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Modeling the Adaptive Role of Negative Signaling

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 significant.
Keywords    Animal communication . collective decision making . social insects .
honey bees . task allocation
Introduction
   Feedback 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;
J Insect Behav (2010) 23:459–471 DOI 10.1007/s10905-010-9229-5
Electronic supplementary material  The online version of this article (doi:10.1007/s10905-010-9229-5) contains supplementary material, which is available to authorized users. B. R. Johnson (*) Department of Environmental Science, Policy & Management, University of California, Berkeley,245 Hilgard Hall, MC3114, Berkeley, CA 94720-3114, USAe-mail: bjohnson741@hotmail.com
J. C. NiehSection of Ecology, Behaviour, and Evolution, Division of Biological Sciences,University of California, San Diego, 9500 Gilman Dr, MC 0116, La Jolla, CA 92093-0116, USAKholodenko 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 2010).
Whereas 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; Schmid-Hempel 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 feeder.
Although  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  larges tockpiles of honey each has stored (Butler and Free 1952; Seeley 1985; Winston1987). 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 460 J Insect Behav (2010) 23:459–471can  get  out  of  control  in  the  unnaturally  high  population  densities  typical  of apiaries.
   Here 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 foraging.

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通过反馈周期建模自适应负收益的作用往往信号昆虫摘要集体决策基础上的社会积极信号。消极信号，不过，被发现在一些情况下有用的信息花费更长的存在，不重视。在这里，我们结合的舞蹈语言，探讨了自适应负信号的基础研究在新的特异性和觅食环境的负面蜜蜂停止信号转换成一个基于Agent的模型。我们的工作表明，停止信号，通过摇摆舞作为一个平衡的，允许殖民地迅速关闭其他殖民地攻击。这可能是一个关键的适应自己，以捍卫作为攻击的成本殖民地足够强大是重要的。关键词动物沟通。集体决策。社会性昆虫。蜜蜂。任务分配简介反馈周期的关键基因的转录过程控制，从生物的，以维持生理平衡，对格局的形成决策和集体决策的社会动物（北野2002;弗兰克斯等。Ĵ昆虫Behav 2002年（2010）23 :459 - 471分类号10.1007/s10905-010-9229-5电子辅助材料本品网络版（分类号：10.1007/s10905-010-9229-5）包含补充材料，这是提供给授权用户（。无线电通信局约翰逊*）环境科学系，政策及管理，邮件加州大学伯克利分校，245希尔加德厅，MC3114，加州柏克莱94720-3114，USAe -：bjohnson741@hotmail.com赛马NiehSection生态，行为及演化，司生物科学学院，美国加州大学圣地亚哥分校，9500吉尔曼博士，三菱商事0116，拉霍亚加州92093-0116，USAKholodenko 2006年桑普特2006年Detrain和Deneubourg 2006年马歇尔和弗兰克斯2009;贝克尔等人2010）。。尽管积极的和消极的信号可以在这些过程一起，被认为是最积极的信号上仅仅依据。作者：蜜蜂的舞蹈语言提供了一个典型的例子（西利1995; Passino和西利2006年）。觅食谁找到了丰富的食物来源，他们通知其所在地的摇摆舞nestmates（在西利1989年，1995年进行审查; Passino和西利2006年）。这个信号导致了来访的快速建立新的食物资源的个人，作为新聘人员随后舞蹈本身。正反馈停止，新的招聘会，当食物来源变得枯竭，新兵停止对他们返回巢（冯弗里希1967;西利1995）跳舞。信号的摇摆舞因此分配没有一个消极的信号抵消其影响救援人员花补丁的能力。蜜蜂，但是，确实有一个负面的信号，停止信号，这会导致蜜蜂摇摆舞停止跳舞（基什内尔1993;聂1993;牧师和西利2005年聂刘和2010年，聂2010）。因为一个信号，以减少不必要的招聘似乎，舞蹈语言的语法复杂的角色，站内的信号，是个谜，直到最近（聂2010）。鉴于积极的反馈信号导致的行为表现的，消极的信号导致一个行为停止（罗宾逊等人。2005年，2008年）。在法老的蚂蚁，警报信息素负径觅食，一个线索是旧的，可能不包含目前有用的信息（罗宾逊等人。2005年，2008年）。最近，它已经表明，蜜蜂停止信号可以在自然的情况下提供负反馈，对资源的战斗。总之，蜜蜂失去战斗进行了大量的停止信号时在同一地点觅食的蜜蜂定向（从而关闭该招聘网站），使用网站气味觅食带来的身体回到同一地点确定舞蹈家（2010年聂）。这些研究侧重于在馈线之间的殖民地侵略。一项联接通常是糖罐子solutio

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