Optimal search patterns in honeybee orientation flights are robust against emerging infectious diseases

Abstract

Lévy flights are scale-free (fractal) search patterns found in a wide range of animals. They can be an advantageous strategy promoting high encounter rates with rare cues that may indicate prey items, mating partners or navigational landmarks. The robustness of this behavioural strategy to ubiquitous threats to animal performance, such as pathogens, remains poorly understood. Using honeybees radar-tracked during their orientation flights in a novel landscape, we assess for the first time how two emerging infectious diseases (Nosema sp. and the Varroa-associated Deformed wing virus (DWV)) affect bees’ behavioural performance and search strategy. Nosema infection, unlike DWV, affected the spatial scale of orientation flights, causing significantly shorter and more compact flights. However, in stark contrast to disease-dependent temporal fractals, we find the same prevalence of optimal Lévy flight characteristics (μ ≈ 2) in both healthy and infected bees. We discuss the ecological and evolutionary implications of these surprising insights, arguing that Lévy search patterns are an emergent property of fundamental characteristics of neuronal and sensory components of the decision-making process, making them robust against diverse physiological effects of pathogen infection and possibly other stressors.

Covert deformed wing virus infections have long-term deleterious effects on honeybee foraging and survival

“…In addition, it would be possible that the disease agent itself benefited from an earlier onset of foraging if this promoted its horizontal transmission to other host colonies [62]. Indeed, in the case of DWV, a direct influence on the behaviour of its host is not unlikely, given that DWV particles have previously been found in the mushroom bodies-a key higher brain centre of these insects [31] (but see [34] for a study where no behavioural effects were found). Irrespective of these possible adaptive causes, it is clear that precocious foraging would have a major effect on colony well-being, as premature foraging partially depletes the nurse bee population [63] and disrupts various activities inside the hive [64][65][66], and rapid behavioural maturation has been shown to strongly accelerate the failure of stressed honeybee colonies [63].…”

“…In addition, another tracking technology-harmonic radarwas recently used by one group to show that the emerging pathogen Nosema ceranae caused impaired homing behaviour in honeybees [45] and that Nosema infection also affected honeybee orientation flight behaviour [34]. The tracking method, however, was unable to reveal any correlation between DWV infection levels and orientation flight characteristic [34].…”

“…Furthermore, two studies in which natural variation in infection levels of DWV was combined with experimentally manipulated variation in infection levels with the microsporidian parasite Nosema showed that DWV-infected bees displayed shortened flight distances and flight durations in flight mill experiments [33], but no differences in orientation flight behaviour in a harmonic radar tracking set-up [34], whereas the reverse pattern was seen for Nosema [33,34]. As yet, however, effects of DWV on honeybee flight behaviour and foraging patterns have not yet been investigated using controlled infection set-ups.…”

“…Nevertheless, applications to the study of pathogen-induced stress on honeybee foraging behaviour are still rare, and are currently limited to one study on Israeli acute paralysis virus (IAPV) [43], which documented virus-induced differences in homing ability, but without taking full advantage of the technology to study the longterm impact on foraging behaviour, and one study that showed adverse effects of a microsporidian gut parasite, Nosema apis, on honeybee foraging and survival [44]. In addition, another tracking technology-harmonic radarwas recently used by one group to show that the emerging pathogen Nosema ceranae caused impaired homing behaviour in honeybees [45] and that Nosema infection also affected honeybee orientation flight behaviour [34]. The tracking method, however, was unable to reveal any correlation between DWV infection levels and orientation flight characteristic [34].…”

Emergence of Lévy Walks from Second-Order Stochastic Optimization

“…However, empirical data indicate that for organisms the observed growth is often faster. Lévy walks (LWs) [1][2][3] and similar Lévy flights (LFs) [2,4,5] have been successfully applied to fit experimental data obtained from the movement patterns of many organisms and their cells, including T cells [6], microglia [7], starved slime mould (Dictyostelium discoideum) [8,9], swarming bacteria [10], fruit flies [11], honey bees [12,13], wandering albatrosses [14,15], marine predators [16], and humans [17][18][19] (also in human's gaze [20] and word association [21] trajectories). In many different random search scenarios, LWs and LFs have been shown to be advantageous over normal diffusion [22][23][24][25][26][27][28][29][30][31][32] and alternative superdiffusive models [33].…”