Task allocation and site fidelity jointly influence foraging regulation in honeybee colonies

Abstract

Variation in behaviour among group members often impacts collective outcomes. Individuals may vary both in the task that they perform and in the persistence with which they perform each task. Although both the distribution of individuals among tasks and differences among individuals in behavioural persistence can each impact collective behaviour, we do not know if and how they jointly affect collective outcomes. Here, we use a detailed computational model to examine the joint impact of colony-level distribution among tasks and behavioural persistence of individuals, specifically their fidelity to particular resource sites, on the collective trade-off between exploring for new resources and exploiting familiar ones. We developed an agent-based model of foraging honeybees, parametrized by data from five colonies, in which we simulated scouts, who search the environment for new resources, and individuals who are recruited by the scouts to the newly found resources, i.e. recruits. We varied the persistence of returning to a particular food source of both scouts and recruits and found that, for each value of persistence, there is a different optimal ratio of scouts to recruits that maximizes resource collection by the colony. Furthermore, changes to the persistence of scouts induced opposite effects from changes to the persistence of recruits on the collective foraging of the colony. The proportion of scouts that resulted in the most resources collected by the colony decreased as the persistence of recruits increased. However, this optimal proportion of scouts increased as the persistence of scouts increased. Thus, behavioural persistence and task participation can interact to impact a colony's collective behaviour in orthogonal directions. Our work provides new insights and generates new hypotheses into how variations in behaviour at both the individual and colony levels jointly impact the trade-off between exploring for new resources and exploiting familiar ones.

Keywords: Apis mellifera; collective behaviour; exploitation; exploration; group composition; persistence.

Figure 1.

Flight dynamics of scouts and recruits. (a) Scouts left the hive at the beginning of the simulation and once they found a resource, they recruited other foragers, referred to as ‘recruits’. (b) Variance of the scouts' deviations from a straight path on outgoing trips ($\tilde{\sigma }=5$, red) was larger than that of the recruits and persistent scouts ($\tilde{\sigma }=2$, blue), resulting in greater spatial dispersion. (c) System dynamics approach based on a compartmental model, with square boxes representing the states of foragers and the green circle representing the amount of food retrieved by all foragers. Black arrows are state-transition rates (see equations (2.6) and (2.7)); the blue dashed arrow represents the recruitment of foragers by scouts; the green double arrows represent foragers delivering food to the hive.

Figure 2.

Empirical results of 206 foraging trips performed on one day by 33 different honeybee foragers from one representative colony of the five colonies we tested. The feeder was positioned 5 m from the hive. (a) Number of visits over time. Each line represents one bee and t = 0 reflects the first bee's first visit to the feeder. (b) Distribution of intervals between consecutive visits to a single feeder. (c) Distribution of persistence, i.e. the number of return visits by each bee to one of two feeders. The average persistence was 6.1 ± 0.3.

Figure 3.

The relationship between colony persistence π and the proportion of scouts affects the amount of resources collected by a colony. The amount of resources collected over time by a simulated colony in which all foragers have either (a) low persistence (π = 1) or (b) high persistence (π = 20) for three different proportions of scouts. Shaded areas represent 1.5 s.d. (c) Total amount of resource collected throughout the entire simulation as a function of the proportion of scouts in the colony for different values of persistence of all foragers (π). Bars are the standard deviation across all simulation runs. (d) Optimal proportion of scouts plateaus near 50% as π increases. Points are the results from our agent-based model and the line is the result from the systems dynamics approach (equation (3.4)). (e) Maximum amount of resources collected scales sublinearly with π. Points are the results from our agent-based model, and the line is the result from the systems dynamics approach (equation (3.3)).

Figure 4.

Differences in collective foraging due to the persistence of either scouts (π^s) or recruits (π^r in the agent-based model). Total amount of resources collected by a colony as a function of the proportion of scouts when (a) the persistence of scouts is set to π^s = 5 for the following values of persistence of recruits: π^r = 1,5,10,15,20 and (b) the persistence of recruits is set to π^r = 5 for the following values of persistence of scouts: π^s = 1,5,10,15,20. Bars are the standard deviation across all simulation runs. Proportion of scouts that resulted in maximal amount of resource collected as a function of (c) recruit persistence for different values of fixed scout persistence π^s and (d) scout persistence for different values of fixed recruit persistence π^r. (e) Heat map of the maximum amount of resources collected for different values of scout π^s and recruit π^r persistence jointly. (f) Heat map of the proportion of scouts that led to the maximum amount of resources collected for different values of scout π^s and recruit π^r persistence jointly.

Figure 5.

The systems dynamics approach captures the opposing effects of scout and recruit persistence on the optimal proportion of scouts. (a) Change in optimal per cent of scouts due to change in the persistence of scouts. (b) Change in optimal per cent of scouts due to change in the persistence of recruits.

Figure 6.

The effect of increase in recruit persistence on the proportion of scouts that resulted in an optimal amount of resource collected was double that of the effect of increase in scout persistence. Bars are the standard deviation across all persistence values.