John D. Stark

Effects of neonicotinoids and fipronil on non-target invertebrates

We assessed the state of knowledge regarding the effects of large-scale pollution with neonicotinoid insecticides and fipronil on non-target invertebrate species of terrestrial, freshwater and marine environments. A large section of the assessment is dedicated to the state of knowledge on sublethal effects on honeybees (Apis mellifera) because this important pollinator is the most studied non-target invertebrate species. Lepidoptera (butterflies and moths), Lumbricidae (earthworms), Apoidae sensu lato (bumblebees, solitary bees) and the section “other invertebrates” review available studies on the other terrestrial species. The sections on freshwater and marine species are rather short as little is known so far about the impact of neonicotinoid insecticides and fipronil on the diverse invertebrate fauna of these widely exposed habitats. For terrestrial and aquatic invertebrate species, the known effects of neonicotinoid pesticides and fipronil are described ranging from organismal toxicology and behavioural effects to population-level effects. For earthworms, freshwater and marine species, the relation of findings to regulatory risk assessment is described. Neonicotinoid insecticides exhibit very high toxicity to a wide range of invertebrates, particularly insects, and field-realistic exposure is likely to result in both lethal and a broad range of important sublethal impacts. There is a major knowledge gap regarding impacts on the grand majority of invertebrates, many of which perform essential roles enabling healthy ecosystem functioning. The data on the few non-target species on which field tests have been performed are limited by major flaws in the outdated test protocols. Despite large knowledge gaps and uncertainties, enough knowledge exists to conclude that existing levels of pollution with neonicotinoids and fipronil resulting from presently authorized uses frequently exceed the lowest observed adverse effect concentrations and are thus likely to have large-scale and wide ranging negative biological and ecological impacts on a wide range of non-target invertebrates in terrestrial, aquatic, marine and benthic habitats.

The Synergistic Toxicity of Pesticide Mixtures: Implications for Risk Assessment and the Conservation of Endangered Pacific Salmon

Background Mixtures of organophosphate and carbamate pesticides are commonly detected in freshwater habitats that support threatened and endangered species of Pacific salmon (Oncorhynchus sp.). These pesticides inhibit the activity of acetylcholinesterase (AChE) and thus have potential to interfere with behaviors that may be essential for salmon survival. Although the effects of individual anticholin-esterase insecticides on aquatic species have been studied for decades, the neurotoxicity of mixtures is still poorly understood. Objectives We assessed whether chemicals in a mixture act in isolation (resulting in additive AChE inhibition) or whether components interact to produce either antagonistic or synergistic toxicity. Methods We measured brain AChE inhibition in juvenile coho salmon (Oncorhynchus kisutch) exposed to sublethal concentrations of the organophosphates diazinon, malathion, and chlorpyrifos, as well as the carbamates carbaryl and carbofuran. Concentrations of individual chemicals were normalized to their respective median effective concentrations (EC50) and collectively fit to a nonlinear regression. We used this curve to determine whether toxicologic responses to binary mixtures were additive, antagonistic, or synergistic. Results We observed addition and synergism, with a greater degree of synergism at higher exposure concentrations. Several combinations of organophosphates were lethal at concentrations that were sublethal in single-chemical trials. Conclusion Single-chemical risk assessments are likely to underestimate the impacts of these insecticides on salmon in river systems where mixtures occur. Moreover, mixtures of pesticides that have been commonly reported in salmon habitats may pose a more important challenge for species recovery than previously anticipated.

Potential for Areawide Integrated Management of Mediterranean Fruit Fly (Diptera: Tephritidae) with a Braconid Parasitoid and a Novel Bait Spray

Abstract The braconid wasp, Fopius arisanus (Sonan), a biological control agent for Mediterranean fruit fly, Ceratitis capitata (Wiedemann), was studied in coffee, Coffea arabica L. Fopius arisanus, comprised 79.3% of the total parasitoids (7,014) recovered from fruits collected at three small coffee farms. Data from seasonal host/parasitoid studies at a large coffee plantation also suggested that the most effective natural enemy of C. capitata in coffee may now reside in Hawaii. The original parasitoids introduced into Hawaii for C. capitata control (Diachasmimorpha tryoni (Cameron), Tetrastichus giffardianus Silvestri, and Dirhinus giffardii Silvestri) are now rare. Abundance of F. arisanus with respect to other parasitoids collected was influenced by elevation (274, 457, 610 m). Fopius arisanus was the dominant parasitoid at all three elevations, Diachasmimorpha longicaudata (Ashmead) occurred consistently, and T. giffardianus was abundant only at low elevation. The impacts on C. capitata and F. arisanus populations of bait sprays containing malathion, spinosad, or phloxine B applied to coffee were also evaluated. All three bait sprays suppressed C. capitata populations. Spinosad and phloxine B bait sprays appeared less harmful to the wasp than malathion. Fopius arisanus offers the potential for areawide management of C. capitata that includes biological control and integration with more environmentally safe chemical controls such as spinosad and phloxine B bait sprays.

Do Biopesticides Affect the Demographic Traits of a Parasitoid Wasp and Its Biocontrol Services through Sublethal Effects

Pesticide risk assessments are usually based on short-term acute toxicity tests, while longer-term population dynamic related traits, critical to the success of biological control and Integrated Pest Management (IPM) programs, are often overlooked. This is increasingly important with respect to new biopesticides that frequently cause no short-term acute effects, but that can induce multiple physiological and behavioral sublethal effects, leading to a decrease in population growth and ecosystem services. In this study we assessed the lethal and sublethal effects of six biopesticides [abamectin, azadirachtin, Bacillus thuringiensis, borax plus citrus oil (Prev-Am®), emamectin benzoate, and spinosad], used in tomato crops to control the invasive pest Tuta absoluta (Lepidoptera: Gelechiidae), on adults and pupae of the parasitoid Bracon nigricans (Hymenoptera: Braconidae). Data on female survival and production of female offspring were used to calculate population growth indexes as a measure of population recovery after pesticide exposure. Spinosad caused 100% and 80% mortality in exposed adults (even 10 d after the treatment) and pupae, respectively. Although most of the biopesticides had low levels of acute toxicity, multiple sublethal effects were observed. The biocontrol activity of both females that survived 1-h and 10-d old residues, and females that emerged from topically treated pupae was significantly affected by the application of the neurotoxic insecticides emamectin benzoate and abamectin. Furthermore, very low B. nigricans demographic growth indices were estimated for these two insecticides, indicating potential local extinction of the wasp populations. Among the tested products, Bt proved to be the safest for B. nigricans adults and pupae. Our findings emphasize that acute toxicity assessment alone cannot fully predict the actual impact of pesticides on non-target parasitoids. Thus, sublethal effects related to the species specific life-history variables must be carefully considered in order to assess pesticide risks and to incorporate new pesticides, including biopesticides, into IPM programmes.

Pesticide-Induced Stress in Arthropod Pests for Optimized Integrated Pest Management Programs

More than six decades after the onset of wide-scale commercial use of synthetic pesticides and more than fifty years after Rachel Carsons Silent Spring, pesticides, particularly insecticides, arguably remain the most influential pest management tool around the globe. Nevertheless, pesticide use is still a controversial issue and is at the regulatory forefront in most countries. The older generation of insecticide groups has been largely replaced by a plethora of novel molecules that exhibit improved human and environmental safety profiles. However, the use of such compounds is guided by their short-term efficacy; the indirect and subtler effects on their target species, namely arthropod pest species, have been neglected. Curiously, comprehensive risk assessments have increasingly explored effects on nontarget species, contrasting with the majority of efforts focused on the target arthropod pest species. The present review mitigates this shortcoming by hierarchically exploring within an ecotoxicology framework applied to integrated pest management the myriad effects of insecticide use on arthropod pest species.

Incorporating Ecologically Relevant Measures of Pesticide Effect for Estimating the Compatibility of Pesticides and Biocontrol Agents

Abstract The compatibility of biological control agents with pesticides is a central concern in integrated pest management programs. The most common assessments of compatibility consist of simple comparisons of acute toxicity among pest species and select biocontrol agents. A more sophisticated approach, developed by the International Organisation of Biological Control (IOBC), is based on a tiered hierarchy made up of threshold values for mortality and sublethal effects that is used to determine the compatibility of pesticides and biological control agents. However, this method is unable to capture longer term population dynamics, which is often critical to the success of biological control and pest suppression. In this article, we used the delay in population growth index, a measure of population recovery, to investigate the potential impacts that the threshold values for levels of lethal and sublethal effects developed by the IOBC had on three biocontrol agents: sevenspotted lady beetle, Coccinella septempunctata L.; the aphid parasitoid Diaeretiella rapae (M’Intosh), and Fopius arisanus (Sonan), a parasitoid of tephritid flies. Based on life histories of these economically important natural enemies, we established a delay of 1-generation time interval as sufficient to disrupt biological control success. We found that delays equivalent to 1-generation time interval were caused by mortality as low as 50% or reductions of offspring as low as 58%, both values in line with thresholds developed by the IOBC. However, combinations of mortality and reduction of offspring lower than these values (from 32 to 43% each) over a simulated 4-mo period caused significant population delays. Furthermore, the species used in these simulations reacted differently to the same levels of effect. The parasitoid D. rapae was the most susceptible species, followed by F. arisanus and C. septempunctata. Our results indicate that it is not possible to generalize about potential long-term impacts of pesticides on biocontrol agents because susceptibility is influenced by differences in life history variables. Additionally, populations of biocontrol agents may undergo significant damage when mortality approaches 50% or when there is mortality of ≈30% and a 30% reduction in offspring caused by a sublethal effect. Our results suggest that more ecologically relevant measures of effect such as delays in population growth may advance our knowledge of pesticide impacts on populations of beneficial species.

Conclusions of the Worldwide Integrated Assessment on the risks of neonicotinoids and fipronil to biodiversity and ecosystem functioning

The side effects of the current global use of pesticides on wildlife, particularly at higher levels of biological organization: populations, communities and ecosystems, are poorly understood (Kohler and Triebskorn 2013). Here, we focus on one of the problematic groups of agrochemicals, the systemic insecticides fipronil and those of the neonicotinoid family. The increasing global reliance on the partly prophylactic use of these persistent and potent neurotoxic systemic insecticides has raised concerns about their impacts on biodiversity, ecosystem functioning and ecosystem services provided by a wide range of affected species and environments. The present scale of use, combined with the properties of these compounds, has resulted in widespread contamination of agricultural soils, freshwater resources, wetlands, non-target vegetation and estuarine and coastal marine systems, which means that many organisms inhabiting these habitats are being repeatedly and chronically expose...

Toxicity of Spinosad in Protein Bait to Three Economically Important Tephritid Fruit Fly Species (Diptera: Tephritidae) and Their Parasitoids (Hymenoptera: Braconidae)

Abstract The feeding toxicity of the natural insecticide spinosad in Provesta protein bait was evaluated for three economically important fruit fly species, the Mediterranean fruit fly, Ceratitis capitata (Wiedemann); the melon fly, Bactrocera cucurbitae Coquillett; and the oriental fruit fly, Bactrocera dorsalis Hendel. Both females and males were evaluated. Spinosad was remarkably similar in toxicity to all three fruit fly species. Male C. capitata (24 h LC50 values and 95% fiducial limits = 2.8 [2.60–3.0] mg/liter spinosad) were significantly, although only slightly more susceptible to spinosad than females (4.2 [3.8–4.6] mg/liter). Male (5.5 [4.7–6.6] mg/liter) and female (4.3 [3.7–4.9] mg/liter) B. cucurbitae were equally susceptible to spinosad. Female (3.3 [3.1–3.6] mg/liter) and male (3.1 [2.9–3.3] mg/liter) B. dorsalis also were equally susceptible to spinosad. Provesta bait containing spinosad also was evaluated against two parasitoids of tephritid fruit flies, Fopius arisanus (Sonan) and Pysttalia fletcheri (Silvestri). These parasitoids did not feed on the bait, so a contact toxicity test was conducted. Significant amounts of mortality were found only after exposure of parasitoids to spinosad-coated glass vials with concentrations ≥500 mg/liter spinosad. Parasitoids were less susceptible than fruit flies to such a degree that use of spinosad in bait spray should be compatible with these parasitoid species. Because the fruit flies tested in this study were so susceptible to spinosad, this product seems to be promising as a bait spray additive and a replacement for malathion for control of these species.

Comparative Demography of Three Hawaiian Fruit Flies (Diptera: Tephritidae) at Alternating Temperatures

Abstract Reproductive and population parameters of melon flies, Bactrocera cucurbitae Coquillett, oriental fruit flies, B. dorsalis Hendel, and Mediterranean fruit flies, Ceratitis capitata (Wiedemann), were measured in environmental chambers maintained at temperatures of (maximum:minimum) 24:13, 24:24, 29:18, and 35:24 ± 1°C. Alternating temperature regimes more realistically approached the variation found in nature and produced higher parameters than an optimal constant temperature (24°C). Intra- and interspecific comparisons were done with 4 separate generations of wild fruit flies reared on a common natural host. All species attained their highest intrinsic rates of population increase at 29:18 or 35:24°C; C. capitata exhibited the highest intrinsic rates of increase at all temperature regimes. All species attained maximum net reproductive rates at 29:18°C, in the order C. capitata > B. dorsalis > B. cucurbitae. The 35:24°C regime caused reductions in net reproductive rates of all species, with B. dorsalis affected most strongly. Male longevity was greater than that of females for all species in all temperature regimes. Two distinctly different life history patterns were evident: (1) early reproduction, short life span, and a high intrinsic rate of increase (C. capitata), and (2) later onset of reproduction, longer life span, and a lower intrinsic rate of increase (B. cucurbitae).

Methyl eugenol and cue-lure traps for suppression of male oriental fruit flies and melon flies (Diptera: Tephritidae) in Hawaii: effects of lure mixtures and weathering.

Abstract Methyl eugenol (4-allyl-1,2-dimethoxybenzene-carboxylate) and cue-lure [4-(p-acetoxyphenyl)-2-butanone] are highly attractive kairomone lures to oriental fruit fly, Bactrocera dorsalis (Hendel), and melon fly, B. cucurbitae (Coquillett), respectively. Plastic bucket traps were evaluated as dispensers for methyl eugenol and cue-lure for suppression of the 2 fruit flies in Hawaii. Methyl eugenol and cue-lure mixtures were compared with pure methyl eugenol or cue-lure over 4 seasons. B. dorsalis captures differed significantly with treatment and season. B. dorsalis captures with 100% methyl-eugenol were significantly greater than all other treatments (25, 50, and 75%). B. cucurbitae captures also differed significantly with treatment but not with season. Captures with 100, 75, and 50% cue-lure were not significantly different. Bucket traps baited with cue-lure (+ malathion) and weathered under Hawaiian climatic conditions were attractive to B. cucurbitae up to 8 wk. Two methyl eugenol dispensers (canec disks and Min-U-Gel) were compared with bucket traps. Dispensers (methyl eugenol + malathion) were weathered for 2–16 wk under Hawaiian climatic conditions and bioassayed during summer and winter. Initially, captures of B. dorsalis were not significantly different for the 3 dispensers. Bucket traps and canec disks were most resistant to weather, remaining attractive to B. dorsalis flies up to 16 wk. Min-U-Gel was least resistant, losing attractiveness to B. dorsalis flies within 2 wk. On the basis of performance, bucket traps and canec disks were equally long-lived up to 14 wk; thereafter, bucket traps were slightly more attractive during winter. Canec disks were cheapest, but on the basis of possible environmental concerns, bucket traps may be the best all-around choice for areawide suppression of fruit flies.