Modeling the Adaptive Role of Negative Signaling in Honey Bee Intraspecific Competition
Brian R. Johnson
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James C. Nieh
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J. C. Nieh Section of Ecology
, Behaviour, and Evolution,
Division of Biological Sciences, University of California
,
San Diego
, 9500 Gilman Dr, MC 0116,
La Jolla, CA 92093-0116, USA
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.
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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;
Electronic supplementary material The online version of this article (doi:10.1007/s10905-010-9229-5)
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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 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
pharaohs 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 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 e (...truncated)