Abstract
A key question in pollination biology is that of how pollinators identify and choose foraging patches. Several approaches have been employed for this, including field studies and large greenhouse flight chambers. Most methods used to date are limited, though, by reliance on a combination of artificial flowers, large spatial scales, or lack of spatially distinct floral patches. To address this issue, we designed and tested a y-maze flight arena and tested it using the bumblebee Bombus impatiens and canola plants. Our results indicate that the system is not biased by environmental conditions, or by an innate “handedness” of Bombus impatiens. We found that bees made all the expected patch choices when presented with soil, plants without flowers, or plants with flowers. This new method is important and useful as it allows researchers to ask questions of both plant health and insect behavior and the chamber system is modular allowing for simple changes to the setup to focus on different questions.
Highlights
• Y-maze flight arena was designed to evaluate foraging behavior on intact plants.
• No evidence of side preference in individual bees.
• Behaviors observed in the y-maze appear to correspond to behaviors observed in other settings.
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Data Availability
Data is available in the Mendeley Data Repository accessed through https://data.mendeley.com/datasets/p8635n3x3t/1.
References
Abada EAE, Sung H, Dwivedi M et al (2009) C. elegans behavior of preference choice on bacterial food. Mol Cells 28:209–213. https://doi.org/10.1007/s10059-009-0124-x
Adler LS, Wink M, Distl M, Lentz AJ (2006) Leaf herbivory and nutrients increase nectar alkaloids. Ecol Lett 9:960–967. https://doi.org/10.1111/j.1461-0248.2006.00944.x
Amaya Márquez M (2009) Memoria y aprendizaje en la escogencia floral de las abejas. Acta Biol Colomb 14:125–136
Austin MW, Horack P, Dunlap AS (2019) Choice in a floral marketplace: the role of complexity in bumble bee decision-making. Behav Ecol 30:500–508. https://doi.org/10.1093/beheco/ary190
Avarguès-Weber A, Lachlan R, Chittka L (2018) Bumblebee social learning can lead to suboptimal foraging choices. Anim Behav 135:209–214. https://doi.org/10.1016/j.anbehav.2017.11.022
Bates D, Mächler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Cartar RV, Abrahams MV (1996) Risk-sensitive foraging in a patch departure context: a test with worker bumble bees. Am Zoo 36:447–458. https://doi.org/10.1093/icb/36.4.447
Cartar RV, Dill LM (1990) Colony energy requirements affect the foraging currency of bumble bees. Behav Ecol Sociobiol 27:377–383. https://doi.org/10.1007/BF00164009
Cartar RV, Real LA (1997) Habitat structure and animal movement: the behaviour of bumble bees in uniform and random spatial resource distributions. Oecologia 112:430–434. https://doi.org/10.1007/s004420050329
Carvell C, Osborne JL, Bourke AFG, Freeman SN, Pywell RF, Heard MS (2011) Bumble bee species’ responses to a targeted conservation measure depend on landscape context and habitat quality. 21:1760–1771. https://doi.org/10.1890/10-0677.1
Chittka L (2017) Bee cognition. Curr Biol 27:1049–1053. https://doi.org/10.1016/j.cub.2017.08.008
Chittka L, Stelzer RJ, Stanewsky R (2013) Daily changes in ultraviolet light levels can synchronize the circadian clock of bumblebees (Bombus terrestris). 30:434–442. https://doi.org/10.3109/07420528.2012.741168
Cibula DA, Zimmerman M (1987) Bumblebee foraging behavior: changes in departure decisions as a function of experimental nectar manipulations. Am Midl Nat 117:386–394. https://doi.org/10.2307/2425981
Comba L (1999) Patch use by bumblebees (Hymenoptera Apidae): temperature, wind, flower density and traplining. Ethol Ecol Evol 11:243–264. https://doi.org/10.1080/08927014.1999.9522826
Conrad CD, Galea LAM, Kuroda Y, McEwen BS (1996) Chronic stress impairs rat spatial memory on the Y-maze, and this effect is blocked by tianeptine treatment. Behav Neurosci 110:1321–1334. https://doi.org/10.1037//0735-7044.110.6.1321
Dunbar RIM (1995) Neocortex size and group size in primates: a test of the hypothesis. J Hum Evol 28:287–296. https://doi.org/10.1006/jhev.1995.1021
Dyer AG, Whitney HM, Arnold SEJ et al (2007) Mutations perturbing petal cell shape and anthocyanin synthesis influence bumblebee perception of Antirrhinum majus flower colour. Arthropod Plant Interact. https://doi.org/10.1007/s11829-007-9002-7
Dyer AG, Spaethe J, Prack S (2008) Comparative psychophysics of bumblebee and honeybee colour discrimination and object detection. J Comp Physiol A Neuroethol Sensory Neural Behav Physiol 194:617–627. https://doi.org/10.1007/s00359-008-0335-1
Fordyce JA, Gompert Z, Forister ML, Nice CC (2011) A hierarchical bayesian approach to ecological count data: a flexible tool for ecologists. PLoS ONE 6:1–7. https://doi.org/10.1371/journal.pone.0026785
Francis JS, Muth F, Papaj DR, Leonard AS (2016) Nutritional complexity and the structure of bee foraging bouts. Behav Ecol 27:903–911. https://doi.org/10.1093/beheco/arv229
Friard O, Gamba M (2016) BORIS: a free, versatile open-source event-logging software for video/audio coding and live observations. Methods Ecol Evol 7:1325–1330. https://doi.org/10.1111/2041-210X.12584
Galen C, Green B (1987) Bumble bee behavior and selection on flower size in the sky pilot, Polemonium viscosum. Oecologia 74:20–23. https://doi.org/10.1007/BF00377340
Goulson D (2000) Why do pollinators visit proportionally fewer flowers in large patches? Oikos 91:485–492. https://doi.org/10.1034/j.1600-0706.2000.910309.x
Groen SC, Jiang S, Murphy AM et al (2016) Virus infection of plants alters pollinator preference: a payback for susceptible hosts? PLoS Pathog 12:1–28. https://doi.org/10.1371/journal.ppat.1005790
Gumbert A (2000) Color choices by bumble bees (Bombus terrestris): innate preferences and generalization after learning. Behav Ecol Sociobiol 48:36–43. https://doi.org/10.1007/s002650000213
Hagen M, Wikelski M, Kissling WD (2011) Space use of bumblebees (Bombus spp.) revealed by radio-tracking. PLoS ONE 6(5). https://doi.org/10.1371/journal.pone.0019997
Jacobsen DJ, Raguso RA (2018) Lingering effects of herbivory and plant defenses on pollinators. Curr Biol 28:1164–1169. https://doi.org/10.1016/j.cub.2018.08.010
James RR, Pitts-Singer TL (2008) Bee pollination in agricultural ecosystems. Oxford University Press
Jaworski CC, Andalo C, Raynaud C et al (2015) The influence of prior learning experience on pollinator choice: an experiment using bumblebees on two wild floral types of Antirrhinum majus. PLoS ONE 10. https://doi.org/10.1371/journal.pone.0130225
Kaczorowski RL, Leonard AS, Dornhaus A, Papaj DR (2012) Floral signal complexity as a possible adaptation to environmental variability: a test using nectar-foraging bumblebees, Bombus impatiens Anim Behav 83:905–913. https://doi.org/10.1016/j.anbehav.2012.01.007
Kapustjansky A, Chittka L, Spaethe J (2010) Bees use three-dimensional information to improve target detection. Naturwissenschaften 97:229–233. https://doi.org/10.1007/s00114-009-0627-5
Klatt BK, Burmeister C, Westphal C et al (2013) Flower volatiles, crop varieties and bee responses. PLoS ONE 8(8). https://doi.org/10.1371/journal.pone.0072724
Lawson DA, Chittka L, Whitney HM, Rands SA (2018) Bumblebees distinguish floral scent patterns, and can transfer these to corresponding visual patterns. Proc R Soc B Biol Sci 285. https://doi.org/10.1098/rspb.2018.0661
Lee PG (1992) Chemotaxis by Octopus maya Voss et Solis in a Y-maze. J Exp Mar Bio Ecol 156:53–67. https://doi.org/10.1016/0022-0981(92)90016-4
Lefebvre D, Pierre J, Outreman Y, Pierre JS (2007) Patch departure rules in bumblebees: evidence of a decremental motivational mechanism. Behav Ecol Sociobiol 61:1707–1715. https://doi.org/10.1007/s00265-007-0402-6
Leonard AS, Masek P (2014) Multisensory integration of colors and scents: insights from bees and flowers. J Comp Physiol A Neuroethol Sensory Neural Behav Physiol 200:463–474. https://doi.org/10.1007/s00359-014-0904-4
Leonard AS, Dornhaus A, Papaj DR (2011) Forget-me-not: complex floral displays, inter-signal interactions, and pollinator cognition. Curr Zool 57:215–224. https://doi.org/10.1093/czoolo/57.2.215
Lichtenstein L, Sommerlandt FMJ, Spaethe J (2015) Dumb and lazy? A comparison of color learning and memory retrieval in drones and workers of the buff-tailed bumblebee, Bombus terrestris, by means of per conditioning. PLoS ONE 10:1–18. https://doi.org/10.1371/journal.pone.0134248
Losey JE, Vaughan M (2006) The economic value of ecological services provided by insects. Bioscience 56:311–323. https://doi.org/10.1641/0006-3568(2006)56[311:TEVOES]2.0.CO;2
Manríquez PH, Jara ME, Mardones ML et al (2014) Ocean acidification affects predator avoidance behaviour but not prey detection in the early ontogeny of a keystone species. Mar Ecol Prog Ser 502:157–167. https://doi.org/10.3354/meps10703
Minahan DF, Brunet J (2018) Strong interspecific differences in foraging activity observed between honey bees and bumble bees using miniaturized radio frequency identification (RFID). Front Ecol Evol 6:1–10. https://doi.org/10.3389/fevo.2018.00156
Morandin LA, Laverty TM, Gegear RJ, Kevan PG (2002) Effect of greenhouse polyethelene covering on activity level and photo-response of bumble bees. Can Entomol 134:539–549. https://doi.org/10.4039/Ent134539-4
Muth F, Papaj DR, Leonard AS (2017) Multiple rewards have asymmetric effects on learning in bumblebees. Anim Behav 126:123–133. https://doi.org/10.1016/j.anbehav.2017.01.010
Muth F, Cooper TR, Bonilla RF, Leonard AS (2018) A novel protocol for studying bee cognition in the wild. Methods Ecol Evol 9:78–87. https://doi.org/10.1111/2041-210X.12852
Muth F, Tripodi AD, Bonilla R et al (2021) No sex differences in learning in wild bumblebees. Behav Ecol 32:638–645. https://doi.org/10.1093/beheco/arab013
National Research Council (2007) Status of pollinators in North America. https://doi.org/10.17226/11761
Odell E, Raguso RA, Jones KN (1999) Bumblebee foraging responses to variation in floral scent and color in snapdragons (Antirrhinum: Scrophulariaceae). Am Midl Nat 142:257–265. https://doi.org/10.1674/0003-0031(1999)142[0257:BFRTVI]2.0.CO;2
Pajor EA, Rushen J, De Passillé AMB (2003) Dairy cattle’s choice of handling treatments in a Y-maze. Appl Anim Behav Sci 80:93–107. https://doi.org/10.1016/S0168-1591(02)00119-3
Palmier KM, Sheffield CS (2019) First records of the common eastern bumble bee, Bombus impatiens Cresson (Hymenoptera: Apidae, Apinae, Bombini) from the Prairies Ecozone in Canada. Biodivers Data J. https://doi.org/10.3897/BDJ.7.e30953
Pearce RF, Giuggioli L, Rands SA (2017) Bumblebees can discriminate between scent-marks deposited by conspecifics. Sci Rep 7:1–11. https://doi.org/10.1038/srep43872
Potts SG, Biesmeijer JC, Kremen C et al (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353. https://doi.org/10.1016/j.tree.2010.01.007
Prager SM, Esquivel I, Trumble JT (2014) Factors influencing host plant choice and larval performance in Bactericera cockerelli. PLoS ONE 9. https://doi.org/10.1371/journal.pone.0094047
Raguso RA (2004) Flowers as sensory billboards: progress towards an integrated understanding of floral advertisement. Curr Opin Plant Biol 7:434–440. https://doi.org/10.1016/j.pbi.2004.05.010
Raine NE, Chittka L (2008) The correlation of learning speed and natural foraging success in bumble-bees. Proc R Soc B Biol Sci 275:803–808. https://doi.org/10.1098/rspb.2007.1652
Rakow G (1993) AC excel summer rape. Can J Plant Sci 73:183–184. https://doi.org/10.4141/cjps93-028
Riveros AJ, Gronenberg W (2012) Decision-making and associative color learning in harnessed bumblebees (Bombus impatiens). Anim Cogn 15:1183–1193. https://doi.org/10.1007/s10071-012-0542-6
Riveros AJ, Leonard AS, Gronenberg W, Papaj DR (2020) Learning of bimodal versus unimodal signals in restrained bumble bees. J Exp Biol 223. https://doi.org/10.1242/jeb.220103
Rivest SA, Austen EJ, Forrest JRK (2017) Foliage affects colour preference in bumblebees (Bombus impatiens): a test in a three-dimensional artificial environment. Evol Ecol 31:435–446. https://doi.org/10.1007/s10682-017-9893-4
Schiestl FP, Steinebrunner F, Schulz C et al (2006) Evolution of ’pollinator’-attracting signals in fungi. Biol Lett 2:401–404. https://doi.org/10.1098/rsbl.2006.0479
Shaw RF, Phillips BB, Doyle T et al (2020) Mass-flowering crops have a greater impact than semi-natural habitat on crop pollinators and pollen deposition. Landsc Ecol 35:513–527. https://doi.org/10.1007/s10980-019-00962-0
Spaethe J, Brockmann A, Halbig C, Tautz J (2007) Size determines antennal sensitivity and behavioral threshold to odors in bumblebee workers. Naturwissenschaften 94:733–739. https://doi.org/10.1007/s00114-007-0251-1
Strauss SY, Irwin RE, Lambrix VM (2004) Optimal defence theory and flower petal colour predict variation in the secondary chemistry of wild radish. J Ecol 94:132–141. https://doi.org/10.1111/j.1365-2745.2004.00843.x
Suchet C, Dormont L, Schatz B et al (2011) Floral scent variation in two Antirrhinum majus subspecies influences the choice of naïve bumblebees. Behav Ecol Sociobiol 65:1015–1027. https://doi.org/10.1007/s00265-010-1106-x
Waage JK (1979) Foraging for patchily-distributed hosts by the parasitoid, Nemeritis canescens J Anim Ecol 48:353–371. https://doi.org/10.2307/4166
Whitehorn PR, O’Connor S, Wackers FL, Goulson D (2012) Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science 80:351–352. https://doi.org/10.1126/science.1215025
Wink M (2017) The role of quinolizidine alkaloids in plant-insect interactions. In: Bernays E (ed) Insect-plant interactions, 1st edn. CRC Press, Boca Raton, pp 131–166. https://doi.org/10.1201/9781351271004
Woodgate JL, Makinson JC, Lim KS et al (2016) Life-long radar tracking of bumblebees. PLoS ONE 11:1–22. https://doi.org/10.1371/journal.pone.0160333
Zahuranec BJ (1983) Shark repellents from the sea: new perspectives. CRC Press, Boca Raton
Acknowledgements
We would like to thank Alicia Caplan, Farrah Fischer, and Dylan Sjolie for assistance in data collection and analysis. We thank Meghan Vankosky, Adam Jewiss-Gaines, Berenice Romero, and Dylan Sjolie for comments on this manuscript. This research was funded by an NSERC Discovery Grant to SMP.
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This research was funded by the National Engineering and Research Council of Canada via a Discovery Grant.
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Caleb Bryan and Sean Prager designed all experiments. Caleb Bryan preformed the experiments and did data analysis. Caleb Bryan and Sean Prager prepared and reviewed the manuscript.
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Bryan, C.B., Prager, S.M. Developing and Evaluating a New Method and Apparatus for Examining Bumble Bee Foraging Behavior. J Insect Behav 36, 120–132 (2023). https://doi.org/10.1007/s10905-023-09827-6
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DOI: https://doi.org/10.1007/s10905-023-09827-6