Sex allocation theory reveals a hidden cost of neonicotinoid exposure in a parasitoid wasp

Whitehorn, Penelope R.; Cook, Nicola; Blackburn, Charlotte V.; Gill, Sophie M.; Green, Jade; Shuker, David M.

doi:10.1098/rspb.2015.0389

Cited by 27 publications

(29 citation statements)

References 38 publications

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“…In our previous research, we demonstrated that exposure to imidacloprid disrupted facultative sex allocation in response to a ‘social’ cue – the presence of co‐foundresses (Whitehorn et al ., ). That initial work showed two important facts about the action of imidacloprid in female N .…”

Section: Discussionmentioning

confidence: 97%

“…the fertilisation or not of eggs), as single foundress female Nasonia laying eggs alone produced the same sex ratios regardless of imidacloprid dose (see Fig. 2a in Whitehorn et al ., ). This means that imidacloprid does not disrupt the ‘fertilisation‐end’ of sex allocation.…”

Section: Discussionmentioning

confidence: 97%

“…In summary, imidacloprid disrupts the use of both host (this paper) and social (Whitehorn et al ., ) LMC cues in Nasonia . Neonicotinoids are important insecticides, but their effects on off‐target insects such as bees (Whitehorn et al ., ; Fischer et al ., ; Kessler et al ., ), butterflies (Gilburn et al ., ), and parasitic wasps is being increasingly recognised.…”

Section: Discussionmentioning

confidence: 99%

“…The fitness ( W ) of a theoretical female producing the optimal sex ratio (

S_{2}^{*}

) was calculated for each treatment according to Whitehorn et al . ():

\begin{matrix} right & center W = [\frac{T S_{2}}{S_{1} + T S_{2}}] [1 - S_{1} + T (1 - S_{2})] [\frac{1 + F}{2}] \\ left + T (1 - S_{2}) [\frac{1 + 3 F}{2}] \end{matrix}

…”

Section: Methodsmentioning

confidence: 99%

“…Recently, we have shown that female N. vitripennis exposed to field-relevant doses of the neonicotinoid insecticide imidacloprid exhibited a reduced ability to allocate sex optimally in the presence of co-foundresses (Whitehorn et al, 2015). Neonicotinoids are neurotoxins that bind to nicotinic acetylcholine receptors (nAChRs), thereby disrupting neurotransmission (Tomizawa & Casida, 2005).…”

Section: Introductionmentioning

confidence: 99%

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Exposure to the neonicotinoid imidacloprid disrupts sex allocation cue use during superparasitism in the parasitoid wasp Nasonia vitripennis

Cook

Green

Shuker

et al. 2016

Ecological Entomology

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Abstract. 1. Neonicotinoid insecticides are potent neurotoxins of significant economic importance. However, it is clear that their use can adversely impact beneficial insects in the environment, even at low, sub-lethal doses.2. It has recently been shown that the neonicotinoid imidacloprid disrupts adaptive sex allocation in the parasitoid wasp Nasonia vitripennis (Walker) by limiting their ability to respond to the presence of other females on oviposition patches. In the present study, that work was extended to explore whether sex allocation when superparasitising -laying eggs on a host that has already been parasitised -is also disrupted by imidacloprid.3. Under superparasitism, sex allocation theory predicts that females should vary their offspring sex ratio in relation to their relative clutch size. It was found that sex allocation under superparasitism in Nasonia is disrupted in a dose-dependent manner, with exposed females producing more daughters.4. Importantly, imidacloprid does not appear to influence the ability of females to estimate the number of eggs already present on a host, suggesting a disassociation between the sex ratio and clutch size cues.5. The present work highlights the fitness costs to beneficial insects of exposure to neonicotinoids, but also provides clues as to how female Nasonia use information when allocating sex.

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Section: Discussionmentioning

confidence: 97%

Section: Discussionmentioning

confidence: 97%

Section: Discussionmentioning

confidence: 99%

“…The fitness ( W ) of a theoretical female producing the optimal sex ratio (

S_{2}^{*}

) was calculated for each treatment according to Whitehorn et al . ():

\begin{matrix} right & center W = [\frac{T S_{2}}{S_{1} + T S_{2}}] [1 - S_{1} + T (1 - S_{2})] [\frac{1 + F}{2}] \\ left + T (1 - S_{2}) [\frac{1 + 3 F}{2}] \end{matrix}

…”

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Exposure to the neonicotinoid imidacloprid disrupts sex allocation cue use during superparasitism in the parasitoid wasp Nasonia vitripennis

Cook

Green

Shuker

et al. 2016

Ecological Entomology

Self Cite

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Chronic Exposure to Environmentally Relevant Concentrations of Imidacloprid Impact Survival and Ecologically Relevant Behaviors of Fathead Minnow Larvae

Jeninga,

Wallace,

Victoria

et al. 2023

Enviro Toxic and Chemistry

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Imidacloprid (IM) has emerged as a contaminant of concern in several areas within the United States due to its frequent detection in aquatic ecosystems and its pseudo‐persistence, which pose potential risks to nontarget species. We evaluated the sublethal toxicity of IM to fathead minnow larvae following chronic exposure beginning just after fertilization. Our in silico analysis and in vivo bioassays suggest that IM has a low binding affinity for the vertebrate nicotinate acetylcholine receptor (nAChR), as expected. However, chronic exposure to ≥0.16 µg IM/L reduced survival by 10%, and exposure to ≥18 µg IM/L reduced survival by approximately 20%–40%. Surviving fish exposed to ≥0.16 µg IM/L showed reduced growth, altered embryonic motor activity, and premature hatching. Furthermore, a significant proportion of fish exposed to ≥0.16 µg IM/L were slower to respond to vibrational stimuli and slower to swim away, indicating that chronic exposure to IM has the potential to impair the ability of larvae to escape predation. The adverse health effects we observed indicate that chronic exposure to environmentally relevant concentrations of IM may elicit sublethal responses that culminate in a significant increase in mortality during early life stages, ultimately translating to reduced recruitment in wild fish populations. Environ Toxicol Chem 2023;00:1–9. © 2023 SETAC

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Sublethal Effects of Four Insecticides Targeting Cholinergic Neurons on Partner and Host Finding in the Parasitic Wasp Nasonia vitripennis

Schöfer,

Ackermann,

Hoheneder

et al. 2023

Enviro Toxic and Chemistry

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Lethal and sublethal effects of pesticides on non‐target organisms are one of the causes of the current decline of many insect species. However, research in the past decades has focused primarily on pollinators, although other beneficial non‐target organisms such as parasitic wasps may also be affected. We studied the sublethal effects of the four insecticides acetamiprid, dimethoate, flupyradifurone, and sulfoxaflor on pheromone‐mediated sexual communication and olfactory host finding of the parasitic wasp Nasonia vitripennis. All agents target cholinergic neurons, which are involved in the processing of chemical information by insects. We applied insecticide doses topically and tested the response of treated wasps to sex pheromones and host‐associated chemical cues. Additionally, we investigated the mating rate of insecticide‐treated wasps. The pheromone response of females surviving insecticide treatment was disrupted by acetamiprid (≥0.63 ng), dimethoate (≥0.105 ng) and flupyradifurone (≥21ng), while sulfoxaflor had no significant effects at the tested doses. Olfactory host finding was affected by all insecticides (acetamiprid: ≥1.05 ng, dimethoate: ≥0.105 ng, flupyradifurone: ≥5.25 ng, sulfoxaflor: ≥0.52 ng). Remarkably, females treated with ≥0.21 ng dimethoate even avoided host odor. The mating rate of treated N. vitripennis couples was decreased by acetamiprid (6.3 ng), flupyradifurone (≥2.63 ng) and sulfoxaflor (2.63 ng) while dimethoate showed only minor effects. Finally, we determined the amount of artificial nectar consumed by N. vitripennis females within 48 hours. Considering this amount (approximately 2 µl) and the maximum concentrations of the insecticides reported in nectar, tested doses can be considered field realistic. Our results suggest that exposure of parasitic wasps to field‐realistic doses of insecticides targeting the cholinergic system reduces their effectiveness as natural enemies by impairing the olfactory sense.

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Sex allocation theory reveals a hidden cost of neonicotinoid exposure in a parasitoid wasp

Cited by 27 publications

References 38 publications

Exposure to the neonicotinoid imidacloprid disrupts sex allocation cue use during superparasitism in the parasitoid wasp Nasonia vitripennis

Exposure to the neonicotinoid imidacloprid disrupts sex allocation cue use during superparasitism in the parasitoid wasp Nasonia vitripennis

Chronic Exposure to Environmentally Relevant Concentrations of Imidacloprid Impact Survival and Ecologically Relevant Behaviors of Fathead Minnow Larvae

Sublethal Effects of Four Insecticides Targeting Cholinergic Neurons on Partner and Host Finding in the Parasitic Wasp Nasonia vitripennis

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