Abstract
The associative learning of spatial and reward information is generally considered an adaptive behavior of foraging animals that collect food from renewable resources. However, learning may not always maximize foraging efficiency if choosing a high-reward location accurately based on learned information imposes a time cost on the forager (speed-accuracy trade-off). To examine the effect of speed-accuracy trade-offs on associative learning, we observed bumble bees, Bombus ignitus (Smith), foraging in mixed arrays of high- and low-rewarding artificial flowers under two conditions, i.e., arrays of small flowers where bees could not easily detect the next nearest flowers on leaving a flower and arrays of large flowers where bees could easily recognize the next nearest flower. When flowers were small, bees created foraging routes by selectively incorporating the locations of high-rewarding flowers with their experience. When flowers were large, bees flew between flowers more quickly than when flowers were small, creating foraging routes without accounting for the locations of high-rewarding flowers. Estimated foraging efficiency was higher when flowers were large than when they were small, at least until flower visitation number reached 3000, suggesting that rapid foraging might be a better choice than accurate foraging when individuals are able to locate flowers easily. These results suggest that associative learning of spatial and reward information might be a choice that foragers can apply according to the cost-benefit balance of learning.
Significance statement
Previous studies focusing on spatial-reward associative learning in foraging animals assumed that foraging efficiency increased as the forager learned the locations of greater rewards. However, this study suggests that bumble bees learn the location of high-rewarding flowers depending on the cost–benefit balance of learning, irrespective of the opportunity or their aptitude for learning. Thus, learning might be a choice that foragers can apply according to the circumstances.
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Change history
02 August 2017
An erratum to this article has been published.
References
Aiello LC, Wheeler P (1995) The expensive-tissue hypothesis: the brain and the digestive system in human and primate evolution. Curr Anthropol 36:99–221. doi:10.1086/204350
Blarer A, Keasar T, Shmida A (2002) Possible mechanisms for the formation of flower size preferences by foraging bumble bees. Ethology 108:345–351. doi:10.1046/j.1439-0310.2002.00778.x
Brink DW, deWet JMJ (1980) Interpopulation variation in nectar production in Aconitum columbianum (Ranunculaceae). Oecologia 47:160–163. doi:10.1007/BF00346814
Broström G (2013) glmmML: generalized linear models with clustering. R package version 1.0. https://CRAN.R-project.org/package=glmmML
Burns JG (2005) Impulsive bees forage better: the advantage of quick, sometimes inaccurate foraging decisions. Anim Behav 70:1–5. doi:10.1016/j.anbehav.2005.06.002
Burns JG, Rodd FH (2008) Hastiness, brain size and predation regime affect the performance of wild guppies in a spatial memory task. Anim Behav 76:911–922. doi:10.1016/j.anbehav.2008.02.017
Burns JG, Thomson JD (2005) A test of spatial memory and movement patterns of bumblebees at multiple spatial and temporal scales. Behav Ecol 17:48–55. doi:10.1093/beheco/arj002
Cartar RV (2004) Resource tracking by bumble bees: responses to plant-level differences in quality. Ecology 85:2764–2771. doi:10.1890/03-0484
Chittka L, Spaethe J (2007) Visual search and the importance of time in complex decision making by bees. Arthropod Plant Interact 1:37–44. doi:10.1007/s11829-007-9001-8
Chittka L, Dyer AG, Bock F, Dornhous A (2003) Bees trade off foraging speed for accuracy. Nature 424:388. doi:10.1038/424388a
Chittka L, Skorupski P, Raine NE (2009) Speed-accuracy tradeoffs in animal decision making. Trends Ecol Evol 24:400–407. doi:10.1098/rspb.2010.1624
Cody ML (1971) Finch flocks in the Mohave desert. Theor Popul Biol 2:142–158. doi:10.1016/0040-5809(71)90012-8
Cresswell JE, Robertson A (1994) Discrimination by pollen-collecting bumble bees among differentially rewarding flowers of an alpine wildflower, Campanula rotundifolia (Campanulaceae). Oikos 69:304–308. doi:10.2307/3546151
Davies NB, Houston AI (1981) Owners and satellites: the economics of territory defence in the pied wagtail, Motacilla alba. J Anim Ecol 50:157–180. doi:10.2307/4038
Endress PK (1994) Diversity and evolutionary biology of tropical flowers. Cambridge University Press, Cambridge, p 511
Farris SM, Robert NS (2005) Coevolution of generalist feeding ecologies and gyrencephalic mushroom bodies in insects. P Natl Acad Sci USA 102:17394–17399. doi:10.1073/pnas.0508430102
Gill FB (1988) Trapline foraging by hermit hummingbirds: competition for an undefended, renewable resource. Ecology 69:1933–1942. doi:10.2307/1941170
Goulsin D, Peat J, Stout JC, Tucker J, Darvill B, Derwent LR, Hughes WHO (2002) Can alloethism in workers of the bumblebee, Bombus terrestris, be explained in terms of foraging efficiency? Anim Behav 64:123–130. doi:10.1006/anbe.2002.3041
Heinrich B (1979) Bumble bee economics. Harvard University Press, Cambridge, p 245
Heitz RP (2014) The speed-accuracy tradeoff: history, physiology, methodology, and behavior. Front Neurosci 8:150. doi:10.3389/fnins.2014.00150
Ings TC, Ward NL, Chittka L (2006) Can commercially imported bumble bees out-compete their native conspecifics? J Appl Ecol 43:940–948. doi:10.1111/j.1365-2664.2006.01199.x
Ishii HS, Harder LD (2006) The size of individual Delphinium flowers and the opportunity for geitonogamous pollination. Funct Ecol 20:1115–1123. doi:10.1111/j.1365-2435.2006.01181.x
Ishii HS, Masuda H (2014) Effect of flower visual angle on flower constancy: a test of the search image hypothesis. Behav Ecol 25:933–944. doi:10.1093/beheco/aru071
Isler K, Schaik CP (2009) The expensive brain: a framework for explaining evolutionary changes in brain size. J Hum Evol 57:392–400. doi:10.1016/j.jhevol.2009.04.009
Janson CH (1998) Experimental evidence for spatial memory in foraging wild capuchin monkeys, Cebus paella. Anim Behav 55:1229–1243. doi:10.1006/anbe.1997.0688
Kudoh H, Whigham FD (1998) The effect of petal size manipulation on pollinator/seed-predator mediated female reproductive success of Hibiscus moscheutos. Oecologia 117:70–79. doi:10.1007/s004420050633
Kuznetsova A, Brockhoff PB, Christensen RHB (2016) lmerTest: tests in linear mixed effects models. R package version 2.0–33. https://CRAN.R-project.org/package=lmerTest
Kwak MM, Bergman P (1996) Early flowers of Bartsia alpina (Scrophulariaceae) and the visitation by bumblebees. Acta Bot Neerl 45:355–366. doi:10.1111/j.1438-8677.1996.tb00522.x
Laughlin SB (2001) Energy as a constraint on the coding and processing of sensory information. Curr Opin Neurobiol 11:475–480. doi:10.1016/S0959-4388(00)00237-3
Laverty TM (1994) Bumble bee learning and flower morphology. Anim Behav 47:531–545. doi:10.1006/anbe.1994.1077
Laverty TM, Plowright RC (1988) Flower handling by bumblebees: a comparison of specialists and generalists. Anim Behav 36(3):733–740
Lefebvre L, Whittle P, Lascaris E, Finkelstein A (1997) Feeding innovations and forebrain size in birds. Anim Behav 53:540–560. doi:10.1006/anbe.1996.0330
Lihoreau M, Chittka L, Raine NE (2011) Trade-off between travel distance and prioritization of high-reward sites in traplining bumblebees. Funct Ecol 25:1284–1292. doi:10.1111/j.1365-2435.2011.01881.x
Lihoreau M, Chittka L, Le Comber SC, Raine NE (2012) Bees do not use nearest-neighbour rules for optimization of multilocation routes. Biol Lett 8:13–16. doi:10.1098/rsbl.2011.0661
Makino TT, Ohashi K (2016) Honest signals to maintain a long-lasting relationship: floral colour change prevents plant-level avoidance by experienced pollinators. Funct Ecol (in press). doi:10.1111/1365-2435.12802
Makino TT, Sakai S (2007) Experience changes pollinator responses to floral display size: from size-based to reward-based foraging. Funct Ecol 21:854–863. doi:10.1111/j.1365-2435.2007.01293.x
Manning A (1956) Some aspects of the foraging behaviour of bumble-bees. Behaviour 9:164–201. doi:10.1163/156853956X00291
Mery F, Kawecki TJ (2004) An operating cost of learning in Drosophila melanogaster. Anim Behav 68:589–598. doi:10.1016/j.anbehav.2003.12.005
Michener CD (2000) The bees of the world. Johns Hopkins University Press, Baltimore, p 992
Muth F, Keasar T, Dornhaus A (2015) Trading off short-term costs for long-term gains: how do bumble bees decide to learn morphologically complex flowers? Anim Behav 101:191–199. doi:10.1016/j.anbehav.2014.12.024
Ohashi K, Thomson JD (2005) Efficient harvesting of renewing resources. Behav Ecol 16:592–605. doi:10.1093/beheco/ari031
Ohashi K, Thomson JD (2012) Trapline foraging by bumble bees: VI. Behavioral alterations under speed–accuracy trade-offs. Behav Ecol 24:182–189. doi:10.1093/beheco/ars152
Ohashi K, Leslie A, Thomson JD (2008) Trapline foraging by bumble bees: V. Effects of experience and priority on competitive performance. Behav Ecol 19:936–948. doi:10.1093/beheco/arn048
Ohashi K, Leslie A, Thompson JD (2012) Trapline foraging by bumble bees: VII. Adjustments for foraging success following competitor removal. Behav Ecol 24:768–778. doi:10.1093/beheco/ars200
Paton DC, Carpenter FL (1984) Peripheral foraging by territorial rufous hummingbirds—defense by exploitation. Ecology 65:1808–1819. doi:10.2307/1937777
Pinheiro J, Bates D, DebRoy S, Sarkar D, R Development Core Team (2016) nlme: linear and nonlinear mixed effects models. R package version 3.1–128, http://CRAN.R-project.org/package=nlme
Pleasants JM, Chaplin SJ (1983) Nectar production rates of Asclepias quadrifolia: causes and consequences of individual variation. Oecologia 59:232–238. doi:10.1007/BF00378842
R Development Core Team (2015) R: A language and environment for statistical computing R Foundation for Statistical Computing, Vienna
Possingham H (1989) The distribution and abundance of resources encountered by a forager. Am Nat 133:42–60. doi:10.1086/284900
Reader SM, Laland KN (2002) Social intelligence, innovation, and enhanced brain size in primates. P Natl Acad Sci USA 99:4436–4441. doi:10.1073/pnas.062041299
Rothman DL, Sibson NR, Hyder F, Shen J, Behar KL, Shulman RG (1999) In vivo nuclear magnetic resonance spectroscopy studies of the relationship between the glutamate-glutamine neurotransmitter cycle and functional neuroenergetics. Philos T Roy Soc B 354:1165–1177. doi:10.1098/rstb.1999.0472
Safi K, Seid MA, Dechmann DKN (2005) Bigger is not always better: when brains get smaller. Biol Lett 1:283–286. doi:10.1098/rsbl.2005.0333
Saleh N, Chittka L (2007) Traplining in bumblebees (Bombus impatiens): a foraging strategy’s ontogeny and the importance of spatial reference memory in short-range foraging. Oecologia 151:719–730. doi:10.1007/s00442-006-0607-9
Schulke O (2003) To breed or not to breed—food competition and other factors involved in female breeding decisions in the pairliving nocturnal fork-marked lemur (Phaner furcifer). Behav Ecol Sociobiol 55:11–21. doi:10.1007/s00265-003-0676-2
Sibson NR, Dhankar A, Mason GF, Rothman DL, Behar KL, Shulman RG (1998) Stoichiometric coupling of brain glucose metabolism and glutamatergic neuronal activity. P Natl Acad Sci USA 95:316–321
Sivinski J (1989) Mushroom body development in nymphalid butterflies: a correlate of learning? J Insect Behav 2:277–283. doi:10.1007/BF01053299
Sol D, Duncan RP, Blackburn TM, Cassey P, Lefebvre L (2005) Big brains, enhanced cognition, and response of birds to novel environments. P Natl Acad Sci USA 102:5460–5465. doi:10.1073/pnas.0408145102
Spaethe J, Chittka L (2003) Interindividual variation of eye optics and single object resolution in bumble bees. J Exp Biol 206:3447–3453. doi:10.1242/jeb.00570
Stout JC, Goulson D (2001) The use of conspecific and interspecific scent marks by foraging bumblebees and honeybees. Anim Behav 62:183–189. doi:10.1006/anbe.2001.1729
Thomson JD, Slatkin M, Thomson B (1997) Trapline foraging in bumble bees: II. Definition and detection from sequence data. Behav Ecol 8:199–210. doi:10.1093/beheco/8.2.199
Wertlen AM, Niggebrugge C, Vorobyev M, Hempel de Ibarra N (2008) Detection of patches of coloured discs by bees. J Exp Biol 211:2101–2104. doi:10.1242/jeb.014571
Wickelgren WA (1977) Speed-accuracy tradeoff and information processing dynamics. Acta Psychol 41:67–85. doi:10.1016/0001-6918(77)90012-9
Williams NM, Thomson JD (1998) Trapline foraging by bumble bees: III. Temporal patterns of visitation and foraging success at single plants. Behav Ecol 9:612–621. doi:10.1093/beheco/9.6.612
Acknowledgements
We are grateful to the Itabashi Ward Firefly Breeding Institute for providing bumble bee colonies. We thank M.P. Tokue, Y.D. Nakamura, and especially N. Mizumaki for their assistance in the experiment, A. Ushimaru and K. Ohashi for insightful discussions about this study, and T.T. Makino for advice on using artificial flowers. We also thank the editor and two anonymous reviewers for their useful comments on this manuscript. This study was supported by the Japan Society for the Promotion of Science, through KAKENHI Grants allocated to S.G.T (JP15J06079) and to H.S.I. (JP23770017 and JP15K07216). All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
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The original version of this article was revised: the name of Hiroshi S. Ishii was incorrectly presented as Hiroshi H. Ishii.
An erratum to this article is available at https://doi.org/10.1007/s00265-017-2354-9.
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Tsujimoto, S.G., Ishii, H.S. Effect of flower perceptibility on spatial-reward associative learning by bumble bees. Behav Ecol Sociobiol 71, 105 (2017). https://doi.org/10.1007/s00265-017-2328-y
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DOI: https://doi.org/10.1007/s00265-017-2328-y