Open access

Impact of Systemic Insecticides on Organisms and Ecosystems

Written By

Francisco Sánchez-Bayo, Henk A. Tennekes and Koichi Goka

Submitted: May 3rd, 2012 Published: January 30th, 2013

DOI: 10.5772/52831

Chapter metrics overview

3,757 Chapter Downloads

View Full Metrics

1. Introduction

Systemic insecticides were first developed in the 1950s, with the introduction of soluble organophosphorus (OP) compounds such as dimethoate, demeton-S-methyl, mevinphos and phorate. They were valuable in controlling sucking pests and burrowing larvae in many crops, their main advantage being their translocation to all tissues of the treated plant. Systemic carbamates followed in the 1960s with aldicarb and carbofuran. Since then, both insecticidal classes comprise a large number of broad-spectrum insecticides used in agriculture all over the world. Nowadays, OPs are the most common pesticides used in tropical, developing countries such as the Philippines and Vietnam, where 22 and 17% of the respective agrochemicals are ‘extremely hazardous’ [126], i.e. classified as WHO class I. Systemic insect growth regulators were developed during the 1980-90s, and comprise only a handful of compounds, which are more selective than their predecessors. Since 1990 onwards, cartap, fipronil and neonicotinoids are replacing the old hazardous chemicals in most developed and developing countries alike [137].

Through seed coatings and granular applications, systemic insecticides pose minimal risk of pesticide drift or worker exposure in agricultural, nurseries and urban settings. Neonicotinoids and fipronil are also preferred because they appear to be less toxic to fish and terrestrial vertebrates. Initially proposed as environmentally friendly agrochemicals [129], their use in Integrated Pest Management (IPM) programs has been questioned by recent research that shows their negative impact on predatory and parasitic agents [221, 258, 299]. New formulations have been developed to optimize the bioavailability of neonicotinoids, as well as combined formulations with pyrethroids and other insecticides with the aim of broadening the insecticidal spectrum and avoid resistance by pests [83]. Indeed, as with any other chemical used in pest control, resistance to imidacloprid by whitefly (Bemisia tabaci), cotton aphids (Aphis gossypii) and other pests is rendering ineffective this and other neonicotinoids such as acetamiprid, thiacloprid and nitenpyram [247, 269].

This chapter examines the negative impacts that systemic insecticides have on organisms, populations and ecosystems. The efficacy of these products in controlling the target pests is assumed and not dealt with here – only the effects on non-target organisms and communities are considered.

Advertisement

2. Exposure to systemic insecticides

Unlike typical contact insecticides, that are usually taken up through the arthropod’s cuticle or skin of animals, systemic insecticides get into the organisms mainly through feeding on the treated plants or contaminated soil. Thus, monocrotophos and imidacloprid are more lethal to honey bees (Apis mellifera)through feeding than contact exposure [143]. Residual or contact exposure affects also some pests and non-target species alike.

Systemic insecticides are applied directly to the crop soil and seedlings in glasshouses using flowable solutions or granules, and often as seed-dressings, with foliar applications and drenching being less common. Being quite water soluble (Table 1), these insecticides are readily taken up by the plant roots or incorporated into the tissues of the growing plants as they develop, so the pests that come to eat them ingest a lethal dose and die. Sucking insects in particular are fatally exposed to systemic insecticides, as sap carries the most concentrated fraction of the poisonous chemical for a few weeks [124], whereas leaf-eating species such as citrus thrips and red mites may not be affected [30]. Systemic insecticides contaminate all plant tissues, from the roots to leaves and flowers, where active residues can be found up to 45-90 days [175, 187], lasting as long as in soil. Thus, pollen and nectar of the flowers get contaminated [33], and residues of imidacloprid and aldicarb have been found at levels above 1 mg/kg in the United States [200]. Guttation drops, in particular, can be contaminated with residues as high as 100-345 mg/L of neonicotinoids during 10-15 days following application [272]. Because these insecticides are incorporated in the flesh of fruits, the highly poisonous aldicarb is prohibited in edible crops such as watermelons, as it has caused human poisoning [106].

As with all poisonous chemicals spread in the environment, not only the target insect pests get affected: any other organism that feeds on the treated plants receives a dose as well, and may die or suffer sublethal effects. For example, uptake of aldicarb by plants and worms results in contamination of the vertebrate fauna up to 90 days after application [41], and honey bees may collect pollen contaminated with neonicotinoids to feed their larvae, which are thus poisoned and die [125]. Newly emerged worker bees are most susceptible to insecticides, followed by foraging workers, while nursery workers are the least susceptible within 72 h of treatment [80]. Insects and mites can negatively be affected by systemic insecticides whenever they feed on:

  1. pollen, nectar, plant tissue, sap or guttation drops contaminated with the active ingredient (primary poisoning);

  2. prey or hosts that have consumed leaves contaminated with the active ingredient (secondary poisoning).

Parasitoids may be indirectly affected because foliar, drench or granular applications may decrease host population to levels that are not enough to sustain them. Furthermore, host quality may be unacceptable for egg laying by parasitoid females [54]. Small insectivorous animals (e.g. amphibians, reptiles, birds, shrews and bats) can also suffer from primary poisoning if the residual insecticide or its metabolites in the prey are still active. It should be noticed that some metabolites of imidacloprid, thiamethoxam, fipronil and 50% of carbamates are as toxic as the parent compounds [29]. Thus, two species of predatory miridbugs were negatively affected by residues and metabolites of fipronil applied to rice crops [159]. However, since systemic insecticides do not bioaccumulate in organisms, there is little risk of secondary poisoning through the food chain.

Apart from feeding, direct contact exposure may also occur when the systemic insecticides are sprayed on foliage. In these cases, using a silicone adjuvant (Sylgard 309) reduces the contact exposure of honey bees to carbofuran, methomyl and imidacloprid, but increases it for fipronil [184]. In general the susceptibility of bees to a range of insecticides is: wild bees > honey bee > bumble bee [185]. In reality a combination of both contact and feeding exposure occurs, which is more deadly than either route of exposure alone [152, 218].

In soil, residues of acephate and methomyl account for most of the cholinesterase inhibition activity found in mixtures of insecticides [233]. Fortunately, repeated applications of these insecticides induces microbial adaptation, which degrade the active compounds faster over time [250]. Degradation of carbamates and OPs in tropical soils or vegetation is also faster than on temperate regions, due mainly to microbial activity [46]. Some neonicotinoids are degraded by soil microbes [172], and the yeast Rhodotorula mucilaginosacan degrade acetamiprid but none of the other neonicotinoids [63], which are quite persistent in this media (Table 2).

ChemicalGroupVapour Pressure(mPa, 25oC)Solubilityin water (mg/L)Log Kow#GUS index*Leaching potential
aldicarbC3.8749301.152.52moderate
bendiocarbC4.62801.720.77low
butocarboximC10.6350001.11.32low
butoxycarboximC0.266209000-0.814.87high
carbofuranC0.083221.83.02high
ethiofencarbC0.519002.043.58high
methomylC0.72550000.092.20marginal
oxamylC0.051148100-0.442.36moderate
pirimicarbC0.4331001.72.73moderate
thiodicarbC5.722.21.62-0.24low
thiofanoxC22.652002.161.67low
triazamateC0.134332.59-0.9low
cartapD1.0 x 10-10200000-0.95-high
halofenozideIGR<0.01312.33.343.75high
hexaflumuronIGR0.0590.0275.68-0.03unlikely to leach
novaluronIGR0.0160.0034.30.03low
teflubenzuronIGR0.0000130.014.3-0.82low
acetamipridN0.00017329500.80.94low
clothianidinN2.8 x 10-83400.9054.91high
dinotefuranN0.001739830-0.5494.95high
imidaclopridN0.00000046100.573.76high
nitenpyramN0.0011590000-0.662.01moderate
thiaclopridN0.00000031841.261.44unlikely to leach
thiamethoxamN0.00000664100-0.133.82high
acephateOP0.226790000-0.851.14low
demeton-S-methylOP40220001.320.88low
dicrotophosOP9.31000000-0.53.08high
dimethoateOP0.25398000.7041.06low
disulfotonOP7.2253.951.29low
fenamiphosOP0.123453.3-0.11low
fosthiazateOP0.5690001.682.48moderate
heptenophosOP6522002.320.26low
methamidophosOP2.3200000-0.792.18moderate
mevinphosOP176000000.1270.19low
monocrotophosOP0.29818000-0.222.3moderate
omethoateOP3.310000-0.742.73moderate
oxydemeton-methylOP2.01200000-0.740.0low
phorateOP112503.861.4low
phosphamidonOP2.9310000000.792.39moderate
thiometonOP39.92003.150.37low
vamidothionOP1.0 x 10-104000000-4.210.55low
fipronilPP0.0023.783.752.45moderate

Table 1.

Physicochemical properties of systemic insecticides.

C = carbamates; D = dithiol; IGR = Insect growth regulator; N = neonicotinoid; OP = organophosphate; PP = phenylpyrazole


# Partition coefficients between n-octanol and water (Kow) indicate bioaccumulation potential when Log Kow > 4.


*The Groundwater Ubiquity Score (GUS) is calculated using soil half-life (DT50) and organic-carbon sorption constant (Koc) as follows: GUS = log(DT50) x (4-log Koc). A compound is likely to leach if GUS > 2.8 and unlikely to leach when GUS < 1.8; other values in between indicate that leaching potential is marginal.

ChemicalGroupWaterField
Photolysis (pH 7)Hydrolysis (pH 5-7)Water-sedimentSoil (range)
aldicarbC8189610 (1-60)
bendiocarbC132524 (3-20
butocarboximCSta blestable-4 (1-8)
butoxycarboximCStable18 (510-16)-42
carbofuranC7137 (46-0.1)9.714 (1-60)
ethiofencarbC-165237 (34-131)
methomylCStablestable47 (5-30)
oxamylC78<111
pirimicarbC6stable1959 (5-13)
thiodicarbC930 (69-0.3)<118 (1-45)
thiofanoxC130-4 (2-6)
triazamateC3012<1<1
cartapD---3
halofenozideIGR10stable-219(60-219)
hexaflumuronIGR6stable-170
novaluronIGRStablestable1897 (33-160)
teflubenzuronIGR10stable1614 (9-16)
acetamipridN34420a-3 (2-20)
clothianidinN0.114 a56545(13-1386)
dinotefuranN0.2stable-82 (50-100)
imidaclopridN0.2~ 365a129191(104-228)
nitenpyramNNA2.9 a-8
thiaclopridNstablestable2816 (9-27)
thiamethoxamN2.711.5 a4050 (7-72)
acephateOP250-3
demeton-S-methylOP-56 (63-8)-2.7
dicrotophosOP---28
dimethoateOP17568 (156-4)157 (5-10)
disulfotonOP43001530
fenamiphosOP<1304602 (1-50)
fosthiazateOPStable104(178-3)5113 (9-17)
heptenophosOP-1371
methamidophosOP905244 (2-6)
mevinphosOP2717211 (1-12)
monocrotophosOP26134-30 (1-35)
omethoateOPStable17514
oxydemeton-methylOP22273 (96-41)35
phorateOP13-63 (14-90)
phosphamidonOP-36 (60-12)1312 (9-17)
thiometonOP-22-2 (2-7)
vamidothionOP-11971 (<1-2)
fipronilPP0.33stable6865 (6-135)

Table 2.

Degradation of systemic insecticides expressed as half-lives in days. Compounds with half-lives longer than 100 days are considered persistent (Sources: Footprint database & [284].

a for pH 9

C = carbamates; D = dithiol; IGR = Insect growth regulator; N = neonicotinoid; OP = organophosphate; PP = phenylpyrazole

Aquatic organisms take up easily whatever residues reach the waterbodies, through runoff from treated fields or contaminated groundwater. Some 20% systemic insecticides are prone to leaching, and 45% are mobile in wet soils (Table 1). For example, acephate leaches more easily than methamidophos [305], and so acephate should be restricted or avoided in tropical areas and rice crops [46]. Residues of aldicarb and methomyl in groundwater can have sublethal effects in mammals [215]. Even if residue levels of systemic insecticides in rivers and lakes are usually at ppb levels (μg/L), persistent compounds such as fipronil, neonicotinoids and growth regulators can have chronic effects due to their constant presence throughout several months in the agricultural season [123]. For example, about 1-2% of imidacloprid in treated soil moves into runoff after rainfall events, with the highest concentrations recorded at 0.49 mg/L [12]. Systemic carbamates and OPs do not last long in water because they breakdown through photolysis or hydrolysis in a few days, or are taken up and degraded by aquatic plants [100]. In any case, their presence and frequency of detection in water depends on local usage patterns [39, 171]. The acute toxicity of most systemic compounds is enhanced in aquatic insects and shrimp under saline stress [22, 253].

A characteristic feature of most systemic insecticides –except carbamates– is their increased toxicity with exposure time, which results from a constant or chronic uptake through either feeding or aquatic exposure (Figure 1). Effects are more pronounced some time after the initial application [16], and could last up to eight months [286]. Also, as a result of chronic intoxication, there may not be limiting toxic concentrations (e.g. NOEC or NOEL) in compounds that have irreversible mechanism of toxicity, since any concentration will produce an effect as long as there is sufficient exposure during the life of the organism [274]. This is precisely their main advantage for pest control: any concentration of imidacloprid in the range 0.2-1.6 ml/L can reduce the population of mango hoppers (Idioscopusspp.) to zero within three weeks [291]. However, it is also the greatest danger for all non-target species affected, e.g. predators, pollinators and parasitoids. By contrast, contact insecticides act usually in single exposures (e.g. spray droplets, pulse contamination after spraying, etc.) and have the highest effects immediately after application.

Figure 1.

Increasing toxicity of several systemic insecticides with time of exposure. LD50 for acephate toEpisyrphus bateatusand for methomyl toBombus terrestris[75]; LC50 for imidacloprid toCypridopsis vidua[234] and thiacloprid toSympetrum striolatum[28].

Advertisement

3. Modes of action of systemic insecticides

Before describing their impacts on organisms and ecosystems, a description of the mechanisms of toxicity of systemic insecticides is briefly outlined.

3.1. Acetylcholinesterase inhibitors

Carbamates and organophosphorus compounds are inhibitors of the acetylcholinesterase enzyme (AChE), thus blocking the transmission of the nervous impulse through the neuronal synapses. The binding of carbamates to the enzyme is slowly reversible and temporary, i.e. < 24 h [197], whereas that of alkyl OPs is irreversible. The binding of methyl-OPs does not last as long as that of alkyl-OPs, and this feature is compound specific [182]. Given their mode of action, all these compounds are broad-spectrum insecticides, extremely toxic to most animal taxa, from worms to mammalian vertebrates. Avian species are often more susceptible to these compounds due to relatively low levels of detoxifying enzymes in birds [207, 297]. Thus, recovery of ducklings exposed to a range of carbamate and OP insecticides occurred within eight days after being depressed 25-58% following dosing [91].

3.2. Insecticides acting on nicotinic acetylcholine receptors (nAChR)

Neonicotinoids are derived from nicotine, which is found in the nightshade family of plants (Solanaceae), and particularly in tobacco (Nicotiana tabacum). They all are agonists of the nicotinic acetylcholinesterase receptor (nAChR), which mediate fast cholinergic synaptic transmission and play roles in many sensory and cognitive processes in invertebrates. Binding of neonicotinoids to these receptors is irreversible in arthropods [40, 307]. Given that nAChRs are embedded in the membrane at the neuronal synapses, their regeneration seems unlikely because neurons do not grow. The lower affinity of neonicotinoids for mammalian nAChRs has been attributed to the different ionic structure of the vertebrate subtypes [283]. The high toxicity of neonicotinoids to insects and worms is comparable to that of pyrethroids, but aquatic crustaceans, particularly waterfleas, are more tolerant [119, 136].

Cartap is a dithiol pro-insecticide that converts to nereistoxin, a natural toxin found in marine Nereismolluscs. Both cartap and nereistoxin are antagonists of the nAChR in insects and other arthropods [164], blocking irreversibly the neuronal functions of these receptors. Unlike neonicotinoids, cartap appears to be very toxic to fish and amphibians [235].

3.3. GABA-R antagonists (fipronil)

Fipronil is a phenylpyrazole antagonist of the γ-aminobutyric acid (GABA)-gated chloride channel, binding irreversibly to this receptor and impeding the nervous transmission [56]. Its mode of action, therefore, appears to be identical to that of cyclodiene organochlorins (e.g. endosulfan), but fipronil is mostly systemic whereas all cyclodienes are insecticides with contact activity. Interestingly, while aquatic organisms (e.g. cladocerans, fish) are quite tolerant of fipronil, vertebrates are more susceptible to this compound than to the old organochlorins [235].

3.4. Insect growth regulators (IGR)

Hexaflumuron, novaluron and teflubenzuron are the only systemic benzoylureas in the market. They are chitin inhibitors, blocking the biosynthesis of this essential component of the arthropod’s exoskeleton. As a consequence, insects and other arthropods cannot moult and die during their development. Since their mode of action is restricted to arthropods, benzoylureas are not very toxic to any other animal taxa, e.g. molluscs, vertebrates, etc. [235].

Halofenozide is the only systemic compound among the hydrazines, a group of chemicals that mimic the steroidal hormone ecdysone, which promotes moulting in arthropods [71]. The premature moulting in larvae of some insect taxa, particularly in Lepidoptera, prevents them from reaching the adult stage. Toxicity of halofenozide is selective to insects only.

Advertisement

4. Effects on organisms and ecosystems

4.1. Direct effects on organisms

Mortality of non-target organisms exposed to insecticides is mostly due to acute toxicity, particularly in the case of carbamates. However, with systemic compounds there are many observations of long-term suppression of populations that suggest a chronic lethal impact over time. The latter impacts are likely due to persistence of residual activity in the soil, foliage or water in the case of reversible toxicants (i.e. carbamates), or to irreversible and persistent binding in other cases. (note: all application rates and concentrations here refer to the active ingredient).

4.1.1. Acetylcholinesterase inhibitors

These compounds can have serious impacts on soil organisms of various taxa. Aldicarb and phorate applied to a cotton crop soil at 0.5 and 1 kg/ha, respectively, eliminated or reduced significantly non-target mesofauna, including mites and springtails. Populations of the latter taxa were reduced for more than 60 days (phorate) and 114 days (aldicarb) [17, 225], with the highest effects peaking after 18 days [16]. Granular applications of phorate (250 mg/kg dry soil) killed almost all earthworms, Collembola, Acarina, free-living saprophytic and parasitic nematodes and Protozoa, with populations of Collembola recovering only when residues went below 2 mg/kg [300]. After a single aldicarb application to soil at 2.5 g/m2, Gamasina predatory mites went to extinction within a year [148]. Bendiocarb impacts on predaceous arthropods and oribatid mites were less severe and temporary compared to the impacts of non-systemic OPs, but increased trap catches of ants two weeks after application [55], possibly as a result of a longer-term effect. Many soil arthropods, in particular mites and springtails, were the most affected by dimethoate –and its metabolite omethoate– residues in soil after sprays of 1-2 ml/L in the farms of the Zendan valley, Yemen [4]. Similar observations were made when dimethoate was sprayed on vegetation of arable fields [85] or in soil microcosms [180]; the springtail populations recovered but attained lower densities a year later, while their dominance structure had changed. However, dimethoate or phosphamidon applied in mustard fields produced only a temporary decline, compared to the long-lasting effect of monocrotophos [141]. Collembola populations do not seem to be affected by pirimicarb applications on cereal crops [95].

Earthworm populations were affected initially after application of phorate and carbofuran to turfgrass, but not thiofanox, and their numbers recovered subsequently [53]. Reduction of earthworm populations by bendiocarb was the highest (99% in one week) among 17 insecticides applied at label rates on turfgrass, with significant effects lasting up to 20 weeks [216]. Juveniles and species living in the surface layers or coming to the soil surface to feed (e.g., Lumbricus terrestris) are most affected, since a high degree of exposure is usually found in the first 2.5 cm of soil [288]. However, systemic carbamates can be selective to plant-parasitic nematodes without affecting fungal or microbial communities [296]. Thus, cholinesterase inhibitors do not have significant impacts on bacteria, fungi and protozoa in soil [133], and consequently do not alter the soil biochemical processes [79]. Nevertheless, a combined dimethoate-carbofuran application reduced active hyphal lengths and the number of active bacteria in a treated forest soil [58].

Populations of beneficial predators can be decimated initially as much as the target pests, but they usually recover quickly. For example, thiodicarb or its degradation product, methomyl, applied at 0.5 kg/ha on soybean crops, significantly reduced populations of the predatory bugs Tropiconabis capsiformisand Nabis roseipenniswithin two days after treatment only [25]. Demeton-S-methyl reduced populations of predatory insects on strawberry patches, whereas pirimicarb and heptenophos had no significant effect on spiders, staphylinids and anthocorids, or on hymenopteran parasitoids [76]. While populations of web spiders and carabid beetles are severely reduced by dimethoate applied to cabbage fields and cereal crops [144], pirimicarb does not seem to have much impact on these taxa [97, 195], affecting mainly aphids [131]. Pirimicarb on wheat crops does not impact on ladybirds, but larvae of Episyrphus balteatusare affected [135]. By contrast, longer impacts have been observed with acephate applied at 0.5 kg/ha on rice paddies, which reduced populations of predatory bugs (Cyrtorrhinus lividipennisand Paederus fuscipes) for at least 10 days [155]. Similar rates of acephate on rice and soybean crops reduced spiders populations for three weeks, but they recovered afterwards [181]. In addition, acephate is deadly to three species of whitefly parasitoid species [267].

Direct mortality of bumble bees (Bombus terrestris) in short exposures to dimethoate is much higher than for heptenophos or ethiofencarb [132]. However, what matters most is the chronic toxicity to the entire bee colony not just the workers. For example, methamidophos contaminated syrup (2 mg/L) produced significant losses of eggs and larvae of honey bees without any appreciable loss of workers after one week of exposure; the colonies would recover completely within 13 weeks if the insecticide was applied only once [301], indicating a long-term impact on the colony. Similarly, the mortality of non-target adult chrysomelid beetles (Gastrophysa polygoni) after foliar treatment with dimethoate on the host plants was low (1.9-7.6%), but because this insecticide was most toxic to the egg stage, the overall beetle population decreased over time due to hatching failure [146].

Primary poisoning of birds and mammals by ingestion of OP and carbamate granules or coated seeds is still a problem despite the many attempts to reduce these impacts [189, 190]. For example, mortality of birds that ingested granules of carbofuran in a corn field was extensive, affecting waterfowl, small songbirds and mice within 24 hours. Residues up to 17 mg/kg body weight (b.w.) were found in the dead animals [19]. The granular formulation of this carbamate was banned in the mid-1990s by the US EPA after numerous cases of direct poisoning by animals; however, the liquid formulation applied to alfalfa and corn is just as deadly to bees, because this systemic insecticide is present in the pollen of those plants [208]. Phosphamidon sprayed at 1 kg/ha to larch forests in Switzerland caused many bird deaths [243]; large bird mortality was also observed in Canadian spruce forests sprayed with phosphamidon (0.55 kg/ha), particularly among insectivorous warblers. There was good evidence that birds picked up the insecticide from sprayed foliage within a few hours of application [94]. Carbofuran and phosphamidon were the most common pesticides implicated in deaths of wild birds in Korea between 1998-2002 [157], and ducklings died in large numbers when phorate was applied to South Dakota wetlands [73]. Usually birds die when their brain AChE depression is over 75% [92, 114]. Thus, 11 out of 15 blue jays (Cyanocitta cristata) which had depression levels ranging 32-72% after disulfoton was sprayed to pecan groves would die [302], but their carcasses would probably not be found. In orchards sprayed with methomyl, oxamyl or dimethoate, the daily survival rates for nests of Pennsylvania mourning dove (Zenaida macroura) and American robin (Turdus migratorius) were significantly lower than in non-treated orchards, and the species diversity was also lower. Repeated applications of these and other insecticides reduced the reproductive success of doves and robins and may have lowered avian species diversity [93].

Secondary poisoning with bendiocarb was attributed to 22 birds that had depressed AChE activity after eating contaminated mole crickets and other soil organisms on the applied turfgrass [224]. Several species of raptors were killed or debilitated after consuming waterfowl contaminated with phorate – the fowl had ingested granules of the insecticide that were applied to potato fields a few months earlier [84]. Equally, ladybugs (Hippodamia undecimnotata) fed upon Aphis fabae, which were reared on bean plants treated with carbofuran, experienced a 67% population reduction due to secondary poisoning [206]. Pirimicarb caused 30-40% mortality of Tasmanian brown lacewing (Micromus tasmaniae) larvae when feeding on contaminated 1st instar lettuce aphid (Nasonovia ribisnigri) for three days [298].

Impacts on aquatic organisms usually do not last more than a month. For example, thiodicarb applied at 0.25-1.0 kg/ha had severe impacts on copepods, mayflies and chironomids in experimental ponds for three weeks, but not so much on aquatic beetle’s larvae; eventually there was recovery of all populations [7]. Pirimicarb can be lethal to common frog (Rana temporaria) tadpoles, but does not appear to have chronic effects [139]. However, vamidothion and acephate are most lethal to non-target organisms in rice crops, and are not recommended in IPM programs [153]. Carbofuran and phorate are very toxic to aquatic invertebrates [140], particularly amphipods and chironomids but not so much to snails, leeches or ostracods [72, 249]. Small negative effects in zooplankton communities (cladocerans copepods and rotifers) were observed in rice paddies treated with carbofuran at recommended application rates, but fish were not affected [107]. Carbofuran should not be used in rice paddies, whether in foliar or granular formulations: not only induces resurgence of the brown planthoppers (Nilaparvata lugens) [122], but it is also more toxic to the freshwater flagellate Euglena gracilisthan the non-systemic malation [15]. It reduces populations of coccinellid beetles, carabid beetles, dragonfly and damselfly nymphs, but does not impact much on spiders [255]. However, it appears that carbofuran at 0.2% per ha can double the densities of Stenocypris majorostracods in rice paddies, whereas other insecticides had negative effects on this species [168]. Repeated applications of carbofuran can also have a significant stimulation of the rhizosphere associated nitrogenase activity, with populations of nitrogen-fixing Azospirillumsp., Azotobactersp. and anaerobic nitrogen-fixing bacteria increasing progressively up to the third application of this insecticide [142].

4.1.2. Insecticides acting on nAChR

Direct toxicity of cartap to fish species is not as high as that of other neurotoxic insecticides, with 3-h LC50s between 0.02 and 6.8 mg/L [161, 308]. However, cartap affects negatively several species of Hymenoptera and aphid parasitoids used to control a number of crop pests [14, 77, 147, 270]. This insecticide also inhibits hatching of eggs of the nematode Agamermis unka, a parasite of the rice pest Nilaparvata lugens[50], and reduces significantly the populations of ladybugs and other predatory insects in cotton crops when applied at the recommended rates, i.e. 20 g/ha [109, 169]. In rice paddies, cartap hydrochloride reduced populations of coccinellid beetles, carabid beetles, dragonflies and damselflies by 20-50% [255]. Pollinators such as honey bees and bumble bees can also be seriously reduced in numbers when feeding on crops treated with cartap hydrochloride, which is included among the most toxic insecticides to bees after neonicotinoids and pyrethroids [179, 278]. For all its negative impacts on parasitoids and predatory insects it is hard to understand why cartap was the third most common insecticide (19% of all applications) used in IPM programs in Vietnam a decade ago [31], and is still among the most widely used in rice farms in China [308].

Cumulative toxicity of neonicotinoids over time of exposure results in long-term pest control compared to the impact of cholinesterase inhibitor insecticides. For example, soil treated with clothianidin at 0.05-0.15% caused increasing mortality in several species of wireworms (Coleoptera: Elateridae), reaching 30-65% after 70 days, whereas chlorpyrifos at 0.15% produced 35% mortality within 30 days but no more afterwards [292]. Soil application of imidacloprid did not eliminate rapidly Asian citrus psyllid (Diaphorina citri) and leafminer (Phyllocnistis citrella) populations, but resulted in chronic residues in leaf tissue and long-term suppression of both pests [245]. Also, soil applications of neonicotinoids are very effective in controlling soil grubs and berry moths (Paralobesia viteana) in vineyards provided there is no irrigation or rain that washes off the insecticide [289]. For the same reason, however, the impact of neonicotinoids on non-target organisms is long-lasting. For example, repeated corn-seed treatement with imidacloprid caused a significant reduction in species richness of rove beetles in three years, even though the abundance of the main species was not affected [88]. In addition to long-term toxicity, acute toxicity of acetamiprid, imidacloprid and thiomethoxam to planthopper and aphid species is similar to that of synthetic pyrethroids, and higher than that of endosulfan or acetylcholinesterease inhibitors [219, 246]. Thus, combinations of pyrethroid-neonicotinoid have been hailed as the panacea for most pest problems as it suppresses all insect resistance [70]. Mixtures of imidacloprid and thiacloprid had additive effects on the toxicity to the nematode Caenorhabditis elegansbut not on the earthworm Eisenia fetida[108].

Acute toxicity of imidacloprid, thiamethoxam, clothianidin, dinotefuran and nitenpyram to honey bees is higher than that of pyrethroids, while toxicity of acetamiprid and thiacloprid is increased by synergism with ergosterol-inhibiting fungicides [134, 242] and antibiotics [116]. Thus, neonicotinoids can pose a high risk to honey bees, bumble bees [176, 263] and wasps [90]. Bees can be killed immediately by direct contact with neonicotinoid droplets ejected from seed drilling machines. Thus, numerous worker bees were killed when seed was coated with clothianidin during drilling of corn in the Upper Rhine Valley (Germany) in spring 2008 [102]. The same problem happened in Italy with thiamethoxam, imidacloprid and clothianidin [105, 285], leading to the banning of this application method on sunflower, canola and corn during 2008-09 [20]. However, most of the time bee colonies are intoxicated by feeding on contaminated pollen and nectar [9, 228]. It has been observed that bee foraging was notably reduced when Indian mustard was treated with 178 mg/ha imidacloprid [10]. Imidacloprid residues in sunflowers are below the no-adverse-effect concentration to honey bees of 20 μg/kg at 48-h [241], with surveys in France showing residue levels in pollen from treated crops in the range 0.1-10 μg/kg and average in nectar of 1.9 μg/kg [33]. However, bees feeding on such contaminated pollen or nectar will reach first sublethal and later lethal levels, with 50% mortality occurring within 1-2 weeks [228, 266]. Such data was disputed [89, 240] as it was in conflict with some long-term field observations of honey bees feeding on sunflowers grown from imidacloprid-treated seeds at 0.24 mg/seed [256]. However, recent evidence suggest that chronic lethality by imidacloprid is implicated in the colony collapse disorder (CCD) that affects honey bees [174]. Based on the fast degradation of imidacloprid in bees (4-5 hours), it is assumed that honey bees which consume higher amounts of imidacloprid die already outside of the hive, before the colony’s demise and before samples are taken, though residues of imidacloprid in bees at 5-8 μg/kg have been found in some cases [111]. Clothianidin residues of 6 μg/kg in pollen from canola fields reduced the number of bumble bee (Bombus impatients) workers slightly (~20%) [96], but exposure to clothianidin-treated canola for three weeks appeared not to have affected honey bee colonies in Canada [61]. Thiamethoxam applied to tomatoes (~150 g/ha) through irrigation water does not have impacts on bumble bees (Bombus terrestris) [244], whereas pollen contaminated with this insecticide causes high mortality and homing failure [125].

Negative impacts of neonicotinoids on non-target soil arthropods are well documented. A single imidacloprid application to soil reduced the abundance of soil mesofauna as well as predation on eggs of Japanese beetle (Popillia japonica) by 28-76%, with impacts lasting four weeks. The same level of impact was observed with single applications of clothianidin, dinotefuran and thiamethoxam, so the intended pest control at the time of beetle oviposition runs into conflict with unintended effects – disruption of egg predation by non-target predators [210]. Among several insecticides applied to home lawns, only imidacloprid suppressed the abundance of Collembola, Thysanoptera and Coleoptera adults, non-oribatid mites, Hymenoptera, Hemiptera, Coleoptera larvae or Diptera taxonomic groups by 54-62% [209]. Imidacloprid applied to the root of eggplants (10 mg/plant) greatly reduced most arthropod communities and the species diversity during the first month. Small amounts of soil residues that moved into the surrounding pasture affected also some species; however, non-target ground arthropods both inside and outside the crop showed significant impacts only in the two weeks after planting [238], probably due to compensatory immigration from nearby grounds.

Foliar applications of thiamethoxam and imidacloprid on soybean crops are preferred to seed treatments, as neonicotinoids appear to have lesser impacts on non-target communities than pyrethroids [204]. However, a foliar application of thiacloprid (0.2 kg/ha) to apple trees reduced the population of earwigs (Forficula auricularia), an important predator of psyllids and woolly apple aphid, by 60% in two weeks, while remaining below 50% after six weeks [294]. Branchlets of hemlock (Tsuga canadensis) treated with systemic imidacloprid (1-100 mg/kg) reduced the populations of two non-target predators of the hemlock woolly adelgid (Adelges tsugae) and had both lethal and sublethal effects on them [78]. Clothianidin, thiamethoxam and acetamiprid were as damaging to cotton crop predators as other broad-spectrum insecticides and cartap [169]. All neonicotinoids are lethal to the predatory mirid Pilophorus typicus, a biological control agent against the whitefly Bemisia tabaci, since their residual activity can last for 35 days on the treated plants [201]. The ladybug Serangium japonicum, also a predator of the whitefly, is killed in large numbers when exposed to residues of imidacloprid on cotton leaves applied at the recommended rate (40 ppm) or lower; apparently, the predator was not affected when imidacloprid was applied as systemic insecticide [120]. Clothianidin is 35 times more toxic to the predatory green miridbug (Cyrtorhinus lividipennis48-h LC50 = 6 μg/L) than to the main pest of rice (Nilaparvata lugens48-h LC50 = 211 μg/L), thus questioning seriously its application in such crops [221]. Not surprisingly, populations of predatory miridbugs and spiders suffered an initial set back when rice paddies were treated with a mixture of ethiprole+imidacloprid (125 g/ha), and their recovery was slow and never attained the densities of the control plots [154]. Mixtures of ethiprole+imidacloprid and thiamethoxam+l λ-cyhalothrin on rice paddies are also highly toxic to mirid and veliid natural enemies of rice pests, with 100% mortalities recorded in 24 h [159].

Secondary poisoning with neonicotinoids reduces or eliminates eventually all predatory ladybirds in the treated areas, compromising biological control in IPM programs. Indeed, exposure of larval stages of Adalia bipunctatato imidacloprid, thiamethoxam, and acetamiprid, and adult stages to imidacloprid and thiamethoxam, significantly reduced all the demographic parameters in comparison with a control –except for the mean generation time–, thus resulting in a reduced coccinellid population; adult exposures produced a significant population delay [162]. Eighty percent of 3rd and 4th instar larvae of the ladybug Harmonia axyridisdied after feeding for 6 hours on corn seedlings grown from seeds treated with clothianidin, compared to 53% mortality caused by a similar treatment with thiamethoxam; recovery occurred only in 7% of cases [196]. Survival of the ladybird Coleomegilla maculataamong flower plants treated with imidacloprid at the label rate was reduced by 62% [251], and Hippodamia undecimnotatafed upon aphids reared on bean plants treated with imidacloprid, experienced a 52% population reduction [206]. Equally, 96% of Tasmanian brown lacewing (Micromus tasmaniae) larvae died after feeding on 1st instar lettuce aphid (Nasonovia ribisnigri) for three days. Low doses did not increase mortality but from days 3 to 8, lacewing larvae showed significant evidence of delayed developmental rate into pupae [298]. Grafton-Cardwell and Wu [110] demonstrated that IGRs, neonicotinoid insecticides, and pyrethroid insecticides have a significant, negative impact on vedalia beetles (Rodolia cardinalis), which are essential to control scale pests in citrus; neonicotinoids were toxic to vedalia larvae feeding on cottony cushion scale that had ingested these insecticides, and survival of adult beetles was also affected but to a lesser extent than other insecticides.

Recent evidence of the negative impacts of neonicotinoids on parasitoids reinforces that these insecticides are not suitable for IPM [271]. All neonicotinoids are deadly to three whitefly parasitoid species (Eretmocerusspp. and Encarsia formosa), with mortality of adults usually greater than the pupae [267]. Thiamethoxam appears to be less toxic to whitefly parasitoids compared to imidacloprid [202]. Imidacloprid, thiamethoxam and nitenpyram appeared to be the most toxic to the egg parasitoids Trichogramma spp. [231, 299]. For example, the acute toxicity of thiomethoxam and imidacloprid to Trichogramma chilonis, an egg parasitoid of leaf folders widely used in cotton IPM, is about 2000 times higher than that of other insecticides used in rice crops in India, such as acephate or endosulfan [220]. Acute toxicity of imidacloprid is more pronounced on Braconidae parasitoids than on T. chilonis, whereas thiacloprid only reduced the parasitization on Microplitis mediator[192]. Thiacloprid is as toxic to the cabbage aphid Brevicoryne brassicaeas to its parasitoid (Diaeretiella rapae), whereas pirimicarb and cypermethrin are more toxic to the aphid and are, therefore, preferred in IPM [3].

Neonicotinoids pose also risks to aquatic taxa. The synergistic toxicity of imidacloprid+thiacloprid on Daphnia magna[173] implies the combined effect of neonicotinoids on aquatic arthropods would be higher than expected, even if Daphniais very tolerant of neonicotinoids [119]. Other contaminants, such as the nonylphenol polyethoxylate (R-11) act also synergistically with imidacloprid [49]. Thiacloprid causes delayed lethal and sublethal effects in aquatic arthropods, which can be observed after 4 to 12 d following exposure to single 24-h pulses [28]. Thus, its 5% hazardous concentration (0.72 μg/L) is one order of magnitude lower than predicted environmental concentrations in water [35]. Also, thiacloprid LC50 for survival of midges (Chironomus riparius) is only 1.6 μg/L, and EC50 for emergence 0.54 μg/L [160], so both acute and chronic toxicity reduce the survival and growth of C. tentansand Hyalella azteca[265]. Acute toxicity of neonicotinoids to red swamp crayfish (Procambarus clarkii) is 2-3 orders of magnitude lower than that of pyrethroids [23]; comparative data such as this gives the neonicotinoids an apparent better environmental profile. However, experimental rice mesocosms treated with imidacloprid at label rates (15 kg/ha) eliminated all zooplankton communities for two months, and their recovery did not reach the control population levels four months later. Equally, mayflies, coleoptera larvae and dragonfly nymphs were significantly reduced while residues of imidacloprid in water were above 1 μg/L [117, 237]. Similarly, streams contaminated with a pulse of thiacloprid (0.1-100 μg/L) resulted in long-term (7 months) alteration of the overall invertebrate community structure [27]. However, while aquatic arthropods with low sensitivity to thiacloprid showed only transient effects at 100 μg/L, the most sensitive univoltine species were affected at 0.1 μg/L and did not recover during one year [167].

4.1.3. Fipronil

Fipronil is very efficient in controlling locust outbreaks, but causes more hazards than chlorpyrifos and deltamethrin to non-target insects in the sprayed areas, although it is more selective to specific taxa [214, 252]. Thus, abundance, diversity and activity of termites and ants were all reduced in northern Australia after spraying several areas with fipronil for locust control [262], and 45% of the termite colonies died within 10 months of a spraying operation with fipronil for controlling locusts in Madagascar [214]. Reducing the recommended application rates by seven times (0.6-2 g/ha) still achieves 91% elimination of locusts while having lesser impacts on non-target organisms, comparable to those inflicted by carbamate and OP insecticides [18].

Despite its selectivity, fipronil in maize crops reduced the abundance of arthropod populations of the soil mesofauna more significantly than other systemic insecticides, i.e. carbofuran [59], although springtails are little affected as they avoid feeding on litter contaminated with fipronil and are more tolerant of this insecticide [232]. When applied to citrus orchards, fipronil was among the most detrimental insecticides affecting two Euseiusspp. of predatory mites [112]. In rice crops, the effectiveness of fipronil in controlling pests was overshadowed by its negative impact on the predatory miridbugs Cyrtorhinus lividipennisand Tytthus parviceps[159].

Of greater concern is the impact of this systemic chemical on honey bees and wild bee pollinators. With an acute contact LD50 of 3.5 ng/bee [166] and acute oral LD50 of 3.7-6.0 ng/bee [2], fipronil is among the most toxic insecticides to bees ever developed. Even more worrying is the finding that the adjuvant Sylgard, used to reduce the toxicity of most insecticidal products on bees, increases the toxic effects of fipronil [184]. The systemic nature of this chemical implies that chronic feeding of the bees on nectar contaminated with fipronil caused 100% honey bee mortality after 7 days, even if the residue concentration was about 50 times lower than the acute lethal dose [8]. Residues of fipronil in pollen have been measured as 0.3-0.4 ng/g, which are 30-40 times higher than the concentration inducing significant mortality of bees by chronic intoxication [33]. Unlike neonicotinoids, no residues of fipronil have been found in guttation drops [272].

The acute toxicity of fipronil to cladocerans is similar to the toxicity to estuarine copepods, with 48-h LC50 in the range 3.5-15.6 μg/L [47, 259], but the chronic toxicity with time of exposure is what determines the fate of the populations exposed. For example, populations of Daphnia pulexwent to extinction after exposure to 80 μg/L for 10 days, equivalent to LC75 [259], and 40% of a population of grass shrimps (Palaemonetes pugio) died in 28 days after being exposed to fipronil concentrations of 0.35 μg/L in marsh mesocosms, and none of the shrimps survived when exposed to 5 mg/L during the same period [303]. Such impacts on zooplankton are likely to occur in estuaries, where waters have been found to contain 0.2-16 μg/L of fipronil residues [45, 163], even if no apparent effect on amphipods, mussels nor fish has been observed [37, 303]. Fipronil sprays on water surfaces to control mosquito larvae have negative impacts not only on cladocerans but also on chironomid larvae exposed to chronic feeding on contaminated residues [183, 264]. Studies on rice mesocosms have shown that significant population reductions due to fipronil application at the recommended rates (50 g per seedling box) are not restricted to zooplankton and benthic species, but affect most species of aquatic insects. Moreover, fipronil impacts on aquatic arthropods were more pronounced after a second application in the following year [118], indicating persistence of this insecticide in rice paddies. Chronic toxicity over time explains the long-term toxicity of this systemic compound, so it is not surprising that concentrations of 1.3 μg/L in paddy water were sufficient to kill 100% of dragonfly (Sympetrum infuscatum) nymphs in nine days [138].

4.1.4. Insect growth regulators

There is little information about the effect of systemic chitin inhibitors on non-target organisms. Obviously these compounds are harmless to fish at levels above 1 mg/L for a week-long exposures [290], and to all vertebrates in general. IGRs affect mainly the larval stages of Lepidoptera, Coleoptera and Hymenoptera, and their activity last longer than that of other pest control products [178]. The effectiveness of these compounds in controlling target pests is demonstrated by comparing the dietary LC50 of hexaflumuron (0.31 mg/L) to the target cotton worm (Helicoverpasp.), which is 35 times lower than that of the systemic carbamate thiodicarb and less damaging to non-target predators [64]. Aquatic communities of non-target arthropods in rice fields (e.g. Cladocera, Copepoda, Odonata, Notonectidae, Coleoptera and Chironomidae taxa) were not affected by teflubenzuron applied at rates to control mosquitoes (5.6 mg/ha), even though this IGR remained active for several weeks during autumn and winter periods [239].

After application of IGRs to a crop, affected insect pests are prey to many species of spiders, some of which are also susceptible to the toxicity of these products, in particular the ground hunter spiders [211]. Larvae and eggs of pests contaminated with systemic IGR are consumed by a number of predators, including earwigs, which undergo secondary poisoning and stop growing beyond the nymph stage [226]. Chitin inhibitors only show effects on the larvae of predatory insects that had consumed treated-prey, not on the adult insects. As a consequence, predatory populations collapse, as it happened with the ladybeetle Chilocorus nigritusthat fed on citrus red scales (Aonidiella aurantii) in African orchards that had been treated with teflubenzuron [177]. Teflubenzuron sprayed at 16.4 g/ha for locust control in Mali did not affect the non-target arthropods in the herb layer, whereas ground-living Collembola, Thysanura, Coleoptera and Lepidoptera larvae were reduced by about 50% [151]. Moreover, teflubenzuron has multigenerational impacts: experiments with springtails exposed to artificial soil contaminated with this IGR showed that the F2 generation suffered significantly from its effects even when only the F0 generation had been exposed for 10 days [42]. Secondary poisoning with chitin inhibitors can be detrimental also to parasitoids such as Diadegma semiclausum, which may fail to produce enough cocoons in the treated hosts, but do not seem to affect the parasitism of other Hymenoptera [98]. For instance, novaluron did not affect the parasitisation of Trichogramma pretiosumon mill moth’s caterpillars, a pest of tomato crops [44]. On the other hand, teflubenzuron appears to be harmless to predatory mites [32]. IPM programs must always consider the implications of using systemic chitin inhibitors to control specific pests without destroying their natural predators in the first place.

Halofenozide does not appear to cause any acute, adverse effects through topical, residual, or dietary exposure of the ground beetle Harpalus pennsylvanicus. In contrast to the negative effects of other systemic insecticides (i.e. imidacloprid), the viability of eggs laid by females fed halofenozide-treated food once, or continuously for 30 days, was not reduced [156].

4.2. Sublethal effects

Very often, sublethal effects of systemic insecticides are a first step towards mortality, as they are caused by the same neurotoxic mechanisms. Apart from these, there may be other effects on reproduction, growth, longevity, etc. when organisms are exposed to low, sublethal doses or concentrations. These effects are only observable in individuals that survive the initial exposure, or in species that are tolerant to insecticides. For a review see [69].

4.2.1. Acetylcholinesterase inhibitors

Longevity of the parasitoid Microplitis croceipesthat fed on nectar from cotton treated with aldicarb was affected for at least 10 days after application, and its foraging ability of the parasitoid’s host was severely impaired for 18 days [257]. Carbofuran caused a significant reduction of adult weight and longevity of the predator ladybug Hippodamia undecimnotata, as well as a 55% reduction in fecundity when fed on aphids contaminated with this insecticide [206]. Longevity and survival of Aphidius ervi, an important parasitoid of the pea aphid (Acyrthosiphon pisum), were significantly reduced after treating with LC25 concentrations of dimethoate or pirimicarb [11]. A significant reduction in body size of females of the predator carabid Pterostichus melas italicusand altered sexual dimorphism were observed after long-term exposure in olives groves treated with dimethoate at a rate that caused 10% mortality after three days [104]. Unlike other insecticides, no behavioural effects of dimethoate or triazamate on honey bees were recorded [67].

Earthworms (Lumbricus terrestris) experienced significant reduction in growth rate and total protein content after soil applications of aldicarb at LC10 or LC25, but only small amounts of residues were detected in the worms [198]. Aldicarb and phorate can also increase infections by Rhizoctoniastem canker in potato fields [280].

A typical pattern of sublethal intoxication was revealed when red-winged blackbirds (Agelaius phoeniceus) were exposed to increasing doses of dimethoate: 2 mg/kg b.w. doses produced ataraxia, defecation and diarrhoea; neuromuscular dysfunctions and breathing complications appeared at 3 mg/kg, and by 5 mg/kg muscle paralysis and death occurred. The estimated LC50 was 9.9 mg/kg, and all birds died at doses above 28 mg/kg [38]. Although sublethal AChE depression by acephate (25% brain) did not affect the attack behaviour in American kestrels (Falco sparverius) [229], nor did alter breeding behaviour in American robins (Turdus migratorius) [65], exposure to 256 mg/kg b.w. acephate impaired the migratory orientation of the white-throated sparrow (Zonotrichia albicollis) [295]. Similarly, low doses of demeton–S-methyl did not affect starlings (Sturnus vulgaris) behaviour [279], but doses of 2.5 mg/kg b.w. of dicrotophos administered to female starlings significantly reduced their parental care and feeding of nestlings [113]. Carbofuran orally administered to pigeons (Columba livia) had profound effects on flight time, with pigeons falling off the pace of the flock when doses were between 0.5 and 1.0 mg/kg b.w. [36].

AChE activities in adductor muscle were depressed in freshwater mussels (Elliptio complanata) exposed for 96 h at concentrations as low as 0.1 mg/L and 1.3 mg/L of aldicarb and acephate respectively, while increasing the water temperature from 21 to 30 oC resulted in mortality [199]. High AChE inhibition (70%) by acephate was not associated with immobility of Daphnia magna, but increasing the concentration of acephate further had a strong detrimental effect on mobility, suggesting that binding sites other than AChE may be involved in acephate toxicity [222].

Exposure of bluegill fish (Lepomis macrochirus) to 30 μg/L carbofuran decreased significantly adenylate parameters in gill, liver, muscle and stomach tissues after 10 days, and then returned to normal [128]. Also, concentrations of carbofuran at half the LC50 dose for fathead minnow (Pimephales promelas) larvae caused reductions in swimming capacity, increased sensitivity to electric shocks, and a reduction in upper lethal temperature [121]. Enzymes of protein and carbohydrate metabolism were altered (some increased, others decreased) in liver and muscle tissues of the freshwater fish, Clarias batrachuswhen exposed to 7.7 mg/L of carbofuran for six days, recovering later to normal levels [26]. Exposure of guppies (Brachydanio rerio) to half the recommended dose for dimethoate (0.025 μl/L) caused morphological changes in hepatocytes within three days, as well as necrosis and other abnormalities [227]. When exposed to a range of monocrotophos concentrations (0.01-1.0 mg/L), male goldfish (Carassius auratus) showed higher levels of 17-β-estradiol and vitollogenin and lower levels of testosterone than normal, interfering with gonadotropin synthesis at the pituitary gland [281]. Eggs of the toad Bufo melanostictusexposed to acephate hatched normally, but the tadpoles exhibited deformities such as tail distortions and crooked trunk; decreased pigmentation, peeling of the skin, inactivity, delay in emergence of limbs and completion of metamorphosis were also apparent [103].

Insecticide mixtures can enhance not only the acute but also the sublethal effects. For example, disulfoton together with endosulfan caused cytological and biochemical changes in liver of rainbow trout (Oncorrhynchus mykiss), independently of their respective modes of action [13]. Mixtures of aldicarb and other insecticides enhanced significantly the establishment of parasitic lungworm nematodes (Rhandias ranae) in leopard frogs (Rana pipiens) some 21 days after infection [101], as the frog’s immune response was suppressed or altered [51]. Similarly, laboratory rats exposed to sublethal mixtures of aldicarb, methomyl and a herbicide (metribuzin) showed learning impairment, immune response and endocrine changes [215].

4.2.2. Insecticides acting on nAChR

Laboratory experiments have shown a number of abnormalities such as less melanin pigmentation, wavy notochord, crooked trunk, fuzzy somites, neurogenesis defects and vasculature defects in zebrafish (Danio rerio) embryos exposed to a range of cartap concentrations. The most sensitive organ was the notochord, which displayed defects at concentrations as low as 25 μg/L [308]. It is obvious that essential enzymatic processes are disturbed during embryo development, among which the inhibition of lysyl oxidase is responsible for the notochord undulations observed.

Imidacloprid does not cause high mortality among eggs or adults of the preparasite nematode Agamermis unka,but impairs the ability of the nematode to infect nymphs of the host brown planthopper (Nilaparvata lugens) [50]. Contrary to this, a synergistic effect of imidacloprid on reproduction of entomopathogenic nematodes against scarab grubs may increase the likelihood of infection by subsequent generations of nematodes, thereby improving their field persistence and biological potential to control grubs. Acetamiprid and thiamethoxam, however, do not show synergist interactions with nematodes [149]. Imidacloprid at 0.1-0.5 mg/kg dry soil disturbs the burrowing ability of Allolobophoraspp. earthworms [43], and the highest concentration can also induce sperm deformities in the earthworm Eisenia fetida[306]. Reduction in body mass (7-39%) and cast production (42-97%) in Allolobophoraspp. and Lumbricus terrestrishave also been observed after 7 days exposure to relevant environmental concentrations of imidacloprid [74]. Residues of imidacloprid in maple leaves from treated forests (3–11 mg/kg) did not affect survival of aquatic leaf-shredding insects or litter-dwelling earthworms. However, feeding rates by aquatic insects and earthworms were reduced, leaf decomposition (mass loss) was decreased, measurable weight losses occurred among earthworms, and aquatic and terrestrial microbial decomposition activity was significantly inhibited, thus reducing the natural decomposition processes in aquatic and terrestrial environments [150].

The dispersal ability of the seven-spotted ladybirds (Coccinella septempunctata) sprayed with imidacloprid was compromised, and this may have critical consequences for biological control in IPM schemes [21]. A significant reduction of adult weight and longevity of the ladybug Hippodamia undecimnotata, as well as 33% reduction in fecundity were observed when this predatory bug fed on aphids contaminated with imidacloprid [206]. Imidacloprid and fipronil had adverse effects on the immune response of the wolf-spider Pardosa pseudoannulata, reducing significantly its phenoloxidase activity, the total number of hemocytes and encapsulation rate [282]; the implications of such effects on this natural enemy of rice pests are unknown. When applied in the egg-larval or pupal stages, acetamiprid or imidacloprid reduced the parasitisation capacity of F1 and F2 generation females of Trichogramma pretiosumon mill moth’s caterpillars (Anagasta kuehniella), a pest of tomato crops [44]. Longevity of females of the parasitoid Microplitis croceipesthat fed on nectar from imidacloprid-treated cotton was affected for at least 10 days after application, while the parasitoid's host foraging ability was severely affected from day 2 onwards [257]. Exposure of western subterranean termites (Reticulitermes hesperus) to acetamiprid (1 mg/kg sand) or imidacloprid also impaired locomotion of termites within 1 hour [230].

Bumble bees (Bombus terrestris) interrupt their activity for several hours when exposed to imidacloprid sprayed on plants [132], and soil treatment at the highest recommended doses extended the handling times of B. impatienson the complex flowers [194]. Such an impairment affects the bees foraging behaviour and can result in a decreased pollination, lower reproduction and finally in colony mortality due to a lack of food [193]. Although Franklin et al. [96] found that clothianidin residues of 6 μg/kg in canola pollen reduced the production of queens and increased the number of males in B. impatients, their study did not find significant differences with controls due to a high variability in the results. Larval development in wild bees (Osmia lignariaand Megachile rotundata) was delayed significantly when fed pollen contaminated with either imidacloprid or clothianidin at 30 or 300 μg/kg [1]. Honey bees are more sensitive to neonicotinoids than bumble bees: at 6 μg/kg, imidacloprid clearly induced a decrease in the proportion of active bees [57], and 50-500 μg/L affect significantly their activity, with bees spending more time near the food source [273]. Other authors found that lower activity of honey bees during the hours following oral exposure to 100-500 μg/L imidacloprid in syrup is transitory [186]. In any case, that may explain the delayed homing behaviour of honey bees exposed to 100 μg/L imidacloprid in syrup and their disappearance at higher doses [34, 304]. Honey bees fed on syrup contaminated with acetamiprid increased their sensitivity to antennal stimulation by sucrose solutions at doses of 1 μg/bee and had impaired long-term retention of olfactory learning at 0.1 μg/bee. Contact exposure at 0.1 and 0.5 μg/bee increased locomotor activity and water-induced proboscis extension reflex but had no effect on behaviour [82]. Similar response was obtained with honey bees exposed to thiomethoxam by contact, having impaired long-term retention of olfactory learning at 1 ng/bee [8]. Winter bees surviving chronic treatment with imidacloprid and its metabolite (5-OH-imidacloprid) had reduced learning performances than in summer: the lowest-effect concentration of imidacloprid was lower in summer bees (12  μg/kg) than in winter bees (48  μg/kg), indicating a greater sensitivity of honey bees behaviour in summer bees compared to winter bees [68].

Honey bees infected with the microsporidian Nosema ceranaeexperienced 7 or 5 times higher mortality than normal when fed syrup contaminated with sublethal doses of thiacloprid (5 mg/L) or fipronil (1 μg/L), respectively [293). N. ceranaeis a key factor in the CCD in honey bees [127], and the synergistic effect of these systemic insecticides on Nosemais probably its underlying cause [213]. Suppression of the immune system is not restricted to bees, as a massive infection of medaka fish by a protozoan ectoparasite (Trichodinaspp.) when exposed to imidacloprid in rice mesocosms has been documented [236].

Imidacloprid residues in water as low as 0.1 μg/L are sufficient to reduce head and torax length in mayfly nymphs of Baetisand Epeorus, whether applied as pulses or in continuous exposures for 20 days [6]. At 1 μg/L the insecticides caused feeding inhibition. However, 12-h pulses induced emergence because of stress, whereas constant exposure reduced survivorship progressively. Also, the aquatic worm Lumbriculus variegatusexperienced immobility during 4 days when exposed to 0.1-10 μg/L imidacloprid [5].

4.2.3. Fipronil

Apart from the extreme acute toxicity of this insecticide to bees, honey bees fed on sucrose syrup contaminated with fipronil (2 μg/kg) reduced significantly their attendance to the feeder [57]. It has also been demonstrated that sublethal concentrations of this insecticide as low as 0.5 ng/bee, whether orally or topically applied, reduce the learning performance of honey bees and impair their olfactory memory but not their locomotor activity [67, 82]. Furthermore, chronic feeding exposure at 1 μg/kg or 0.01 ng/bee reduced learning and orientation, whilst oral treatment of 0.3 ng/bee reduced the number of foraging trips among the exposed workers [66]. In addition to their activity, honey bees fed with sucrose syrup containing 1 μg/L fipronil increased significantly the mortality of bees infected with the endoparasite Nosema ceranae, suggesting a synergistic effect between the insecticide and the pathogen [293]. All these sublethal effects reduce the performance of the hive and help explain the decline in honey bee and wild bee pollinators in many countries [205], although fipronil is not alone in causing this demise – neonicotinoids are equally implicated.

Female zebra finches (Taeniopygia guttata) fed with single sublethal doses of fipronil (1, 5, and 10 mg/kg b.w.) failed to hatch 6 out of 7 eggs laid. The only chick born was underdeveloped and had fiprole residues in the brain, liver and adipose tissues. By contrast, 12-day-old chicken eggs injected with fipronil (5.5 to 37.5 mg/kg egg weight) hatched normally although the chicks from the highest dose group showed behavioural and developmental abnormalities [145].

Low residues of fipronil in estuary waters (0.63 μg/L) inhibited reproduction of the copepod Amphiascus tenuiremisby 73-89%, and this effect seems to be more prevalent on males than on females [45]. Even lower residue levels (0.22 μg/L) halted egg extrusion by 71%, whereas exposure to 0.42 μg/L nearly eliminated reproduction (94% failure) on this species. Based on these results from chronic and sublethal toxicity, a three-generation Leslie matrix model predicted a 62% decline in population size of A. tenuiremisat only 0.16 μg/L [47]. Unlike other insecticides, the stress on Ceriodaphnia dubiacaused by predatory cues of bluegill fish (Lepomis macrochirus) was significantly exacerbated when the cladocerans were exposed to 80-160 μg/L of fipronil [223]; however, these concentrations are much higher than the residue levels usually found in waters [99, 163].

While fipronil applied at the recommended rates in rice fields induces biochemical alterations in carp (Cyprinus carpio), such metabolic disturbances do not appear to have any effect on growth nor mortality of this fish after 90 days exposure at <0.65 μg/L [52]. However, similar residue levels (<1 μg/L) reduced significantly the growth of adult medaka fish (Oryzias latipes) after two weeks of exposure, as well as growth of their offspring in the first 35 days, even if residues of fipronil by that time were below the analytical detection limit (0.01 μg/L) [117].

4.2.4. Insect growth regulators

Longevity of predatory bug Podisus maculiventriswas reduced after preying on Colorado potato beetles that fed on foliage treated with novaluron at 85 g/ha. Females produced fewer eggs and their hatching was significantly suppressed, while 5th instars that also preyed on the beetles failed to moult into adults [62]. Novaluron and hexaflumuron significantly decrease (<30%) the total protists population in the guts of termites (Reticultermes flavipes), thus upsetting their digestive homeostasis [165].

4.3. Indirect effects on populations and communities

Indirect effects result from the dynamics of ecosystems. Thus, applications of granular phorate to soil eliminate most soil invertebrates (see 4.1) except for Enchytraeidae worms, which increase in large numbers and take over the leaf-litter decomposition function carried out by the eliminated springtails [300].

Resurgence or induction of pests by altering the prey-predator relationships in favour of the herbivore species is most common. When carbofuran was applied to corn plantations in Nicaragua, the population levels of the noctuid pest Spodoptera frugiperdaincreased because of lesser foraging activity by predatory ants [212]. Methomyl eliminated the phytoseiid predatory mite Metaseiulus occidentalisfor 10 days, thus causing an increase in Pacific spider mites (Tetranychus pacificus) and leafhopper (Eotetranychus willamettei) populations in the treated vineyards [130]. Unexpected outbreaks of a formerly innocuous herbivore mite (Tetranychus schoenei) were observed after imidacloprid applications to elms in Central Park, New York. A three-year investigation on the outbreaks showed that elimination of its predators and the enhanced fecundity of T.schoeneiby this insecticide were responsible for that outcome [268].

The widespread use of insecticides usually tips the ecological balance in favour of herbivore species. For example, dimethoate sprayed on clover fields indirectly reduced the populations of house mice (Mus musculus) in the treated areas as the insect food source was depleted. However, herbivore species such as prairie voles (Microtus ochrogaster) and prairie deer mouse (Peromyscus maniculatus) increased in density levels [24], since they had more clover available due to either higher clover yields or through less competition with the house mice or both.

A reduction in arthropod populations often implies starvation of insectivorous animals. For example, densities of two species of lizards and hedgehogs in Madagascar were reduced 45-53% after spraying with fipronil to control a locust outbreak, because their favourite termite prey was almost eliminated (80-91%) by this chemical [214]. However, this type of indirect impact is difficult to observe and measure in birds, since they can move to other areas or change their resource diet. For example, hemlock forests treated with imidacloprid to control hemlock woolly adelgid (Adelges tsugae) reduced significantly Hemiptera and larval Lepidoptera, but not other insect taxa. Although larval Lepidoptera are the primary prey for insectivorous foliage-gleaning birds, many birds were able to find other food resources in the mixed hemlock-deciduous stands that were not treated [87]. Similarly, post-treatment with fipronil for grasshopper control in Wyoming did not affect bird densities, perhaps due to the large initial insect populations; fipronil plots generally had higher avian population densities (nongregarious, insectivores and total birds) than other areas treated with carbaryl [203]. Although some early studies found that fipronil did not have much impact on aquatic communities of Sahelian ponds [158], nor in predatory invertebrates in the Camargue marshes, herons in the latter region avoid rice fields treated with fipronil because of the scarcity of invertebrate food in there [188].

Food aversion to pesticide-treated seeds or plants is a mechanism that may indirectly ameliorate the toxic effects of systemic insecticides such as carbofuran in mice and other small rodents [170]. Some Collembola species (i.e. Folsomia fimetaria) avoid dimethoate sprayed areas [86], and female parasitoids (Cotesia vestalis) are discouraged from getting to their host –the diamond-back month (Plutella xylostella) – in turnip plants treated with methomyl, whereas clothianidin does not produce aversion [248]. Equally, dimethoate and oxydemeton-methyl sprayed on peach trees discourage honey bees from visiting in the first two days after application, while treatments with imidacloprid, acetamiprid and thiamethoxam allow honey bees visits [246]. This helps explain the high long-term impact of neonicotinoids on bees compared to the effect of OP insecticides, even if imidacloprid at high experimental concentrations in syrup (>0.5 mg/L) may also have repellent effect on honey bees [34].

Advertisement

5. Risk assessment of systemic insecticides

All systemic compounds have effects with time of exposure. However, only the persistent chemicals (fipronil, neonicotinoids, cartap and some OPs) have cumulative effects over time, since the non-persistent compounds are quickly degraded in soil and water.

For risk assessment of these compounds it is important to understand their chronic impacts. Unlike traditional protocols based on acute toxicity, the persistent activity of the parent and toxic metabolites requires that exposure time must be taken into consideration [115]. Concerns about the impacts of dietary feeding on honey bees and other non-target organisms are thus justified [9, 60, 228], because the accumulation of small residue levels ingested repeatedly over time will eventually produce a delayed toxic effect [276]. For example, bees that feed on contaminated nectar and pollen from the treated crops are exposed to residues of imidacloprid and fipronil in the range 0.7-10 μg/kg and 0.3-0.4 μg/kg respectively [33], which appear in 11% and 48% of the pollen surveyed in France [48]. Based on those findings an estimate of the predicted environmental concentrations that bees are ingesting in that country can be made for each insecticide. Since there is a log-to-log linear relationship between concentration and time of exposure [234], the critical levels of residue and time of exposure can be determined.

The declining populations of predatory and parasitic arthropods after exposure to recommended applications of most systemic insecticides are worrying. In view of the above, it not so much the small concentrations they are exposed to but the time of exposure that makes the population decline progressively over weeks, months and even years of treatment, as described in this chapter. Lethal and sublethal effects on reproduction are equally implicated. This is the reason why systemic insecticides should be evaluated very carefully before using them in IPM schemes. Obviously, recovery rates are essential for the populations affected to come back, and this usually occurs by recolonisation and immigration of individuals from non-affected areas. For example, modelling based on recovery data after dimethoate application to wheat fields [277] demonstrates that a non-target organism that is reduced by only 20% but is unable to recover is likely to be far more at risk from exposure to a pesticide than an organism that is reduced 99% for a short period but has a higher recovery potential.

The above is also relevant to the impact of small residues of those systemic insecticides that have cumulative effects (e.g. neonicotinoids, fipronil and cartap) on aquatic ecosystems. Because of the short life-cycle of many zooplankton species, the negative population parameters that result from sublethal and chronic effects on such organisms can lead their local populations to extinction [260]. Immediate reductions in populations and species may not always be apparent due to the small residue concentrations and the delayed effects they cause. For example, in recent surveys of pesticide residues in freshwaters of six metropolitan areas of USA, fipronil appears regularly in certain states [254]. Fipronil and its desulfinyl, sulfide, and sulfone degradates were detected at low levels (≤ 0.18–16 μg/L) in estuary waters of Southern California [163], and make some 35% of the residues found in urban waters, with a median level of 0.2-0.44 μg/L, most frequently during the spring-summer season [99]. Imidacloprid was detected in 89% of water samples in agricultural areas of California, with 19% exceeding the US Environmental Protection Agency’s chronic invertebrate Aquatic Life Benchmark of 1.05 μg/L [261]. In the Netherlands, imidacloprid appeared in measurable quantities in 30% of the 4,852 water samples collected between 1998 and 2007 [287]. These figures indicate there is already a widespread contamination of waterways and estuaries with persistent systemic insecticides.

The first consequence of such contamination is the progressive reduction, and possible elimination, of entire populations of aquatic arthropods from the affected areas. As time is a critical variable in this type of assessment, it is envisaged that should this contamination continue at the current pace over the years to come the biodiversity and functionality of many aquatic ecosystems will be seriously compromised [191]. Secondly, as these organisms are a primary food source of a large number of vertebrates (e.g. fish, frogs and birds), the depletion of their main food resource will inevitably have indirect impacts on the animal populations that depend on them for their own survival. The case of the partridge in England is an example of how a combination of herbicides and insecticides can bring the demise of a non-target species by indirectly suppressing its food requirements [217]. Therefore, warnings about the possible role of environmental contamination with neonicotinoids in steeply declining populations of birds, frogs, hedgehogs, bats and other insectivorous animals are not far fetched and should be taken seriously [275].

Advertisement

6. Conclusions

This review has brought some light on the direct, sublethal and indirect effects that systemic insecticides have on species populations and ecosystems. Some long-term impacts have been known for some time (e.g. carbofuran, phorate), but it is the rapid increase in the usage of neonicotinoids and other systemic products that poses a new challenge to the ecological risk assessment of agrochemicals. Indeed, current risk protocols, based on acute, short-term toxic effects are inadequate to cope with the chronic exposure and cumulative, delayed impacts of the new compounds. Awareness of the increasing contamination of the environment with active residues of these chemicals should help regulators and managers to implement new approaches for risk assessment of these substances.

References

  1. 1. AbbottV. A.NadeauJ. L.HigoH. A.WinstonM. L.2008Lethal and sublethal effects of imidacloprid onOsmia lignariaand clothianidin onMegachile rotundata(Hymenoptera: Megachilidae)J. Econ. Entomol.1013784796
  2. 2. Agritox2002Liste des substances actives.Paris, France: Institut National de la Recherche Agronomique.
  3. 3. Al-AntaryT. M.AteyyatM. A.AbussaminB. M.2010Toxicity of certain insecticides to the parasitoidDiaeretiella rapae(Mcintosh) (Hymenoptera: Aphidiidae) and its host, the cabbage aphidBrevicoryne brassicae L.(Homoptera: Aphididae).Aust. J. Basic Appl. Sci.469941000
  4. 4. Al-HaifiM. A.KhanM. Z.MurshedV. A.GholeS.2006Effect of dimethoate residues on soil micro-arthropods population in the valley of Zendan, Yemen.J. Appl. Sci. Environ. Manage.1023741
  5. 5. AlexanderA. C.CulpJ. M.LiberK.CessnaA. J.2007Effects of insecticide exposure on feeding inhibition in mayflies and oligochaetes.Environ. Toxicol. Chem.26817261732
  6. 6. AlexanderA. C.HeardK. S.CulpJ. M.2008Emergent body size of mayfly survivorsFreshwat. Biol.531171180
  7. 7. AliA.StanleyB. H.1982Effects of a new carbamate insecticide, Larvin (UC-51762), on some nontarget aquatic invertebratesFlorida Entomol.654477483
  8. 8. AliouaneY.El -HassaniA. K.GaryV.ArmengaudC.LambinM.GauthierM.2009Subchronic exposure of honeybees to sublethal doses of pesticides: effects on behaviorEnviron. Toxicol. Chem.281113122
  9. 9. AlixA.VergnetC.2007Risk assessment to honey bees: a scheme developed in France for non-sprayed systemic compounds.Pest Manage. Sci.631110691080
  10. 10. AnoopK.RamS.2012Effect of biopesticides and insecticides on aphid population, bee visits and yield of mustard.Ann. Plant Protect. Sci.201206209
  11. 11. ArayaJ. E.ArayaM.GuerreroM. A.2010Effects of some insecticides applied in sublethal concentrations on the survival and longevity ofAphidius ervi(Haliday) (Hymenoptera: Aphidiidae) adultsChilean J. Agric. Res.702221227
  12. 12. ArmbrustK. L.PeelerH. B.2002Effects of formulation on the run-off of imidacloprid from turf.Pest Manage. Sci.587702706
  13. 13. ArnoldH.PlutaH. J.BraunbeckT.1995Simultaneous exposure of fish to endosulfan and disulfoton in vivo: ultrastructural, stereological and biochemical reactions in hepatocytes of male rainbow trout (Oncorhynchus mykiss)Aquat. Toxicol.331734
  14. 14. AteyyatM.2012Selectivity of four insecticides to woolly apple aphid, Eriosoma lanigerum (Hausmann) and its sole parasitoid,Aphelinus mali(Hald.)World Appl. Sci. J.16810601064
  15. 15. AzizullahA.RichterP.HäderD. P.2011Comparative toxicity of the pesticides carbofuran and malathion to the freshwater flagellateEuglena gracilisEcotoxicology20614421454
  16. 16. BabuB. S.GuptaG. P.1986Effect of systemic insecticides on the population of soil arthropods in a cotton field.J. Soil Biol. Ecol.613241
  17. 17. BabuB. S.GuptaG. P.1988Efficacy of systemic insecticides against cotton jassid (Amrasca devastans) and their effect on non-target organisms in upland cotton (Gossypium hirsutum).Indian J. Agric. Sci.586496499
  18. 18. BalancaG.VisscherM. N.d1997Effects of very low doses of fipronil on grasshoppers and non-target insects following field trials for grasshopper controlCrop Protection16553564
  19. 19. BalcombR.BowenC. I.WrightD.LawM.1984Effects on wildlife of at-planting corn applications of granular carbofuranJ. Wildl. Manage.48413531359
  20. 20. BalconiC.MazzinelliG.MottoM.2011Neonicotinoid insecticide seed coatings for the protection of corn kernels and seedlings, and for plant yield.Maize Genetics Cooperation Newsletter843
  21. 21. BanksJ. E.StarkJ. D.2011Effects of a nicotinic insecticide, imidacloprid, and vegetation diversity on movement of a common predator,Coccinella septempunctata Biopestic. Int.72113122
  22. 22. BarahonaM. V.Sánchez-FortúnS.1999Toxicity of carbamates to the brine shrimpArtemia salinaand the effect of atropine, BW284c51, iso-OMPA and 2-PAM on carbaryl toxicityEnviron. Pollut.1043469476
  23. 23. BarbeeG. C.StoutM. J.2009Comparative acute toxicity of neonicotinoid and pyrethroid insecticides to non-target crayfish (Procambarus clarkii) associated with rice-crayfish crop rotationsPest Manage. Sci.651112501256
  24. 24. BarrettG. W.DarnellR. M.1967Effects of dimethoate on small mammal populationsAm. Midland Nat.77164175
  25. 25. BaurM. E.EllisJ.HutchinsonK.BoethelD. J.2003Contact toxicity of selective insecticides for non-target predaceous hemipterans in soybeansJ. Entomol. Sci.382269277
  26. 26. BegumG.2004Carbofuran insecticide induced biochemical alterations in liver and muscle tissues of the fishClarias batrachus(linn) and recovery response.Aquat. Toxicol.6618392
  27. 27. BeketovM.SchaferR. B.MarwitzA.PaschkeA.LiessM.2008Long-term stream invertebrate community alterations induced by the insecticide thiacloprid: effect concentrations and recovery dynamicsSci. Total Environ.40596108
  28. 28. BeketovM. A.LiessM.2008Acute and delayed effects of the neonicotinoid insecticide thiacloprid on seven freshwater arthropodsEnviron. Toxicol. Chem.272461470
  29. 29. BelfroidA. C.van DrunenM.BeekM. A.SchrapS. M.van GestelC. A. M.van HattumB.1998Relative risks of transformation products of pesticides for aquatic ecosystemsSci. Total Environ.2223167183
  30. 30. BellowsT. S.MorseJ. G.GastonL. K.BaileyJ. B.1988The fate of two systemic insecticides and their impact on two phytophagous and a beneficial arthropod in a citrus agroecosystem.J. Econ. Entomol.813899904
  31. 31. BergH.2001Pesticide use in rice and rice-fish farms in the Mekong Delta, VietnamCrop Protection2010897905
  32. 32. BluemelS.StolzM.1993Investigations on the effect of insect growth regulators and inhibitors on the predatory mitePhytoseiulus persimilisA.H. with particular emphasis on cyromazineZeitschrift fuer Pflanzenkrankheiten und Pflanzenschutz1002150154
  33. 33. BonmatinJ. M.MarchandP. A.CotteJ. F.AajoudA.CasabiancaH.GoutaillerG.CourtiadeM.2007Bees and systemic insecticides (imidacloprid, fipronil) in pollen: subnano-quantification by HPLC/MS/MS and GC/MS.Environmental fate and ecological effects of pesticides, Re, A.A.M.d. et al., editors827834978-8-87830-473-4
  34. 34. BortolottiL.MontanariR.MarcelinoJ.MedrzyckiP.MainiS.PorriniC.2003Effects of sublethal imidacloprid doses on the homing rate and foraging activity of honey bees.Bull. Insectology5616367
  35. 35. BottgerR.SchallerJ.MohrS.2012Closer to reality - the influence of toxicity test modifications on the sensitivity ofGammarus roeselito the insecticide imidacloprid.Ecotoxicol. Environ. Saf.8104954
  36. 36. BraselJ.CollierA.PritsosC.2007Differential toxic effects of carbofuran and diazinon on time of flight in pigeons (Columba livia): potential for pesticide effects on migrationToxicol. Appl. Pharmacol.2192-3241246
  37. 37. BringolfR. B.CopeW. G.EadsC. B.LazaroP. R.BarnhartM. C.SheaD.2007Acute and chronic toxicity of technical-grade pesticides to glochidia and juveniles of freshwater mussels (Unionidae).Environ. Toxicol. Chem.261020942100
  38. 38. BrunetR.GirardC.CyrA.1997Comparative study of the signs of intoxication and changes in activity level of red-winged blackbirds (Agelaius phoeniceus) exposed to dimethoate.Agric. Ecosyst. Environ.64201209
  39. 39. BrunettoR.BurgueraM.BurgueraJ. L.1992Organophosphorus pesticide residues in some watercourses from Merida, Venezuela.Sci. Total Environ.114195204
  40. 40. BuckinghamS.LapiedB.CorroncH.SattelleF.1997Imidacloprid actions on insect neuronal acetylcholine receptorsJ. Exp. Biol.2002126852692
  41. 41. BunyanP. J.HeuvelM. J.v.dStanleyP. I.WrightE. N.1981An intensive field trial and a multi-site surveillance exercise on the use of aldicarb to investigate methods for the assessment of possible environmental hazards presented by new pesticidesAgro-Ecosystems73239262
  42. 42. CampicheS.L’ArnbertG.TarradellasJ.Becker-vanSlooten. K.2007Multigeneration effects of insect growth regulators on the springtailFolsomia candidaEcotoxicol. Environ. Saf.672180189
  43. 43. CapowiezY.BastardieF.CostagliolaG.2006Sublethal effects of imidacloprid on the burrowing behaviour of two earthworm species: modifications of the 3D burrow systems in artificial cores and consequences on gas diffusion in soilSoil Biol. Biochem.382285293
  44. 44. CarvalhoG. A.GodoyM. S.ParreiraD. S.RezendeD. T.2010Effect of chemical insecticides used in tomato crops on immatureTrichogramma pretiosum(Hymenoptera: Trichogrammatidae).Revista Colombiana de Entomologia3611015
  45. 45. CaryT. L.ChandlerG. T.VolzD. C.WalseS. S.FerryJ. L.2003Phenylpyrazole insecticide fipronil induces male infertility in the estuarine meiobenthic crustaceanAmphiascus tenuiremis.Environ. Sci. Technol.382522528
  46. 46. ChaiL. K.WongM. H.Mohd-TahirN.HansenH. C. B.2010Degradation and mineralization kinetics of acephate in humid tropic soils of MalaysiaChemosphere794434440
  47. 47. ChandlerG. T.CaryT. L.VolzD. C.WalseS. S.FerryJ. L.KlosterhaS. L.2004Fipronil effects on estuarine copepod (Amphiascus tenuiremis) development, fertility, and reproduction: a rapid life-cycle assay in 96-well microplate format.Environ. Toxicol. Chem.231117124
  48. 48. ChauzatM.P.MartelA. C.CougouleN.PortaP.LachaizeJ.ZegganeS.AubertM.CarpentierP.FauconJ.P.2011An assessment of honeybee colony matrices,Apis mellifera(Hymenoptera: Apidae) to monitor pesticide presence in continental France.Environ. Toxicol. Chem.301103111
  49. 49. ChenX. D.CulbertE.HebertV.StarkJ. D.2010Mixture effects of the nonylphenyl polyethoxylate, R-11 and the insecticide, imidacloprid on population growth rate and other parameters of the crustacean,Ceriodaphnia dubiaEcotoxicol. Environ. Saf.732132137
  50. 50. ChooH. Y.KimH. H.KayaH. K.1998Effects of selected chemical pesticides on Agamermis unka (Nematoda: Mermithidae), a parasite of the brown plant hopper, Nilaparvata lugensBiocontrol Sci. Technol.83413427
  51. 51. ChristinM. S.GendronA. D.BrousseauP.MénardL.MarcoglieseD. J.CyrD.RubyS.FournierM.2003Effects of agricultural pesticides on the immune system ofRana pipiensand on its resistance to parasitic infection.Environ. Toxicol. Chem.22511271133
  52. 52. ClasenB.LoroV. L.CattaneoR.MoraesB.LopesT.AvilaL.A.dZanellaR.ReimcheG. B.BaldisserottoB.2012Effects of the commercial formulation containing fipronil on the non-target organismCyprinus carpio: implications for rice-fish cultivationEcotoxicol. Environ. Saf.774551
  53. 53. ClementsR. O.BentleyB. R.JacksonC. A.1986The impact of granular formulations of phorate, terbufos, carbofuran, carbosulfan and thiofanox on newly sown Italian ryegrass,Lolium multiflorum.Crop Protection56389394
  54. 54. CloydR. A.BethkeJ. A.2011Impact of neonicotinoid insecticides on natural enemies in greenhouse and interiorscape environments.Pest Manage. Sci.67139
  55. 55. CockfieldS. D.PotterD. A.1983Short-term effects of insecticidal applications on predaceous arthropods and oribatid mites in Kentucky blue grass turf.Environ. Entomol.12412601264
  56. 56. ColeL. M.NicholsonR. A.CasidaJ. E.1993Action of phenylpyrazole insecticides at the GABA-gated chloride channelPestic. Biochem. Physiol.4614754
  57. 57. ColinM. E.BonmatinJ. M.MoineauI.GaimonC.BrunS.VermandereJ. P.2004A method to quantify and analyze the foraging activity of honey bees: relevance to the sublethal effects induced by systemic insecticidesArch. Environ. Contam. Toxicol.473387395
  58. 58. ColinasC.InghamE.MolinaR.1994Population responses of target and non-target forest soil organisms to selected biocidesSoil Biol. Biochem.2614147
  59. 59. CortetJ.Poinsot-BalaguerN.2000Impact of phytopharmaceutical products on soil microarthropods in an irrigated maize field: The use of the litter bag method.Can. J. Soil Sci.802237249
  60. 60. CresswellJ.2011A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (imidacloprid) on honey beesEcotoxicology201149157
  61. 61. CutlerG. C.Scott-DupreeC. D.2007Exposure to clothianidin seed-treated canola has no long-term impact on honey beesJ. Econ. Entomol.1003765772
  62. 62. CutlerG. C.Scott-DupreeC. D.TolmanJ. H.HarrisC. R.2006Toxicity of the insect growth regulator novaluron to the non-target predatory bugPodisus maculiventris(Heteroptera: Pentatomidae)Biol. Control382196204
  63. 63. DaiY.JiW.ChenT.ZhangW.LiuZ.GeF.YuanS.2010Metabolism of the neonicotinoid insecticides acetamiprid and thiacloprid by the yeastRhodotorula mucilaginosastrain IM-2.J. Agric. Food Chem.58424192425
  64. 64. DastjerdiH. R.HejaziM. J.GanbalaniG. N.SaberM.2008Toxicity of some biorational and conventional insecticides to cotton bollworm,Helicoverpa armigera(Lepidoptera: Noctuidae) and its ectoparasitoid,Habrobracon hebetor(Hymenoptera: Braconidae).J. Entomol. Soc. Iran2812737
  65. 65. DecarieR.DesGranges. J. L.LepineC.MorneauF.1993Impact of insecticides on the American robin (Turdus migratorius) in a suburban environment.Environ. Pollut.80231238
  66. 66. DecourtyeA.DevillersJ.AupinelP.BrunF.BagnisC.FourrierJ.GauthierM.2011Honeybee tracking with microchips: a new methodology to measure the effects of pesticidesEcotoxicology202429437
  67. 67. DecourtyeA.DevillersJ.GenecqueE.MenachK. L.BudzinskiH.CluzeauS.Pham-DelègueM. H.2005Comparative sublethal toxicity of nine pesticides on olfactory learning performances of the honeybeeApis mellifera.Arch. Environ. Contam. Toxicol.482242250
  68. 68. DecourtyeA.LacassieE.Pham-DelègueM. H.2003Learning performances of honeybees (Apis melliferaL) are differentially affected by imidacloprid according to the season.Pest Manage. Sci.593269278
  69. 69. DesneuxN.DecourtyeA.DelpuechJ.M.2007The sublethal effects of pesticides on beneficial arthropods.Annu. Rev. Entomol.5281106
  70. 70. DewarA. M.HaylockL. A.GarnerB. H.SandsR. J. N.PilbrowJ.2005Neonicotinoid seed treatments - the panacea for most pest problems in sugar beet.Aspects Appl. Biol.76312
  71. 71. DhadiallaT. S.CarlsonG. R.LeD. P.1998New insecticides with ecdysteroidal and juvenile hormone activity.Annu. Rev. Entomol.431545569
  72. 72. DieterC. D.DuffyW. G.FlakeL. D.1996The effect of phorate on wetland macroinvertebratesEnviron. Toxicol. Chem.153308312
  73. 73. DieterC. D.FlakeL. D.DuffyW. G.1995Effects of phorate on ducklings in northern prairie wetlands.J. Wildl. Manage.593498505
  74. 74. DittbrennerN.TriebskornR.MoserI.CapowiezY.2010Physiological and behavioural effects of imidacloprid on two ecologically relevant earthworm species (Lumbricus terrestrisandAporrectodea caliginosa)Ecotoxicology1915671573
  75. 75. DrescherW.Geusen-PfisterH.1991Comparative testing of the oral toxicity of acephate, dimethoate and methomyl to honeybees, bumblebees and Syrphidae.Acta Horticulturae288133138
  76. 76. EasterbrookM. A.1997A field assessment of the effects of insecticides on the beneficial fauna of strawberryCrop Protection162147152
  77. 77. EcoliC. C.MoraesJ. C.VilelaM.2010Suplementos alimentares e isca toxica no manejo do bicho-mineiro e de seus inimigos naturais.Coffee Sci.52167172
  78. 78. EisenbackB. M.SalomS. M.KokL. T.LagalanteA. F.2010Lethal and sublethal effects of imidacloprid on hemlock woolly adelgid (Hemiptera: Adelgidae) and two introduced predator speciesJ. Econ. Entomol.1034122234
  79. 79. EisenhauerN.KlierM.PartschS.SabaisA. C. W.ScherberC.WeisserW. W.ScheuS.2009No interactive effects of pesticides and plant diversity on soil microbial biomass and respirationAppl. Soil Ecol.4213136
  80. 80. El -DinH. A. S.GirgisN. R.1997Susceptibility of honey bee workers,Apis melliferaL. to nine different insecticides.Ann. Agric. Sci. Moshtohor35425712582
  81. 81. El -HassaniA. K.DacherM.GaryV.LambinM.GauthierM.ArmengaudC.2008Effects of sublethal doses of acetamiprid and thiamethoxam on the behavior of the honeybee (Apis mellifera)Arch. Environ. Contam. Toxicol.544653661
  82. 82. El -HassaniA. K.DacherM.GauthierM.ArmengaudC.2005Effects of sublethal doses of fipronil on the behavior of the honeybee (Apis mellifera)Pharmacol. Biochem. Behavior8213039
  83. 83. ElbertA.HaasM.SpringerB.ThielertW.NauenR.2008Applied aspects of neonicotinoid uses in crop protectionPest Manage. Sci.641110991105
  84. 84. ElliottJ. E.WilsonL. K.LangelierK. M.MineauP.SinclairP. H.1997Secondary poisoning of birds of prey by the organophosphorus insecticide, phorateEcotoxicology64219231
  85. 85. EndlweberK.SchädlerM.ScheuS.2005Effects of foliar and soil insecticide applications on the collembolan community of an early set-aside arable fieldAppl. Soil Ecol.311-2136146
  86. 86. FabianM.PetersenH.1994Short-term effects of the insecticide dimethoate on activity and spatial distribution of a soil inhabiting collembolanFolsomia fimetariaLinne (Collembola:Isotomidae).Pedobiologia384289302
  87. 87. FalconeJ. F.De WaldL. E.2010Comparisons of arthropod and avian assemblages in insecticide-treated and untreated eastern hemlock (Tsuga canadensisL. Carr) stands in Great Smoky Mountains National Park, USA.Forest Ecol. Manage.2605856863
  88. 88. FarinosG. P.de la PozaM.Hernandez-CrespoP.OrtegoF.CastaneraP.2008Diversity and seasonal phenology of aboveground arthropods in conventional and transgenic maize crops in Central SpainBiol. Control443362371
  89. 89. FauconJ. P.AurièresC.DrajnudelP.MathieuL.RibièreM.MartelA. C.ZegganeS.ChauzatM. P.AubertM. F. A.2005Experimental study on the toxicity of imidacloprid given in syrup to honey bee (Apis mellifera) colonies.Pest Manage. Sci.612111125
  90. 90. FernandesM.E.dS.FernandesF. L.PicancoM. C.QueirozR. B.SilvaR. S.dHuertasA. A. G.2008Physiological selectivity of insecticides toApis mellifera(Hymenoptera: Apidae) andProtonectarina sylveirae(Hymenoptera: Vespidae) in citrusSociobiology513765774
  91. 91. FlemingW.BradburyS.1981Recovery of cholinesterase activity in mallard ducklings administered organophosphorus pesticides.J. Toxicol. Environ. Health B85-688597
  92. 92. FlickingerE. L.WhiteD. H.MitchellC. A.LamontT. G.1984Monocrotophos and dicrotophos residues in birds as a result of misuse of organophosphates in Matagorda County, Texas.J.A.O.A.C.67827828
  93. 93. FluetschK. M.SparlingD. W.1994Avian nesting success and diversity in conventionally and organically managed apple orchardsEnviron. Toxicol. Chem.131016511659
  94. 94. FowleC. D.1966The effects of phosphamidon on birds in New Brunswick forestsJ. Appl. Ecol.3169170
  95. 95. FramptonG. K.BrinkP.J.v.d2007Collembola and macroarthropod community responses to carbamate, organophosphate and synthetic pyrethroid insecticides: direct and indirect effectsEnviron. Pollut.14711425
  96. 96. FranklinM. T.WinstonM. L.MorandinL. A.2004Effects of clothianidin onBombus impatiens(Hymenoptera: Apidae) colony health and foraging abilityJ. Econ. Entomol.972369373
  97. 97. FreulerJ.BlandenierG.MeyerH.PignonP.2001Epigeal fauna in a vegetable agroecosystem.Mitteilungen der Schweizerischen Entomologischen Gesellschaft741-21742
  98. 98. FurlongM. J.VerkerkR. H. J.WrightD. J.1994Differential effects of the acylurea insect growth regulator teflubenzuron on the adults of two endolarval parasitoids ofPlutella xylostella, Cotesia plutellaeandDiadegma semiclausumPestic. Sci.414359364
  99. 99. GanJ.BondarenkoS.OkiL.HaverD.LiJ. X.2012Occurrence of fipronil and its biologically active derivatives in urban residential runoffEnviron. Sci. Technol.46314891495
  100. 100. GaoJ.GarrisonA. W.HoehamerC.MazurC. S.WolfeN. L.2000Uptake and phytotransformation of organophosphorus pesticides by axenically cultivated aquatic plants.J. Agric. Food Chem.4861146120
  101. 101. GendronA. D.MarcoglieseD. J.BarbeauS.ChristinM. S.BrousseauP.RubyS.CyrD.FournierM.2003Exposure of leopard frogs to a pesticide mixture affects life history characteristics of the lungwormRhabdias ranae.Oecologia135469476
  102. 102. GeorgiadisP. T.PistoriusJ.HeimbachU.2010Vom Winde verweht- Abdrift von Beizstauben- ein Risiko fur Honigbienen (Apis melliferaL.)?Julius-Kuhn-Archiv42433
  103. 103. GhodageriM. G.KattiP.2011Morphological and behavioral alterations induced by endocrine disrupters in amphibian tadpoles.Toxicol. Environ. Chem.931020122021
  104. 104. GiglioA.GiulianiniP. G.ZettoT.TalaricoF.2011Effects of the pesticide dimethoate on a non-target generalist carabid,Pterostichus melas italicus(Dejean, 1828) (Coleoptera: Carabidae).Italian J. Zool.784471477
  105. 105. GirolamiV.MarzaroM.VivanL.MazzonL.GreattiM.GiorioC.MartonD.TapparoA.2012Fatal powdering of bees in flight with particulates of neonicotinoids seed coating and humidity implicationJ. Appl. Entomol.1361/21726
  106. 106. GoldmanL. R.SmithD. F.NeutraR. R.1990Pesticide food poisoning from contaminated watermelons in California, 1985. Arch.Environ. Health454229236
  107. 107. GolombieskiJ. I.MarchesanE.BaumartJ. S.ReimcheG. B.JuniorC. R.StorckL.SantosS.2008Cladocera, Copepoda e Rotifera em rizipiscicultura tratada com os herbicidas metsulfuron-metílico e azimsulfuron e o inseticida carbofuran.Ciencia Rural38820972102
  108. 108. Gomez-EylesJ. L.SvendsenC.ListerL.MartinH.HodsonM. E.SpurgeonD. J.2009Measuring and modelling mixture toxicity of imidacloprid and thiacloprid onCaenorhabditis elegansandEisenia fetidaEcotoxicol. Environ. Saf.7217179
  109. 109. GourI. S.PareekB. L.2005Relative toxicity of some insecticides to coccinellid,Coccinella septempunctata Linn.and Indian honey bee,Apis cerana indicaIndian J. Agric. Res.394299302
  110. 110. Grafton-CardwellE. E.GuP.2003Conserving vedalia beetle,Rodolia cardinalis(Mulsant) (Coleoptera: Coccinellidae), in citrus: A continuing challenge as new insecticides gain registrationJ. Econ. Entomol.96513881398
  111. 111. GregorcA.BozicJ.2004Is honey bee colonies mortality related to insecticide use in agriculture? [Ali cebelje druzine odmirajo zaradi uporabe insekticida v kmetijstvu?].Sodobno Kmetijstvo3772932
  112. 112. GroutT. G.RichardsG. I.StephenP. R.1997Further non-target effects of citrus pesticides onEuseius addoensisandEuseius citri(Acari: Phytoseiidae)Exp. Appl. Acarol.213171177
  113. 113. GrueC. E.PowellG. V. N.Mc ChesneyM. J.1982Care of nestlings by wild female starlings exposed to an organophosphate pesticideJ. Appl. Ecol.19327335
  114. 114. GrueC. E.ShipleyB. K.1984Sensitivity of nestling and adult starlings to dicrotophos, an organophosphate pesticide.Environ. Res.352454465
  115. 115. HalmM. P.RortaisA.ArnoldG.TaséiJ. N.RaultS.2006New risk assessment approach for systemic insecticides: the case of honey bees and imidacloprid (Gaucho).Environ. Sci. Technol.40724482454
  116. 116. HawthorneD. J.DivelyG. P.2011Killing them with kindness? In-hive medications may inhibit xenobiotic efflux transporters and endanger honey beesPLoS One(November)e26796
  117. 117. HayasakaD.KorenagaT.Sánchez-BayoF.GokaK.2012aDifferences in ecological impacts of systemic insecticides with different physicochemical properties on biocenosis of experimental paddy fieldsEcotoxicology211191201
  118. 118. HayasakaD.KorenagaT.SuzukiK.SaitoF.Sánchez-BayoF.GokaK.2012bCumulative ecological impacts of two successive annual treatments of imidacloprid and fipronil on aquatic communities of paddy mesocosmsEcotoxicol. Environ. Saf.80355362
  119. 119. HayasakaD.KorenagaT.SuzukiK.Sánchez-BayoF.GokaK.2012cDifferences in susceptibility of five cladoceran species to two systemic insecticides, imidacloprid and fipronilEcotoxicology212421427
  120. 120. HeY.ZhaoJ.ZhengY.DesneuxN.WuK.2012Lethal effect of imidacloprid on the coccinellid predatorSerangium japonicumand sublethal effects on predator voracity and on functional response to the whiteflyBemisia tabaciEcotoxicology110
  121. 121. HeathA. G.JosephJ.CechJ.BrinkL.MobergP.ZinklJ. G.1997Physiological responses of fathead minnow larvae to rice pesticides.Ecotoxicol. Environ. Saf.373280288
  122. 122. HeinrichsE. A.AquinoG. B.ChelliahS.ValenciaS. L.ReissigW. H.1982Resurgence ofNilaparvata lugens(Stal) populations as influenced by method and timing of insecticide applications in lowland rice.Environ. Entomol.1117884
  123. 123. HelaD. G.LambropoulouD. A.KonstantinouI. K.AlbanisT. A.2005Environmental monitoring and ecological risk assessment for pesticide contamination and effects in Lake Pamvotis, northwestern GreeceEnviron. Toxicol. Chem.24615481556
  124. 124. HeldD. W.ParkerS.2011Efficacy of soil applied neonicotinoid insecticides against the azalea lace bug,Stephanitis pyrioides, in the landscapeFlorida Entomol.943599607
  125. 125. HenryM.l.BeguinM.RequierF.RollinO.OdouxJ. F.oAupinelP.AptelJ.TchamitchianS.DecourtyeA.2012A common pesticide decreases foraging success and survival in honey bees.Science336348350
  126. 126. HeongK. L.EscaladaM. M.MaiV.1994An analysis of insecticide use in rice: case studies in the Philippines and VietnamInt. J. Pest Manage.402173178
  127. 127. HigesM.Martín-HernándezR.Martínez-SalvadorA.Garrido-BailónE.González-PortoA. V.MeanaA.BernalJ. L.Del NozalM. J.BernalJ.2010A preliminary study of the epidemiological factors related to honey bee colony loss in SpainEnviron. Microbiol. Rep.22243250
  128. 128. HohreiterD. W.ReinertR. E.BushP. B.1991Effects of the insecticides carbofuran and fenvalerate on adenylate parameters in bluegill sunfish (Lepomis macrochirus).Arch. Environ. Contam. Toxicol.213325331
  129. 129. HoshinoT.TakaseI.1993New insecticide imidacloprid - Safety assessment.Noyaku Kenkyu3933745
  130. 130. HoyM. A.FlahertyD.PeacockW.CulverD.1979Vineyard and laboratory evaluations of methomyl, dimethoate and permethrin for a grape pest management program in the San Joaquin Valley of California, USA.J. Econ. Entomol.722250255
  131. 131. Huusela-VeistolaE.2000Effects of pesticide use on non-target arthropods in a Finnish cereal fieldAspects Appl. Biol.626772
  132. 132. IncertiF.BortolottiL.PorriniC.SbrennaA. M.SbrennaG.2003An extended laboratory test to evaluate the effects of pesticides on bumblebees. Preliminary resultsBull. Insectology561159164
  133. 133. InghamE. R.ColemanD. C.CrossleyD. A. Jr1994Use of sulfamethoxazole-penicillin, oxytetracycline, carbofuran, carbaryl, naphthalene and Temik to remove key organism groups in soil in a corn agroecosystemJ. Sustain. Agric.43730
  134. 134. IwasaT.MotoyamaN.AmbroseJ. T.RoeR. M.2004Mechanism for the differential toxicity of neonicotinoid insecticides in the honey bee,Apis melliferaCrop Protection235371378
  135. 135. JansenJ. P.2000A three-year field study on the short-term effects of insecticides used to control cereal aphids on plant-dwelling aphid predators in winter wheatPest Manage. Sci.566533539
  136. 136. JemecA.TislerT.DrobneD.SepcićK.FournierD.TrebseP.2007Comparative toxicity of imidacloprid, of its commercial liquid formulation and of diazinon to a non-target arthropod, the microcrustaceanDaphnia magna.Chemosphere688140818
  137. 137. JeschkeP.NauenR.SchindlerM.ElbertA.2010Overview of the status and global strategy for neonicotinoidsJ. Agric. Food Chem.59728972908
  138. 138. JingujiH.ThuyetD.UedaT.WatanabeH.2012Effect of imidacloprid and fipronil pesticide application onSympetrum infuscatum(Libellulidae: Odonata) larvae and adults.Paddy Water Environ.online first:18
  139. 139. JohanssonM.PihaH.KylinH.MeriläJ.2006Toxicity of six pesticides to common frog (Rana temporaria) tadpoles.Environ. Toxicol. Chem.251231643170
  140. 140. JohnsonB. T.1986Potential impact of selected agricultural chemical contaminants on a northern prairie wetland: a microcosm evaluationEnviron. Toxicol. Chem.55473485
  141. 141. JoyV. C.ChakravortyP. P.1991Impact of insecticides on nontarget microarthropod fauna in agricultural soil.Ecotoxicol. Environ. Saf.221816
  142. 142. KanungoP. K.AdhyaT. K.RaoV. R.1995Influence of repeated applications of carbofuran on nitrogenase activity and nitrogen-fixing bacteria associated with rhizosphere of tropical riceChemosphere31532493257
  143. 143. KarnatakA. K.ThoratP. V.2006Effect of insecticidal micro-environment on the honey bee,Apis melliferainBrassica napus.J. Appl. Biosci.3219394
  144. 144. KennedyP. J.ConradK. F.PerryJ. N.PowellD.AegerterJ.ToddA. D.WaltersK. F. A.PowellW.2001Comparison of two field-scale approaches for the study of effects of insecticides on polyphagous predators in cerealsAppl. Soil Ecol.173253266
  145. 145. KitulagodageM.ButtemerW.AstheimerL.2011Adverse effects of fipronil on avian reproduction and development: maternal transfer of fipronil to eggs in zebra finch Taeniopygia guttata and in ovo exposure in chickensGallus domesticus.Ecotoxicology204653660
  146. 146. KjaerC.ElmegaardN.AxelsenJ. A.AndersenP. N.SeidelinN.1998The impact of phenology, exposure and instar susceptibility on insecticide effects on a chrysomelid beetle populationPestic. Sci.524361371
  147. 147. KoboriY.AmanoH.2004Effects of agrochemicals on life-history parameters ofAphidius gifuensisAshmead (Hymenoptera: Braconidae)Appl. Entomol. Zool.392255261
  148. 148. KoehlerH. H.1997Mesostigmata (Gamasina, Uropodina), efficient predators in agroecosystems.Agric. Ecosyst. Environ.622-3105117
  149. 149. KoppenhoferA. M.CowlesR. S.CowlesE. A.FuzyE. M.KayaH. K.2003Effect of neonicotinoid synergists on entomopathogenic nematode fitnessEntomol. exp. appl.1061718
  150. 150. KreutzweiserD. P.GoodK. P.ChartrandD. T.ScarrT. A.HolmesS. B.ThompsonD. G.2008Effects on litter-dwelling earthworms and microbial decomposition of soil-applied imidacloprid for control of wood-boring insectsPest Manage. Sci.642112118
  151. 151. KrokeneP.1993The effect of an insect growth regulator on grasshoppers (Acrididae) and non-target arthropods in MaliJ. Appl. Entomol.1163248266
  152. 152. KrupkeC. H.HuntG. J.EitzerB. D.AndinoG.GivenK.2012Multiple routes of pesticide exposure for honey bees living near agricultural fieldsPLoS One71e29268
  153. 153. KuT. Y.WangS. C.1981Insecticidal resistance of the major insect rice pests, and the effect of insecticides on natural enemies and non-target animals.NTU Phytopathologist and Entomologist8118
  154. 154. KumarB. V.BoomathiN.KumaranN.KuttalamS.2010Non target effect of ethiprole+imidacloprid 80 WG on predators of rice planthoppers.Madras Agric. J.974/6153156
  155. 155. KumaranN.KumarB. V.BoomathiN.KuttalamS.GunasekaranK.2009Non-target effect of ethiprole 10 SC to predators of rice planthoppers.Madras Agric. J.961/6208212
  156. 156. KunkelB. A.HeldD. W.PotterD. A.2001Lethal and sublethal effects of bendiocarb, halofenozide, and imidacloprid onHarpalus pennsylvanicus(Coleoptera: Carabidae) following different modes of exposure in turfgrassJ. Econ. Entomol.9416067
  157. 157. KwonY. K.WeeS. H.KimJ. H.2004Pesticide poisoning events in wild birds in Korea from 1998 to 2002.J. Wildl. Dis.404737740
  158. 158. LahrJ.1998An ecological assessment of the hazard of eight insecticides used in desert locust control, to invertebrates in temporary ponds in the Sahel.Aquat.Ecol.322153162
  159. 159. LakshmiV. J.KrishnaiahN. V.KattiG. R.2010Potential toxicity of selected insecticides to rice leafhoppers and planthoppers and their important natural enemiesJ. Biol. Control243244252
  160. 160. Langer-JaesrichM.KohlerH. R.GerhardtA.2010Assessing toxicity of the insecticide thiacloprid onChironomus riparius(Insecta: Diptera) using multiple end pointsArch. Environ. Contam. Toxicol.584963972
  161. 161. LannaconeJ.OnofreR.HuanqujO.2007Ecotoxicological effects of cartap onPoecilia reticulata"guppy"(Poecilidae) andParacheirodon innesi"Neon Tetra" (Characidae).Gayana712170177
  162. 162. LanzoniA.SangiorgiL.LuigiV.d.ConsoliniL.PasqualiniE.BurgioG.2012Evaluation of chronic toxicity of four neonicotinoids toAdalia bipunctata L.(Coleoptera: Coccinellidae) using a demographic approach.IOBC/WPRS Bulletin74211217
  163. 163. LaoW.TsukadaD.GreensteinD. J.BayS. M.MaruyaK. A.2010Analysis, occurrence, and toxic potential of pyrethroids, and fipronil in sediments from an urban estuary.Environ. Toxicol. Chem.294843851
  164. 164. LeeS. J.TomizawaM.CasidaJ. E.2003Nereistoxin and cartap neurotoxicity attributable to direct block of the insect nicotinic receptor/channel.J. Agric. Food Chem.51926462652
  165. 165. LewisJ. L.ForschlerB. T.2010Impact of five commercial baits containing chitin synthesis inhibitors on the protist community inReticulitermes flavipes(Isoptera: Rhinotermitidae)Environ. Entomol.39198104
  166. 166. LiX.BaoC.YangD.ZhengM.LiX.TaoS.2010Toxicities of fipronil enantiomers to the honeybeeApis melliferaL. and enantiomeric compositions of fipronil in honey plant flowersEnviron. Toxicol. Chem.291127132
  167. 167. LiessM.BeketovM.2011Traits and stress: keys to identify community effects of low levels of toxicants in test systemsEcotoxicology20613281340
  168. 168. LimR. P.WongM. C.1986The effect of pesticides on the population dynamics and production ofStenocypris majorBairo (Ostracoda) in ricefieds.Arch. Hydrobiol.1063421427
  169. 169. LimaJunior.I.dS.d.NogueiraR. F.BertoncelloT. F.MeloE.P.dSuekaneR.DegrandeP. E.2010Seletividade de inseticidas sobre o complexo de predadores das pragas do algodoeiroPesquisa Agropecuaria Tropical403347353
  170. 170. LinderG.RichmondM. E.1990Feed aversion in small mammals as a potential source of hazard reduction for environmental chemicals: agrochemical case studies.Environ. Toxicol. Chem.9195105
  171. 171. LiskerE.EnsmingerM.GillS.GohK.2011Detections of eleven organophosphorus insecticides and one herbicide threatening Pacific salmonids,Oncorhynchusspp., in California, 1991-2010.Bull. Environ. Contam. Toxicol.874355360
  172. 172. LiuZ.DaiY.HuangG.GuY.NiJ.WeiH.YuanS.2011Soil microbial degradation of neonicotinoid insecticides imidacloprid, acetamiprid, thiacloprid and imidaclothiz and its effect on the persistence of bioefficacy against horsebean aphidAphis craccivoraKoch after soil application.Pest Manage. Sci.671012451252
  173. 173. LoureiroS.SvendsenC.FerreiraA. L. G.PinheiroC.RibeiroF.SoaresA. M. V. M.2010Toxicity of three binary mixtures toDaphnia magna: Comparing chemical modes of action and deviations from conceptual modelsEnviron. Toxicol. Chem.29817161726
  174. 174. LuC.WarcholK. M.CallahanR. A.2012In situ replication of honey bee colony collapse disorderBull. Insectology65199106
  175. 175. LueL. P.LewisC. C.MelchorV. E.1984The effect of aldicarb on nematode population and its persistence in carrots, soil and hydroponic solution.J. Environ. Sci. Health B193343354
  176. 176. MaccagnaniB.FerrariR.ZucchiL.BariselliM.2008Nei medicai dell’emilia-romagna: difendersi dalle cavallette, ma tutelare le apiInformatore Agrario64255356
  177. 177. MagagulaC. N.SamwaysM. J.2000Effects of insect growth regulators onChilocorus nigritus(Fabricius) (Coleoptera: Coccinellidae), a non-target natural enemy of citrus red scale,Aonidiella aurantii(Maskell) (Homoptera: Diaspididae), in southern Africa: evidence from laboratory and field trials.African Entomol.814756
  178. 178. MalinowskiH.2006Bioroznorodnosc a ochrona lasu przed szkodliwymi owadami.Progress in Plant Protection461319325
  179. 179. MarlettoF.PatettaA.ManinoA.2003Laboratory assessment of pesticide toxicity to bumble bees.Bull. Insectology561155158
  180. 180. MartikainenE.HaimiJ.AhtiainenJ.1998Effects of dimethoate and benomyl on soil organisms and soil processes- a microcosm study.Appl. Soil Ecol.91-3381387
  181. 181. MartinsG. L. M.ToscanoL. C.TomquelskiG. V.MaruyamaW. I.2009Inseticidas no controle deAnticarsia gemmatalis(Lepidoptera: Noctuidae) e impacto sobre aranhas predadoras em sojaRevista Brasileira de Ciencias Agrarias42128132
  182. 182. MatsumuraF.1985Toxicology of Pesticides.Plenum Press0-306-41979-3, New York, USA.
  183. 183. MaulJ. D.BrennanA. A.HarwoodA. D.LydyM. J.2008Effect of sediment-asociated pyrethroids, fipronil, and metabolites onChironomus tentansgrowth rate, body mass, condition index, immobilization, and survival.Environ. Toxicol. Chem.271225822590
  184. 184. MayerD. F.LundenJ. D.1994Effects of the adjuvant Sylgard 309 on the hazard of selected insecticides to honey bees.Bee Sci.33135138
  185. 185. MayerD. F.PattenK. D.MacfarlaneR. P.ShanksC. H.1994Differences between susceptibility of four pollinator species (Hymenoptera: Apoidea) to field weathered insecticide residues.Melanderia502427
  186. 186. MedrzyckiP.MontanariR.BortolottiL.SabatiniA. G.MainiS.PorriniC.2003Effects of imidacloprid administered in sublethal doses on honey bee behaviour. Laboratory tests.Bull. Insectology5615962
  187. 187. MeherH. C.GajbhiyeV. T.SinghG.KamraA.ChawlaG.2010Persistence and nematicidal efficacy of carbosulfan, cadusafos, phorate, and triazophos in soil and uptake by chickpea and tomato crops under tropical conditions.J. Agric. Food Chem.58318151822
  188. 188. MesléardF.GarneroS.BeckN.RosecchiE.2005Uselessness and indirect negative effects of an insecticide on rice field invertebrates.Comptes Rendus Biologies32810-1195562
  189. 189. MineauP.1988Avian mortality in agroecosystems. I. The case against granule insecticides in Canada.In: Field Methods for the Study of Environmental Effects of Pesticides, GreavesM.P. et al., editors, British Crop Protection Council, London312
  190. 190. MineauP.WhitesideM.2006Lethal risk to birds from insecticide use in the United States- A spatial and temporal analysis.Environ. Toxicol. Chem.25512141222
  191. 191. MirandaG. R. B.RaetanoC. G.SilvaE.DaamM. A.CerejeiraM. J.2011Environmental fate of neonicotinoids and classification of their potential risks to hypogean, epygean, and surface water ecosystems in Brazil.Hum. Ecol. Risk Assess.174981995
  192. 192. MoensJ.TirryL.ClercqP.d.2012Susceptibility of cocooned pupae and adults of the parasitoidMicroplitis mediatorto selected insecticidesPhytoparasitica40159
  193. 193. MommaertsV.ReyndersS.BouletJ.BesardL.SterkG.SmaggheG.2010Risk assessment for side-effects of neonicotinoids against bumblebees with and without impairing foraging behaviorEcotoxicology191207215
  194. 194. MorandinL. A.WinstonM. L.2003Effects of novel pesticides on bumble bee (Hymenoptera: Apidae) colony health and foraging abilityEnviron. Entomol.323555563
  195. 195. MorebyS. J.SouthwayS.BarkerA.HollandJ. M.2001A comparison of the effect of new and established insecticides on nontarget invertebrates on winter wheat fields.Environ. Toxicol. Chem.201022432254
  196. 196. MoserS. E.ObryckiJ. J.2009Non-target effects of neonicotinoid seed treatments; mortality of coccinellid larvae related to zoophytophagyBiol. Control513487492
  197. 197. MoserV. C.Mc DanielK. L.PhillipsP. M.LowitA. B.2010Time-course, dose-response, and age comparative sensitivity of N-methyl carbamates in rats.Toxicol. Sci.1141113123
  198. 198. MoslehY. Y.Paris-PalaciosS.CouderchetM.VernetG.2003Acute and sublethal effects of two insecticides on earthworms (Lumbricus terrestrisL.) under laboratory conditions.Environ. Toxicol.18118
  199. 199. MoultonC. A.FlemmingW. J.PurnellC. E.1996Effects of two cholinesterase-inhibiting pesticides on freshwater musselsEnviron. Toxicol. Chem.152131137
  200. 200. MullinC. A.FrazierM.FrazierJ. L.AshcraftS.SimondsR.D.vE.PettisJ. S.2010High levels of miticides and agrochemicals in North American apiaries: implications for honey bee healthPLoS One53e9754
  201. 201. NakahiraK.KashitaniR.TomodaM.KodamaR.ItoK.YamanakaS.MomoshitaM.ArakawaR.TakagiM.2011Systemic nicotinoid toxicity against the predatory miridPilophorus typicus: residual side effect and evidence for plant suckingJ. Faculty Agric. Kyushu University5615355
  202. 202. NaveedM.SalamA.SaleemM. A.RafiqM.HamzaA.2010Toxicity of thiamethoxam and imidacloprid as seed treatments to parasitoids associated to control Bemisia tabaciPakistan J. Zool.425559565
  203. 203. NoreliusE.LockwoodJ.1999The effects of reduced agent-area insecticide treatments for rangeland grasshopper (Orthoptera: Acrididae) control on bird densities.Arch. Environ. Contam. Toxicol.374519528
  204. 204. OhnesorgW. J.JohnsonK. D.O’NealM. E.2009Impact of reduced-risk insecticides on soybean aphid and associated natural enemies.J. Econ. Entomol.102518161826
  205. 205. OldroydB. P.2007What’s killing American honey bees?PLOS Biology56e168
  206. 206. PapachristosD. P.MilonasP. G.2008Adverse effects of soil applied insecticides on the predatory coccinellidHippodamia undecimnotata(Coleoptera: Coccinellidae)Biol. Control4717781
  207. 207. ParkerM.GoldsteinM.2000Differential toxicities of organophosphate and carbamate insecticides in the nestling European starling (Sturnus vulgaris).Arch. Environ. Contam. Toxicol.392233242
  208. 208. PattersonK.1991Killing the birds and the bees.Environmental Action23178
  209. 209. PeckD. C.2009Comparative impacts of white grub (Coleoptera: Scarabaeidae) control products on the abundance of non-target soil-active arthropods in turfgrassPedobiologia525287299
  210. 210. PeckD. C.OlmsteadD.2010Neonicotinoid insecticides disrupt predation on the eggs of turf-infesting scarab beetlesBull. Entomol. Res.1006689700
  211. 211. PekárS.1999Foraging mode: a factor affecting the susceptibility of spiders (Araneae) to insecticide applicationsPestic. Sci.551110771082
  212. 212. PerfectoI.1990Indirect and direct effects in a tropical agroecosystem: the maize-pest-ant system in Nicaragua.Ecology71621252134
  213. 213. PettisJ.van EngelsdorpD.JohnsonJ.DivelyG.2012Pesticide exposure in honey bees results in increased levels of the gut pathogenNosemaNaturwissenschaften992153158
  214. 214. PevelingR.Mc WilliamA. N.NagelP.RasolomananaH.RaholijaonaRakotomianina. L.RavoninjatovoA.DewhurstC. F.GibsonG.RafanomezanaS.et.al2003Impact of locust control on harvester termites and endemic vertebrate predators in MadagascarJ. Appl. Ecol.404729741
  215. 215. PorterW. P.GreenS. M.DebbinkN. L.CarlsonI.1993Groundwater pesticides: interactive effects of low concentrations of carbamates aldicarb and methomyl and the triazine metribuzin of thyroxine and somatotropin levels in white rats.J. Toxicol. Environ. Health4011534
  216. 216. PotterD. A.BuxtonM. C.RedmondC. T.PattersonC. G.PoweluA. J.1990Toxicity of pesticides to earthworms (Oligochaeta: Lumbricidae) and effect on thatch degradation in Kentucky bluegrass turf.J. Econ. Entomol.83623622369
  217. 217. PottsG. R.1986The Partridge - Pesticides, Predation and Conservation.Collins, London, UK.
  218. 218. PozzebonA.DusoC.TirelloP.OrtizP. B.2011Toxicity of thiamethoxam toTetranychus urticaeKoch andPhytoseiulus persimilisAthias-Henriot (Acari Tetranychidae, Phytoseiidae) through different routes of exposure.Pest Manage. Sci.673352359
  219. 219. PrabhakerN.CastleS.ByrneF.HenneberryT. J.ToscanoN. C.2006Establishment of baseline susceptibility data to various insecticides for Homalodisca coagulata (Homoptera: Cicadellidae) by comparative bioassay techniquesJ. Econ. Entomol.991141154
  220. 220. PreethaG.ManoharanT.StanleyJ.KuttalamS.2010aImpact of chloronicotinyl insecticide, imidacloprid on egg, egg-larval and larval parasitoids under laboratory conditions.J. Plant Protection Res.504535540
  221. 221. PreethaG.StanleyJ.SureshS.SamiyappanR.2010bRisk assessment of insecticides used in rice on miridbug,Cyrtorhinus lividipennisReuter, the important predator of brown planthopper,Nilaparvata lugens(Stal.)Chemosphere805498503
  222. 222. PrintesL. B.CallaghanA.2004A comparative study on the relationship between acetylcholinesterase activity and acute toxicity inDaphnia magnaexposed to acetylcholineesterase insecticides.Environ. Toxicol. Chem.23512411247
  223. 223. QinG. Q.PresleyS. M.AndersonT. A.GaoW. M.MaulJ. D.2011Effects of predator cues on pesticide toxicity: toward an understanding of the mechanism of the interaction.Environ. Toxicol. Chem.30819261934
  224. 224. RainwaterT. R.LeopoldV. A.HooperM. J.KendallR. J.1995Avian exposure to organophosphorous and carbamate pesticides on a coastal South Carolina golf course.Environ. Toxicol. Chem.141221552161
  225. 225. RamS.GuptaG. P.1994Bioefficacy of systemic insecticides against target pest jassid (Amrasca devastans) and their impact on non-target soil microarthropods in cotton (Gossypiumspp.).Indian J. Entomol.564313321
  226. 226. RedoanA. C.CarvalhoG. A.CruzI.FigueiredoM.d. L. C.SilvaR. B.d2010Efeito de inseticidas usados na cultura do milho (Zea maysL.) sobre ninfas e adultos deDoru luteipes(Scudder) (Dermaptera: Forficulidae) em semicampo.Revista Brasileira de Milho e Sorgo93223235
  227. 227. RodriguesE.d. L.FantaE.1998Liver histopathology of the fishBrachydanio rerioHamilton-Buchman after acute exposure to sublethal levels of the organophosphate dimethoate 500Revista Brasileira de Zoologia152441450
  228. 228. RortaisA.ArnoldG.HalmM. P.Touffet-BriensF.2005Modes of honeybees exposure to systemic insecticides: estimated amounts of contaminated pollen and nectar consumed by different categories of beesApidologie3617183
  229. 229. RudolphS. G.ZinklJ. G.AndersonD. W.SheaP. J.1984Prey-capturing ability of American kestrels fed DDE and acephate or acephate alone.Arch. Environ. Contam. Toxicol.13367372
  230. 230. RustM. K.SaranR. K.2008Toxicity, repellency, and effects of acetamiprid on western subterranean termite (Isoptera: Rhinotermitidae).J. Econ. Entomol.101413601366
  231. 231. SaberM.2011Acute and population level toxicity of imidacloprid and fenpyroximate on an important egg parasitoid,Trichogramma cacoeciae(Hymenoptera: Trichogrammatidae)Ecotoxicology20614761484
  232. 232. SanMiguel. A.RavetonM.LemperiereG.RavanelP.2008Phenylpyrazoles impact onFolsomia candida(Collembola). Soil Biol.Biochem.40923512357
  233. 233. SánchezMeza. J. C.AvilaPerez. P.BorjaSalin. M.PachecoSalazar. V. F.LapointT.2010Inhibition of cholinesterase activity by soil extracts and predicted environmental concentrations (PEC) to select relevant pesticides in polluted soilsJ. Environ. Sci. Health B453214221
  234. 234. Sánchez-BayoF.2009From simple toxicological models to prediction of toxic effects in timeEcotoxicology183343354
  235. 235. Sánchez-BayoF.2012Insecticides mode of action in relation to their toxicity to non-target organisms.J. Environ. Anal. Toxicol.S4S4002
  236. 236. Sánchez-BayoF.GokaK.2005Unexpected effects of zinc pyrithione and imidacloprid on Japanese medaka fish (Oryzias latipes).Aquat. Toxicol.744285293
  237. 237. Sánchez-BayoF.GokaK.2006Ecological effects of the insecticide imidacloprid and a pollutant from antidandruff shampoo in experimental rice fields.Environ. Toxicol. Chem.25616771687
  238. 238. Sánchez-BayoF.YamashitaH.OsakaR.YonedaM.GokaK.2007Ecological effects of imidacloprid on arthropod communities in and around a vegetable crop.J. Environ. Sci. Health B423279286
  239. 239. SchaeferC. H.MiuraT.DuprasE. F. JrWilderW. H.MulliganF. S. III1988Efficacy of CME 134 against mosquitoes (Diptera: Culicidae): effects on nontarget organisms and evaluation of potential chemical persistence.J. Econ. Entomol.81411281132
  240. 240. SchmuckR.2004Effects of a chronic dietary exposure of the honeybeeApis mellifera(Hymenoptera: Apidae) to imidacloprid.Arch. Environ. Contam. Toxicol.474471478
  241. 241. SchmuckR.SchöningR.StorkA.SchramelO.2001Risk posed to honeybees (Apis melliferaL, Hymenoptera) by an imidacloprid seed dressing of sunflowers.Pest Manage. Sci.573225238
  242. 242. SchmuckR.StadlerT.SchmidtH. W.2003Field relevance of a synergistic effect observed in the laboratory between an EBI fungicide and a chloronicotinyl insecticide in the honeybee (Apis melliferaL, Hymenoptera).Pest Manage. Sci.593279286
  243. 243. SchneiderF.1966Some pesticide-wildlife problems in SwitzerlandJ. Appl. Ecol.31520
  244. 244. SechserB.FreulerJ.2003The impact of thiamethoxam on bumble bee broods (Bombus terrestrisL.) following drip application in covered tomato cropsAnzeiger fur Schadlingskunde7637477
  245. 245. SétamouM.RodriguezD.SaldanaR.SchwarzloseG.PalrangD.NelsonS. D.2010Efficacy and uptake of soil-applied imidacloprid in the control of Asian citrus psyllid and a citrus leafminer, two foliar-feeding citrus pestsJ. Econ. Entomol.103517119
  246. 246. SharmaD. R.2010Bioefficacy of insecticides against peach leaf curl aphid,Brachycaudus helichrysi(Kaltenbach) in PunjabIndian J. Entomol.723217222
  247. 247. ShiX.JiangL.WangH.QiaoK.WangD.WangK.2011Toxicities and sublethal effects of seven neonicotinoid insecticides on survival, growth and reproduction of imidacloprid-resistant cotton aphid,Aphis gossypiiPest Manage. Sci.671215281533
  248. 248. ShimodaT.YaraK.KawazuK.2011The effects of eight insecticides on the foraging behavior of the parasitoid waspCotesia vestalisJ. Plant Interact.62/3189190
  249. 249. SimpsonI. C.RogerP. A.OficialR.GrantI. F.1994Effects of nitrogen fertiliser and pesticide management on floodwater ecology in a wetland ricefieldBiol. Fertil. Soils183219227
  250. 250. SmeltJ. H.CrumS. J. H.TeunissenW.LeistraM.1987Accelerated transformation of aldicarb, oxamyl and ethoprophos after repeated soil treatmentsCrop Protection65295303
  251. 251. SmithS. F.KrischikV. A.1999Effects of systemic imidacloprid onColeomegilla maculata(Coleoptera: Coccinellidae).Environ. Entomol.28611891195
  252. 252. SokolovI. M.2000How does insecticidal control of grasshoppers affect non-target arthropods?
  253. 253. SongM. Y.BrownJ. J.2006Influence of fluctuating salinity on insecticide tolerance of two euryhaline arthropodsJ. Econ. Entomol.993745751
  254. 254. SpragueL. A.NowellL. H.2008Comparison of pesticide concentrations in streams at low flow in six metropolitan areas of the United StatesEnviron. Toxicol. Chem.272288298
  255. 255. SrinivasK.MadhumathiT.2005Effect of insecticide applications on the predator population in rice ecosystem of Andhra Pradesh.Pest Manage. Econ. Zool.1317175
  256. 256. StadlerT.MartinezGines. D.ButelerM.2003Long-term toxicity assessment of imidacloprid to evaluate side effects on honey bees exposed to treated sunflower in ArgentinaBull. Insectology5617781
  257. 257. StapelJ. O.CorteseroA. M.LewisW. J.2000Disruptive sublethal effects of insecticides on biological control: altered foraging ability and life span of a parasitoid after feeding on extrafloral nectar of cotton treated with systemic insecticidesBiol. Control17243249
  258. 258. StaraJ.OurednickovaJ.KocourekF.2011Laboratory evaluation of the side effects of insecticides onAphidius colemani(Hymenoptera: Aphidiidae),Aphidoletes aphidimyza(Diptera: Cecidomyiidae), andNeoseiulus cucumeris(Acari: Phytoseidae)J. Pest Sci.8412531
  259. 259. StarkJ.VargasR.2005Toxicity and hazard assessment of fipronil toDaphnia pulex Ecotoxicol.Environ. Saf.6211116
  260. 260. StarkJ. D.BanksJ. E.VargasR.2004How risky Is risk assessment: the role that life history strategies play in susceptibility of species to stressPNAS1013732736
  261. 261. StarnerK.GohK.2012Detections of the neonicotinoid insecticide imidacloprid in surface waters of three agricultural regions of California, USA, 2010-2011.Bull. Environ. Contam. Toxicol.883316321
  262. 262. SteinbauerM. J.PevelingR.2011The impact of the locust control insecticide fipronil on termites and ants in two contrasting habitats in northern AustraliaCrop Protection307814825
  263. 263. SterkG.BenuzziM.2004Nuovi fitofarmaci, prove di tossicita sui bombi in serraColture Protette3317577
  264. 264. StevensM. M.BurdettA. S.MudfordE. M.HelliwellS.DoranG.2011The acute toxicity of fipronil to two non-target invertebrates associated with mosquito breeding sites in AustraliaActa Tropica1172125130
  265. 265. StoughtonSarah. J.KarstenLiber.JosephCulp.AllanCessna.2008Acute and chronic toxicity of imidacloprid to the aquatic invertebratesChironomus tentansandHyalella aztecaunder constant- and pulse-exposure conditions.Arch. Environ. Contam. Toxicol.544662673
  266. 266. SuchailS.GuezD.BelzuncesL. P.2001Discrepancy between acute and chronic toxicity induced by imidacloprid and its metabolites inApis mellifera.Environ. Toxicol. Chem.201124822486
  267. 267. SugiyamaK.KatayamaH.SaitoT.2011Effect of insecticides on the mortalities of three whitefly parasitoid species,Eretmocerus mundus,Eretmocerus eremicusandEncarsia formosa(Hymenoptera: Aphelinidae).Appl. Entomol. Zool.463311317
  268. 268. SzczepaniecA.CrearyS. F.LaskowskiK. L.NyropJ. P.RauppM. J.2011Neonicotinoid insecticide imidacloprid causes outbreaks of spider mites on elm trees in urban landscapesPLoS One65e20018
  269. 269. SzendreiZ.GrafiusE.ByrneA.ZieglerA.2012Resistance to neonicotinoid insecticides in field populations of the Colorado potato beetle (Coleoptera: Chrysomelidae).Pest Manage. Sci.686941946
  270. 270. TakadaY.KawamuraS.TanakaT.2001Effects of various insecticides on the development of the egg parasitoidTrichogramma dendrolimi(Hymenoptera: Trichogrammatidae)J. Econ. Entomol.94613401343
  271. 271. TanakaT.MinakuchiC.2011Insecticides and parasitoids.In: Insecticides- Advances in Integrated Pest ManagementPerveen, F., editor, InTech, Rijeka, Croatia115140
  272. 272. TapparoA.GiorioC.MarzaroM.MartonD.SoldaL.GirolamiV.2011Rapid analysis of neonicotinoid insecticides in guttation drops of corn seedlings obtained from coated seedsJ. Environ. Monit.13615641568
  273. 273. TeetersB. S.JohnsonR. M.EllisM. D.SiegfriedB. D.2012Using video-tracking to assess sublethal effects of pesticides on honey bees (Apis melliferaL.)Environ. Toxicol. Chem.31613491354
  274. 274. TennekesH. A.2010aThe significance of the Druckrey-Küpfmüller equation for risk assessment - The toxicity of neonicotinoid insecticides to arthropods is reinforced by exposure time.Toxicology276114
  275. 275. TennekesH. A.2010bThe Systemic Insecticides: A Disaster in the MakingETS Nederland BV, Zutphen, The Netherlands.978-90-79627-06-6
  276. 276. TennekesH. A.Sánchez-BayoF.2012Time-dependent toxicity of neonicotinoids and other toxicants: implications for a new approach to risk assessment.J. Environ. Anal. Toxicol.S4S4001
  277. 277. ThackerJ. R. M.JepsonP. C.1993Pesticide risk assessment and non-target invertebrates: integrating population depletion, population recovery, and experimental design.Bull. Environ. Contam. Toxicol.514523531
  278. 278. ThomazoniD.SoriaM. F.KodamaC.CarbonariV.FortunatoR. P.DegrandeP. E.ValterJunior. V. A.2009Selectivity of insecticides for adult workers ofApis mellifera(Hymenoptera: Apidae)Revista Colombiana de Entomologia352173176
  279. 279. ThompsonH.WalkerC.HardyA.1991Changes in activity of avian serum esterases following exposure to organophosphorus insecticidesArch. Environ. Contam. Toxicol.204514518
  280. 280. ThorntonM.MillerJ.HutchinsonP.AlvarezJ.2010Response of potatoes to soil-applied insecticides, fungicides, and herbicidesPotato Research534351358
  281. 281. TianH.RuS.BingX.WangW.2010Effects of monocrotophos on the reproductive axis in the male goldfish (Carassius auratus): potential mechanisms underlying vitellogenin inductionAquat. Toxicol.9816773
  282. 282. TianJ.ChenY.LiZ.PengY.YeG.2011Assessment of effect of transgenic rice with cry1Ab gene and two insecticides on immune of non-target natural enemy,Pardosa pseudoannulataChinese J. Biol. Control274559563
  283. 283. TomizawaM.LeeD. L.CasidaJ. E.2000Neonicotinoid insecticides: molecular features conferring selectivity for insect versus mammalian nicotinic receptors.J. Agric. Food Chem.481260166024
  284. 284. TomlinC. D. S.2009The e-Pesticide Manual.Tomlin, C.D.S.,editor. 12 ed. Surrey, U.K.: British Crop Protection Council.
  285. 285. TremoladaP.MazzoleniM.SaliuF.ColomboM.VighiM.2010Field trial for evaluating the effects on honeybees of corn sown using cruiser® and Celest ®Treated Seeds.Bull. Environ. Contam. Toxicol.853229234
  286. 286. TurnerA. S.BaleJ. S.ClementsR. O.1987The effect of a range of pesticides on non-target organisms in the grassland environment.Proceedings, Crop Protection in Northern Britain ‘87, Dundee University, 15-17 March.290295
  287. 287. van DijkT. C.2010Effects of neonicotinoid pesticide pollution of Dutch surface water on non-target species abundanceUniversiteit Utrecht.77
  288. 288. Van GestelC. A. M.1992Validation of earthworm toxicity tests by comparison with field studies: a review of benomyl, carbendazim, carbofuran, and carbarylEcotoxicol. Environ. Saf.23221236
  289. 289. van TimmerenS.WiseJ. C.IsaacsR.2012Soil application of neonicotinoid insecticides for control of insect pests in wine grape vineyards.Pest Manage. Sci.684537542
  290. 290. VasukiV.1992Sublethal effects of hexaflumuron, an insect growth regulator, on some non-target larvivorous fishes.Indian J. Exp. Biol.301211631165
  291. 291. VergheseA.1998Effect of imidacloprid on mango hoppers,Idioscopusspp. (Homoptera: Cicadellidae).Pest Manage. Hort. Ecosyst.427074
  292. 292. VernonR. S.HerkW.v.TolmanJ.SaavedraH. O.ClodiusM.GageB.2008Transitional sublethal and lethal effects of insecticides after dermal exposures to five economic species of wireworms (Coleoptera: Elateridae)J. Econ. Entomol.1012365374
  293. 293. VidauC.DiogonM.AufauvreJ.FontbonneR.ViguesB.BrunetJ. L.TexierC.BironD. G.BlotN.El -AlaouiH.et.al.2011Exposure to sublethal doses of fipronil and thiacloprid highly increases mortality of honeybees previously infected byNosema ceranaePLoS One(June)e21550
  294. 294. VogtH.JustJ.GrutzmacherA.2009Einfluss von Insektiziden im Obstbau auf den OhrwurmForficula auricularia.Mitteilungen der Deutschen Gesellschaft fur allgemeine und angewandte Entomologie17211214
  295. 295. VyasN. B.KuenzelW. J.HillE. F.SauerJ. R.1995Acephate affects migratory orientation of the white-throated sparrow (Zonotrichia albicollis).Environ. Toxicol. Chem.141119611965
  296. 296. WadaS.ToyotaK.2008Effect of three organophosphorous nematicides on non-target nematodes and soil microbial communityMicrobes and Environments234331336
  297. 297. WalkerC. H.HopkinS. P.SiblyR. M.PeakallD. B.2001Principles of Ecotoxicology2nd), Taylor & Francis, Glasgow, UK.0-7484-0940-8
  298. 298. WalkerM. K.StufkensM. A. W.WallaceA. R.2007Indirect non-target effects of insecticides on Tasmanian brown lacewing (Micromus tasmaniae) from feeding on lettuce aphid (Nasonovia ribisnigri)Biol. Control4313140
  299. 299. WangY.YuR.ZhaoX.AnX.ChenL.WuC.WangQ.2012Acute toxicity and safety evaluation of neonicotinoids and macrocyclic lactiones to adult wasps of fourTrichogrammaspecies (Hymenoptera: Trichogrammidae)Acta Entomologica Sinica5513645
  300. 300. WayM. J.ScopesN. E. A.1968Studies on the persistence and effects on soil fauna of some soil-applied systemic insecticidesAnn. Appl. Biol.62199214
  301. 301. WebsterT. C.PengY. S.1989Short-term and long-term effects of methamidophos on brood rearing in honey bee (Hymenoptera: Apidae) colonies.J. Econ. Entomol.8216974
  302. 302. WhiteD. H.SegmakJ. T.1990Brain cholinesterase inhibition in songbirds from pecan groves sprayed with phosalone and disulfoton.J. Wildl. Dis.26103106
  303. 303. WirthE. F.PenningtonP. L.LawtonJ. C.De LorenzoM. E.BeardenD.ShaddrixB.SivertsenS.FultonM. H.2004The effects of the contemporary-use insecticide (fipronil) in an estuarine mesocosm.Environ. Pollut.1313365371
  304. 304. YangE. C.ChuangY. C.ChenY. L.ChangL. H.2008Abnormal foraging behavior induced by sublethal dosage of imidacloprid in the honey bee (Hymenoptera: Apidae)J. Econ. Entomol.101617431748
  305. 305. YenJ. H.LinK. H.WangY. S.2000Potential of the insecticides acephate and methamidophos to contaminate groundwater.Ecotoxicol. Environ. Saf.4517986
  306. 306. ZangY.ZhongY.LuoY.KongZ. M.2000Genotoxicity of two novel pesticides for the earthworm,Eisenia fetida.Environ. Pollut.1082271278
  307. 307. ZhangA.KaiserH.MaienfischP.CasidaJ. E.2000Insect nicotinic acetylcholine receptor: conserved neonicotinoid specificity of [3H]imidacloprid binding site.J. Neurochem.75312941303
  308. 308. ZhouS.DongQ.LiS.GuoJ.WangX.ZhuG.2009Developmental toxicity of cartap on zebrafish embryosAquat. Toxicol.954339346

Written By

Francisco Sánchez-Bayo, Henk A. Tennekes and Koichi Goka

Submitted: May 3rd, 2012 Published: January 30th, 2013