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Neuroethology of the Waggle Dance: How Followers Interact with the Waggle Dancer and Detect Spatial Information

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Neuroethology of the Waggle Dance: How Followers Interact with the Waggle Dancer and Detect Spatial Information insects Review Neuroethology of the Waggle Dance: How Followers Interact with the Waggle Dancer and Detect Spatial Information Hiroyuki Ai 1,* , Ryuichi Okada 2, Midori Sakura 2, Thomas Wachtler 3 and Hidetoshi Ikeno 4 1 Department of Earth System Science, Fukuoka University, Fukuoka 814-0180, Japan 2 Department of Biology, Kobe University, Kobe 657-8501, Japan 3 Department of Biology II, Ludwig-Maximilians-Universität München, Planegg-Martinsried 82152, Germany 4 Department of Human Science and Environment, University Hyogo, Kobe 670-0092, Japan * Correspondence: [email protected] Received: 1 September 2019; Accepted: 6 October 2019; Published: 11 October 2019 Abstract: Since the honeybee possesses eusociality, advanced learning, memory ability, and information sharing through the use of various pheromones and sophisticated symbol communication (i.e., the “waggle dance”), this remarkable social animal has been one of the model symbolic animals for biological studies, animal ecology, ethology, and neuroethology. Karl von Frisch discovered the meanings of the waggle dance and called the communication a “dance language.” Subsequent to this discovery, it has been extensively studied how effectively recruits translate the code in the dance to reach the advertised destination and how the waggle dance information conflicts with the information based on their own foraging experience. The dance followers, mostly foragers, detect and interact with the waggle dancer, and are finally recruited to the food source. In this review, we summarize the current state of knowledge on the neural processing underlying this fascinating behavior. Keywords: honeybee; waggle dance; distance information; brain; antenna-mechanosensory center; vibration; sensory processing; standard brain; computational analysis; polarized light processing 1. Behavioral Significance of the Waggle Dance The honeybee (Apis mellifera) is well known to possess the ability to communicate to its nestmates to convey the locational information of a profitable food source she has visited [1]. Once a scout bee has found a profitable food source and returned to the hive, she will perform a dance (round dance or waggle dance for a short or long distance food source, respectively) to recruit new bees to visit the food source (Figure1). During the waggle dance, the bee runs relatively straight with her body waggling (a waggle run) and circles back to the starting point of the waggle run without wagging or wing-beating (the return run). On the vertical comb, the direction to a food source from the hive relative to the sun’s azimuth is encoded according to the angle between the upward direction and the waggle run direction, and the distance from the hive to the food source is related to the duration of the waggle run [1]. Bees in close proximity to the dancing bee (followers) receive this information, and some of them may be recruited to the same food source, with many foragers ultimately visiting there [2]. Insects 2019, 10, 336; doi:10.3390/insects10100336 www.mdpi.com/journal/insects Insects 2019, 10, 336 2 of 16 Insects 2019, 10, x 2 of 15 Figure 1.1. TheThe wagglewaggle dance. dance. (A ()A A) dancerA dancer (arrow) (arrow) on theon wagglethe waggle run and run many and beesmany (followers) bees (followers) around thearound dancer. the dancer. (B) Encoding (B) Encoding a direction a direction of a food of source.a food source. The direction The direction of a waggle of a waggle run in run relation in relation to the positionto the position of the sunof the when sun dancingwhen dancing on a horizontal on a horizo combntal andcomb in and relation in relation to upwards to upwards/anti-gravity/anti-gravity when dancingwhen dancing on a vertical on a vertical comb indicatescomb indicates//representsrepresents the direction the direction of a food of a source. food source. A largelarge number number of of studies studies have have reported reported the effithecacy efficacy of the danceof the fordance food for collection food collection in a controlled in a environmentcontrolled environment [3–5]. There [3–5]. are, however, There are, only however, a few studies only a in few which studies the dancein which behavior the dance was evaluatedbehavior underwas evaluated natural conditions.under natural Sherman conditions. and Sherman Visscher [an6]d compared Visscher [6] foraging compared success foraging at natural success food at sourcesnatural food by measuring sources by the measuring mass of the experimental mass of experi colonies.mental They colonies. found They that found bees that bees were that allowed were toallowed perform to perform a dance a with dance the with directional the directional information information intact (an intact oriented (an oriented dance) dance) could could generate generate more foodmore collectionfood collection than those than who those performed who performed a dance a in dance which in the which directional the directional information information was disrupted was (adisrupted disoriented (a disoriented dance). Importantly, dance). Importantly, a significant a significant difference difference was found was only found in only winter in winter and not and in summernot in summer or autumn. or autumn. Experiments Experiments in diff inerent different habits habits within within a year a foundyear found that foragingthat foraging efficiency efficiency was substantiallywas substantially impaired impaired in a tropicalin a tropical forest, forest, but was but not was significantly not significantly impaired impaired in a temperate in a temperate habitat whenhabitat dance when information dance information was lost was [7]. Recentlost [7]. experiments Recent experiments [8] performed [8] performed in three citiesin three in threecities di inff threeerent yearsdifferent found years that found physically that preventingphysically dancepreventing communication dance communication enhanced the lossenhanced of the colony the loss weight of the in autumncolony weight (Figure in2A). autumn Although (Figure those 2A). studies Although show thatthose the studies fitness show benefits that of the the fitness dance arebenefits influenced of the bydance experimental are influenced area-, by season-, experimental year-, andarea-, colony-specific season-, year-, e andffects, colony-specific those studies effects, proposed those that studies these dancesproposed help that a beethese colony dances to findhelp food, a bee particularly colony to find in habitats food, particularly in which food in habitats is scarce. in which food is scarce.A waggle dance generally consists of more than one pair of a waggle run and a return run. ThereforeA waggle each ofdance the waggle generally runs consists conveying of directionalmore than informationone pair of containsa waggle a certainrun and range a return ( 10–15 run.) ± ◦ ofTherefore error from each a of mean the waggle direction runs of allconveying waggle runsdirectional that a information dancer performed contains [9 –a11 certain]. The range number (±10– of waggle15°) of error runs infrom a dance a mean increases direction as theof all profitability waggle runs of anthat artificial a dancer feeder performed (e.g., concentration [9–11]. The number of sucrose of solution)waggle runs increases in a dance at both increases individual as the [12 –profitabil14] and colonyity of an levels artificial [15]. Consequently,feeder (e.g., concentration the colony can of rapidlysucrose respondsolution) to increases changes at in both the foraging individual environment. [12–14] and In colony Seeley’s levels experiment [15]. Consequently, [15], two feeders the colony were placedcan rapidly 400 m respond away from to changes the hive, in onethe toforaging the south envi andronment. one to In the Seeley’s north. Theexperiment concentrations [15], two of sucrosefeeders solutionwere placed in the 400 south m away and northfrom feedersthe hive, were one 2.5 to Mthe and south 1.0 M,and respectively. one to the north. After 4The h, theconcentrations concentrations of weresucrose changed solution to 0.75in the M andsouth 2.5 and M, respectively.north feeders They were found 2.5 M that and the 1.0 colony M, respectively. altered its feeder After visitation 4 h, the habitsconcentrations in response were to thechanged change to in0.75 the M concentration and 2.5 M, respectively. of the sucrose They solution. found Mathematical that the colony modeling altered suggestsits feeder that visitation such adaptive habits in colony-level response to decision the change making in the can concentration be achieved not of by the a centralsucrose command solution. systemMathematical but on modeling an individual suggests basis that [16 such] and adaptive that the colony-level dance is beneficial decision under making such can a dynamicallybe achieved changingnot by a central environment command (Figure system2B) [ 17but,18 on]. Furthermore,an individual such basis flexible [16] and foraging that the may dance be achieved is beneficial by an errorunder in such dance a information.dynamically Simulationchanging environment experiments (F [18igure] showed 2B) [17,18]. that flexibility Furthermore, of foraging such depends flexible onforaging the degree may ofbe error.achieved When by thean error error in range dance is large,information. such as Simulation 30◦ or more, experiments the dance was [18] not showed beneficial that forflexibility food collection. of foraging When depends the error on the range degree is small, of erro suchr. asWhen 0◦ or the 5◦ ,error the successful range is large,
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