Pesticide reduces bumblebee colony initiation and increases probability of population extinction

Abstract

Pollinators are in global decline and agricultural pesticides are a potential driver of this. Recent studies have suggested that pesticides may significantly impact bumblebee colonies-an important and declining group of pollinators. Here, we show that colony-founding queens, a critical yet vulnerable stage of the bumblebee lifecycle, are less likely to initiate a colony after exposure to thiamethoxam, a neonicotinoid insecticide. Bombus terrestris queens were exposed to field-relevant levels of thiamethoxam and two natural stressors: the parasite Crithidia bombi and varying hibernation durations. Exposure to thiamethoxam caused a 26% reduction in the proportion of queens that laid eggs, and advanced the timing of colony initiation, although we did not detect impacts of any experimental treatment on the ability of queens to produce adult offspring during the 14-week experimental period. As expected from previous studies, the hibernation duration also had an impact on egg laying, but there was no significant interaction with insecticide treatment. Modelling the impacts of a 26% reduction in colony founding on population dynamics dramatically increased the likelihood of population extinction. This shows that neonicotinoids can affect this critical stage in the bumblebee lifecycle and may have significant impacts on population dynamics.

Figure 1

The proportion of B. terrestris queens that had undergone a short (6 week) or long (12 week) hibernation, and had either been exposed to the pesticide thiamethoxam or a control, which initiated a colony (by laying eggs) within ten weeks of emergence from hibernation. Total sample size for each treatment group: short hibernation, control group = 50; short hibernation, pesticide group = 49; long hibernation, control group = 48; long hibernation, pesticide group = 50 queens (includes queens which survived the whole experiment only).

Figure 2

The event history curve showing the cumulative probability of egg laying from the end of hibernation (time = 0 days) until the first egg was laid, by B. terrestris queens exposed to either the pesticide thiamethoxam, or a control. Total sample size for each treatment group: control group = 98; pesticide group = 99 (includes queens which survived the whole experiment only).

Figure 3

Heat maps showing the likelihood profile for the colony capacity with (panels b and d) or without thiamethoxam exposure (panels a and c). The heat maps in Figure 3 represent the probability distribution (normalised likelihoods) of the colony capacity (where lighter colours indicate higher probability, see scale to right of graphs) as a function of p_nm, the probability with which queens successfully mate and find a new nest site in the natural environment, and the colony capacity itself. The colony capacity is the product of p_nm with the number of gynes produced, the probability to survive hibernation and the probability to be able initiate a colony following survival. Panel (a) depicts the probability that the colony capacity takes a certain value, for different values of p_nm, (using data from75, 42). Panel (b) shows the likelihood profile of colony capacity after exposure to thiamethoxam: the distribution is lower than in panel (a) due to the reduction in colony initiation (as found in our empirical results, see Supplementary Material for methodology). Panel (c) shows the likelihood profile of the colony capacity without exposure to thiamethoxam, conditioned to take a value of at least one to take account that the natural bumblebee population of B. terrestris is extant. The colony capacity must therefore be at least one. The likelihoods for the colony capacities below one are therefore set to zero, and the profile renormalised. Panel (d) shows the likelihood profile for the colony capacity as in (c) after the effect of thiamethoxam exposure was taken into account. Because of the reduction in colony initiation caused by thiamethoxam exposure colony capacities below one a have positive probability. The total probability of a colony capacity below one is found by integrating all probabilities below the dashed line in Fig. 3d.