Effects of insect growth regulators on honey bees and non-Apis bees. A review

The insect growth regulators (IGRs) are ecdysone or juvenile hormone mimics, or chitin synthesis inhibitors. They are more likely to be hazardous to larval insects than to adults. Application of JH mimics to adult honey bees may affect foraging behaviour and some physiological traits. Topical and feeding tests revealed that application of IGRs to larvae may result in death and larval ejection by workers, malformed larvae and pupae with typical rimmed eyes, or malformed adults. Several laboratory “larvae tests” using artificially contaminated diets have been described for honey bees and bumble bees. Field and cage methods have also been published for honey bees and bumble bees respectively. Diflubenzuron was generally safe for honey bee brood in fields treated at 35 to 400 g.ha–1 a.i. and harmful to bumble bees at 300 g.ha–1 a.i. Fenoxycarb was safe for bumble bees at 1200 g.ha–1 a.i. and hazardous to honey bees causing damage to honey bee brood at 140 g.ha–1. insect growth regulator / honey bee / non-Apis bee / toxicity / risk assessment characters are maintained by the juvenile hormones (JH) which are secreted by corpora allata. The JH are hormones of isoprenoid nature which prevent the breakdown of the thoracic gland (Wigglesworth, 1972). Pupal moulting is determined by a circulating hormone: the moulting hormone, secreted by the prothoracic glands which are activated by neurosecretory cells. This hormone triggers changes in the epidermis and deposition of the new cuticle. The purified form, of steroid nature is called ecdysone. Similar substances can be isolated from many plants. IGRs are commercial hormones mimics that influence moulting as hormones do, acting at the cellular level in various ways depending on their chemical constitution: tebufenozide influences moulting as ecdysone does, while pyriproxyfen and fenoxycarb are JH mimics. A third class is that of chitin inhibitors such as diflubenzuron, flufenoxuron, hexaflumuron, and lufenuron. In addition, a natural substance from neem tree, Azadirachta indica, proved to be a potent IGR (Rembold et al., 1980). According to Engels (1990) IGRs cause little or no damage to adult honey bees and generally the typical effects of these compounds can be seen after the moult of the exposed stage. All natural or synthetic compounds with IGR properties may be suspected of being hazardous to the brood of Apis or non-Apis bees since their larvae can be exposed to insecticides by an oral route. Davis (1989) contributed to the understanding of the oral pathway of insecticides, mediated by adult nurse honey bees which regurgitate honey sac content to feed larvae. In solitary bees, George and Rincker (1985), Tasei and Carré (1987), and Tasei et al. (1988), showed that Megachile rotundata Fabr. females provisioning their nest with pollen and nectar can also transfer insecticides to their larvae via the food stored in the cell prior to egg laying. Most of scientific articles on IGR effects on bees are concerned with Apis mellifera L. They describe the symptoms observed on larvae, and report on various methods to test the toxicity of different compounds to adults or larvae or to assess the risks of field treatments. Fewer articles report studies on nonApis bees, most of which are concerned with the bumble bee, Bombus terrestris L. 2. EFFECTS OF IGRS ON HONEY BEES 2.1. Symptoms of IGR intoxication in adults The effects of juvenile hormone mimics such as methoprene were studied on workers by Redfern and Knox (1974). They tested this chemical, formulated in acetone, by topical application on adult workers lightly anaesthetised and did not find any mortality for concentrations ranging from 1 to 1000 μg/bee. Robinson (1985) also applied methoprene dissolved in acetone topically on workers which were marked and reintroduced into their colony for behavioural observations. He found that bees treated with 250 μg of JH analogue started foraging earlier than control ones. Lower doses, 25 and 2.5 μg caused no significant effect. Foraging performances estimated by the number of foraging trips per hour and the duration of the foraging period were not influenced by methoprene whereas the production of two alarm pheromones was induced prematurely. Jaycox et al. (1974) tested another synthetic JH mimic, the LawWilliams mixture. They injected experimental doses ranging from10 to 200 μg/bee, between metasomal tergites, using either olive or mineral oil as a carrier and found bees ate less pollen after injection of JH mimic. Treated bees could not develop their hypopharyngeal glands and started to move out of the brood nest, to guard the hive entrance, to fly and to collect pollen, sooner than control bees. There was a dose-effect relation in the onset of activity outside the colony. JH mimic treatment also reduced longevity by 39%. Rutz et al. (1974) applied JH III and the IGR triprene on freshly J.-N. Tasei 528