How lasting are the effects of pesticides on earwigs? A study based on energy metabolism, body weight and morphometry in two generations of Forficula auricularia from apple orchards.

Widespread use of pesticides to control pests is the dominant system in conventional apple orchards. To avoid adverse side effects, there is a growing interest in promoting alternative methods including biological control based on the use of natural enemies. The European earwig Forficula auricularia L. (Dermaptera: Forficuidae) is an effective predator in apple orchards. Pesticide pressure has been shown to divert energy resources which could have a negative impact on life history traits. In this study we assessed (i) whether variations in pesticide exposure could differentially impact energy reserves, body weight and morphometric parameters of F. auricularia, and (ii) whether these effects persist into the next generation reared under optimal conditions. Individuals from the first generation were collected in late October from organic, IPM and conventional orchards. The next generation was obtained under a rearing program, in the absence of pesticide exposure. Earwigs collected from conventional orchards exhibited lower values for all morphometric parameters compared to those collected in organic orchards. However, a relaxed period without pesticide exposure (in autumn) appears to have allowed the females to recover their energy reserves to ensure reproduction and maternal care. Glycogen contents were the reserves that were more easily restored. However, probably due to the rearing conditions (food ad libitum), all the earwigs from the second generation exhibited higher body weights and energy reserves than their parents.

An exploratory study of energy reserves and biometry as potential tools for assessing the effects of pest management strategies on the earwig, Forficula auricularia L.

Apple orchards are heavily treated crops and some sprayed insecticides are recognized to have toxic effects on non-target arthropods. Earwigs are important natural enemies in pip-fruit orchards and contribute to the biological control of aphids. In addition, due to their ease of capture and identification, they are an interesting potential bioindicator of the possible detrimental effects of different orchard management strategies. In this study, we measured the energy reserves and some morphological traits of Forficula auricularia L. sampled in apple orchards under management strategies (organic versus integrated pest management (IPM)). We observed a significant decrease in mass (22 to 27%), inter-eye width (3%), and prothorax width (2 to 5%) in earwigs from IPM compared to organic orchards. Energy body reserves also confirmed these results with a significant decrease of 48% in glycogen and 25 to 42% in lipid content in earwigs from IPM compared to organic orchards. However, the protein content was approximately 70% higher in earwigs from IPM than in organic orchards. Earwigs sampled in IPM orchards may adapt to minimize the adverse toxic effects of pesticide treatments using a large number of strategies, which are reflected in changes to their energy reserves. These strategies could, in turn, influence the population dynamics of natural enemies and impair their role in the biological control of pests in apple orchards.

Does wastewater treatment plant upgrading with activated carbon result in an improvement of fish health?

In the present study, the efficiency of a wastewater treatment plant (WWTP) upgraded with a powdered activated carbon unit for the reduction of micropollutants and the related advantages for fish health have been analyzed by means of different biomarkers, i.e. histopathological investigations, analyses of glycogen content and stress proteins, as well as by chemical analyses in different matrices. Comparative analyses were conducted prior and subsequent to the installation of the additional purification unit. Chemical analyses revealed a significant reduction of several pharmaceuticals, including diclofenac, carbamazepine and metoprolol, in samples of effluent and surface water downstream of the WWTP after its upgrade. In addition, diminished concentrations of diclofenac and PFOS were detected in tissues of analyzed fish. Histopathological investigations of fish liver, gills, and kidney revealed improved tissue integrity in fish after improved wastewater treatment. In parallel, biochemical measurements of glycogen revealed increased energy resources in fish liver and, furthermore, hsp70 levels in livers of exposed rainbow trout and in kidneys of exposed brown trout were lower after than before the WWTP upgrade. In summary, additional treatment with powdered activated carbon led to a reduction of potentially hazardous chemicals in the effluent and the adjacent river and, consequently, to an improvement of fish health in the receiving water course.

Colony adaptive response to simulated heat waves and consequences at the individual level in honeybees (Apis mellifera).

Since climate change is expected to bring more severe and frequent extreme weather events such as heat waves, assessing the physiological and behavioural sensitivity of organisms to temperature becomes a priority. We therefore investigated the responses of honeybees, an important insect pollinator, to simulated heat waves (SHW). Honeybees are known to maintain strict brood thermoregulation, but the consequences at the colony and individual levels remain poorly understood. For the first time, we quantified and modelled colony real-time activity and found a 70% increase in foraging activity with SHW, which was likely due to the recruitment of previously inactive bees. Pollen and nectar foraging was not impacted, but an increase in water foragers was observed at the expense of empty bees. Contrary to individual energetic resources, vitellogenin levels increased with SHW, probably to protect bees against oxidative stress. Finally, though immune functions were not altered, we observed a significant decrease in deformed wing virus loads with SHW. In conclusion, we demonstrated that honeybees could remarkably adapt to heat waves without a cost at the individual level and on resource flow. However, the recruitment of backup foraging forces might be costly by lowering the colony buffering capacity against additional environmental pressures.

Stress response in honeybees is associated with changes in task-related physiology and energetic metabolism.

In a rapidly changing environment, honeybee colonies are increasingly exposed to diverse sources of stress (e.g., new parasites, pesticides, climate warming), which represent a challenge to individual and social homeostasis. However, bee physiological responses to stress remain poorly understood. We therefore exposed bees specialised in different tasks (nurses, guards and foragers) to ancient (immune and heat stress) or historically more recent sources of stress (pesticides), and we determined changes in the expression of genes linked to behavioural maturation (vitellogenin - vg and juvenile hormone esterase - jhe) as well as in energetic metabolism (glycogen level, expression level of the receptor to the adipokinetic hormone - akhr, and endothermic performance). While acute exposure to sublethal doses of two pesticides did not affect vg and jhe expression, immune and heat challenges caused a decrease and increase in both genes, respectively, suggesting that bees had responded to ecologically relevant stressors. Since vg and jhe are expressed to a higher level in nurses than in foragers, it is reasonable to assume that an immune challenge stimulated behavioural maturation to decrease potential contamination risk and that a heat challenge promoted a nurse profile for brood thermoregulation. All behavioural castes responded in the same way. Though endothermic performances did not change upon stress exposure, the akhr level dropped in immune and heat-challenged individuals. Similarly, the abdomen glycogen level tended to decline in immune-challenged bees. Altogether, these results suggest that bee responses are stress specific and adaptive but that they tend to entail a reduction of energetic metabolism that needs to be studied on a longer timescale.

Influence of pollen nutrition on honey bee health: do pollen quality and diversity matter?

Honey bee colonies are highly dependent upon the availability of floral resources from which they get the nutrients (notably pollen) necessary to their development and survival. However, foraging areas are currently affected by the intensification of agriculture and landscape alteration. Bees are therefore confronted to disparities in time and space of floral resource abundance, type and diversity, which might provide inadequate nutrition and endanger colonies. The beneficial influence of pollen availability on bee health is well-established but whether quality and diversity of pollen diets can modify bee health remains largely unknown. We therefore tested the influence of pollen diet quality (different monofloral pollens) and diversity (polyfloral pollen diet) on the physiology of young nurse bees, which have a distinct nutritional physiology (e.g. hypopharyngeal gland development and vitellogenin level), and on the tolerance to the microsporidian parasite Nosemaceranae by measuring bee survival and the activity of different enzymes potentially involved in bee health and defense response (glutathione-S-transferase (detoxification), phenoloxidase (immunity) and alkaline phosphatase (metabolism)). We found that both nurse bee physiology and the tolerance to the parasite were affected by pollen quality. Pollen diet diversity had no effect on the nurse bee physiology and the survival of healthy bees. However, when parasitized, bees fed with the polyfloral blend lived longer than bees fed with monofloral pollens, excepted for the protein-richest monofloral pollen. Furthermore, the survival was positively correlated to alkaline phosphatase activity in healthy bees and to phenoloxydase activities in infected bees. Our results support the idea that both the quality and diversity (in a specific context) of pollen can shape bee physiology and might help to better understand the influence of agriculture and land-use intensification on bee nutrition and health.

In vivo distribution and metabolisation of 14C-imidacloprid in different compartments of Apis mellifera L.

In vivo distribution of the neonicotinoid insecticide, imidacloprid, was followed during 72 h in six biological compartments of Apis mellifera L: head, thorax, abdomen, haemolymph, midgut and rectum. Honeybees were treated orally with 100 microg of 14C-imidacloprid per kg of bee, a dose close to the median lethal dose. Elimination half-life of total radioactivity in honeybee was 25 h. Haemolymph was the compartment with the lowest and rectum that with the highest level of total radioactivity during the whole study, with a maximum 24h after treatment. Elimination half-life of imidacloprid in whole honeybee was 5 h. Imidacloprid was readily distributed and metabolised only by Phase I enzymes into five metabolites: 4/5-hydroxy-imidacloprid, 4,5-dihydroxy-imidacloprid, 6-chloronicotinic acid, and olefin and urea derivatives. The guanidine derivative was not detected. The urea derivative and 6-chloronicotinic acid were the main metabolites and appeared particularly in midgut and rectum. The olefin derivative and 4/5-hydroxy-imidacloprid preferentially occurred in head, thorax and abdomen, which are nicotinic acetylcholine receptor-rich tissues. Moreover, they presented a peak value around 4 h after imidacloprid ingestion. These results explain the prolongation of imidacloprid action in bees, and particularly the differences between rapid intoxication symptoms and late mortality.

Metabolism of imidacloprid in Apis mellifera.

Biotransformation of imidacloprid and the appearance of olefin and 5-hydroxyimidacloprid metabolites in the honeybee were studied by HPLC-MS/MS analysis. Honeybees were treated orally with imidacloprid at 20 and 50 microg kg(-1) bee. Imidacloprid was metabolised relatively quickly and thoroughly. Twenty minutes after the beginning of imidacloprid ingestion, the sum of the residues from the three compounds amounted to only 70% of the actual given dose. Imidacloprid, 5-hydroxyimidacloprid and olefin represented, respectively, 50%, 9% and 8% of the actual ingested dose. Six and 24 h, respectively, after ingestion of imidacloprid at 20 and 50 microg kg(-1) bee, imidacloprid could no longer be detected in the honeybee. Imidacloprid had a half-life ranging between 4.5 and 5 h and was rapidly metabolised into 5-hydroxyimidacloprid and olefin. Except 5-hydroxyimidacloprid in the 20 microg kg(-1) treatment, these two metabolites presented a peak value 4 h after ingestion of the 20 and 50 microg kg(-1) doses. This time fully coincided with the appearance of mortality induced by imidacloprid after acute oral intoxication. These results suggested that the immediate neurotoxicity symptoms are due to the action of imidacloprid, whereas 5-hydroxyimidacloprid and/or olefin are involved in honeybee mortality. In addition, it was likely that the 30% of residues undetected 20 min after intoxication were imidacloprid metabolites, although not 5-hydroxyimidacloprid or olefin. Thus, 5-hydroxyimidacloprid and olefin could not be the major metabolites in the worker bees.