Neonicotinoid insecticides limit the potential of spiders to re-colonize disturbed agroecosystems when using silk-mediated dispersal

Abstract

Agroecosystems are subject to regular disturbances that cause extinction or migration of much of their fauna, followed by recolonization from surrounding refuges. In small-sized aeronaut spiders, such recolonization is potentiated by their ability to rappel and balloon. These are complex behaviors that we hypothesized to be affected by neurotoxins, namely, neonicotinoids. We tested this hypothesis using two common farmland spider species, Oedothorax apicatus (Linyphiidae) and Phylloneta impressa (Theridiidae). The spiders were topically exposed by dorsal wet application or tarsal dry exposure to commercial neonicotinoid formulations Actara 25 WG, Biscaya 240 OD, Mospilan 20 SP and Confidor 200 OD at concentrations that are recommended for application in agriculture. Contact exposure to neonicotinoids suppressed the ability of spiders to produce the major ampullate fiber and anchor it to the substratum by piriform fibrils. Contact exposure to neonicotinoids also suppressed the ballooning behavior that was manifested by climbing to elevated places, adopting a tiptoe position and producing silk gossamer in the wind. Impaired ability of affected common farmland spiders to quickly recolonize disturbed agroecosystems by silk-mediated dispersal may explain their decline in multiple farmland ecosystems, in which neonicotinoids are applied.

The sublethal effects of neonicotinoids on spiders are independent of their nutritional status

“…We recorded the length (distance) that the spiders descended toward the bottom of the apparatus while being secured by the dragline, which also required the dragline to be successfully anchored to the substratum. The rappelling stimulation lasted 15 min or until the rappelling was completed 20 .…”

“…The conditions to stimulate ballooning lasted 15 min or until ballooning was performed. We recorded any ballooning displayed during the 15-min evaluation period as a positive test result 20 .…”

“…Predators, especially invertebrates such as spiders, have repeatedly been shown to have food-limited population sizes in nature 10 – 12 ; as a result, they have evolved physiological adaptations to allow them to adjust their metabolism to food availability 13 – 17 . Moreover, recently published data suggest that diet affects various aspects of spider behavior 18 , 19 ; therefore, there is a potential for synergistic, additive or potentiating effects of combined exposure to altered diet and exposure to compounds known to affect spider behavior, such as neonicotinoid insecticides 20 , 21 . In nature, prey may vary widely in nutritional content both within and among species (e.g., 5–30% of lipids and 20–80% of proteins) 22 – 25 .…”

“…Spiders are less affected by neonicotinoids than bees are, owing to differences in the structure of acetylcholine receptors that mediate the action of neonicotinoids in invertebrates 49 . Regardless, neonicotinoids are partially lethal to spiders in field-realistic concentrations, inducing also temporary paralysis, impairing the structure of spider silk and affecting spider chemoreception 20 , 21 , 50 , 51 . Moreover, neonicotinoids deter feeding and therefore negatively affect the food consumption rates and likely the nutritional status of spiders 52 .…”

“…In the present study, we used a model invertebrate predator, the large wolf spider Hogna antelucana (Montgomery, 1904) (Araneae: Lycosidae), which is widely distributed across North America 56 – 58 . Based on previous observations of the effects of a high-fat diet 19 and neonicotinoids 20 on spiders, we hypothesized the existence of synergy between the effects of diet and concurrent exposure to field-realistic concentrations of neonicotinoid insecticides. To address this hypothesis, we fed first-instar H. antelucana with two types of diets and exposed them to field-realistic concentrations of three formulations of neonicotinoids.…”