Effects of Insect Growth Regulators on Honey Bees and Non-Apis Bees. a Review
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Apidologie 32 (2001) 527–545 527 © INRA/DIB-AGIB/EDP Sciences, 2001 Review article Effects of insect growth regulators on honey bees and non-Apis bees. A review Jean-Noël TASEI* Unité de Recherches de Zoologie, INRA, 86600 Lusignan, France (Received 26 December 2000; revised 17 May 2001; accepted 24 July 2001) Abstract – 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. Top- ical and feeding tests revealed that application of IGRs to larvae may result in death and larval ejec- tion by workers, malformed larvae and pupae with typical rimmed eyes, or malformed adults. Sev- eral 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 1. INTRODUCTION insect growth regulators or IGRs, have been used in insect pest control for more than After Wigglesworth’s pioneering studies 25 years. These insecticides of the third gen- performed during 1933–1940 (Wiggelsworth, eration appeared after the early generation of 1972) on the control of insect growth by arsenates, insecticides of mineral origin, and endocrine organs, Williams (1956) suggested the second generation of organic synthetic that in addition to their theoretical interest, compounds such as DDT. The mode of juvenile hormones could be accurately iden- action of IGRs is quite original since they tified, then synthesised and used as insec- are not stomach poisons and they do not ticides. His prospects have been achieved exhibit neurotoxicity but they disrupt moult- since several commercial compounds called ing process or cuticle formation. Larval * Correspondence and reprints E-mail: [email protected] 528 J.-N. Tasei characters are maintained by the juvenile the toxicity of different compounds to adults hormones (JH) which are secreted by cor- or larvae or to assess the risks of field treat- pora allata. The JH are hormones of iso- ments. Fewer articles report studies on non- prenoid nature which prevent the breakdown Apis bees, most of which are concerned with of the thoracic gland (Wigglesworth, 1972). the bumble bee, Bombus terrestris L. Pupal moulting is determined by a circulat- ing hormone: the moulting hormone, secreted by the prothoracic glands which 2. EFFECTS OF IGRS ON HONEY are activated by neurosecretory cells. This BEES hormone triggers changes in the epidermis and deposition of the new cuticle. The 2.1. Symptoms of IGR intoxication purified form, of steroid nature is called in adults ecdysone. Similar substances can be iso- lated from many plants. IGRs are commer- The effects of juvenile hormone mimics cial hormones mimics that influence moult- such as methoprene were studied on ing as hormones do, acting at the cellular workers by Redfern and Knox (1974). They level in various ways depending on their tested this chemical, formulated in acetone, chemical constitution: tebufenozide influ- by topical application on adult workers ences moulting as ecdysone does, while lightly anaesthetised and did not find any pyriproxyfen and fenoxycarb are JH mimics. mortality for concentrations ranging from 1 A third class is that of chitin inhibitors such to 1000 µg/bee. Robinson (1985) also applied as diflubenzuron, flufenoxuron, hexaflu- methoprene dissolved in acetone topically on muron, and lufenuron. In addition, a natural workers which were marked and reintro- substance from neem tree, Azadirachta duced into their colony for behavioural indica, proved to be a potent IGR (Rembold observations. He found that bees treated et al., 1980). According to Engels (1990) with 250 µg of JH analogue started foraging IGRs cause little or no damage to adult earlier than control ones. Lower doses, 25 honey bees and generally the typical effects and 2.5 µg caused no significant effect. For- of these compounds can be seen after the aging performances estimated by the num- moult of the exposed stage. All natural or ber of foraging trips per hour and the dura- synthetic compounds with IGR properties tion of the foraging period were not may be suspected of being hazardous to the influenced by methoprene whereas the pro- brood of Apis or non-Apis bees since their duction of two alarm pheromones was larvae can be exposed to insecticides by an induced prematurely. Jaycox et al. (1974) oral route. Davis (1989) contributed to the tested another synthetic JH mimic, the Law- understanding of the oral pathway of insec- Williams mixture. They injected experi- ticides, mediated by adult nurse honey bees mental doses ranging from10 to 200 µg/bee, which regurgitate honey sac content to feed between metasomal tergites, using either larvae. In solitary bees, George and Rincker olive or mineral oil as a carrier and found (1985), Tasei and Carré (1987), and Tasei bees ate less pollen after injection of JH et al. (1988), showed that Megachile rotun- mimic. Treated bees could not develop their data Fabr. females provisioning their nest hypopharyngeal glands and started to move with pollen and nectar can also transfer out of the brood nest, to guard the hive insecticides to their larvae via the food entrance, to fly and to collect pollen, sooner stored in the cell prior to egg laying. than control bees. There was a dose-effect Most of scientific articles on IGR effects relation in the onset of activity outside the on bees are concerned with Apis mellifera L. colony. JH mimic treatment also reduced They describe the symptoms observed on longevity by 39%. Rutz et al. (1974) applied larvae, and report on various methods to test JH III and the IGR triprene on freshly Impact of insect growth regulators on bees 529 emerged workers by feeding or injection and observed abnormal leucocytes, the inhi- and found that both hormones caused a bition of hypopharyngeal glands, the reduction in the total protein content of decrease of the total haemolymph proteins the haemolymph and a change in the form and the reduction of longevity. of leucocytes. At a high dose of JH III (1 µg/bee) the hypopharyngeal glands regressed which hampered larva feeding by 2.2. Symptoms of IGR intoxication workers. Triprene at 1 µg/bee shortened the in larvae life of queen-less workers. Atkins et al. (1976) measured the effects of hundreds of After topical application of the juvenile pesticides on bees and listed active sub- hormone analogue methoprene on 3 and stances and formulations according to their 5 day old larvae Hussein and Abdel-Aal hazards to bees in field tests for commonly (1978) observed malformations of the used materials. For less frequently used abdomen, wings and wax glands in adults. In compounds they referred to laboratory data. addition, more than 50% of treated larvae were removed from their brood cell. Zdarek Dimilin®, formulated with diflubenzuron, and Haragsim (1974) studied the morpho- one of the most common commercial IGR genetic action of 33 structurally unrelated appeared in the group of the “relatively non- JH analogues chemicals by applying them toxic” insecticides. Usha and Kandasamy on worker bee larvae either during their (1986) exposed Apis cerana Fabr. for 90 min feeding period or later. The early treatment to surfaces treated with several insecticides induced the development of imaginal char- including diflubenzuron. As no mortality acters of queen and the late administration . –1 occurred even at 10000 mg kg the authors inhibited the differentiation of imaginal concluded that this chitin synthesis inhibitor structures. Beetsma and Ten Houten (1975) was the safest and should be recommended tested JH I, II, III, IV, V and VI by mixing for integrated pest management. Difluben- the compounds with the food supplied to zuron was also tested on newly emerged small colonies or by spraying it on rape- adults of A. mellifera and A. cerana indica seed flowering in a flight cage. After treat- by Gupta and Chandel (1995). They found ment with JH I, II, IV and V they did not that topical applications of 100 µg doses observe any mortality in workers but found were tolerated by treated bees but resulted in incompletely coloured adults with queen- a reduced weight gain. The same dose like characters. With JH IV and V, the administrated per os proved fatal, but 50 µg queens died and all larvae disappeared were tolerated and suppressed the develop- within the week following application. JH V ment of hypopharyngeal glands in both inactivated hypopharyngeal glands of adult species. This oral treatment also affected workers. Almost no brood was affected by weight gain, indicating that at high doses, JH III and VI, and JH I and II resulted in an this IGR can be harmful to adults. Acute increase of brood. Similar methods were toxicity tests performed on adult A. mellifera used by Hrdy and Skrobal (1976) who found with another IGR, flucycloxuron (Andalin®) that application of JH I and JH II reduced proved this material safe in integrated pest brood quantity. Gerig (1975) found that control (Ceparano and Job, 1989). Pyriprox- kinoprene inhibited the development of yfen, applied at concentrations higher than hypopharyngeal glands. 1.25 µg, to newly emerged workers, impaired Feeding small colonies with difluben- vitellogenin synthesis in the haemolymph zuron reduced the amount of capped and (Pinto et al., 2000).