Great tits (Parus major) flexibly learn that herbivore-induced plant volatiles indicate prey location: An experimental evidence with two tree species

. 2021 Aug ; 11 (16) : 10917-10925. [epub] 20210721

Status PubMed-not-MEDLINE Jazyk angličtina Země Velká Británie, Anglie Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid34429890

When searching for food, great tits (Parus major) can use herbivore-induced plant volatiles (HIPVs) as an indicator of arthropod presence. Their ability to detect HIPVs was shown to be learned, and not innate, yet the flexibility and generalization of learning remain unclear.We studied if, and if so how, naïve and trained great tits (Parus major) discriminate between herbivore-induced and noninduced saplings of Scotch elm (Ulmus glabra) and cattley guava (Psidium cattleyanum). We chemically analyzed the used plants and showed that their HIPVs differed significantly and overlapped only in a few compounds.Birds trained to discriminate between herbivore-induced and noninduced saplings preferred the herbivore-induced saplings of the plant species they were trained to. Naïve birds did not show any preferences. Our results indicate that the attraction of great tits to herbivore-induced plants is not innate, rather it is a skill that can be acquired through learning, one tree species at a time.We demonstrate that the ability to learn to associate HIPVs with food reward is flexible, expressed to both tested plant species, even if the plant species has not coevolved with the bird species (i.e., guava). Our results imply that the birds are not capable of generalizing HIPVs among tree species but suggest that they either learn to detect individual compounds or associate whole bouquets with food rewards.

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Amo, L., Dicke, M., & Visser, M. E. (2016). Are naïve birds attracted to herbivore‐induced plant defences? Behaviour, 153, 353–366.

Amo, L., Jansen, J. J., Dam, N. M., Dicke, M., & Visser, M. E. (2013). Birds exploit herbivore‐induced plant volatiles to locate herbivorous prey. Ecology Letters, 16, 1348–1355. 10.1111/ele.12177 PubMed DOI

Amo, L., Rodríguez‐Gironés, M. Á., & Barbosa, A. (2013). Olfactory detection of dimethyl sulphide in a krill‐eating Antarctic penguin. Marine Ecology Progress Series, 474, 277–285. 10.3354/meps10081 DOI

Anderson‐Teixeira, K. J., Davies, S. J., Bennett, A. C., Gonzalez‐Akre, E. B., Muller‐Landau, H. C., Joseph Wright, S., Joseph Wright, S., Abu Salim, K., Almeyda Zambrano, A. M., Alonso, A., Baltzer, J. L., Basset, Y., Bourg, N. A., Broadbent, E. N., Brockelman, W. Y., Bunyavejchewin, S., Burslem, D. F. R. P., Butt, N., Cao, M., … Zimmerman, J. (2015). CTFS‐Forest GEO: A worldwide network monitoring forests in an era of global change. Global Change Biology, 21, 528–549. 10.1111/gcb.12712 PubMed DOI

Bonadonna, F., Caro, S., Jouventin, P., & Nevitt, G. (2006). Evidence that blue petrel, Halobaena caerulea, fledglings can detect and orient to dimethyl sulfide. Journal of Experimental Biology, 209, 2165–2169. PubMed

Brooks, M. E., Kristensen, K., van Benthem, K. J., Magnusson, A., Berg, C. W., Nielsen, A., Skaug, H. J., Mächler, M., & Bolker, B. M. (2017). glmmTMB balances speed and flexibility among packages for zero‐inflated generalized linear mixed modeling. The R Journal, 9, 378–400. 10.32614/RJ-2017-066 DOI

Cai, X.‐M., Sun, X.‐L., Dong, W.‐X., Wang, G.‐C., & Chen, Z.‐M. (2014). Herbivore species, infestation time, and herbivore density affect induced volatiles in tea plants. Chemoecology, 24, 1–14. 10.1007/s00049-013-0141-2 DOI

Caspers, B. A., Hoffman, J. I., Kohlmeier, P., Krüger, O., & Krause, E. T. (2013). Olfactory imprinting as a mechanism for nest odour recognition in zebra finches. Animal Behaviour, 86, 85–90. 10.1016/j.anbehav.2013.04.015 DOI

Cunningham, G. B., & Nevitt, G. A. (2011). Evidence for olfactory learning in procellariiform seabird chicks. Journal of Avian Biology, 42, 85–88. 10.1111/j.1600-048X.2010.05184.x DOI

De Moraes, C. M., Lewis, W. J., Pare, P. W., Alborn, H. T., & Tumlinson, J. H. (1998). Herbivore‐infested plants selectively attract parasitoids. Nature, 393, 570–573. 10.1038/31219 DOI

Dicke, M. (2015). Herbivore‐induced plant volatiles as a rich source of information for arthropod predators: Fundamental and applied aspects. Journal of Indian Institute of Science, 95, 35–42.

Dicke, M., & Baldwin, I. T. (2010). The evolutionary context for herbivore‐induced plant volatiles: Beyond the ‘cry for help’. Trends in Plant Science, 15, 167–175. 10.1016/j.tplants.2009.12.002 PubMed DOI

Dicke, M., Sabelis, M. W., Takabayashi, J., Bruin, J., & Posthumus, M. A. (1990). Plant strategies of manipulating predator‐prey interactions through allelochemicals: Prospects for application in pest control. Journal of Chemical Ecology, 16, 3091–3118. 10.1007/BF00979614 PubMed DOI

Dicke, M., Takabayashi, J., Posthumus, M. A., Schütte, C., & Krips, O. E. (1998). Plant—Phytoseiid interactions mediated by herbivore‐induced plant volatiles: Variation in production of cues and in responses of predatory mites. Experimental and Applied Acarology, 22, 311–333.

Dicke, M., & van Loon, J. J. A. (2000). Multitrophic effects of herbivore‐induced plant volatiles in an evolutionary context. Entomologia Experimentalis Et Applicata, 97, 237–249. 10.1046/j.1570-7458.2000.00736.x DOI

Dicke, M., van Loon, J. J., & Soler, R. (2009). Chemical complexity of volatiles from plants induced by multiple attack. Nature Chemical Biology, 5, 317–324. 10.1038/nchembio.169 PubMed DOI

Fox, J., & Weisberg, S. (2018). An R companion to applied regression. Sage publications.

Girling, R. D., Stewart‐Jones, A., Dherbecourt, J., Staley, J. T., Wright, D. J., & Poppy, G. M. (2011). Parasitoids select plants more heavily infested with their caterpillar hosts: A new approach to aid interpretation of plant headspace volatiles. Proceedings of the Royal Society B: Biological Sciences, 278(1718), 2646–2653. 10.1098/rspb.2010.2725 PubMed DOI PMC

Gwinner, H., & Berger, S. (2008). Starling males select green nest material by olfaction using experience‐independent and experience‐dependent cues. Animal Behaviour, 75, 971–976. 10.1016/j.anbehav.2007.08.008 DOI

Hare, J. D. (2011). Ecological role of volatiles produced by plants in response to damage by herbivorous insects. Annual Reviews of Entomology, 56, 161–180. 10.1146/annurev-ento-120709-144753 PubMed DOI

Kallenbach, M., Veit, D., Eilers, E. J., & Schuman, M. C. (2015). Application of Silicone Tubing for Robust, Simple, High‐throughput, and Time‐resolved Analysis of Plant Volatiles in Field Experiments. Bio‐Protocol, 5, e1391, 1–13. 10.21769/BioProtoc.1391 PubMed DOI PMC

Klimm, F. S., Weinhold, A., & Volf, M. (2020). Volatile production differs between oak leaves infested by leaf‐miner Phyllonorycter harrisella (Lepidoptera: Gracillariidae) and galler Neuroterus quercusbaccarum (Hymenoptera: Cynipidae). European Journal of Entomology, 117, 101–109. 10.14411/eje.2020.011 DOI

Koski, T. M., Laaksonen, T., Mäntylä, E., Ruuskanen, S., Li, T., Girón‐Calva, P. S., Huttunen, L., Blande, J. D., Holopainen, J. K., & Klemola, T. (2015). Do insectivorous birds use volatile organic compounds from plants as olfactory foraging cues? Three experimental tests. Ethology, 121, 1131–1144. 10.1111/eth.12426 DOI

Kuhl, C., Tautenhahn, R., Bottcher, C., Larson, T. R., & Neumann, S. (2012). CAMERA: An integrated strategy for compound spectra extraction and annotation of liquid chromatography/mass spectrometry data sets. Analitical Chemistry, 84, 283–289. 10.1021/ac202450g PubMed DOI PMC

Lenth, R. V. (2007). Statistical power calculations. Journal of Animal Science, 85, E24–E29. PubMed

Li, G., Bartram, S., Guo, H., Mithöfer, A., Kunert, M., & Boland, W. (2019). SpitWorm, a herbivorous robot: Mechanical leaf wounding with simultaneous application of salivary components. Plants, 8, 318. 10.3390/plants8090318 PubMed DOI PMC

Mäntylä, E., Alessio, G. A., Blande, J. D., Heijari, J., Holopainen, J. K., Laaksonen, T., Piirtola, P., & Klemola, T. (2008). From plants to birds: Higher avian predation rates in trees responding to insect herbivory. PLoS One, 3, 2832. 10.1371/journal.pone.0002832 PubMed DOI PMC

Mäntylä, E., Kipper, S., & Hilker, M. (2020). Insectivorous birds can see and smell systemically herbivore‐induced pines. Ecology and Evolution, 10, 9358–9370. 10.1002/ece3.6622 PubMed DOI PMC

Mäntylä, E., Kleier, S., Kipper, S., & Hilker, M. (2016). The attraction of insectivorous tit species to herbivore‐damaged Scots pines. Journal of Ornithology, 158, 479–491.

Mäntylä, E., Klemola, T., & Haukioja, E. (2004). Attraction of willow warblers to sawfly‐damaged mountain birches: Novel function of inducible plant defences? Ecology Letters, 7, 915–918. 10.1111/j.1461-0248.2004.00653.x DOI

Mennerat, A., Bonadonna, F., Perret, P., & Lambrechts, M. (2005). Olfactory conditioning experiments in a food‐searching passerine bird in semi‐natural conditions. Behavioural Processes, 70, 264–270. 10.1016/j.beproc.2005.07.005 PubMed DOI

Mrazova, A., & Sam, K. (2018). Application of methyl jasmonate to grey willow (Salix cinerea) attracts insectivorous birds in nature. Arthropod‐Plant Interactions, 12, 1–8. 10.1007/s11829-017-9558-9 DOI

Mrazova, A., Sam, K., & Amo, L. (2019). What do we know about birds’ use of plant volatile cues in tritrophic interactions? Current Opininions in Insect Science, 32, 131–136. 10.1016/j.cois.2019.02.004 PubMed DOI

Mullié, W. C. (2009). Birds, locusts and grasshoppers. In Zwarts L., Bijlsma R. G., van der Kamp J. & Wymenga E. (Eds.), Living on the Edge (pp. 202–223). KNNV Publishing.

Mumm, R., & Dicke, M. (2010). Variation in natural plant products and the attraction of bodyguards involved in indirect plant defense. Canadian Journal of Zoology, 88, 628–667.

Murakami, M. (1998). Foraging habitat shift in the narcissus flycatcher, Ficedulanarcissina, due to the response of herbivorous insects to the strengthening defenses of canopy trees. Ecological Research, 13, 73–82.

Murakami, M. (2002). Foraging mode shifts of four insectivorous bird species under temporally varying resource distribution in a Japanese deciduous forest. Ornithological Science, 1, 63–69. 10.2326/osj.1.63 DOI

Nevitt, G., & Dittman, A. (1998). A new model for olfactory imprinting in salmon. Integrative Biology: Issues, News, and Reviews: Published in Association with the Society for Integrative and Comparative Biology, 1, 215–223. 10.1002/(SICI)1520-6602(1998)1:6<215:AID-INBI3>3.0.CO;2-V DOI

Pisani Gareau, T. L., Letourneau, D. K., & Shennan, C. (2013). Relative densities of natural enemy and pest insects within California hedgerows. Environmental Entomology, 42, 688–702. 10.1603/EN12317 PubMed DOI

Royama, T. (1970). Factors governing the hunting behaviour and selection of food by the great tit (Parus major L.). Journal of Animal Ecology, 39(3), 619–668. 10.2307/2858 DOI

Semke, E., Distel, H., & Hudson, R. (1995). Specific enhancement of olfactory receptor sensitivity associated with foetal learning of food odors in the rabbit. Naturwissenschaften, 82, 148–149. 10.1007/BF01177279 PubMed DOI

Sneddon, H., Hadden, R., & Hepper, P. (1998). Chemosensory learning in the chicken embryo. Physical Behaviour, 64, 133–139. 10.1016/S0031-9384(98)00037-7 PubMed DOI

Steidle, J. L., & Van Loon, J. J. (2003). Dietary specialization and infochemical use in carnivorous arthropods: Testing a concept. Entomologial Experimentalis Et Applicata, 108, 133–148. 10.1046/j.1570-7458.2003.00080.x DOI

Takabayashi, J., Takahashi, S., Dicke, M., & Posthumus, M. (1995). Developmental stage of herbivore Pseudaletia separata affects production of herbivore‐induced synomone by corn plants. Journal of Chemical Ecology, 21, 273–287. 10.1007/BF02036717 PubMed DOI

Vallat, A., Gu, H., & Dorn, S. (2005). How rainfall, relative humidity and temperature influence volatile emissions from apple trees in situ. Phytochemistry, 66, 1540–1550. 10.1016/j.phytochem.2005.04.038 PubMed DOI

Vesey‐FitzGerald, D. F. (1955). Birds as predators of the red locust: (Nomadacris septemfasciata Serv.). Ostrich, 26(2), 128–133. 10.1080/00306525.1955.9633036 DOI

Vet, L. E. M., & Dicke, M. (1992). Ecology of infochemical use by natural enemies in a tritrophic context. Annual Reviews of Entomology, 37, 141–172. 10.1146/annurev.en.37.010192.001041 DOI

Vet, L. E., Lewis, W. J., & Carde, R. T. (1995). Parasitoid foraging and learning. In Carde R. T. & Bell W. J. (Eds.), Chemical ecology of insects 2 (pp. 65‐101). Boston, MA: Springer.

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