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

Apidologie volume 44, pages 467–480 (2013)Cite this article

Abstract

Most studies that have shown negative sublethal effects of the pesticide imidacloprid on honeybees concern behavioral effects; only a few concern physiological effects. Therefore, we investigated sublethal effects of imidacloprid on the development of the hypopharyngeal glands (HPGs) and respiratory rhythm in honeybees fed under laboratory conditions. We introduced newly emerged honeybees into wooden mesh-sided cages and provided sugar solution and pollen pastry ad libitum. Imidacloprid was administered in the food: 2 μg/kg in the sugar solution and 3 μg/kg in the pollen pastry. The acini, the lobes of the HPGs of imidacloprid-treated honeybees, were 14.5 % smaller in diameter in 9-day-old honeybees and 16.3 % smaller in 14-day-old honeybees than in the same-aged untreated honeybees; the difference was significant for both age groups. Imidacloprid also significantly affected the bursting pattern of abdominal ventilation movements (AVM) by causing a 59.4 % increase in the inter-burst interval and a 56.99 % decrease in the mean duration of AVM bursts. At the same time, the quantity of food consumed (sugar solution and pollen pastry) per honeybee per day was the same for both treated and untreated honeybees.

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References

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Berger, B., Carmargo Abdalla, F. (2005) Braz. J Morphol. Sci 22(1), 1–4

    Google Scholar 

  • 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.

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Breer, H., Sattelle, D.B. (1987) Molecular properties and functions of insect acetylcholine receptors. J. Insect Physiol. 33, 771–790

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Bujok, B., Kleinhenz, M., Fuchs, S. (2002) Hot spots in the bee hive. Naturwissenschaften 89, 229–301

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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.

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Haydak, M.H. (1970) Honey bee nutrition. Annu. Rev. Entomol. 15, 143–156

    Article  Google Scholar 

  • Heinrich, B. (1972) Physiology of brood incubation in the bumblebee queens, Bombus vosnesenskii. Nature 239, 223–225

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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.

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Ishay, J. (1972) Thermoregulatory pheromones in wasps. Experienta 28, 1185–1187

    Article  Google Scholar 

  • Kaiser, W. (1988) Busy bees need rest, too: behavioural and electromyographical sleep signs in honeybees. J. Comp. Physiol. A 163, 565–584

    Article  Google Scholar 

  • Khoury, D.S., Myerscough, M.R., Barron, A.B. (2011) A quantitative model of honey bee colony population dynamics. Plos One 6, e18491

    Article  PubMed  CAS  Google Scholar 

  • Kirchner, W.H. (1999) Mad-bee-disease? Sublethal effects of Imidacloprid (Gaucho ®) on the behavior of honey-bees. Apidologie 30, 422

    Article  Google Scholar 

  • Knecht, D., Kaatz, H.H. (1990) Patterns of larval food production by hypopharyngeal glands in adult worker honey bees. Apidologie 21, 457–468

    Article  Google Scholar 

  • Kovac, H., Stabentheiner, A., Hetz, S.K., Petz, M., Crailsheim, K. (2007) Respiration of resting honeybees. J. Insect. Physiol. 53, 1250–1261

    Article  PubMed  CAS  Google Scholar 

  • Kühnholz, S., Seeley, T.D. (1997) The control of water collection in honey bee colonies. Behav. Ecol. Sociobiol. 41, 407–422

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Maini, S., Medrycki, P., Porrini, C. (2010) The puzzle of honey bee losses: a brief review. Bull. Insectology 63, 153–160

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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.

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Shawky, S., Abdel-Geleel, Μ., Aly, A. (2005) Sorption of uranium by non-living water hyacinth roots. J. Radioanal. Nucl. Chem. 265(1), 81–84

    Article  CAS  Google Scholar 

  • Simpson, J. (1961) Nest climate regulation in honey bee colonies. Science 133, 1327–1333

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Suchail, S., De Sousa, G., Rahmani, R., Belzunces, L. (2004) In vivo distribution and metabolization of 14Cimidacloprid in different compartments of Apis mellifera L. Pest Manag. Sci. 60, 1056–1062

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Winston, M.L. (1987) The biology of the honey bee, p. 281. Harvard University Press, Cambridge

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

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Acknowledgments

This work was supported by a joint project from the EU and the Greek Ministry of Agricultural Development and Food (2008–2010) and by a Greek-French bilateral collaboration project, PLATON 09 FR75. We thank Dimitra Fouka, laboratory technician in Hellenic Institute of Apiculture, for technical assistance. We are also profoundly indebted to Sharilynn Wardrop, for stylistic and linguistic improvements as well to the anonymous reviewers for valuable suggestions.

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Authors and Affiliations

  1. Hellenic Institute of Apiculture, Hellenic Agricultural Organization ‘DEMETER’, N. Moudania, 63 200, Greece

    Fani Hatjina & Leonidas Charistos

  2. Laboratory of Animal Physiology, Department of Zoology, School of Biology, Aristotle University, 541 24, Thessaloniki, Greece

    Chrisovalantis Papaefthimiou

  3. Mugla University, Science Faculty, Biology Department, 48000, Mugla, Turkey

    Taylan Dogaroglu

  4. Lab of Agricultural Zoology and Entomology, Agricultural University of Athens, 75 Iera Odos Str, Athens, 118 55, Greece

    Maria Bouga & Christina Emmanouil

  5. Laboratoire Evolution, Génomes, Spéciation, CNRS UPR 9034, 91198 Gif-sur-Yvette, France and Université Paris-Sud 11, Orsay, France

    Gerard Arnold

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  1. Fani Hatjina
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  2. Chrisovalantis Papaefthimiou
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  3. Leonidas Charistos
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Correspondence to Fani Hatjina.

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Manuscript editor: Monique Gauthier

Des doses sublétales d’imidaclopride réduisent la taille des glandes hypopharyngiennes et agissent sur le rythme respiratoire des abeilles

Insecticide / abeille / essai en laboratoire / respiration / glande salivaire

Subletale Imidaclopriddosierungen verringern die Größe der Futtersaftdrüsen und den Atemrhythmus von Honigbienen in vivo

Imidacloprid / Honigbiene / Futtersaftdrüse / Atemrhythmus

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Hatjina, F., Papaefthimiou, C., Charistos, L. et al. Sublethal doses of imidacloprid decreased size of hypopharyngeal glands and respiratory rhythm of honeybees in vivo. Apidologie 44, 467–480 (2013). https://doi.org/10.1007/s13592-013-0199-4

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