Interaction effects of different drivers of wild bee decline and their influence on host–pathogen dynamics

Highlights

• Wild bee decline is a multi-factorial problem.

• Assessment of the effect of a single driver within the context of accompanying stressors is crucial.

• Disturbance of natural host–pathogen dynamics can lead to host extinction in extreme cases.

• Invasive species and bee domestication can disturb host–pathogen dynamics.

• Habitat loss, climate change and insecticides can disturb host–pathogen dynamics.

Wild bee decline is a multi-factorial problem, yet it is crucial to understand the impact of a single driver. Hereto the interaction effects of wild bee decline with multiple natural and anthropogenic stressors need to be clear. This is also true for the driver ‘pathogens’, as stressor induced disturbances of natural host–pathogen dynamics can unbalance settled virulence equilibria. Invasive species, bee domestication, habitat loss, climate changes and insecticides are recognized drivers of wild bee decline, but all influence host–pathogen dynamics as well. Many wild bee pathogens have multiple hosts, which relaxes the host-density limitation of virulence evolution. In conclusion, disturbances of bee-pathogen dynamics can be compared to a game of Russian roulette.

Introduction

The treasure chest of life, Earth's biodiversity, is under pressure. Population declines and extirpations are of the magnitude to call it the sixth major extinction event [1]. This biological annihilation impairs ecosystem services. Insect pollination underpins plant-derived ecosystem services supporting the seed set in 85% of all flowering plants [2], but direct human benefits are also gained with pollination of 76% of the leading agricultural crops [3]. Insect pollination is performed by different families of insects; herein bees (the Apiformes within the superfamily Apoidea) are the most exemplary as the nutritional needs of all their life stages are fully dependent on nectar and pollen [4].

The decline of insect pollinators, especially wild bees, is acknowledged worldwide [5, 6]. A full overview of the population decline of wild bees, their status and of the drivers thereof fall outside the scope of this review. For this we refer to the report by the International Platform on Biodiversity and Ecosystem Services and the references therein [7, 8].

Wild bee decline is often described as a multi-factorial problem. While this is true, it is also an evasive answer. In order to further comprehend this complex puzzle, three things are essential: firstly, it is important to understand the impact of single drivers within an environmental context where multiple natural and anthropogenic stressors act on wild bee populations [9]; secondly, these drivers are expected to show interaction effects which can be antagonistic or synergistic [10]; thirdly, the impact of drivers can differ based on the target species. For bumble bees the interaction among pathogens, pesticides, and diet is identified as the most crucial stressor. Although bumble bees are the best monitored wild bee species, we still only have patchy and incomplete evidence of the specific role of different drivers of bumble bee decline, with challenges associated with the setup of environmentally realistic experiments to study interacting stressors [11].

Here we will address the interaction effects of drivers of wild bee decline with the stressor parasites and viruses (from here on referred to as pathogens). When talking about bee pathogens one must recognize the historical context and knowledge gathered from the domesticated western honey bee, Apis mellifera. For example, the term honey bee viruses is persistently used, while most of these viruses have a much larger host-range and for many of them the honey bee will most likely not even be the prime host [12]. Another consequence of honey bee diseases as a key information source is a biased view on host–pathogen dynamics. In domesticated animals a pathogen is sometimes considered as an aberrant factor, which needs to be eradicated. In a natural ecosystem, however, pathogens play an important role [13]. In an undisturbed natural ecosystem the population size of a species fluctuates around the environment's carrying capacity. The population size is driven by bottom-up forces such as food and nesting availability. Top-down forces such as predation and pathogens negatively affect the population size. The driver of wild bee decline called ‘pathogens or parasites’ should therefore be seen in the context of factors which disturb natural host–pathogen dynamics. Pathogens are often not the main player regulating the population size [14] and have often evolved a virulence equilibrium with their hosts [15]. However, disturbance of the natural ecosystem can unbalance this virulence equilibrium, increasing the role of pathogens as a top-down force on a population. In extreme cases pathogens can cause dramatic declines in host populations and eventually lead to host extinction [16].