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Aversive learning in Bombus terrestris Audax (Hymenoptera: Apidae): responses to electric shock in a simulated environment | ||
| Journal of Entomological Society of Iran | ||
| مقاله 1، دوره 43، شماره 4، بهمن 2023، صفحه 323-335 اصل مقاله (1.23 M) | ||
| نوع مقاله: Paper, English | ||
| شناسه دیجیتال (DOI): 10.61186/jesi.43.4.1 | ||
| نویسندگان | ||
| Sajedeh Sarlak؛ Ahmad Ashouri* ؛ Seyed Hosein Goldansaz | ||
| Department of Plant Protection, College of Agriculture and Natural Resources, University of Tehran, Karaj, Iran | ||
| چکیده | ||
| The study of animal behavior, particularly in insects, is crucial for understanding their biological and evolutionary aspects, with wide-ranging applications in agricultural science, pest management, conservation biology, and neuroscience. Investigating cognitive characteristics, specifically aversive learning, plays a pivotal role in comprehending the success of insects. This adaptive ability enables animals to efficiently cope with the stressful factors in their environment. In this study, we investigated the aversive learning capabilities of Bombus terrestris Audax workers, crucial pollinators across diverse ecosystems. Bees were trained and tested in a flight arena using artificial flowers equipped with electric shocks to simulate conditions wherebees could associate punishment alongside food resources with available cues. The result suggested that bees possess the ability to simultaneously detect potential threats and food resources, indicating a dual aversive-appetitive memory. Furthermore, comparing groups trained with aversive (electric shock) and neutral (distilled water) stimuli showed that danger cues led to faster learning and stronger memory formation. This conditioning setup aimed to simulate real-life foraging situations, exploring bee responses when confronted with potential dangers. These findings provide insights into the survival strategies of insects in challenging environments that negatively impact bee populations. | ||
| کلیدواژهها | ||
| aversive learning؛ pollination؛ pollinator؛ cognitive abilities؛ insect behavior؛ free-flying bees؛ conditioning | ||
| عنوان مقاله [English] | ||
| یادگیری اجتنابی در Bombus terrestris Audax (Hymenoptera: Apidae): پاسخ به شوک الکتریکی در یک محیط شبیهسازی شده | ||
| نویسندگان [English] | ||
| ساجده سرلک؛ احمد عاشوری؛ سید حسین گلدانساز | ||
| گروه گیاهپزشکی، دانشکده کشاورزی و منابع طبیعی، دانشگاه تهران، کرج، ایران | ||
| چکیده [English] | ||
| مطالعه رفتار حیوانات، به ویژه حشرات، برای درک جنبههای بیولوژیکی و تکاملی آنها، کاربردهای گسترده در علومکشاورزی، مدیریت آفات، زیستشناسی حفاظتی و علوم اعصاب دارد. بررسی ویژگیهای شناختی، بهویژه یادگیری اجتنابی، نقشی اساسی در درک موفقیت حشرات دارد. این توانایی تطبیقی حیوانات را قادر میسازد تا در محیط خود به طور موثر با عوامل استرسزا مقابله کنند. در این مطالعه، توانایی یادگیری اجتنابی زنبورهای کارگر Bombus terrestris Audax، گردهافشان مهم در اکوسیستمهای مختلف، مورد بررسی قرار گرفت. زنبورها در یک محفظهی پرواز با استفاده از گلهای مصنوعی مجهز به شوک الکتریکی برای شبیهسازی شرایطی که بتوانند تنبیه را در کنار منابع غذایی موجود شناسایی و با نشانهها مرتبط کنند، آموزش داده و آزمایش شدند. نتایج نشان داد که زنبورها توانایی شناسایی همزمان تهدیدات بالقوه همراه با منابع غذایی را دارند، که نشاندهنده یک حافظه دوگانه اجتنابی - اشتیاقی است. علاوه بر این، مقایسه گروههایی که با محرکهای آزاردهنده (شوک الکتریکی) و خنثی (آب مقطر) آموزش داده شدند، نشان داد که نشانههای خطر منجر به یادگیری سریعتر و شکلگیری حافظه قویتر میشود. هدف این دستگاه شرطیسازی بررسی واکنش زنبورها در مواجهه با خطرات احتمالی، شبیه به موقعیتهای جستجوگری در زندگی واقعی بود. این یافتهها بینشی در مورد استراتژیهای بقای حشرات در محیطهای چالشبرانگیزی که تأثیرات منفی بر جمعیت زنبورها دارد، ارائه میدهد. | ||
| کلیدواژهها [English] | ||
| رفتارشناسی حشرات, زنبور مخملی, یادگیری اجتنابی, گرده افشانی, گرده افشان ها, یادگیری شرطی, تواناییهای شناختی | ||
| مراجع | ||
|
Agarwal, M., Giannoni Guzmán, M., Morales-Matos, C., Del Valle Díaz, R. A., Abramson, C. I. & Giray, T. (2011) Dopamine and octopamine influence avoidance learning of honey bees in a place preference assay. PloS One, 6 (9), e25371. https://doi.org/10.1371/journal.pone.0025371
Aquino, I. S., Abramson, C. I., Soares, A. E., Fernandes, A. C. & Benbassat, D. (2004) Classical conditioning of proboscis extension in harnessed Africanized honey bee queens (Apis mellifera L.). Psychological Reports 94(3_suppl), 1221-1231. https://doi.org/10.2466/pr0.94.3c.1221-1231
Bates, D., Mächler, M., Bolker, B. & Walker, S. (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67(1), 1–48. https://doi.org/10.18637/jss.v067.i01
Black, T. E., Stauch, K. L. N., Wells, H. & Abramson, C. I. (2021) Effects of ethanol ingestion on aversive conditioning in honey bees (Apis mellifera L.). Journal of Comparative Psychology 135(4), 559. https://doi.org/10.1037/com0000296
Boyd, I. L. (1999) Foraging and provisioning in Antarctic fur seals: interannual variability in time-energy budgets. Behavioral Ecology 10(2), 198-208. https://doi.org/10.1093/beheco/10.2.198
Carcaud, J., Roussel, E., Giurfa, M. & Sandoz, J. C. (2009) Odor aversion after olfactory conditioning of the sting extension reflex in honeybees. Journal of Experimental Biology 212(5), 620-626. https://doi.org/10.1242/jeb.026641
Chittka, L. (2017) Bee cognition. Current Biology 27(19), R1049-R1053. https://doi.org/10.1016/j.cub.2017.08.008
Cholé, H., Carcaud, J., Mazeau, H., Famié, S., Arnold, G. & Sandoz, J. C. (2019) Social contact acts as appetitive reinforcement and supports associative learning in honeybees. Current Biology 29(8), 1407-1413. https://doi.org/10.1016/j.cub.2019.03.025
Craig, C. L. (1994) Predator foraging behavior in response to perception and learning by its prey: interactions between orb-spinning spiders and stingless bees. Behavioral Ecology and Sociobiology 35, 45-52. https://doi.org/10.1007/bf00167059
De Bruijn, J. A., Vet, L. E., Smid, H. M. & De Boer, J. G. (2021) Memory extinction and spontaneous recovery shaping parasitoid foraging behavior. Behavioral Ecology 32(5), 952-960. https://doi.org/10.1093/beheco/arab066
Delkash-Roudsari, S. Goldansaz, S. H., Telebi-Jahromi, K., Ashouri, A. & Abramson, C. I. (2020) Effects of sub-lethal dose of imidacloprid on responsiveness of honey bee Apis mellifera. Iranian Journal of Plant Protection Science 51(2), 181-194. (In Persian)
Desneux, N., Decourtye, A. & Delpuech, J. M. (2007) The sublethal effects of pesticides on beneficial arthropods. Annual Review of Entomology 52, 81-106. https://doi.org/10.1146/annurev.ento.52.110405.091440
Devaud, J. M., Papouin, T., Carcaud, J., Sandoz, J. C., Grünewald, B. & Giurfa, M. (2015) Neural substrate for higher-order learning in an insect: mushroom bodies are necessary for configural discriminations. Proceedings of the National Academy of Sciences 112(43), E5854-E5862. https://doi.org/10.1073/pnas.1508422112
Dinges, C. W., Avalos, A., Abramson, C. I., Craig, D. P. A., Austin, Z. M., Varnon, C. A., Dal, F. N., Giray, T. & Wells, H. (2013) Aversive conditioning in honey bees (Apis mellifera anatolica): a comparison of drones and workers. Journal of Experimental Biology 216(21), 4124-4134. https://doi.org/10.1242/jeb.098947
Dukas, R. (2008) Evolutionary biology of insect learning. Annual Review of Entomology 53, 145-160. https://doi.org/10.1146/annurev.ento.53.103106.093343
Dukas, R. & Morse, D. H. (2003) Crab spiders affect flower visitation by bees. Oikos 101(1), 157-163. https://doi.org/10.1034/j.1600-0706.2003.12143.x
Forman, R. R. (1984) Leg position learning by an insect. I. A heat avoidance learning paradigm. Journal of Neurobiology 15(2), 127-140. https://doi.org/10.1002/neu.480150206
Gholami, M. (2023) Investigating the relative increase of oxygen on bumblebee. Master Thesis. University of Tehran. (In Persian)
Gholipour Faramarzi, F. (2020) Investigating the effect of carbon dioxide on learning and memory of Bombus terrestris. Master Thesis. University of Tehran. (In Persian)
Gill, R. J., Ramos-Rodriguez, O. & Raine, N. E. (2012) Combined pesticide exposure severely affects individual-and colony-level traits in bees. Nature 491(7422), 105-108. https://doi.org/10.1038/nature11585
Giurfa, M. (2015) Learning and cognition in insects. Wiley Interdisciplinary Reviews: Cognitive Science 6(4), 383-395. https://doi.org/10.1002/wcs.1348
Giurfa, M., Fabre, E., Flaven-Pouchon, J., Groll, H., Oberwallner, B., Vergoz, V., Roussel, E. & Sandoz, J. C. (2009) Olfactory conditioning of the sting extension reflex in honeybees: memory dependence on trial number, interstimulus interval, intertrial interval, and protein synthesis. Learning & Memory 16(12), 761-765. https://doi.org/10.1101/lm.1603009
Giurfa, M. & Sandoz, J. C. (2012) Invertebrate learning and memory: fifty years of olfactory conditioning of the proboscis extension response in honeybees. Learning & Memory 19(2), 54-66. https://doi.org/10.1101/lm.024711.111
Goulson, D., Lye, G. C. & Darvill, B. (2008) Decline and conservation of bumble bees. Annual Review of Entomology 53, 191-208. https://doi.org/10.1146/annurev.ento.53.103106.093454
Grueter, C. & Leadbeater, E. (2014) Insights from insects about adaptive social information use. Trends in Ecology & Evolution 29(3), 177-184. https://doi.org/10.1016/j.tree.2014.01.004
Guerrieri, F., Schubert, M., Sandoz, J. C. & Giurfa, M. (2005) Perceptual and neural olfactory similarity in honeybees. PLoS Biology 3(4), e60. https://doi.org/10.1371/journal.pbio.0030060
Guiraud, M., Hotier, L., Giurfa, M. & de Brito Sanchez, M. G. (2018) Aversive gustatory learning and perception in honey bees. Scientific Reports 8(1), 1343. https://doi.org/10.1038/s41598-018-19715-1
Hadar, R. & Menzel, R. (2010) Memory formation in reversal learning of the honeybee. Frontiers in Behavioral Neuroscience 4, 186. https://doi.org/10.3389/fnbeh.2010.00186
Hollis, K. L., McNew, K., Sosa, T., Harrsch, F. A. & Nowbahari, E. (2017) Natural aversive learning in Tetramorium ants reveals ability to form a generalizable memory of predators’ pit traps. Behavioral Processes 139, 19-25. https://doi.org/10.1016/j.beproc.2017.03.003
Horridge, G. A. (1962) Learning of leg position by the ventral nerve cord in headless insects. Proceedings of the Royal Society of London. Series B. Biological Sciences 157(966), 33-52. https://doi.org/10.1098/rspb.1962.0061
Ings, T. C. & Chittka, L. (2008) Speed-accuracy tradeoffs and false alarms in bee responses to cryptic predators. Current Biology 18(19), 1520-1524. https://doi.org/10.1016/j.cub.2008.07.074
Iqbal, J. & Mueller, U. (2007) Virus infection causes specific learning deficits in honeybee foragers. Proceedings of the Royal Society B: Biological Sciences 274(1617), 1517-1521. https://doi.org/10.1098/rspb.2007.0022
Itzhak, Y., Perez‐Lanza, D. & Liddie, S. (2014) The strength of aversive and appetitive associations and maladaptive behaviors. IUBMB Life 66(8), 559-571. https://doi.org/10.1002/iub.1310
Jones, E. I. & Dornhaus, A. (2011) Predation risk makes bees reject rewarding flowers and reduce foraging activity. Behavioral Ecology and Sociobiology 65, 1505-1511. https://doi.org/10.1007/s00265-011-1160-z
Jones, P. L. & Agrawal, A. A. (2017) Learning in insect pollinators and herbivores. Annual Review of Entomology 62, 53-71. https://doi.org/10.1146/annurev-ento-031616-034903
Junca, P., Carcaud, J., Moulin, S., Garnery, L. & Sandoz, J. C. (2014) Genotypic influence on aversive conditioning in honeybees, using a novel thermal reinforcement procedure. PLoS One 9(5), e97333. https://doi.org/10.1371/journal.pone.0097333
Khalifa, S. A., Elshafiey, E. H., Shetaia, A. A., El-Wahed, A. A. A., Algethami, A. F., Musharraf, S. G., AlAjmi, M. F., Zhao, C., Masry, S. H., Abdel-Daim, M. M. & Halabi, M. F. (2021) Overview of bee pollination and its economic value for crop production. Insects 12(8), 688. https://doi.org/10.3390/insects12080688
Klein, S., Cabirol, A., Devaud, J. M., Barron, A. B. & Lihoreau, M. (2017) Why bees are so vulnerable to environmental stressors. Trends in Ecology & Evolution 32(4), 268-278. https://doi.org/10.1016/j.tree.2016.12.009
Laloi, Dorine, J. C. Sandoz, A. L. Picard‐Nizou, A. Marchesi, A. Pouvreau, J. N. Taséi, G. & Poppy, M. H. (1999) Olfactory conditioning of the proboscis extension in bumble bees. Entomologia Experimentalis et Applicata 90(2), 123-129. https://doi.org/10.1046/j.1570-7458.1999.00430.x
Lenschow, M., Cordel, M., Pokorny, T., Mair, M. M., Hofferberth, J. & Ruther, J. (2018) The post-mating switch in the pheromone response of Nasonia females is mediated by dopamine and can be reversed by appetitive learning. Frontiers in Behavioral Neuroscience 12, 14. https://doi.org/10.3389/fnbeh.2018.00014
Litvin, Y., Blanchard, D. C., Arakawa, H. & Blanchard, R. J. (2008) Aversive Learning. In: Binder, M.D., Hirokawa, N., Windhorst, U. (eds) Encyclopedia of Neuroscience. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-29678-2_500
Mayack, C. & Naug, D. (2010) Parasitic infection leads to decline in hemolymph sugar levels in honeybee foragers. Journal of Insect Physiology 56(11), 1572-1575. https://doi.org/10.1016/j.jinsphys.2010.05.016
Mench, J. (1998) Why it is important to understand animal behavior. ILAR Journal 39(1), 20-26. https://doi.org/10.1093/ilar.39.1.20
Menzel, R. (1993) Associative learning in honey bees. Apidologie 24(3), 157-168. https://doi.org/10.1051/apido:19930301
Menzel, R. (2001) Searching for the memory trace in a mini-brain, the honeybee. Learning & Memory 8(2), 53-62. https://doi.org/10.1101/lm.38801
Menzel, R., Greggers, U. & Hammer, M. (1993) Functional organization of appetitive learning and memory in a generalist pollinator, the honey bee. In: Papaj, D.R., Lewis, A.C. (eds) Insect Learning: Ecology and Evolutionary Perspectives 79-125. https://doi.org/10.1007/978-1-4615-2814-2_4
Moret, Y. & Schmid-Hempel, P. (2000) Survival for immunity: the price of immune system activation for bumblebee workers. Science 290(5494), 1166-1168. https://doi.org/10.1126/science.290.5494.1166
Nouvian, M. & Galizia, C. G. (2019) Aversive training of honey bees in an automated Y-maze. Frontiers in Physiology 10, 678. https://doi.org/10.3389/fphys.2019.00678
Núñez, J., Almeida, L., Balderrama, N. & Giurfa, M. (1997) Alarm pheromone induces stress analgesia via an opioid system in the honeybee. Physiology & Behavior 63(1), 75-80. https://pubmed.ncbi.nlm.nih.gov/9402618/
Núñez, J., Maldonado, H., Miralto, A. & Balderrama, N. (1983) The stinging response of the honeybee: effects of morphine, naloxone and some opioid peptides. Pharmacology, Biochemistry and Behavior 19(6), 921-924. https://doi.org/10.1016/0091-3057(83)90391-x
Pearce, J. M. & Bouton, M. E. (2001) Theories of associative learning in animals. Annual Review of Psychology 52(1), 111-139. https://doi.org/10.1146/annurev.psych.52.1.111
Ravi, S., Garcia, J. E., Wang, C. & Dyer, A. G. (2016) The answer is blowing in the wind: free-flying honeybees can integrate visual and mechano-sensory inputs for making complex foraging decisions. Journal of Experimental Biology 219(21), 3465-3472. https://doi.org/10.1242/jeb.142679
Reser, D. H., Wijesekara Witharanage, R., Rosa, M. G. & Dyer, A. G. (2012) Honeybees (Apis mellifera) learn color discriminations via differential conditioning independent of long wavelength (green) photoreceptor modulation. PLoS One 7(11), e48577. https://doi.org/10.1371/journal.pone.0048577
Ritzmann, R. E. & Büschges, A. (2007) Adaptive motor behavior in insects. Current Opinion in Neurobiology 17(6), 629-636. https://doi.org/10.1016/j.conb.2008.01.001
Riveros, A. J. & Gronenberg, W. (2009) Learning from learning and memory in bumblebees. Communicative & Integrative Biology 2(5), 437-440. https://doi.org/10.4161/cib.2.5.9240
Roussel, E., Carcaud, J., Sandoz, J. C. & Giurfa, M. (2009) Reappraising social insect behavior through aversive responsiveness and learning. PLoS One 4(1), e4197. https://doi.org/10.1371/journal.pone.0004197
Russell, W. M. S. & Burch, R. L. (1959). The Principles of Humane Experimental Technique. London, Methuen & Co. Limited.
Schäfer, M. O., Ritter, W., Pettis, J. S., & Neumann, P. (2011). Concurrent parasitism alters thermoregulation in honey bee (Hymenoptera: Apidae) winter clusters. Annals of the Entomological Society of America, 104(3), 476-482. https://doi.org/10.1603/an10142
Santoro, D., Hartley, S., Suckling, D. M. & Lester, P. J. (2015) The stinging response of the common wasp (Vespula vulgaris): plasticity and variation in individual aggressiveness. Insectes Sociaux 62, 455-463. https://doi.org/10.1007/s00040-015-0424-4
Schipanski, A., Yarali, A., Niewalda, T. & Gerber, B. (2008) Behavioral analyses of sugar processing in choice, feeding, and learning in larval Drosophila. Chemical Senses 33(6), 563-573. https://doi.org/10.1093/chemse/bjn024
Schneider, C. W., Tautz, J., Grünewald, B. & Fuchs, S. (2012) RFID tracking of sublethal effects of two neonicotinoid insecticides on the foraging behavior of Apis mellifera. PloS One 7(1), e30023. https://doi.org/10.1371/journal.pone.0030023
Simons, M. & Tibbetts, E. (2019) Insects as models for studying the evolution of animal cognition. Current Opinion in Insect Science 34, 117-122. https://doi.org/10.1016/j.cois.2019.05.009
Smith, E. H. & Kennedy, G. G. (2009) History of entomology. In: Encyclopedia of Insects (pp. 449-458). Academic Press. https://doi.org/10.1016/b978-0-12-374144-8.00128-4
Tan, K., Chen, W., Dong, S., Liu, X., Wang, Y. & Nieh, J. C. (2014) Imidacloprid alters foraging and decreases bee avoidance of predators. PLoS One 9(7), e102725. https://doi.org/10.1371/journal.pone.0102725
Tedjakumala, S. R. & Giurfa, M. (2013) Rules and mechanisms of punishment learning in honey bees: the aversive conditioning of the sting extension response. Journal of Experimental Biology 216(16), 2985-2997. https://doi.org/10.1242/jeb.086629
Thiagarajan, D. & Sachse, S. (2022) Multimodal information processing and associative learning in the insect brain. Insects 13(4), 332. https://doi.org/10.3390/insects13040332
Urlacher, E., Francés, B., Giurfa, M. & Devaud, J. M. (2010) An alarm pheromone modulates appetitive olfactory learning in the honey bee (Apis mellifera). Frontiers in Behavioral Neuroscience 4, 157. https://doi.org/10.3389/fnbeh.2010.00157
Van Huis, A. (2019) Welfare of farmed insects. Journal of Insects as Food and Feed 5(3), 159-162. https://doi.org/10.3920/jiff2019.x004
Vergoz, V., Roussel, E., Sandoz, J. C. & Giurfa, M. (2007) Aversive learning in honeybees revealed by the olfactory conditioning of the sting extension reflex. PloS One 2(3), e288. https://doi.org/10.1371/journal.pone.0000288
Vinauger, C., Buratti, L. & Lazzari, C. R. (2011) Learning the way to blood: first evidence of dual olfactory conditioning in a blood-sucking insect, Rhodnius prolixus. I. Appetitive learning. Journal of Experimental Biology 214(18), 3032-3038. https://doi.org/10.3410/f.13294002.14653126
Williamson, S. M. & Wright, G. A. (2013) Exposure to multiple cholinergic pesticides impairs olfactory learning and memory in honeybees. Journal of Experimental Biology 216(10), 1799-1807. https://doi.org/10.1242/jeb.083931
Zabala, N. A., Miralto, A., Maldonado, H., Nunez, J. A., Jaffe, K. & Calderon, L. D. C. (1984) Opiate receptor in praying mantis: effect of morphine and naloxone. Pharmacology Biochemistry and Behavior 20(5), 683-687. https://doi.org/10.1016/0091-3057(84)90185-0 | ||
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