Modeling the Adaptive Role of Negative Signaling i

Authors: Brian R Johnson James C Nieh

Publish Date: 2010/09/14

Volume: 23, Issue: 6, Pages: 459-471

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Abstract

Collective decision making in the social insects often proceeds via feedback cycles based on positive signaling Negative signals have however been found in a few contexts in which costs exist for paying attention to no longer useful information Here we incorporate new research on the specificity and context of the negative stop signal into an agent based model of honey bee foraging to explore the adaptive basis of negative signaling in the dance language Our work suggests that the stop signal by acting as a counterbalance to the waggle dance allows colonies to rapidly shut down attacks on other colonies This could be a key adaptation as the costs of attacking a colony strong enough to defend itself are significantFeedback cycles are key to biological processes ranging from the control of gene transcription to maintaining physiological homeostasis to pattern formation and collective decision making in animal societies Kitano 2002 Franks et al 2002 Kholodenko 2006 Sumpter 2006 Detrain and Deneubourg 2006 Marshall and Franks 2009 Becker et al 2010 Although positive and negative signaling can work together in such processes most are thought to be based on positive signaling alone The dance language of the honey bees provides a classic example Seeley 1995 Passino and Seeley 2006 Foragers who find a rich food source inform their nestmates of its location with the waggle dance reviewed in Seeley 1989 1995 Passino and Seeley 2006 This signal leads to a rapid build up of new individuals visiting the food resource as new recruits subsequently dance themselves Positive feedback ceases and new recruitment stops when the food source becomes depleted and recruits cease dancing on their return to the nest von Frisch 1967 Seeley 1995 The waggle dance signal is thus capable of allocating workers to flower patches without the aid of a negative signal to counterbalance its effects The honey bee however does have a negative signal the stop signal which causes waggle dancing bees to stop dancing Kirchner 1993 Nieh 1993 Pastor and Seeley 2005 Lau and Nieh 2010 Nieh 2010 Because a signal to reduce recruitment seemed unnecessary the role of the stop signal within the complex syntax of the dance language was a mystery until recently Nieh 2010Whereas positive feedback signals lead to the performance of a behavior negative signals lead to the cessation of a behavior Robinson et al 2005 2008 In the pharaoh’s ant a negative trail pheromone alerts foragers that a trail is old and probably does not contain currently useful information Robinson et al 2005 2008 Recently it has been shown that the honey bee stop signal can provide negative feedback in a natural context fighting over a resource In short bees that lose fights perform large numbers of stop signals directed at bees foraging at the same site thus turning off recruitment to that site using site odor brought back on foragers’ bodies to identify dancers for the same site Nieh 2010 These studies have focused on aggression between colonies at feeders A feeder is generally a jar of sugar solution often as calorically rich as honey arranged such that a large number of bees can feed from it ad libitum The only natural context in which bees are able to feed in such a way is either robbing another colony or fighting between colonies over a dying colony Fighting over dying colonies which die from the plethora of diseases known to affect Apis mellifera Winston 1987 SchmidHempel 1998 Tarpy and Seeley 2006 is thought to be common and critical for the spread of many diseases Hence it is reasonable to assume that bees are making use of behavior that has evolved in the context of intraspecific competition when more than one colony fights over a feederAlthough it has been understudied relative to intraspecific aggressive behavior in ants honey bees commonly engage in colony level fights with their neighbors that can lead to the death of weak colonies reviewed in Winston 1987 Butler and Free 1952 As Seeley 1985 showed honey bees in the temperate zone only spend a minority of the summer foraging for nectar The rest of the time few flowers are blooming Bee keepers typically refer to such dearth periods as robbing seasons when bees fight with one another over the large stockpiles of honey each has stored Butler and Free 1952 Seeley 1985 Winston 1987 Characteristic flight behavior by robbers and intense guarding by defenders has been described Butler and Free 1952 Winston 1987 but little experimental work has been conducted as researchers are loathe to start their bees fighting as it can get out of control in the unnaturally high population densities typical of apiariesHere we explore how the recent results on the specificity and context of the stop signal affect the functioning of the much explored self organizing dance language Although the stop signal is known to play a role in normal foraging Pastor and Seeley 2005 we focus on the hypothesis that the stop signal plays a major role in intraspecific competition At the colony level the bees have to make a decision regarding the strength of a colony they could attack At the individual level the bees have only their experience at the foreign nest This consists of whether they got honey from the other nest with or without getting into a fight Thus for example if ten bees got honey with or without getting into fights but 50 got driven away by guards with a few killed then this pattern might indicate that the attacked colony is strong enough to defend itself and the attack should be called off This could theoretically be done the same way recruitment to a valuable food site is shut down by simple attenuation as fewer and fewer bees have success and fewer positive signals waggle dances are performed However in the context of robbing this could be quite costly because of the mortality of bees sent to the opposing colony Thus the stop signal should provide a selective benefit to the colony by counteracting the effect of the waggle dance when there is strong cost and little benefit associated with continued waggle dancing We test this hypothesis with simulations of intraspecific competition using an agent based model of honey bee foragingFlow diagram of the behavioral control structure for foraging honey bees Grey shading indicates behavioral states while white shading indicates a decision making procedure Black bubbles represent yes while white bubbles represent no The structure is a simplification of that of de Vries and Biesmeijer 1998 To improve readability some connections are replaced with a color coding pattern to indicate the next transition After Delay2 for example the bee transitions to scouting which then results in leaving the nest and either finding a site or not The other two examples of transitioning to scouting are shaded the same color to indicate that their following acts are identical This choice was made because including lines to the next state in these cases would decrease the readability of the figure Return to nectar source is treated in the same manner Find r find receiver

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