**5. Risk assessment of systemic insecticides**

While fipronil applied at the recommended rates in rice fields induces biochemical altera‐ tions 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

Longevity of predatory bug *Podisus maculiventris* was reduced after preying on Colorado po‐ tato 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 de‐ crease (<30%) the total protists population in the guts of termites (*Reticultermes flavipes*), thus

Indirect effects result from the dynamics of ecosystems. Thus, applications of granular pho‐ rate 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

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 Ni‐ caragua, the population levels of the noctuid pest *Spodoptera frugiperda* increased because of lesser foraging activity by predatory ants [212]. Methomyl eliminated the phytoseiid preda‐ tory mite *Metaseiulus occidentalis* for 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. schoenei* by 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 popula‐ tions of house mice (*Mus musculus*) in the treated areas as the insect food source was deplet‐ ed. 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

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 ter‐

limit (0.01 µg/L) [117].

*4.2.4. Insect growth regulators*

upsetting their digestive homeostasis [165].

386 Insecticides - Development of Safer and More Effective Technologies

the eliminated springtails [300].

or both.

**4.3. Indirect effects on populations and communities**

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]. Con‐ cerns 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 re‐ peatedly 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 be‐ tween concentration and time of exposure [234], the critical levels of residue and time of ex‐ posure can be determined.

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 ani‐

Impact of Systemic Insecticides on Organisms and Ecosystems

http://dx.doi.org/10.5772/52831

389

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 im‐ pacts of the new compounds. Awareness of the increasing contamination of the environ‐ ment with active residues of these chemicals should help regulators and managers to

and Koichi Goka3

[1] Abbott, V. A., Nadeau, J. L., Higo, H. A., & Winston, M. L. (2008). Lethal and suble‐ thal effects of imidacloprid on *Osmia lignaria* and clothianidin on *Megachile rotundata*

[2] Agritox. (2002). Liste des substances actives. *Paris, France: Institut National de la Re‐*

[3] Al-Antary, T. M., Ateyyat, M. A., & Abussamin, B. M. (2010). Toxicity of certain in‐ secticides to the parasitoid *Diaeretiella rapae* (Mcintosh) (Hymenoptera: Aphidiidae)

mals are not far fetched and should be taken seriously [275].

implement new approaches for risk assessment of these substances.

2 Experimental Toxicology Services (ETS) Nederland BV, The Netherlands

(Hymenoptera: Megachilidae). *J. Econ. Entomol.*, 101(3), 784-796.

Francisco Sánchez-Bayo1\*, Henk A. Tennekes2

1 University of Technology Sydney, Australia

*cherche Agronomique.*

\*Address all correspondence to: sanchezbayo@mac.com

3 National Institute for Environmental Sciences, Japan

**6. Conclusions**

**Author details**

**References**

The declining populations of predatory and parasitic arthropods after exposure to recom‐ mended 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 implicat‐ ed. 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 af‐ fected to come back, and this usually occurs by recolonisation and immigration of individu‐ als 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 recov‐ ery 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. Be‐ cause of the short life-cycle of many zooplankton species, the negative population parame‐ ters 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 wa‐ ters 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 elim‐ ination, of entire populations of aquatic arthropods from the affected areas. As time is a crit‐ ical 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 Eng‐ land 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 ani‐ mals are not far fetched and should be taken seriously [275].
