Direct contact toxicity of technical grade insecticides after 48 h to bumble bees [10]
1. Introduction
Bumblebees are important pollinators of many crops and wild flowers and there are both conservation and economic reasons for taking action to assess the impact of pesticides on bumblebees. Pesticide risk assessments for honeybees are based on hazard ratios which rely on application rates and toxicity data and are unlikely to be appropriate for bumblebees. Bumblebees are active at different times and on different crop species and are, therefore, likely to have different exposure profiles. Unlike honeybees, deaths of bumblebees due to pesticides are unlikely to be reported, since the bees are not kept domestically and will die in small numbers. During the last decades side-effects of insecticides on bees have gained great attention due to their value as pollinators. In Europe insecticides are tested following the EPPO (European and Mediterranean Plant Protection Organization) guidelines to exclude any harm to honeybees
Mechanisms of insecticide resistance found in insects may include three general categories. Modified behavioral mechanisms can let the insects avoid the exposure to toxic compounds. The second category is physiological mechanisms such as altered penetration, rapid excretion, lower rate transportation, or increase storage of insecticides by insects. The third category relies on biochemical mechanisms including the insensivity of target sites to insecticides and enhanced detoxification rate by several detoxifying mechanisms [1]. The representative detoxifying enzymes are general esterases and monooxygenases that catalyse the toxic compounds to be more water-soluble forms and the secondary metabolism is followed by conjugation reactions including those catalysed by glutathion S-transferases.
Insecticide resistance is the development by some insects in a population of an ability to survive doses of a toxicant which would prove lethal to the majority of individuals in a normal population of the same species [2]. Insecticide resistance has serious consequences, such as outright control failure, increased application rates, decreased yields, environmental contamination and wildlife and natural enemy destruction [3].
2. Effect of insecticides
Insecticides affect insect behavior, such as reducing movements and affecting feeding levels. To date risks assessment studies conducting the side-effects of conventional insecticides are mostly limited to acute toxicity studies. Overall, when considering conventional insecticides it is remarkable that several litle of all compounds included (n=63) was considered as non-toxic (Figure 1)
Cases where insecticides have altered insect behavior have only been reported for imidacloprid (systemic neonicotinoid and insect neurotoxin). Perhaps imidacloprid has been the most investigated insecticide because for a long time it was considered to be relatively safe to non-target organisms, and thus was desired as a companion to biological control systems in integrated pest management systems. They may not only affect pest insects but also non-target organisms such as pollinators. Three different key aspects determining the risks of neonicotinoid concentrations for bee populations: (1) the environmental neonicotinoid residue levels in plants, bees and bee products in relation to pesticide application, (2) the reported side-effects with special attention for sublethal effects, and (3) the usefulness for the evaluation of neonicotinoids of an already existing risk assessment scheme for systemic compounds [5].
Imidacloprid probably migrate into nectar and pollen, then modify flower attractiveness, homing behavior, and colony development [6]. It was concluded that applying imidacloprid at the registered dose did not significantly affect the foraging and homing behavior of
The imidacloprid was exposed adult worker bumble bees,
Neonicotinoid insecticides have been implicated in these declines because they occur at trace levels in the nectar and pollen of crop plants [8]. Colonies of the bumble bee
The insecticide Teppeki can be selective about bumble and have a good compatibility with the activity of the apiaries [11]. This insecticide has the active ingredient flonicamid belonging to a new chemical class, called pyridinecarboxamides: the product has systemic effect and is known as having a long lasting efficacy against all important aphid species The flonicamid has a minor effect of interference with the activity of pollination by
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Clothianidin | 0.39 | act on the central nervous system of insects as an agonist of acetylcholine |
Imidacloprid | 3.22 | central nervous system, acetylcholine agonist |
Deltamethrin | 6.90 | due to irreversible damage to the nervous systém of insect |
Spinosad | 8.95a | binding sites on nicotinic acetylcholine receptors (nAChRs) of the insect nervous system, binding leads to disruption of acetylcholine neurotransmission |
Novaluron | >100 |
insect growth regulator that disrupts cuticle formation and prevents molting |
As has been already shown pesticide risk assessments are routinely carried out for honeybees, but the results of these are probably not directly applicable to bumblebees [12]. Pyrethroids are commonly applied to flowering oilseed rape in the early morning or evening, when bumblebees are often active. Laboratory and field-based bioassays appropriate to bumblebees have been developed in response to the growing use of bumblebees for the pollination of greenhouse crops, but these are not widely used and few toxicological data are available [12]. Almost all tests conducted so far have been on
Despite risk assessments, widespread poisoning of honeybees has been reported [15]. Such effects are obvious in domestic hives where dead bees are ejected and form piles by the nest. It seems probable that pesticides would have similar effects on bumblebees but they are unlikely to be noticed in most situations. In Canada, the use of the insecticide fenitrothion in forests led to a decline in yield of nearby
A growing appreciation of the damaging effects of broad-spectrum pesticides has led to the development of a new generation of more target-specific compounds. EU, US and Canadian law now demand that oral and acute toxicity tests are carried out on honeybees prior to the registration of any new pesticide [17]. However, there is no obligation to study sub-lethal effects on any bees, or to look at specific effects on bumblebees. Some of these substances cause no mortality in bumblebees if used appropriately [18,19]), but there is evidence that supplementary trials for non-lethal effects are necessary.
The spinosad is a commonly used insect neurotoxin which, based on studies of honeybees, has been deemed harmless to bees. However, it has recently been shown that bumblebee larvae fed with pollen containing this pesticide give rise to workers with reduced foraging efficiency [20]. Mommaerts et al. [21] screened eight chitin synthesis inhibitors currently registered as pesticides and found that although no lethal effect could be found on adults, the use of these pesticides has strong effects on colony growth and the development of larvae. Diflubenzuron and teflubenzuron were found to be the most harmful to bumblebees, greatly reducing reproductive output at concentrations far below the recommended field concentrations.
The effects of a naturally derived biopesticide, spinosad, was tested on bumble bee (
The toxicity of this Pyridalyl an insecticide of a novel chemical class (unclassified insecticides) to the pollinating insect
Gradish et al., determined the lethal and sub-lethal effects of four insecticides (imidacloprid, abamectin, metaflumizone and chlorantraniliprole) tested for use in greenhouse vegetable production to
The potential side effects of the novel insecticide spinetoram in comparison with spinosad on the bumblebee
Upon topical treatment, nitro-containing neonicotinoids (imidacloprid, clothianidin, thiamethoxam, nitenpyram and dinotefuran) were more toxic than the cyano-group containing ones (acetamiprid and thiacloprid) [25,26]. A similar high toxicity of imidacloprid and thiamethoxam was also found for the bumble bee
3. The effect of insecticides on insect immunity
Individual immune defences in the bee parallel the innate immune systems of vertebrates [33], Figure 2. Insect immunity is basically composed of three parts: (1) the cuticle, which presents physical and chemical barriers to the outside world of microbes, (2) humoral responses, and (3) cellular responses. The primary defences are the cuticle, the spiracles and trachea and the alimentary canal including the intestinal epithelium and peritrophic membrane [34-36] If these are breached cellular immune defences include the cellular response represented by phagocytosis by haemocytes and melanisation.Insecticides affect the insect humoral and cellular immune responses. In the initial humoral response, pattern recognition proteins identify invading microbes and initiate the synthesis of various ofantimicrobial proteins [37], (Figure 2). Phagocytosis is typically accompanied by melanin production and melanization of nodules and capsules (Figure 1). Melanin production can occur morerapidly than the production of antimicrobial peptides, can lead to the formation of reactive oxidative species that can contribute to killing pathogens and are regulated through the phenoloxidase cascade [38], (Figure 2). The humoral and cellular responses are interdependent defensive forces involving detoxificationmechanisms that are also utilized by insects to prevent damage from environmental toxins. The humoral response is represented by secretion of antimicrobial peptides (AMPs, inducible antibioticpeptides such as apidaecins) [39,40] from within the fat body due to the activation of one or several intracellular signalling pathways (Toll, Imd and Jak-Stat) which degrade pathogens as well as the action of reactive oxygen and nitrogen species (Figure 2).
To date risks assessment studies conducting the side-effects of conventional insecticides are mostly limited to acute toxicity studies. A summary of the effects of the insecticides including the organochlorides, organophosphates, carbamates, pyrethroids, organophosphates and neonicotinoids on insect is given in Table 2.
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Organochlorides | - neurotoxin, disrupt the nervous system |
Organophosphates | - neurotoxin, interfere with the enzymes acetylcholinesterase and other cholinesterases, disrupting nerve impulses, killing or disabling the insect - have an accumulative toxic effect to wildlife, so multiple exposures to the chemicals amplifies the toxicity - kill insects by inhibiting the enzyme cholinesterase, which is essential in the functioning of the nervous system |
Carbamates | - have similar toxic mechanisms to organophosphates, but have a much shorter duration of action and are thus somewhat less toxic - are rapidly detoxified and eliminated from animal tissues - toxicity is thought to arise from a mechanism somewhat similar to that for the organophosphates. |
Pyrethroids | - are nonpersistent sodium channel modulators, and are much less acutely toxic than organophosphates and carbamates. |
Neonicotinoids | - broad spectrum systemic insecticides are nicotinic acetylcholine receptor agonists - have a rapid action (minutes-hours). - treated insects exhibit leg tremors, rapid wing motion, stylet withdrawal (aphids), disoriented movement, paralysis and death |
4. Detoxifying enzymes
Pesticide resistance in arthropods has been shown to evolve by two main mechanisms at the molecular level either (1) the increased production of metabolic enzymes (esterases, glutathione
Although acetylcholinesterase (AChE) is a specific target enzyme for organophosphate and carbamate poisoning (specific protein binding), other pesticides or their metabolites can inhibit AChE activity by unspecific protein binding (e.g., interaction with serine groups outside of the catalytic subunit). The latter interaction would also result in a reduction of AChE activity.
4.1. Glutathione-S-transferases
Glutathione-S-transferases (EC 2.5.1.18) constitute a family of enzymes that participe in 1) detoxification of xenobiotics, 2) protection from oxidative damage, and 3) intracellular transport of hormones, endogenous metabolites and exogenous chemicals. It is involved in insecticide resistance. Glutathione S-transferases (GSTs) are present in almost all animals and in most of them in multiple isoenzymic forms, constituting a significant intracellular mechanism of detoxification. The enzymes catalyse the conjugation of a large variety of compounds bearing an electrophilic site, with reduced glutathione (GSH) [54]. In insects, they represent a very interesting detoxification mechanism due to their involvement in tolerance to insecticides [55-58]. GSTs of different sub-families and classes are universally present in all forms of life, from invertebrates to vertebrates, plants and microorganisms. They have been identified and characterized in such diverse species as
Increased levels of GSTs have been associated with resistence to a wide variety of insecticides, maily organophosphates, organochlorides and cyclodienes [68]. Other insecticide classes, such as pyrethroids and carbamates, are probably not detoxified by GSTs [69]. Induction of GST activity has been reported in many insects following treatment with insecticides [70,71]. The activity of insect GSTs has been found to be present in the midgut [72], fat body [73], hemolymph cells and other but more precise sites of GSTs need to be determined. The multiple isoenzymic forms of GST are distinguished by differences in structure and catalytic properties. The expression of isoenzymes depends on many internal and external factors. Age-dependent alteration of GST activities has been demonstrated in both vertebrates and invertebrates [74-76]. Alteration of GST expression induced by various substances in insets has also been reported (e.g.,food quality and administration of certain insecticides) [77-80]. Significant alterations in the isoenzymic profile, leading to the suggestion that the multiple GST isoenzymes present in insects are regulated independently, have also been reported as a result of stress, caused by a variety of factors [78,81]. The role of other enzymatic systems (such as esterases and monooxygenases) is emphasized by many investigators as even more important than GSTs in insecticide metabolism by insects [82].
Kim at all. [83] show the expression profiles of
In line with the mammalian GST classification, insect GSTs have been classified into six classes: delta, epsilon, omega, theta, sigma, and zeta [84-86]. Due to the important role of GSTs, most studies of GSTs in insects have focused on their role in detoxifying exogenous compounds, in particular insecticides and plant allelochemicals [87-92]. In addition, insect GSTs have been studied for their role in mediating oxidative stress responses.
4.2. Esterases
The esterase family of enzymes hydrolyse ester bonds, which are present in a wide range of insecticides; therefore, these enzymes may be involved in resistance to the main chemicals employed in control programs. Acetylcholinesterase (AChE) is a specific target enzyme for organophosphate and carbamate poisoning (specific protein binding), other pesticides or their metabolites can inhibit AChE activity by unspecific protein binding (e.g., interaction with serine groups outside of the catalytic subunit). The latter interaction would also result in a reduction of AChE activity. AChE has been shown in aphid
4.3. Cytochrome P450 monooxygenases
Cytochrome P450 monooxygenases (P450s) are enzymes important in insects both for the detoxification of xenobiotics, such as pesticides and phytochemicals, and the biosynthesis of endogenous compounds, such as hormones and pheromones. The monooxygenases of insect have several functional roles, including growth, development, feeding and protection against xenobiotics, including resistance to pesticides and tolerance to plant toxins [103].
Monooxygenases are involved in the synthesis and degradation of insect hormones and pheromones. They catalyse many types of reactions including oxygenations, dehalogenations, dealkylations, deaminations, dehydrogenations and isomerations [104]. The enzyme reactions are based on activation of molecular oxygen within sertion of one of its atoms into the substrate and reduction of the other to form water [105]. The genome of every insect species may carry a hundred or so different P450 genes, all evolved from a common ancestral gene. The P450 family is thus one of the oldest and largest gene superfamilies. They do many things: P450 enzymes are found in the biosynthetic pathways of ecdysteroids and juvenile hormones, which are at the center stage of insect growth, development, and reproduction. P450 enzymes metabolize insecticides, resulting either in bioactivation or, more often, in detoxification, the latter process being enhanced in many strains with metabolic resistance to insecticides. Furthermore, P450 metabolism of certain plant chemicals is often the key to the adaptation of insect herbivores to their host plants. P450 enzymes play important roles in the synthesis or degradation of odorants, pheromones, or defensive chemicals. Insect P450 genes are expressed in many tissues; not surprisingly, the digestive tract and fat body are a rich source of P450–dependent metabolism of model substrates. Developmental regulation of P450 gene expression is well documented by biochemical means [106]. It is well established that many cases of metabolic resistance to insecticides are the result of elevated levels of P450 [92]. In vivo suppression or decrease in resistance by application of P450 inhibitors such as the synergist piperonyl butoxide is often used as a diagnostic for P450 involvement. In vitro demonstration of increased P450–dependent metabolism of the insecticide is done more infrequently. Because of the multiplicity of P450 genes, correlations between resistance and activity of P450 enzymes measured by model substrates, though indicative, are seldom demonstrative. The cytochrome P450-dependent monooxygenases are an extremely important metabolic system involved in the metabolism of xenobiotics and endogenous compounds. The number of P450s in a given insect species currently ranges from 48 in
Cytochrome P450 is a hemoprotein which acts as the terminal oxidase in monooxygenase systems. In eukaryotes, most P450s are found in the endoplasmic reticulum or mitochondria. Monooxygenases can oxidize widely diverse substrates and are capable of catalyzing a large array of reactions [107]. This is because each species contains numerous P450s and because of the broad substrate specificity of some isoforms. Insect monooxygenases can be detected in a wide range of tissues. Highest monooxygenase activities are usually associated with the midgut, fat bodies and Malpighian tubules [108], but again the expression of individual P450s can vary between these tissues [95]. In general, total P450 levels are undetectable in eggs, rise and fall in each larval instar, are undetectable in pupae and are expressed at high levels in adults [106]. The patterns of expression of individual P450s can vary within and/or between life stages [107-110].
5. Conclusion
Bumblebees are of crucial importance for the pollination of wild flowers and economical important crops in modern agri/horticulture. These pollinators as
Over the last three decades, bumble bee populations have experienced global population declines due to environmental factors such as pathogens, pesticide exposure and habitat fragmentation. Given the importance of bumble bees as pollinators of crops and wild flowers, steps must be taken to prevent further declines.
Acknowledgments
Authors thank the research programme of the Institute of Organic Chemistry and Biochemistry RVO: 61388963 the Czech Science Foundation (grant No. 203/09/1446) and Technology Agency of the Czech Republic (grant No. TA01020969)
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