Abstract
Classical conditioning has been well studied in social Hymenoptera, exploring how members of a colony gain foraging benefits from learning to associate various stimuli. While some of this work has been extended into Blattodea, learning in eusocial termite societies has not been well documented. Termites mainly rely on chemical cues for feeding; thus, they would be predicted to associate odor with food. In this study, we tested the ability of species Zootermopsis angusticollis to learn via classical conditioning. We used a natural odorant in conjunction with sugar water to attempt to elicit a feeding response. Termites were individually exposed to our unconditioned and conditioned stimuli through a series of trials, after which the response to the conditioned stimulus alone was recorded and compared to controls. We found that those trained exhibited a significantly greater frequency of feeding responses to the conditioned stimulus. Thus, Z. angusticollis can associate a novel odor with food.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
The data from this study are available from the corresponding author on reasonable request.
References
Abramson CI, Aquino IS, Silva MC, Price JM (1997) Learning in the africanized honey bee: Apis mellifera L. Physiol Behav 62:657–674. https://doi.org/10.1016/S0031-9384(97)00194-7
Adams ES (1991) Nest-mate recognition based on heritable odors in the termite Microcerotermes arboreus. Proc Nat Acad Sci 88:2031–2034. https://doi.org/10.1073/pnas.88.5.2031
Arango RA, Green Iii F, Hintz K, Lebow PK, Miller RB (2006) Natural durability of tropical and native woods against termite damage by Reticulitermes flavipes (Kollar). Int Biodeter Biodegr 57:146–150. https://doi.org/10.1016/j.ibiod.2006.01.007
Arenas A, Ramirez GP, Balbuena MS, Farina WM (2013) Behavioral and neural plasticity caused by early social experiences: the case of the honeybee. Front Physiol 4:1–11. https://doi.org/10.3389/fphys.2013.00041
Arican C, Bulk J, Deisig N, Nawrot M (2019) Cockroaches show individuality in learning and memory during classical and operant conditioning. Front Physiol 10:1539. https://doi.org/10.3389/fphys.2019.01539
Bitterman ME, Menzel R, Fietz A, Schäfer S (1983) Classical conditioning of proboscis extension in honeybees (Apis mellifera). J Comp Psychol 97:107–119. https://doi.org/10.1037/0735-7036.97.2.107
Botch PS, Brennan CL, Judd TM (2010) Seasonal effects of calcium and phosphate on the feeding preference of the termite Reticulitermes flavipes (Isoptera: Rhinotermitidae). Sociobiology 55:42–56
Chouvenc T, Šobotník J, Engel MS, Bourguignon T (2021) Termite evolution: mutualistic associations, key innovations, and the rise of Termitidae. Cell Mol Life Sci 78:2749–2769. https://doi.org/10.1007/s00018-020-03728-z
Daly K, Smith BH (2000) Associative olfactory learning in the moth Manduca sexta. J Exp Biol 203:2025–2038. https://doi.org/10.1242/jeb.203.13.2025
Daniel WW (1990) Applied Nonparametric Statistics, 2nd edn. PWS-Kent, Boston
Davey G (1989) Ecological learning theory. Routlage, London
Delamater AR, Matthew Lattal K (2014) The study of associative learning: mapping from psychological to neural levels of analysis. Neurobiol Learn Mem 108:1–4. https://doi.org/10.1016/j.nlm.2013.12.006
Dukas R, Real LA (1991) Learning foraging tasks by bees: a comparison between social and solitary species. Anim Behav 42:269–276. https://doi.org/10.1016/S0003-3472(05)80558-5
von Frisch K (1943) Versuche über die Lenkung des Bienenfluges durch Duftstoffe. Naturwissenschaften 31:445–460. https://doi.org/10.1007/BF01468310
Gadd CA, Raubenheimer D (2000) Nutrient-specific learning in an omnivorous insect: the american cockroach Periplaneta americana l. learns to associate dietary protein with the odors citral and carvone. J Insect Behav 13:851–864. https://doi.org/10.1023/A:1007862501311
Gámez AM, León SP (2018) The role of learning in the oviposition behavior of the silkworm moth (Bombyx mori). Behav Process 157:286–290. https://doi.org/10.1016/j.beproc.2018.10.023
Giunti G, Canale A, Messing RH, Donati E, Stefanini C, Michaud JP, Benelli G (2015) Parasitoid learning: current knowledge and implications for biological control. Biol Control 90:208–219. https://doi.org/10.1016/j.biocontrol.2015.06.007
Giurfa M, Sandoz J-C (2012) Invertebrate learning and memory: fifty years of olfactory conditioning of the proboscis extension response in honeybees. Learn Mem 19:54–66. https://doi.org/10.1101/lm.024711.111
Goulson D, Ollerton J, Sluman C (1997) Foraging strategies in the small skipper butterfly, Thymelicus flavus: when to switch? Anim Behav 53:1009–1016. https://doi.org/10.1006/anbe.1996.0390
Grace JK (1989) Habituation in termite orientation response to fungal semiochemicals. Sociobiology 16:175–182
Guerrieri FJ, d’Ettorre P (2010) Associative learning in ants: conditioning of the maxilla-labium extension response in Camponotus aethiops. J Insect Physiol 56:88–92. https://doi.org/10.1016/j.jinsphys.2009.09.007
Inward D, Beccaloni G, Eggleton P (2007) Death of an order: a comprehensive molecular phylogenetic study confirms that termites are eusocial cockroaches. Biol Lett 3:331–335. https://doi.org/10.1098/rsbl.2007.0102
Ishida Y, Chiang VP, Haverty MI, Leal WS (2002) Odorant-binding proteins from a primitive termite. J Chem Ecol 28:1887–1893. https://doi.org/10.1023/a:1020537319805
de Jong R, Pham-Delègue M (1991) Electroantennogram responses related to olfactory conditioning in the honey bee (Apis mellifera ligustica). J Insect Physiol 37:319–324. https://doi.org/10.1016/0022-1910(91)90066-9
Judd TM (2018) Cues used by subterranean termites during foraging and food assessment. In: Khan MA, Ahmad W (eds) Termites and sustainable management. Sustainability in Plant and Crop Protection, vol 1, 1st edn. Springer International Publishing AG, Cham, pp 159–180
Kandori I, Yamaki T (2012) Reward and non-reward learning of flower colours in the butterfly Byasa alcinous (Lepidoptera: Papilionidae). Naturwissenschaften 99:705–713. https://doi.org/10.1007/s00114-012-0952-y
Klahn JE (1979) Philopatric and nonphilopatric foundress associations in the social wasp Polistes fuscatus. Behav Ecol Sociobiol 5:417–424. https://doi.org/10.2307/4599248
Liu J-L, Sakuma M (2013) Olfactory conditioning with single chemicals in the german cockroach, Blattella germanica (Dictyoptera: Blattellidae. Appl Entomol Zool 48:387–396. https://doi.org/10.1007/s13355-013-0199-x
Van Loon JJA, Everaarts TC, Smallegange RC (1992) Associative learning in host-finding by female Pieris brassicae butterflies: relearning preferences. In: Menken SBJ, Visser JH, Harrewijn P (eds) Proceedings of the 8th International Symposium on Insect-Plant Relationships. Dordrecht: Kluwer Academic Publishing, Netherlands, pp 162–164. https://doi.org/10.1007/978-94-011-1654-1_54
Matsumoto Y, Noji S, Mizunami M (2003) Time course of protein synthesis-dependent phase of olfactory memory in the cricket Gryllus bimaculatus. Zool Sci 20:409–416. https://doi.org/10.2108/zsj.20.409
Mc Cabe SI, Farina WM (2010) Olfactory learning in the stingless bee Tetragonisca angustula (Hymenoptera, Apidae, Meliponini). J Comp Physiol A 196:481–490. https://doi.org/10.1007/s00359-010-0536-2
Mc Cabe SI, Hartfelder K, Santana WC, Farina WM (2007) Odor discrimination in classical conditioning of proboscis extension in two stingless bee species in comparison to africanized honeybees. J Comp Physiol A 193:1089–1099. https://doi.org/10.1007/s00359-007-0260-8
McMahan EA (1966) Studies of termite wood-feeding preferences. Proc Hawaiin Entomol Soc 29:239–250
Menzel R, Erber J (1978) Learning and memory in bees. Sci Am 239:102–111
Morales-Ramos JA, Rojas MG (2003) Nutritional ecology of the formosan subterranean termite (Isoptera: Rhinotermitidae): growth and survival of incipient colonies feeding on preferred wood species. J Econ Entomol 96:106–116. https://doi.org/10.1603/0022-0493-96.1.106
Palottini F, Estravis Barcala MC, Farina WM (2018) Odor learning and its experience-dependent modulation in the south american native bumblebee Bombus atratus (Hymenoptera: Apidae). Front Psychol 9. https://doi.org/10.3389/fpsyg.2018.00603
Pavlov IP (1927) Conditioned reflexes: an investigation of the physiological activity of the cerebral cortex. Ann Neurosci 17:136–141
Röseler P-F (1991) Reproductive competition during colony development. In: Ross KG, Matthews RW (eds) The Social Biology of Wasps. Comstock Publishing Associates, Ithaca, New York, pp 309–335
Saran RK, Rust MK (2005) Feeding, uptake, and utilization of carbohydrates by western subterranean termite (Isoptera: Rhinotermitidae). J Econ Entomol 98:1284–1293. https://doi.org/10.1603/0022-0493-98.4.1284
Shanbhag RR, Sundararaj R (2013) Physical and chemical properties of some imported woods and their degradation by termites. J Insect Sci 13:1–8. https://doi.org/10.1673/031.013.6301
Shellman Reeve JS (1997) Advantages of biparental care in the wood-dwelling termite, Zootermopsis nevadensis. Anim Behav 54:163–170. https://doi.org/10.1006/anbe.1996.0412
Shellman-Reeve JS (1990) Dynamics of biparental care in the dampwood termite, Zootermopsis nevadensis (Hagen): response to nitrogen availability. Behav Ecol Sociobiol 26:389–397. https://doi.org/10.1007/BF00170895
Shelton TG, Grace JK (1997) Suggestion of an environmental influence on intercolony agonism of formosan subterranean termites (Isoptera: Rhinotermitidae). Environ Entomol 26:632–637. https://doi.org/10.1093/ee/26.3.632
Smythe RV, Carter FL (1969) Feeding responses to sound wood by the eastern subterranean termite, Reticulitermes flavipes. Ann Entomol Soc Amer 62:335–337. https://doi.org/10.1093/aesa/62.2.335
Thorne BL, Haverty MI (1989) Accurate identification of Zootermopsis species (Isoptera: Termopsidae) based on a mandibular character of nonsoldier castes. Ann Entomol Soc Am 82:262–266. https://doi.org/10.1093/aesa/82.3.262
Traynier RMM (1984) Associative learning in the ovipositional behaviour of the cabbage butterfly, Pieris rapae. Phys Entom 9:465–472. https://doi.org/10.1111/j.1365-3032.1984.tb00789.x
Wallace BA, Judd TM (2010) A test of seasonal responses to sugars in four populations of the termite Reticulitermes flavipes. J Econ Entomol 103:2126–2131. https://doi.org/10.1603/EC09326
Waller DA, La Fage JP (1987) Nutritional ecology of termites. In: Slansky F Jr, Rodriguez JG (eds) Nutritional Ecology of Insects, Mites, Spiders and related invertebrates. John Wiley & Sons, New York, pp 487–532
Waller DA, Jones CG, La Fage JP (1990) Measuring wood preference in termites. Entomol Exp Appl 56:117–123. https://doi.org/10.1111/j.1570-7458.1990.tb01388.x
Watanabe H, Kobayashi Y, Sakura M, Matsumoto Y, Mizunami M (2003) Classical olfactory conditioning in the cockroach Periplaneta americana. Zool Sci 20:1447–1454. https://doi.org/10.2108/zsj.20.1447
Watanabe H, Mizunami M (2006) Classical conditioning of activities of salivary neurones in the cockroach. J Exp Biol 209:766–779. https://doi.org/10.1242/jeb.02049
Watanabe H, Mizunami M (2007) Pavlov’s cockroach: classical conditioning of salivation in an insect. PLoS One 2:e529. https://doi.org/10.1371/journal.pone.0000529
Wood TG (1978) Food and feeding habits of termites. In: Brian MV (ed) Production Ecology of Ants and Termites. Cambridge University Press, Cambridge, pp 55–80
Yarmolinsky DA, Zuker CS, Ryba NJP (2009) Common sense about taste: from mammals to insects. Cell 139:234–244. https://doi.org/10.1016/j.cell.2009.10.001
Acknowledgements
Thanks to Christine Parry and Kaitlyn Scheffler for their comments on earlier drafts of this manuscript.
Funding
This project was funded by Southeast Missouri State University.
Author information
Authors and Affiliations
Contributions
All authors helped develop the assay and experimental design. Joseph Norman conducted the trials. Joseph Norman and Timothy Judd wrote the manuscript and prepared the figures. Timothy Judd analyzed the data. All authors reviewed the manuscript.
Corresponding author
Ethics declarations
The authors have no relevant financial or non-financial interests to disclose.
Competing Interests
The authors declare no competing interests.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Norman, J.H., Gass, H.L. & Judd, T.M. Odorant Classical Conditioning in the Termite Zootermopsis angusticollis. J Insect Behav 36, 150–155 (2023). https://doi.org/10.1007/s10905-023-09832-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10905-023-09832-9