (Owen and Zelaya, 2005 / O); 36 (Squire et al., 2003  O); 37 (Hole et al., 2005  R); 38 (Firbank et al., 2006  O); 39 (Larson et al., 2006  O); 40 (Benachour and Séralini, 2009  O); 41 (Popp et al., 2008  O); 42 (Sanyal et al., 2008  E,O); 43 (Kelly et al., 2010  O); 44 (Johnson et al., 2009  R); 45 (Kremer and Means, 2009  O); 46 (Zobiole et al., 2010 / O)

2Evidence of effects among the references based on the data quality aspects a) how closely the measured or observed effects and indicators resemble the actual effects and indicators about which information is desired; b) quality, mode and accuracy of the methodological design and the degree to which empirical or expert observations have been used to produce the data; c) statistical design, number of replications, spatio-temporal representativeness (Graef, 2009)

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