Sublethal doses of imidacloprid decreased size of hypopharyngeal glands and respiratory rhythm of honeybees in vivo

Apidologie

Volumn 44, Issue 4, 2013, Pages 467-480

  Hatjina, Fani ^a   Papaefthimiou, Chrisovalantis ^b   Charistos, Leonidas ^a   Dogaroglu, Taylan ^c   Bouga, Maria ^d   Emmanouil, Christina ^d   Arnold, Gerard ^e,f  

^a INSTITUTE OF TECHNOLOGY OF AGRICULTURAL PRODUCTS   (Greece)

^b ARISTOTLE UNIVERSITY OF THESSALONIKI   (Greece)

^c MUGLA SITKI KOCMAN UNIVERSITY   (Turkey)

^d AGRICULTURAL UNIVERSITY OF ATHENS   (Greece)

^e France and University of Paris Sud   (France)

^f UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

honeybee; hypopharyngeal gland; imidacloprid; respiratory rhythm

Indexed keywords

ACTIVITY PATTERN; BEHAVIORAL RESPONSE; BIOLOGICAL DEVELOPMENT; DOSE-RESPONSE RELATIONSHIP; HONEYBEE; IMIDACLOPRID; POLLUTION EFFECT; RESPIRATION; SIZE; SUBLETHAL EFFECT;

APIS MELLIFERA;

EID: 84878841248     PISSN: 00448435     EISSN: 12979678     Source Type: Journal    
DOI: 10.1007/s13592-013-0199-4     Document Type: Article

References (74)

1. Alaux, C.; Brunet, J.L.; Dussaubat, C.; Mondet, F.; Tchamitchan, S.; Cousin, M.; Brillard, J.; Baldy, A.; Belzunces, L.P.; Le Conte, Y. (2010) Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera). Environ. Microbiol. 12(3), 774-782
2. Babendreier, D.; Kalbere, R.N.M.; Romeis, J.; Fluri, P.; Mulligan, E.; Bigler, F. (2005) Influence of Bt-transgenic pollen, Bt-toxin and protease inhibitor (SBTI) ingestion on development of the hypopharyngeal glands in honeybees. Apidologie 36, 585-594
3. Benson, J.A. (1992) Electrophysiological pharmacology of the nicotinic and muscarinic cholinergic responses of isolated neuronal somata from locust thoracic ganglia. J. Exp. Biol. 170, 203-233
4. Berger, B.; Carmargo Abdalla, F. (2005) Braz. J Morphol. Sci 22(1), 1-4
5. Bonmatin, J.M.; Moineau, I.; Lecoublet, S.; Colin, M. E.; Fléché, C.; Bengsch E. R. (2001) Neurotoxiques systémiques: Biodisponibilité, toxicité et risques pour les insectes pollinisateurs - le cas de l'imidaclopride. In Proceedings of the 30éme Congrés du Groupe Français des Pesticides, Produits phytosanitaires; Couderchet, M.; Eullaffroy, P.; Vernet, G.; Eds.; Presses Universitaires de Reims: Reims, France, pp: 175-181.
6. Bonmatin, J.M.; Moineau, I.; Charvet, R.; Fleche, C.; Colin, M.E.; Bengsch, E.R. (2003) A LC/APCI-MS/MS method for analysis of imidacloprid in soils, in plants, and in pollens. Anal. Chem. 7, 2027-2033
7. Bonmatin, J.M.; Marchand, P.A.; Charvet, R.; Moineau, I.; Bengsch, E.R.; Colin, M.E. (2005) Quantification of imidacloprid uptake in maize crops. J. Agric. Food. Chem. 53, 5336-5341
8. Bortolotti, L.; Montanari, R.; Marcelino, J.; Medrzycki, P.; Maini, S.; Porrini, C. (2003) Effects of sub-lethal imidacloprid doses on the homing rate and foraging activity of honey bees. Bull. Insectology 56(1), 63-67
9. Breer, H.; Sattelle, D.B. (1987) Molecular properties and functions of insect acetylcholine receptors. J. Insect Physiol. 33, 771-790
10. Brown, L.A.; Ihara, M.; Buckingham, S.D.; Matsuda, K.; Sattelle, B.D. (2006) Neonicotinoid insecticides display partial and super agonist actions on native insect nicotinic acetylcholine receptors. J. Neurochem. 99, 608-615
11. Buckingham, S.D.; Lapied, B.; Corronc, H.L.; Grolleau, F.D.; Sattelle, D.B. (1997) Imidacloprid actions on insect neuronal acetylcholine receptors. J. Exp. Biol. 200, 2685-2692
12. Bujok, B.; Kleinhenz, M.; Fuchs, S. (2002) Hot spots in the bee hive. Naturwissenschaften 89, 229-301
13. Bustami, H.P.; Hustert, R. (2000) Typical ventilatory pattern of the intact locust is produced by the isolated CNS. J. Insect Physiol. 46, 1285-1293
14. Chapman, R.F. (1988) Sensory aspects of host-plant recognition by Acridoidea: questions associated with the multiplicity of receptors and variability of response. J. Insect Physiol. 34, 167-74
15. Chauzat, M.P.; Faucon, J.P.; Martel, A.C.; Lachaize, J.; Cougoule, N.; Aubert, M. (2006) A survey of pesticide residues in pollen loads collected by honey bees in France. J. Econ. Entomol. 99, 253-262
16. Chauzat, M.P.; Martel, A.C.; Cougoule, N.; Porta, P.; Lachaize, J.; Zeggane, S.; Aubert, M.; Carpentier, P.; Faucon, J.P. (2011) An assessment of honeybee colony matrices, Apis mellifera (Hymenoptera Apidae) to monitor pesticide presences in continental France. Environ. Toxicol. Chem. 30, 103-111
17. Colin, M.E.; Bonmatin, J.M.; Moineau, I.; Gaimon, C.; Brun, S.; Vermandere, J.P. (2004) A method to quantify and analyze the foraging activity of honey bees: relevance to the sublethal effects induced by systemic insecticides. Arch. Environ. Contam. Toxicol. 47, 387-395
18. Contreras, H.L.; Bradley, T.J. (2010) Transitions in insect respiratory patterns are controlled by changes in metabolic rate. J. Insect Physiol. 56, 522-528
19. Crailsheim, K.; Stolberg, E. (1989) Influence of diet, age and colony condition upon intestinal proteolytic activity and size of the hypopharyngeal glands in the honeybee (Apis mellifera L.). J. Insect Physiol 35, 595-602
20. Crailsheim, K.; Schneider, L.H.W.; Hrassnigg, N.; Bühlmann, G.; Brosch, U.; Gmeinbauer, R.; Schöffmann, B. (1992) Pollen consumption and utilization in worker honeybees (Apis mellifera carnica): Dependence on individual age and function. J. Insect Physiol. 38, 409-419
21. Decourtye, A.; Lacassie, E.; Pham-Delegue, M.H. (2003) Learning performances of honeybees (Apis mellifera L) are differentially affected by imidacloprid according to the season. Pest Manag. Sci. 59, 269-278
22. Decourtye, A.; Devillers, J.; Cluzeau, S.; Charreton, M.; Pham-Delegue, M.H. (2004a) Effects of imidacloprid and deltamethrin on associative learning in honeybee under semi-field and laboratory conditions. Ecotoxicol. Environ. Saf. 57, 410-419
23. Decourtye, A.; Armengaud, C.; Renou, M.; Devillers, J.; Cluzeau, S.; Gauthier, M.; Pham-Delegue, M.H. (2004b) Imidacloprid impairs memory and brain metabolism in the honeybee (Apis mellifera L.). Pest. Biochem. Physiol. 78, 83-92
24. Deseyn, J.; Billen, J. (2005) Age-dependent morphology and ultrastructure of the hypopharyngeal gland of Apis mellifera L. workers (Hymenoptera, Apidae). Apidologie 36, 49-57
25. Fluri, P.; Lucher, M.; Wille, H.; Gerig, L. (1982) Changes in weight of the pharyngeal gland and haemolymph titres of juvenile hormone protein and vitellogenin in worker honey bees. J. Insect Physiol. 28, 61-68
26. Girolami, V.; Mazzon, L.; Squartini, A.; Mori, N.; Marzaro, M.; Di Bernardo, A.; Greatti, M.; Giorio, C.; Tapparo, A. (2009) Translocation of neonicotinoid insecticides from coated seeds to seedling guttation drops: a novel way of intoxication for bees. J. Econ. Entomol. 102(5), 1808-1815
27. Girolami, V.; Marzaro, M.; Vivan, L.; Mazzon, L.; Greatti, M.; Giorio, C.; Marton, D.; Tapparo, A. (2011) Fatal powdering of bees in flight with particulates of neonicotinoids seed coating and humidity implication. J. Appl. Entomol. 136(1-2), 17-26
28. Greatti, M.; Sabatini, A.G.; Barbattini, R.; Rossi, S.; Stravisi, A. (2003) Risk of environmental contamination by the active ingredient imidacloprid used for corn seed dressing. Preliminary results. Bull. Insectology 56, 69-72
29. Greatti, M.; Barbattini, R.; Stravisi, A.; Sabatini, A.G.; Rossi, S. (2006) Presence of the a.i. imidacloprid on vegetation near corn fields sown with Gaucho® dressed seeds. Bull. Insectology 59, 99-103
30. Guez, D.; Suchail, S.; Gauthier, M.; Maleszka, R.; Belzunces, L.P. (2001a) Sublethal effects of imidacloprid on learning and memory in honeybees. In: Proceedings of the 7th International Symposium "Hazards of pesticides to bees", September 7-9, 1999, Avignon, France (Belzunces L. P.; Pelissier C.; Lewis G. B.; Eds). Les Colloques de l'INRA, 98, 279.
31. Guez, D.; Suchail, S.; Gauthier, M.; Maleszka, R.; Belzunces, L.P. (2001b) Contrasting effects of imidacloprid on habituation in 7- and 8- day-old honeybees (Apis mellifera). Neurobiol. Learn. Mem. 76, 183-191
32. Haydak, M.H. (1970) Honey bee nutrition. Annu. Rev. Entomol. 15, 143-156
33. Heinrich, B. (1972) Physiology of brood incubation in the bumblebee queens, Bombus vosnesenskii. Nature 239, 223-225
34. Heinrich, B. (1985) The social physiology of temperature regulation in honeybees, in: Holldobler J.M.; Lindauer G. (Eds.), Experimental Behavioral Ecology. Fortschr. Zool. 31, 393-406
35. Henry, M.; Beguin, M.; Requir, F.; Rollin, O.; Odoux, J-F.; Aupinel, P.; Aptel, J.; Tchamitchian, S.; Decourtye, A. (2012) A common pesticide decreases foraging success and survival in honey bees. Scienc 336(6079):348-350. doi: 10.1126/science.1215039.
36. Heylen, K.; Gobin, B.; Arckens, L.; Huybrechts, R.; Billen, J. (2010) The effects of four crop protection products on the morphology and ultrastructure of the hypopharyngeal gland of the European honeybee, Apis mellifera. Apidologie 42, 103-116
37. Hrassnigg, N.; Crailsheim, K. (1998) The influence of brood on the pollen consumption of worker bees (Apis mellifera L.). J. Insect. Physiol. 44, 393-404
38. Jeschke, P.; Nauen, R.; Schindler, M.; Elbert, A. (2011) Overview of the Status and Global Strategy for Neonicotinoids. J. Agric. Food Chem. 59(7), 2897-2908
39. Ishay, J. (1972) Thermoregulatory pheromones in wasps. Experienta 28, 1185-1187
40. Kaiser, W. (1988) Busy bees need rest, too: behavioural and electromyographical sleep signs in honeybees. J. Comp. Physiol. A 163, 565-584
41. Khoury, D.S.; Myerscough, M.R.; Barron, A.B. (2011) A quantitative model of honey bee colony population dynamics. Plos One 6, e18491
42. Kirchner, W.H. (1999) Mad-bee-disease? Sublethal effects of Imidacloprid (Gaucho ®) on the behavior of honey-bees. Apidologie 30, 422
43. Knecht, D.; Kaatz, H.H. (1990) Patterns of larval food production by hypopharyngeal glands in adult worker honey bees. Apidologie 21, 457-468
44. Kovac, H.; Stabentheiner, A.; Hetz, S.K.; Petz, M.; Crailsheim, K. (2007) Respiration of resting honeybees. J. Insect. Physiol. 53, 1250-1261
45. Kühnholz, S.; Seeley, T.D. (1997) The control of water collection in honey bee colonies. Behav. Ecol. Sociobiol. 41, 407-422
46. Lambin, M.; Armengaud, C.; Raymond, S.; Gauthier, M. (2001) Imidacloprid induced facilitation of the proboscis extension reflex habituation in the honeybee. Arch. Insect Biochem. Physiol. 48, 129-134
47. Lass, A.; Crailsheim, K. (1996) Influence of age and caging upon protein metabolism, hypopharyngeal glands and trophallactic behavior in the honey bee (Apis mellifera L). Insectes Soc. 43, 347-358
48. Lighton, J.R.B.; Lovegrove, B.G. (1990) A temperature-induced switch from diffusive to connective ventilation in the honeybee. J. Exp. Biol. 154, 509-516
49. Maini, S.; Medrycki, P.; Porrini, C. (2010) The puzzle of honey bee losses: a brief review. Bull. Insectology 63, 153-160
50. Malone, L.A.; Todd, J.H.; Burgess, E.P.J.; Christeller, J.T. (2004) Development of hypopharyngeal glands in adult honey bees fed with a Bt toxin, a biotin binding protein and a protease inhibitor. Apidologie 35, 655-664
51. Marzaro, M.; Vivan, L.; Targa, A.; Mazzon, L.; Mori, N.; Greatti, M.; Toffolo, E.P.; Di Bernardo, A.; Giorio, C.; Marton, D.; Tapparo, A.; Girolami, V. (2011) Lethal aerial powdering of honey bees with neonicotinoids from fragments of maize seed coat. Bull. Insectology 64, 119-126
52. Matsuda, K.; Buckingham, S.D.; Kleier, D.; Rauh, J.J.; Grauso, M.; Sattelle, D.B. (2001) Neonicotinoids: insecticides acting on insect nicotinic acetylcholine receptors. Trends Pharmacol. Sci. 22, 573-580
53. Matsuda, K.; Shimomura, M.; Ihara, M.; Akamatsu, M.; Satelle, D.B. (2005) Neonicotinoids show selective and diverse actions on their nicotinic receptor targets: electrophysiology, molecular biology, and receptor modelling studies. Biosci. Biotechnol. Biochem 69, 1442-1452
54. Nicolas, H.; Badre, M.; Martin, E.; Robin, L.; Cooper, T. (2005) The physiological and behavioral effects of carbon dioxide on Drosophila melanogaster larvae. Comp. Biochem. Physiol. A 140, 363-376
55. Ohashi, K.; Natori, S.; Kubo, T. (1997) Change in the mode of gene expression of the hypopharingeal gland cells with an age-dependent role change of the worker honeybee Apis mellifera L. Eur. J. Biochem. 249, 797-802
56. Ramirez, J.M.; Pearson, K.G. (1989) Distribution of intersegmental interneurones that can reset the respiratory rhythm of the locust. J. Exp. Biol. 141, 151-176
57. Ramirez-Romero, R.; Chaufaux, J.; Pham-Delegue, M.H. (2005) Effects of Cry1Ab protoxin, deltamethrin and imidacloprid on the foraging activity and the learning performances of the honeybee Apis mellifera, a comparative approach. Apidologie 36, 601-611
58. Rhodes, J.W.; Somerrville, D.C. (2003) Introduction and early performance of queen bees. Report: Rural Industries Research & Development Corporation, NSW Agriculture Pub# 03/049.
59. Rortais, A.; Arnold, G.; Halm, M.P.; Touffet-Briens, F. (2005) Modes of honeybees exposure to systemic insecticides: estimated amounts of contaminated pollen and nectar consumed by different categories of bees. Apidologie 36, 71-83
60. Seeley, T.D.; Heinrich, B. (1981) Regulation of temperature in the nests of social insects. In: Heinrich, B. (ed.) Insect thermoregulation, pp. 159-234. Wiley, New York
61. Shawky, S.; Abdel-Geleel, M Aly, A. (2005) Sorption of uranium by non-living water hyacinth roots. J. Radioanal. Nucl. Chem. 265(1), 81-84
62. Simpson, J. (1961) Nest climate regulation in honey bee colonies. Science 133, 1327-1333
63. Smodiš Šker, M.I.; Gregorc, A. (2010) Heat shock proteins and cell death in situ localisation in hypopharyngeal glands of honeybee (Apis mellifera carnica) workers after imidacloprid or coumaphos treatment. Apidologie 41, 73-86
64. Standifer, L.N. (1967) A comparison of the protein quality of pollens for growth-stimulation of the hypopharyngeal glands and longevity of honey bees, Apis mellifera. (Hymenoptera: Apidae). Insectes Soc 14, 415-426
65. Stork, A. (1999) A residue of 14C-NTN33893 (imidacloprid) in blossoms of sunflowers (Helianthus annus) after seed dressing, p. 56. Bayer A. G.; Crop Protection Development, Institute for Metabolism Research and Residue Analysis, Leverkusen
66. 14Cimidacloprid in different compartments of Apis mellifera L. Pest Manag. Sci. 60, 1056-1062
67. Vidau, C.; Diogon, M.; Aufauvre, J.; Fontbonne, R.; Viguès, B.; et al. (2011) Exposure to sublethal doses of fipronil and thiacloprid highly increases mortality of honeybees previously infected by Nosema ceranae. PLoS ONE 6(6), e21550
68. Visscher, H.; Brinkhuiss, H.; Dilcher, D.L.; Elsik, W.C.; Eshet, Y.; Looy, C.V.; Rampino, M.R.; Traverse, A. (1996) The terminal Paleozoic fungal event: Evidence of terrestrial ecosystem destabilization and collapse. Proc. Natl. Acad. Sci. USA 93, 2155-2158
69. Der Wang, L.; Moller, F.E. (1969) Histological comparisons of the development of hypopharyngeal glands in healthy and Nosema-infect worker honey bees. J. Invertebr. Pathol. 17, 308-320
70. Winston, M.L. (1987) The biology of the honey bee, p. 281. Harvard University Press, Cambridge
71. Wolf, T.J.; Schmid-Hempel, P.; Ellington, C.P.; Stevenson, R.D. (1989) Physiological correlates of foraging efforts in honey-bees: oxygen consumption and nectar load. Funct. Ecol. 3, 417-424
72. Yang, E.C.; Chuang, Y.C.; Chen, Y.L.; Chang, L.H. (2008) Abnormal foraging behavior induced by sublethal dosage of imidacloprid in the honey bee (Hymenoptera: Apidae). J. Econ. Entomol. 101, 1743-1748
73. Zafeiridou, G.; Theophilidis, G. (2004) The action of the insecticide imidacloprid on the respiratory rhythm of an insect: the beetle Tenebrio molitor. Neurosci. Lett. 365, 205-209
74. Zafeiridou, G.; Theophilidis, G. (2006) A simple method for monitoring the respiratory rhythm in intact insects and assessing the neurotoxicity of insecticide. Pestic. Biochem. Physiol. 87, 211-217