REVIEW: 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.

Multiyear survey targeting disease incidence in US honey bees

“…From September through November, only 30-45 % of samples tested were below the three-mite threshold. Thus, more than half of all beekeepers surveyed entered the winter with elevated mite infestations, which have been shown to contribute significantly to winter colony mortality (Becher et al 2013;Carreck et al 2010;Francis et al 2013;Le Conte et al 2010;vanEngelsdorp et al 2012). …”

Differential responses of Apis mellifera heat shock protein genes to heat shock, flower-thinning formulations, and imidacloprid

“…CCD has caused a significant economic impact owing to the decline of pollination of agricultural crops as well as wild plants (Klein et al, 2007;Schacker, 2008). The mechanisms of CCD remains unknown, although many possible causes have been proposed, such as pesticides (primarily neonicotinoids), infectious pathogens (e.g., Varroa mites and viruses), malnutrition, genetic factors, immunodeficiency, loss of habitat, changed beekeeping practices, or a combination of these factors (Becher et al, 2013;Smith et al, 2013). However, the effects of these impacts have been evaluated mostly at the whole organism level by determining mortality or infertility in bee colonies.…”

Protecting an Ecosystem Service

“…suggest that a combination of stressors may be sufficient to trigger failure of social bee 359 colonies (Bryden et al, 2013;Perry et al, 2015), yet empirical studies looking at interactive 360 effects are typically limited to two (or few) factors (Baron et al, 2014;Becher et al, 2013;361 Doublet et al, 2015;Fauser-Misslin et al, 2014;Gill et al, 2012;Gonzalez-Varo et al, 2013;362 Hoover et al, 2012;Kennedy et al, 2013;Kleijn and van Langevelde, 2006;Oliver et al, 363 2012;Pettis et al, 2013;Schweiger et al, 2010;Vanbergen et al, 2013). Land-use change 364 and management is seen as one of the leading drivers of insect pollinator declines (Garibaldi 365 et al, 2014;Ollerton et al, 2014;Vanbergen, 2014).…”

“…Unlike honeybees where close monitoring of colonies has provided detailed insights into 910 social colony dynamics (Becher et al, 2013(Becher et al, , 2014Khoury et al, 2011Khoury et al, , 2013Naug, 2008), 911…”