CHAPTER 43 CHAPTER 43 Indirect Effects of Pesticides on Farmland Wildlife
43.4 INDIRECT EFFECTS OF PESTICIDES ON OTHER FARMLAND WILDLIFE .1 Benefits of Conservation Headlands for Other Farmland Wildlife
Evidence for the indirect effects of pesticides on grey partridges can be readily extended to declines of other farmland species of wildlife. Certainly, in our large-scale experiments in southern and eastern England, other species of gamebirds responded to the presence of increased food resources provided in cereal crop edges where pesticide regimes were modified. Although not in decline, the red-legged partridge also responded to the increased food resource. Mean brood sizes were generally larger with increased chick-food insect densities, but differences become statistically significant between treatment only when data from all study areas were pooled.21 The benefits of Conservation Headlands have been similarly demonstrated for a wide range of species, not just in the United Kingdom but also in Sweden120 and The Netherlands.121 Mean brood sizes of ring-necked pheasant (Phasianus colchicus) also increased significantly in the presence of crop edges receiving reduced levels of pesticides.21,106
Data on the effects of Conservation Headlands on other species of birds are more variable. In an extensive survey of passerine birds in hedgerows and adjacent crops during the breeding season, the presence of three species of bird — greenfinch (Carduelis chloris), robin (Erithacus rubecula), and song thrush (Turdus philomelos) — was lower in hedgerows adjacent to autumn-sown cereals, which had received pesticides, compared to the presence of those species adjacent to autumn crops which were fully sprayed. Most other species showed similar, but insignificant, differences. How- ever, most species showed a tendency towards higher incidences in hedgerows adjacent to spring- sown cereals with reduced pesticide inputs than in those adjacent to fully sprayed spring-sown crops.
There was no manipulative or experimental aspect to this study, and no comment as to mechanisms involved was made.122 Insecticide drift into hedgerows poses a threat to birds, both directly as found for nesting great tits (Parus major) and also indirectly through the removal of invertebrate food.123 In the Netherlands, Conservation Headlands were used in preference to standard crop edges by the insectivorous bird, Motacilla flava flava,124 probably because phytophagous insect densities were higher. However, skylarks (Alauda arvensis), which feed on plants as well as insects at ground level, avoided the Conservation Headlands, probably because of their extensive weed growth.124
In another survey of the use made by a farmland bird in an arable farmland habitat, it was found that corn buntings (Miliaria calandra), a species in steep decline in the United Kingdom,
also responded to the use of pesticides and the density of insect chick-food items thereby pro- duced.125 Adults preferentially foraged in areas of high chick-food-insect density, and density was negatively correlated with the number of insecticide applications made that season. Low chick- food-insect abundance close to nests resulted in greater distances travelled from the nest by foraging parents and longer trip durations. Nestling weight was positively correlated with insect abundance.
Finally, the probability of nest survival was negatively correlated with the abundance of chick-food insects close to the nest, apparently as a result of increased predation.125
During the course of the experiments on crop margins, the recommendations for pesticide use changed from a no-spray moratorium after January 1 to a selective regime called Conservation Headlands, whereby broad-leaved weed herbicides and summer insecticides were restricted. At this time, the study on nongame species began. Benefits of Conservation Headlands to butterflies (Lepidoptera) started in the mid-1980s with some simple censuses using standard techniques. Over a 5-year period, significantly more individuals representing 13 species were found in Conservation Headlands compared to headlands that were fully sprayed. When pesticide use was reduced, Lepidoptera numbers increased.126–128
Detailed observations of butterfly behavior in the two headland treatments have shown that flight speed and duration were lower in Conservation Headlands.129 Activity patterns also changed, with some species showing different behaviors between spray management regimes. Small white (Pieris rapae) males spent almost all of their time in flight in field margins that had fully sprayed headlands, with little time devoted to either feeding or resting. In field margins with Conservation Headlands, the proportion of time spent in flight was radically reduced, with a much higher proportion of time spent in feeding and resting.129 Pieris rapae males observed in fully sprayed field margins also spent most of their time in the hedgerow area, whereas the hedgerows were virtually ignored in field margins where there were Conservation Headlands.
For many species of strongly flying butterflies (Pieridae and Nymphalidae), the nectar provided by weeds such as charlock (Sinapsis arvensis), field pansy (Viola arvensis), and creeping thistle (Cirsium arvense) attracted them into Conservation Headlands. The larval host plants of some of the Pieridae (S. arvensis and rape, Brassica napus) were found in Conservation Headlands126 and were exploited as larval food plants. Increased numbers of such species as green-veined white (Pieris napi), P. rapae and orange tip (Anthocharis cardamines) may also have been caused by their presence. However, the host plants of the Satyridae, Hesperiidae, Nymphalidae, and Lycae- nidae were not found in the Conservation Headlands. Indeed, those of the satyrids and hesperiids (Graminea) were selectively controlled using herbicides. This was fortunate, as any eggs laid in Conservation Headlands could constitute lost reproductive effort following destruction by harvest and tillage.
For some species, it was not possible to make sufficient observations in fully sprayed headlands because of low numbers. However, such an explanation cannot be applied to all species recorded on farmland in southern England. No such speculation of time spent between the sprayed and selectively sprayed headland treatments could be found for meadow brown (Maniola jurtina) males,129 while other species such as the gatekeeper (Pyronica tighonus) spent their time in the hedgerow regardless of the spray regime in the adjacent cereal crop edge. However, the abundance of both these species was clearly greater adjacent to Conservation Headlands,126 despite our inability to explain these differences in terms of their behavior. It may have been that when hedgerow nectar was scarce, unsuitable, or unavailable, headland nectar was used to “top-up,” or act as the major nectar source.
Another possible explanation for the increased abundance of hedgerow species could be the reduced pesticide drift into field boundaries where the spray boom was switched off 6 m away from the field edge. Conservation Headlands may be acting as buffer zones, protecting hedgerows from summer insecticides and broad-leaved residual herbicides throughout the year. The amount of pesticide deposition into field boundaries adjacent to Conservation Headlands and fully sprayed crop edges has been measured in both the autumn and summer. The crop in the Conservation
Headland buffer zone absorbed a significant amount of pesticide before it reached the noncropped area of the field boundary, thereby reducing spray drift.130 Levels of mortality of P. brassicae larvae exposed to grass upon which insecticide deposits had drifted from fully sprayed and selectively sprayed crops were significantly different. Very high mortality (100%) was found in larvae exposed to vegetation collected from fully sprayed sections of crop compared to much lower levels of mortality of larvae (18%) exposed to vegetation collected from vegetation adjacent to an nonsprayed headland.130 Conservation Headlands were also shown to reduce pesticide drift by 95%, and thus contamination of watercourses and risk to aquatic wildlife decreased.121
So, for the Lepidoptera, evidence for both direct and indirect routes of exposure to pesticides was found. Longer-term trends in relative abundance have been established on the study farm over a 5-year period and comparisons made with data derived from the U.K.’s National Butterfly Monitoring Scheme. For two satyrid species (M. jurtina and P. tithonus), populations were either maintained or increased relative to 1984 levels at the study farm. This compares with the south–southeast region of the National Butterfly Monitoring Scheme (many of the incorporated sites being National Nature Reserves), where these species showed declines over the same period.126
Other groups of beneficial insects, including the stenophagous and polyphagous natural enemies of cereal pests, may also benefit from the resources provided in Conservation Headlands or from the degree of exclusion of the adverse effects of pesticides that they provide. Reinvasion of a dimethoate-treated field by epigeal invertebrates was quicker and more extensive in the half sur- rounded by unsprayed outer 6-m border compared to areas fully sprayed.71 The authors concluded that this was because the margins from which the reinvading arthropods originated were protected from spray drift. Indeed, arthropod abundance is usually greatest at the field edges, declining into the field.94,131 Preliminary work has also shown how some economically important species of hover fly (Diptera: Syrphidae) such as Episyrphus balteatus made use of the nectar and pollen of flowering weeds in Conservation Headlands such as S. arvensis, Matricaria spp., and C. arvense.132,133 Similarly, bumblebees made use of the pollen resources provided by arable weeds in Conservation Headlands.134 Again, analysis of the behavior of adult flies showed that they were retained in the weedy strips because they were foraging on the weeds.135
Overall numbers and, in some years, diversity of carabid beetles were higher in unsprayed edges; this was especially true of the spermophagous species, which were responding to the greater abundance of weeds.136 Microclimate will change if weed cover increases, and this may influence species composition, as carabids differ in their environmental requirements.137 Polyphagous species, such as the carabid beetles Pterostichus melanarius and Agonum dorsale were also better fed (i.e., a significantly higher proportion of males, gravid females, and nongravid females had all four portions of their digestive tracts full of solid food remains) in Conservation Headlands compared to individuals from fully sprayed crop edges. It is possible that the greater prey availability (larger numbers and more diverse alternative prey items) may increase predator numbers through improved diet and fecundity.100 For all these groups of nontarget insects, there is evidence of benefit from the increased provision of food resources (pollen, nectar invertebrates) as a result of the reduced use of pesticides.
43.4.1.1 Farmland Birds
In a recent review of the indirect effects of pesticides on birds, the authors concluded that many species of birds fed on a varied diet of plant and invertebrate species found on farmed land. In most groups of farmland birds, populations are either declining or stable and increasing, but in two
— the thrushes and the buntings — all species are in decline.41 The authors conclude from the available data that their food items are also in decline on U.K. farmland. They found that in the majority of studies, the use of pesticides resulted in short-term reductions in the abundance of bird food items and that such effects could persist for weeks or months after initial applications.41 Many cite these short-term reductions as being unimportant and of little impact on breeding success of
birds. For example, when the impact of two insecticides, Deltamethrin and Furadan, on the chestnut- collared longspurs (Calcarius ornatus), which feeds predominantly on grasshoppers, were com- pared, both insecticides decreased grasshopper populations by more than 90%, but the number of grasshoppers in nestling diets was only decreased in nests within the deltamethrin-sprayed plots.138 However, the insecticide spraying did not decrease the total biomass of arthropods delivered to the nestlings, and nestling weight and size were unaffected. In this case, birds overcame the effect of the insecticide spraying by foraging further, although previously this was shown not to occur.
Instead, their diet changed.138 In contrast, another species present, the Baird’s sparrow (Ammodra- mus bairdii), abandoned many of its nests in plots treated with the other insecticide, Furadan.138 This difference between species occurred because the design of experiments, the pesticides, and bird species involved can all influence the outcome of field based studies.139 Thus, the timing of such insect reductions during the stage when nestlings need feeding could be crucial.
Strong temporal associations between the start of the declines and the widespread use of pesticides in cereals were also found.41 Strong associations (more than 50% of cereals treated at the beginning of the population decline) of 11 bird species to the use patterns of herbicides were cited. For fungicides, the researchers found associations with six species but no associations for insecticides or molluscicides. For these two pesticide groups, they only refer to probable associations where between 10 and 50% of cereals were treated. However, for 11 out of 12 species, they identify the year the decline started, and those were during a period of increasing pesticide use.41
For other declining species, there is evidence, but not experimental proof, that the cause is related to pesticide use and the resulting reductions of bird food, both plant and insect material, in the summer to feed chicks and as seeds to feed birds over the winter. However, for these species, other hypotheses linking the declines to changing agriculture practices are equally compelling to explain these declines in the United Kingdom and Canada.41,93
Where pesticides use is eliminated, as in organic production, the benefits would be expected to be greatest. A survey of farms in the United Kingdom revealed higher numbers of birds on organic compared to conventional farms.140 However, the organic farms were characterized by smaller fields with a greater proportion of hedgerows and more diverse crop rotations, and the effect of eliminating pesticide use could consequently not be separated out as the determining factor in the bird increases. Invertebrate food sources for birds have been found to be higher in Danish organic cereal fields,141 but the differences were lower at the edge compared to the field center, which explains why fewer differences were found between organic compared to conventional cereal fields in the United Kingdom, where only edge samples were taken.142 In Canada, birds typical of wetland areas were more abundant in the wetland areas on organic farms and in wild areas compared to on conventional farms or those using conservation tillage.143 Overall differences in avifaunal density and diversity between the farming systems were small in comparison to differences between farms and wild sites, again emphasizing the importance of noncrop habitats.
43.4.1.2 Other Wildlife
Evidence for the direct and indirect effects of pesticides on other wildlife is less comprehensive than for birds and invertebrates. The pyrethroid insecticides commonly used in temperate farmland areas are not regarded as toxic to mammals,144 but organophosphorus insecticides are highly toxic and can also reduce activity levels.145 Insecticides have also been shown to directly reduce the reproductive ability of small mammals, the impact varying between species leading to a change in their competitive ability.146 As a consequence, the duration of effect lasted longer than the insecticide (diazinon) persisted in the environment.
Amphibians are in worldwide decline, but the causes behind these declines are complex,147 although pesticides are considered to be the most important factor in agricultural areas.16 Insecticides originating from intensive agricultural areas were responsible for the decline in riverine amphibian populations,148 and this may occur through direct toxicity149 or morphological changes that reduce
survival.16,150 The herbicide atrazine has also been shown to cause morphological changes.151 However, there is no evidence that indirect effects through reduced food availability or habitat modification are contributing to these declines, although this is a possibility.