Genetically Modified Crops and Farmland Biodiversity

Sep 6, 2000

SCIENCE / 1 September, 2000 / Les G. Firbank and Frank Forcella*

The decline in farmland biodiversity is a serious conservation issue in
Great Britain (1). So, it is not surprising that the decision to allow
commercial introduction of genetically modified herbicide-tolerant (GMHT)
crops has been delayed until after the completion of farm-scale evaluations
of the effects of these crops on farmland biodiversity (2). On page 1554 of
this issue, Watkinson et al. (3) propose a mathematical model that seeks to
measure the impact of GMHT sugar beet crops on weed populations in British
fields and the consequences for farmland birds that are dependent on the
weed seeds for food. Their model ties together weed population dynamics,
farmer decision-making, and regional impacts on farmland birds (see the
figure).

Weeds, seeds, and hungry birds. Roger Duncan, a farmer near Hancock,
Minnesota, is a strong advocate of GMHT crops. Behind him is a field of
conventional sugar beet that was grown after 4 years of GMHT
glyphosate-tolerant soybean and glufosinate-tolerant corn. Note that the
weed, Chenopodium album (the large green bush in the foreground), whose
seeds form an important food source for farmland birds, is still abundant.
(Right) Thistles, such as Cirsium arvense, are another important food
source for birds. They are often controlled well in fields of GMHT
glyphosate-tolerant soybean by herbicides such as glyphosate, but not,
however, in this instance where the herbicide was applied only once.
CREDIT: DEAN PETERSON

In their model, a conventional (that is, not genetically modified) sugar
beet crop is grown in a 5-year rotation: Winter cereals are grown for 4
years and then conventional sugar beet is grown in the fifth year. The weed
that Watkinson and colleagues selected to investigate in their model,
Chenopodium album (lambsquarters or fat hen), is found worldwide and its
seeds are an important food source for farmland birds. The seeds of this
annual weed stay dormant in the soil for several years; each year a
proportion of this weed seedbank germinates. The modelers assume that weed
control is perfect during the years that cereals are grown so that new weed
seeds are produced only during the 1 year in 5 that sugar beet is
cultivated. They also assume that the numbers of skylarks (Alauda arvensis)
that feed on C. album seeds is greatest in fields where lots of the weed
seeds are available. Although the authors selected just one weed and one
bird for their model, they presume that their model reflects a wider range
of farmland birds and the weeds that are their food source. With the help
of existing data from herbicide trials, the modelers examined what happens
to the population density of C. album when GMHT rather than conventional
sugar beet is grown in the fifth year of the crop rotation. They calculate
how the altered use of herbicides with the GMHT crop affects the growth of
C. album and hence its seed production, and how this will impact the
skylark that feeds on these seeds.

The model considers a population of British farms, most starting with a
small weed seedbank and the remainder starting with far higher densities of
weed seeds. The use of GMHT sugar beet by the farmers is assumed to depend
on their attitude to the new technology and on whether they wish to apply
it to fields where the weeds are already well under control, or to fields
that are particularly weedy. Watkinson et al. attempt to mimic this in
their model by assuming different weed seed densities before the
introduction of the GMHT crop. Their model assumes that overall seed
production by the weed is a function of the efficiency of weed control by
herbicide during growth of the GMHT crop relative to that during growth of
a conventional sugar beet crop. The seeds of C. album are considered to be
the principal food for wintering skylarks that congregate to fields
according to the density of the weed seedbanks.

Watkinson et al. have provided us with an elegant way to exploit existing
data on herbicide treatment of conventional and GMHT crops and to calculate
the impact of herbicide use on weed seed production and farmland bird
numbers. However, their conclusion that "consequent effects on the local
use of fields by birds might be severe" if GMHT crops are introduced
commercially is questionable in light of experiences with growing GMHT
maize, soybean, canola, and sugar beet in the United States (4).

In the state of Minnesota, sowing dates for conventional crops and their
GMHT counterparts are the same, as are the patterns of weed germination.
Early weed emergence can be controlled by pre-emergence herbicides in both
GMHT and conventional crops. Typically, herbicides are applied at least
twice to conventional crops (more if the crop is sugar beet), often using
different chemicals in sequence to control different weeds. In the case of
GMHT crops, a single broad-spectrum herbicide can be applied without
killing the crop and is used only once or twice after weeds have emerged.
The model considers whether herbicides are applied only when the weed
population density reaches a certain threshold or whether they are applied
regardless of weed density (which is probably more typical). When GMHT
crops are first introduced, weeds are generally well controlled (5).
However, some weed species (for example, Amaranthus rudis) escape control
by germinating after the application of herbicide, and others by being
somewhat tolerant to it (including, ironically, Chenopodium album, which
can become tolerant to glyphosate, the herbicide most widely used with GMHT
sugar beet) (6). There is also the potential for herbicide-resistant weed
varieties to develop over time. Such species will produce more seeds,
changing the weed spectrum and reducing the control achieved with sowing
GMHT crops.

Data from the southern United States, where GMHT crops have been grown
since the mid-1990s, show that there is sometimes less success with weed
control when growing GMHT crops than when cultivating conventional
varieties (7-9). An informal poll that we conducted among weed scientists
indicates that farmers who grow GMHT soybean do so not because weed
management with this crop is more effective, but because it is simpler
(fewer types and fewer applications of herbicide are needed, and timing of
applications is often less critical).

The Watkinson model considers weed densities at equilibrium. Yet, by the
time this equilibrium is reached (presumably over several 5-year rotation
cycles), weed control may be, on balance, comparable between GMHT crops and
conventional varieties (if indeed the technology has not been replaced by
other farming and weed management systems by that time). When equilibrium
is reached, however, the composition of the weed community will have
changed, translating into either gains or losses of food reserves for birds
(10).

Although the assumptions of trophic relations between weed seeds and
skylarks can be questioned in detail, the Watkinson et al. model is
probably robust enough to be applied to many birds and arable plants.
However, the dynamics between weed seeds and birds also depend on what
happens after the seeds have been shed. Many weed seeds will be buried
during harvest and cultivation of GMHT and conventional sugar beet alike,
making them unavailable as food for birds during the winter (11). More to
the point, the main problem for farmland biodiversity in the Watkinson
model is perhaps less the effects of managing weeds during the cultivation
of the GMHT beet crop and more the zero weed seed production during the 4
years of cultivating intensively managed cereals.

Their model considers the relation between adopting GMHT crops and the
numbers of weed seeds in the soil. Experience in Minnesota demonstrates
that farmers may adopt GMHT crops quickly in fields with both high and low
weed seedbanks. This may have less to do with socioeconomic responses to
new technology between farmers than with the desire to simplify weed
control in general while clearing out weeds from fields with high
seedbanks. This seems especially true for sugar beet farmers, who have
found cost-effective weed control very difficult with non-GMHT crops.
Therefore, the relative weed control efficiency factor in the model is
actually a distribution of values, the shape of which may well be a
function of both farmer behavior and the size of the weed seedbank. The
model may not have captured these dynamics very well in detail, but it does
demonstrate the potential sensitivity of farmland bird populations to the
management of very weedy fields. We agree with Watkinson et al.'s
suggestion that "the regional-scale consequences of farm-level decisions
might be the key to predicting the impacts of GMHT crops on biodiversity";
this point has already been recognized within the site selection protocol
for the farm-scale evaluation of GMHT crops in Britain (12).

The Watkinson model provides a welcome conceptual framework for assessing
the impacts of GMHT crops on farmland birds. However, the authors have
concentrated on assumptions and scenarios that emphasize harmful effects,
to the exclusion of those that suggest benefits to biodiversity. For
example, herbicide use in current GMHT crops is frequently later than in
conventional crops, potentially favoring breeding birds. Also, sowing GMHT
crops facilitates minimum tillage, which favors the conservation and
biodiversity of soils, tends to keep more weed seeds near the surface,
increases weed numbers and, again, changes the weed spectrum (13). Both
GMHT and non-GMHT systems can be modified to favor biodiversity: Field
patches can be left unsprayed to provide food for skylark chicks until they
fledge, and winter stubbles and selective spraying can be used to help
maintain bird food resources in the cereal phase of the rotation.

Are GMHT crops good or bad for wildlife? It is simply too soon to tell.
Watkinson et al.'s model raises important scientific questions that only
experiments can answer. As the authors note, these effects depend on the
choices that individual farmers make as well as on the effects of
particular crop management systems. In Britain, the farm-scale evaluations
will provide data on the effects of GMHT crop management on weed
populations and seed return across a representative range of crops and
conditions, including those where the farmer may want to use the new
technology to control high weed levels. The Watkinson analysis shows just
how vital these evaluations will be for revealing the overall effects of
growing GMHT crops on British wildlife.

References and Notes

J. R. Krebs, J. D. Wilson, R. B. Bradbury, G. M. Siriwardena, Nature 400,
611 (1999)

L. G. Firbank et al., Nature 339, 727 (1999).

A. R. Watkinson, R. P. Freckleton, R. A. Robinson, W. J. Sutherland,
Science 289, 1554 (2000).

We thank extension workers and farmers for sharing their experiences with
us.

Genetically Modified Crops and Farmland Biodiversity

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