Towards a systems approach for understanding honeybee decline: a stocktaking and synthesis of existing models

Abstract

The health of managed and wild honeybee colonies appears to have declined substantially in Europe and the United States over the last decade. Sustainability of honeybee colonies is important not only for honey production, but also for pollination of crops and wild plants alongside other insect pollinators. A combination of causal factors, including parasites, pathogens, land use changes and pesticide usage, are cited as responsible for the increased colony mortality.However, despite detailed knowledge of the behaviour of honeybees and their colonies, there are no suitable tools to explore the resilience mechanisms of this complex system under stress. Empirically testing all combinations of stressors in a systematic fashion is not feasible. We therefore suggest a cross-level systems approach, based on mechanistic modelling, to investigate the impacts of (and interactions between) colony and land management.We review existing honeybee models that are relevant to examining the effects of different stressors on colony growth and survival. Most of these models describe honeybee colony dynamics, foraging behaviour or honeybee - varroa mite - virus interactions.We found that many, but not all, processes within honeybee colonies, epidemiology and foraging are well understood and described in the models, but there is no model that couples in-hive dynamics and pathology with foraging dynamics in realistic landscapes.Synthesis and applications. We describe how a new integrated model could be built to simulate multifactorial impacts on the honeybee colony system, using building blocks from the reviewed models. The development of such a tool would not only highlight empirical research priorities but also provide an important forecasting tool for policy makers and beekeepers, and we list examples of relevant applications to bee disease and landscape management decisions.

Keywords: Apis mellifera; colony decline; feedbacks; integrated model; multiple stressors; predictive systems ecology; review.

Figure 1

Schematic overview of main processes in honeybee models. (a) Colony models: based on an egg‐laying rate, bees pass through the developmental stages of eggs, larvae, pupa and adults, with a specific mortality acting on each of these stages. Some models distinguish between workers and drones, others only simulate workers. (b) Varroa models: phoretic mites (i.e. carried by bees) invade drone or worker cells, reproduce, emerge together with the adult bees, face the risk to die by falling from the comb and finally join again the group of phoretic mites. (c) Foraging models: the main processes of foraging models include waiting in the hive, searching for a nectar source, collect nectar if successful, unload nectar back in the colony (which might require receiver bees) and recruit new bees.

Figure 2

Simplified overview of the BEEHAVE model structure (Becher et al., unpublished): based on the egg‐laying rate and interacting with the varroa and foraging modules, the structure of a single honeybee colony is modelled. A separate landscape module allows to determine detection probabilities of flower patches (%) and to define their nectar and pollen flows over the season. This information is then taken into account, when foragers collect food in an agent‐based foraging module. Note that the various mortalities implemented in the model are not shown in this graph.