- Top of page
Indirect effects of pesticides, operating through the food chain, have been proposed as a possible causal factor in the decline of farmland bird species. To demonstrate such a link, evidence is needed of (1) an effect of food abundance on breeding performance or survival; (2) an effect of breeding performance or survival on population change; and (3) pesticide effects on food resources, sufficient to reduce breeding performance or survival, and hence to affect the rate of population change. Evidence under all three categories is only available for one species, the Grey Partridge Perdix perdix, although data showing effects of pesticides on food resources and relationships between food resources and breeding performance are also available for some other species. This paper reports on recent work investigating the effects of pesticides on Yellowhammer Emberiza citrinella and Skylark Alauda arvensis during the breeding season. The probability of brood reduction in Yellowhammer was affected by the proportion of the foraging area around the nest which was sprayed with insecticide. No significant effects of pesticides were recorded on Skylark chick condition or growth rate, but sample sizes were small. Invertebrate food abundance affected chick condition (Skylark) and the number of chicks fledging (Yellowhammer and Corn Bunting Miliaria calandra; relationship for the latter derived from re-analysis of data from an earlier study). Other recent work is briefly reviewed and the current evidence for the indirect effects of pesticides is summarized. Significant knowledge gaps are identified and some of the issues involved in resolving these are discussed.
Concern about the effects of pesticides on birds in the UK was first stimulated by the effects of organochlorine insecticides in the 1950s and 1960s (Newton 1995). Since the withdrawal of these pesticides, populations of affected bird species have largely recovered, and there is now little evidence of significant population effects arising from direct effects of pesticides in the UK, with the possible exception of the potential impacts of new generation rodenticides on predatory bird species such as the Barn Owl Tyto alba and the Red Kite Milvus milvus (Burn 2000).
Although direct effects of pesticides are now less evident than previously, there is still concern about the potential indirect effects of pesticides, operating through the food chain. Impacts of pesticides on weeds and invertebrates may reduce the availability of food resources, affecting productivity and/or adult survival. Three main mechanisms have been identified through which pesticides may affect food availability for birds:
insecticides may deplete or eliminate arthropod food supplies, which are exploited by adults and their dependent young during the breeding season and, in so doing, reduce breeding productivity;
herbicides may reduce the abundance of, or eliminate, non-crop plants that are hosts for arthropods taken as food by farmland birds during the breeding season, and thereby reduce breeding productivity;
herbicides may also deplete or eliminate weed species, which provide either green matter or seeds for herbivorous and granivorous species, respectively, thereby reducing survival of those birds that rely on those food supplies.
The effects of pesticides on arthropods important in chick diet were identified as a major causal factor in the decline of the Grey Partridge Perdix perdix, and this species provides the best documented case study of such effects (Potts 1986). Campbell et al. (1997) reviewed the evidence for the role of indirect effects of pesticides on farmland birds, and concluded that there were possible effects on at least 11 further species, though only for Grey Partridge had such effects been conclusively demonstrated.
In order to test the hypothesis that indirect effects of pesticides are a significant causal factor in declines of bird species, it is necessary to test the existence of relationships at a number of levels within a causal framework or conceptual model. The three key steps in this conceptual model are:
evidence of a relationship between food abundance/availability and breeding performance or survival;
evidence of a relationship between breeding performance or survival and population change;
evidence of pesticide effects on abundance and/or availability of bird food resources, sufficient to reduce breeding performance or survival, and hence to affect the rate of population change.
Evidence of pesticide effects on food resources and relationships between food resources and breeding performance can be obtained through autecological or experimental studies. Apart from research on the Grey Partridge, reviewed by Campbell et al. (1997), such studies have been carried out for Red-legged Partridge Alectoris rufa (Green 1984), Pheasant Phasianus colchicus (Hill 1985), Corn Bunting Miliaria calandra (Brickle et al. 2000) and Yellowhammer Emberiza citrinella (Morris et al. 2002, 2004).
Hill (1985) found a positive relationship between chick survival and insect densities, which accounted for 75% of the variation in chick survival rate. However, Green (1984) found that the diet of Red-legged Partridge chicks was dominated by seeds, leaves and flowers, and they were less dependent upon invertebrates than Grey Partridge and Pheasant chicks. Neither of these studies tested effects of pesticides. Brickle et al. (2000) found that both chick weight and nest survival at the nestling stage for Corn Bunting were negatively correlated with invertebrate food availability, and chick food items were more abundant in foraging areas than in non-foraging areas. Chick food abundance was negatively correlated with number of insecticide applications to cereal fields, although relationships with herbicide and fungicide use were non-significant. However, when all foraging habitats were considered, chick food abundance was significantly negatively correlated with numbers of applications of insecticides, fungicides and herbicides. Furthermore, fields in which Corn Buntings foraged received fewer applications of herbicide, fungicide and insecticide on average than fields which were not used.
Morris et al. (2002, 2004) found that three measures of invertebrate numbers (‘all’ invertebrates, ‘important’ invertebrates and invertebrates ≥ 5 mm) and biomass were all significantly lower in fields treated with insecticide during the summer than in fields with no or winter-only insecticide applications. There was weaker and less consistent evidence for effects of fungicides and herbicides.
Yellowhammer nestling diet on British arable farmland includes cultivated cereal grain, once it becomes semi-ripe. For earlier nests, where foraging took place before grain was available, foraging density (Morris et al. 2001) in fields that received no summer applications of insecticide was nearly four times higher than in fields with summer applications. However, for later nests where grain was available, insecticides did not significantly affect foraging patterns.
Chick condition was related to number of insecticide applications. There was a weak positive relationship between mean brood condition and number of applications up to one application, and a strong negative relationship with more than one application. However, no relationships were detected between pesticide use and chick survival in this study.
Further evidence of pesticide effects on food resources comes from the Game Conservancy Trust's Sussex study. Analysis of long-term monitoring data over an area of 62 km2 showed negative relationships between herbicide use and weeds, and also between insecticide use and invertebrates, over a period of 25 years. Effects of summer insecticides on invertebrate numbers were greater than effects of insecticides applied in the autumn, although significant effects of autumn-applied insecticides were detected. Densities of Grey Partridge, Corn Bunting and Skylark were higher where the number of pesticide applications was low (Ewald et al. 2002).
Relationships between food abundance and survival are more difficult to demonstrate because of the difficulty in measuring adult survival for most species at a local level, and predictive depletion modelling has therefore been recommended to estimate the potential impacts of variations in food supply, in the absence of direct measurements (Stephens et al. 2003). The establishment of relationships between breeding performance and/or survival and population change relies on the availability of long-term monitoring or survey data. Demographic models of such relationships have been developed for a number of species, based on large-scale survey data (e.g. Siriwardena et al. 1998a, 1998b, 2000), but only for Grey Partridge has a direct relationship between breeding performance and survival of a monitored population been demonstrated (Potts 1986, Potts & Aebischer 1991, 1995).
This paper describes further work carried out since the review of Campbell et al. (1997), and summarizes the current evidence for indirect effects of pesticides. Previously unpublished results are presented from autecological work on Skylark Alauda arvensis, carried out on commercially farmed study sites, and models are derived relating Corn Bunting and Yellowhammer chick survival to invertebrate food abundance, based on data collected by Brickle et al. (2000) and Morris et al. 2004). We also present data for Yellowhammer from a designed experiment set up specifically to test the hypothesis that indirect effects can impact on spring settling densities and breeding success.
- Top of page
In the studies described above, we have identified and defined relationships between invertebrate abundance and chick condition or survival for three passerines: Yellowhammer, Corn Bunting and Skylark. In addition, new evidence is provided that the probability of brood reduction in Yellowhammer was related to the proportion of the foraging area around the nest which was sprayed with insecticide. Yellowhammers are known to forage in non-crop areas such as field margins as well as within crops (Perkins et al. 2002), but although such alternative habitats were available at the study sites, either the food resources were not adequate to offset the effects of the insecticide applications or the insecticides also affected invertebrate populations in the field margins. The analyses did not include any allowance for the amount of non-crop habitat available, but in most cases this is likely to have been similar between nests.
Further evidence obtained from analysis of a subsample of Yellowhammer nests from the Yorkshire experimental site, for which nest-specific invertebrate samples were available, showed significant relationships between insecticide use and chick food arthropods, between chick food arthropods and chick condition, between chick food arthropods and chick growth rate, and between chick growth rate and chick survival (J. Hart unpubl. data). Although no significant effects of pesticides on Skylark chick condition or growth rate were detected, sample sizes were small, and so it is not possible to rule these out. At Loddington, a significant relationship was detected between Skylark chick condition and the abundance of chick food invertebrates, in spite of the very small sample size (11 nests). Further data on Skylarks are required before firm conclusions can be drawn about potential effects of pesticide use.
Table 5 summarizes current knowledge derived from quantitative studies of the indirect effects of pesticides on bird species via impacts on chick food abundance. In addition to the galliforms Grey Partridge, Red-legged Partridge and Pheasant, there is now evidence that pesticide use can affect breeding performance of the passerine species Yellowhammer and Corn Bunting. However, studies on Barn Swallow Hirundo rustica showed no effects of pesticides on food taxa or foraging behaviour of this species (Evans 2001).
Table 5. Evidence of effects of pesticides on farmland birds.
|Species||Effect of pesticides||Effect of chick food availability||Effect of breeding performance on population change|
|Food abundance||Foraging behaviour||Chick condition||Chick growth rate||Brood size/ chick survival|
|Grey Partridge1||*||*||*|| ||*||*|
|Red-legged Partridge2|| || || || ||*|| |
|Pheasant3||*|| || || ||*|| |
|Barn Swallow4||NS||NSa|| || || || |
|Skylark5|| || ||*||NSa||NSa|| |
|Corn Bunting7||*||*||*|| ||*|| |
Effects of pesticides may still occur even when their effects are not readily apparent. For example, even where no effects on brood reduction occur, chicks that fledge in poor condition are likely to have a lower probability of post-fledging survival. Furthermore, with low probabilities of survival to the next breeding season, parent birds may compromise their own survival probability by working harder to feed their chicks when density of invertebrate prey is low (Bradbury et al. 2003).
Unfortunately, there are no studies that provide evidence to assess the relationship between breeding performance and population change for these species. Demographic analyses have been used to indicate the key demographic rates causing population change. On the basis of such analyses, changes in adult survival rates have been proposed as the causal factor in the decline of the Yellowhammer, although the demographic mechanisms are by no means certain. There are some aspects of these analyses that may cause difficulties in interpretation, for example the lack of data on post-fledging survival rates and numbers of breeding attempts, and the exclusion of density dependence from such analyses (Siriwardena et al. 2000). Furthermore, the source of data on breeding productivity used in these analyses was the BTO's Nest Record Scheme, which provides estimates of nest failure rates but does not provide data on partial brood loss.
Bradbury et al. (2000) found that Yellowhammer nest survival rates in Oxfordshire were high, but that productivity per pair was probably too low to maintain a stable population. In the current study, data from the designed experiment indicated that productivity per pair was lower at all three sites in the treatment year than the mean of 3.27 recorded by Bradbury et al. (2000) (J. Hart unpubl. data). Whereas Yellowhammers typically have two or three nesting attempts (Bradbury et al. 2000), Corn Buntings are now largely single brooded, at least in Sussex (Brickle & Harper 2002). Brickle (1999) modelled the population dynamics of Corn Buntings in Sussex, and concluded that productivity was the most likely cause of decline in his study area. Evidence of indirect effects of pesticides was found in the same study, indicating that pesticides could have played a role in the Corn Bunting decline, at least in this area.
In the absence of direct relationships between breeding performance and population change, simple population models based on the types of relationship reported here could be used to model the potential impact of pesticides on population change under different scenarios, using estimated distributions of values from the literature for life-cycle stages for which data have not been collected. The predictions of such models could inform the development of a framework for risk assessment (Boatman et al. 2003).
Of the three main mechanisms identified in the introduction to this paper, through which pesticides may affect food availability for birds, the evidence presented here is concerned solely with Type 1 effects, i.e. the effects of insecticides acting directly on invertebrates eaten by birds. Evidence for Type 2 effects has only been convincingly demonstrated for the Grey Partridge. The use of herbicides affects the abundance of invertebrate prey (e.g. Moreby & Southway 1999, Hawes et al. 2003), but data are largely limited to empirical observations of relationships between weed and invertebrate abundance, and information needed for the construction of mechanistic models is generally lacking.
Herbicides also affect weed seed production, thereby potentially reducing the availability of seed food for granivorous bird species (e.g. Heard et al. 2003), resulting in possible Type 3 effects. Relationships between bird feeding densities and seed densities have been demonstrated for several species (e.g. Robinson & Sutherland 1999), but the implications for survival and population change remain unclear. Yellowhammers responded to the provision of supplementary seed in the designed experiment described above, in terms of numbers of feeding birds, and there was some evidence of greater settling densities in the following spring where seed was supplied (T. Milsom unpubl. data).
There is some evidence that population dynamics of Linnet Carduelis cannnabina and Turtle Dove Steptopelia turtur have been influenced by Type 3 indirect effects. The decline in the Linnet population coincided with reductions in the abundance of key weed species that provided the bulk of seeds for chicks, and preceded a dietary switch by Linnets to the unripe seeds of oilseed rape and dandelions (Moorcroft et al. 1997). The key weed species are known to be vulnerable to herbicides. Evidence for a demographic response by Linnets to changes or reductions in the availability of seeds for chicks is circumstantial: Linnet populations breeding in areas where oilseed rape and dandelions are scarce settle at low densities, breed later, and suffer high levels of brood reduction and of complete brood starvation (Moorcroft 2002).
Turtle Doves also feed extensively on weed seed supplies during the breeding season (Browne & Aebischer 2003) and may ultimately rely upon them. Several of the weed species that feature extensively in the Turtle Dove diet (e.g. Chickweed Stellaria media) have undergone widespread declines on farmland in Britain in recent years (Firbank & Smart 2002), and are susceptible to the frequency of herbicide use (Ewald & Aebischer 1999). It is probable that the reduction in the number of breeding attempts made each year may be responsible for the decline in Turtle Dove numbers (Browne & Aebischer 2004). The shortening of the breeding season may be the result of food shortages later in the summer but further work will be required to confirm this.
Table 6 compares the current situation, regarding evidence for indirect effects of pesticides, with the list of definite and potential effects presented by Campbell et al. (1997). The current list of species considered to be at risk from the indirect effects of pesticides differs significantly from that compiled by Campbell et al. (1997). Indirect effects on one species in the ‘possible’ category in Campbell's list, Barn Swallow, have been provisionally ruled out, whereas they have been demonstrated for two species on the ‘qualified possible’ list, Corn Bunting and Yellowhammer. Turtle Dove, which was not considered by Campbell et al., is provisionally identified as being at risk. Finally, the position of nine species on Campbell's list, five in the ‘possible’ category and four in the ‘qualified possible’ category, is unclear because the requisite data are still lacking.
Table 6. Comparison of lists compiled by Campbell et al. (1997), and the present status of evidence for species regarded as being at risk from the indirect effects of pesticides.
|Species1||Campbell et al.2||Current evidence3|
|Grey Partridge Perdix perdix||Y||Y|
|Tree Sparrow Passer montanus||P||(P)|
|Bullfinch Pyrrhula pyrrhula||P||n.d.|
|Song Thrush Turdus philomelos||P||n.d.|
|Lapwing Vanellus vanellus||P||(N)|
|Reed Bunting Emberiza schoeniclus||P||n.d.|
|Skylark Alauda arvensis||P||P|
|Linnet Carduelis cannabina||P||(P)|
|Barn Swallow Hirundo rustica||P||(N)|
|Blackbird Turdus merula||P||n.d.|
|Starling Sturnus vulgaris||P||n.d.|
|Corn Bunting Miliaria calandra||(P)||Y|
|Spotted Flycatcher Muscicapa striata||(P)||n.d.|
|Sand Martin Riparia riparia||(P)||n.d.|
|Mistle Thrush Turdus viscivorus||(P)||n.d.|
|Yellow Wagtail Motacilla flava flavissima||(P)||(P)|
|Dunnock Prunella modularis||(P)||n.d.|
|Yellowhammer Emberiza citronella||(P)||Y|
|Red-backed Shrike Lanius collurio||(P)||(P)|
|Turtle Dove Streptopelia turtur||–||(P)|
A number of potential measures are available to offset indirect effects of pesticides. The most obvious is minimizing the use of potentially damaging pesticides. This applies particularly to insecticides, which are generally applied in response to a pest outbreak. Wherever possible, thresholds should be applied and spraying only carried out when pest levels exceed thresholds. In some cases, a choice of products is available, and in such cases, the product that is less toxic to non-target species is to be preferred. There may also be scope for altering the timing or dose applied to reduce impacts on non-target organisms.
Where there is use of products known to be harmful to bird food resources, measures to reduce impact may be taken, such as leaving an untreated buffer zone around the edge of the field (mitigation), or alternative food-rich habitat may be provided (compensation). An example of the former is the use of unsprayed or ‘conservation’ headlands around cereal fields, which have been shown to increase the survival of Grey Partridge chicks (Rands 1985, 1986). A number of suitable measures are now funded by the European Union and national governments under agri-environment schemes.