Measuring ontogenetic shifts in central-place foraging insects: a case study with honey bees

Abstract

13 7 INRAE, UE 1255 APIS "Abeilles paysages interactions et systèmes de culture", Abstract 27 1. Measuring time-activity budgets over the complete individual lifespan is now 28 possible for many animals with the recent advances of life-long individual 29 monitoring devices. Although analyses of changes in the patterns of time-activity 30 budgets have revealed ontogenetic shifts in birds or mammals, no such technique 31has been applied to date on insects. 32 2. We tested an automated breakpoint-based procedure to detect, assess and 33 quantify shifts in the temporal pattern of the flight activities in honey bees. We 34 assumed that the learning and foraging stages of honey bees will differ in several 35 respects, to detect the age at onset of foraging (AOF). 36 3. Using an extensive dataset covering the life-long monitoring of 2,100 individuals, 37 we compared the AOF outputs with the more conventional approaches based on 38 arbitrary thresholds. We further evaluated the robustness of the different methods 39 comparing the foraging time-activity budget allocations between the presumed 40 foragers and confirmed foragers.41 4. We revealed a clear-cut learning-foraging ontogenetic shift that differs in duration, 42 frequency, and time of occurrence of flights. Although AOF appeared to be highly 43 plastic among bees, the breakpoint-based procedure seems better able to detect it 44 than arbitrary threshold-based methods that are unable to deal with inter-individual 45 variation. 46 5. We developed the aof R-package including a broad range of examples with both 47 simulated and empirical dataset to illustrate the simplicity of use of the procedure.48 This simple procedure is generic enough to be derived from any individual life-long 49 monitoring devices recording the time-activity budgets of honey bees, and could 50 3 propose new ecological applications of bio-logging to detect ontogenetic shifts in 51 the behaviour of central-place foraging insects. 52 53

Honeybee lifespan: the critical role of pre-foraging stage

“…We then calculated the age of first exit and entrance sequence (AFE, in days), the lifespan (i.e. the age at last exit) and AOF for each bee using the aof function developed in the aof R-package [ 47 , 54 ]. The aof function is a simple statistical procedure, derived from the behavioural change point analysis approach [ 55 ], a well-appreciated technique of likelihood comparisons to statistically determine behavioural changes.…”

“…The aof function works at the individual level thus accounting for inter-individual variation to detect, assess and quantify shifts in the temporal pattern of time-activity budgets recorded by individual lifelong monitoring. Indeed, a clear breakpoint in duration, frequency and time of occurrence in the day was found between learning and foraging flights of honeybees, so-called AOF [ 47 ]. Thus, AOF is estimated from three daily activities, (i) the number of exit and entrance sequences per day, (ii) the duration of these sequences, and (iii) the hour of the day that they were performed.…”

“…Then, these three values are averaged to give an AOF estimate in days. The aof function is freely available through the aof R-package that includes documentation, source code and examples using both simulated and empirical dataset [ 47 , 54 ].…”

“…[ 22 ] and Requier et al . [ 47 ]. Therefore, there may be a trade-off between the risks associated with the performance of pre-foraging flights and the benefits from accumulating flight experience during this stage, which might translate into higher performances and survival at the foraging stage.…”

“…Variability in environmental contexts was notably achieved by tracking bees originating from different source colonies each month from April to September in two different geographical sites in France. We then measured their life-history traits and, particularly, identified AOF based on the detection of ontogenetic changes in time-activity budget series of individual bees [ 47 ]. The overarching aim was to assess whether lifespan is influenced by flight experience, in order to better characterize the patterns and drivers of natural mortality risk in free-range honeybees.…”