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.
Highlights
Motivation to forage may lead to more complex sequential patterns[23], most forms of physiological stress entailed an overall reduction of behavioural complexity[24,25,26], resulting in more stereotypical and suboptimal behavioural sequences
We found that the spatial scale of the orientation flight was significantly reduced in bees with Nosema infection in comparison to bees free of spores (Table 2; Fig. 2, Supplementary Fig. S3) with infection intensity playing a secondary role in shaping behavioural performance
Analysing the individual bee movement patterns in relation to their disease load, we found no significant difference in the prevalence of Lévy flight characteristics (AIC >0 .5) between bees infected with either Nosema or DWV as compared to bees without these pathogens (Fig. 3, Table 3)
Summary
Motivation to forage may lead to more complex sequential patterns[23], most forms of physiological stress (social disharmony, pregnancy, intoxication, pathogen load) entailed an overall reduction of behavioural complexity[24,25,26], resulting in more stereotypical and suboptimal behavioural sequences. Honeybees are central-place foragers exploring vast areas of up to 300 km[2] in search of floral resources[28,29] Their navigation relies on learned and memorized landmarks; though there is a debate about exactly how bees utilize landmark information[30,31,32,33,34]. When they first leave the hive, honeybee workers have to efficiently acquire a sufficient set of informative landmarks to allow them to navigate back to the hive They do so by performing successive and spatially increasing orientation flights around the colony[35,36,37]. We ask if infection levels of these two fundamentally different pathogen types affect 1) behavioural performance i.e. flight characteristics and spatial exploration of the landscape, and 2) spatial exploration patterns in orientating bees, i.e. consistency with an optimized Lévy-flight searching pattern. Our study provides the first insights into the effects of these physiological stressors on the robustness of navigational optimization strategies in animals
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