Influence of combined pesticide and parasite exposure on bumblebee colony traits in the laboratory

Abstract

Summary1. Pollinating insects provide vital ecosystem services of enormous importance for economies and biodiversity. Yet, there is a concerning global trend of pollinator declines. Parasites and pesticides are among the suspected principle drivers of these declines. However, especially in the case of key wild pollinators, there are insufficient data on the relative impact of these individual environmental stressors and whether they interact to increase detrimental effects. 2. Using a fully crossed factorial design, we investigated how laboratory exposure to neonicotinoid insecticides, thiamethoxam and clothianidin, over a 9-week period and a prevalent trypanosome gut parasite Crithidia bombi affects various crucial colony traits of the bumblebee Bombus terrestris. 3. We show that chronic dietary exposure from an early stage of colony development to doses of thiamethoxam and clothianidin that could be encountered in the field truncated worker production, reduced worker longevity and decreased overall colony reproductive success. Further, we demonstrate a significant interaction between neonicotinoid exposure and parasite infection on mother queen survival. The fate of the mother queen is intrinsically linked to colony success, and under combined pressure of parasite infection and neonicotinoid exposure, mother queen survival was lowest. This indicates increased detrimental effects of combined exposure on this crucial colony trait. Combined effects may be exacerbated in stressful natural environments where more pronounced parasite virulence is expected. 4. Synthesis and applications. Our findings reiterate that dietary exposure to neonicotinoids can impact on bumblebee colony performance and fitness. The indication of combined negative effects of ecologically relevant pressures suggests additional adverse consequences for long-term population dynamics under complex field conditions. To help safeguard pollinator health, whole life-cycle fitness assessments, particularly for non-Apis bees, stringently incorporating chronic and sublethal side effects of pesticides, as well as interactions with common natural stressors, such as prevalent parasites, should be considered in the corresponding test guidelines.

Neonicotinoids override a parasite exposure impact on hibernation success of a key bumblebee pollinator

“…As mentioned earlier, when multiple stresses (such as pesticides and parasites) are combined, the outcome for individual bees, colonies and populations is predicted to be negative (Bryden et al, 2013;Vanbergen et al, 2013;Goulson et al, 2015). Indeed, studies supporting this idea are on the increase (Alaux et al, 2010;Vidau et al, 2011;Fauser-Misslin et al, 2014;Retschnig et al, 2014;Doublet et al, 2015; but see Retschnig et al, 2015), but significant knowledge gaps relating the effects of potential ecologically relevant threats to diverse pollinators persist (Lundin et al, 2015).…”

“…Both the sugar water and honeybee collected pollen sources were previously shown to be free of detectable levels of neonicotinoid pesticides (Fauser-Misslin et al, 2014). The colonies had been initiated in the laboratory in spring using wild caught queens collected in northern Switzerland.…”

“…Exposure can be in the range of parts per billion in nectar and pollen (Sanchez-Bayo & Goka, 2014) and presents a season-long threat in temperate agroecosystems (Long & Krupke, 2016). Exposure of bumblebees to neonicotinoid trace residues have shown detrimental effects on numerous key traits of these social insects both in the laboratory and under semi-field conditions (Gill et al, 2012;Whitehorn et al, 2012;Larson et al, 2013;Fauser-Misslin et al, 2014;Gill & Raine, 2014;Scholer & Krischik, 2014;Goulson, 2015;Rundlöf et al, 2015;Stanley et al, 2015Stanley et al, , 2016. As mentioned earlier, when multiple stresses (such as pesticides and parasites) are combined, the outcome for individual bees, colonies and populations is predicted to be negative (Bryden et al, 2013;Vanbergen et al, 2013;Goulson et al, 2015).…”

“…Both have been routinely used in agricultural settings, and in some regions, such as Britain, have exceeded imidacloprid in their application in more recent years (Simon-Delso et al, 2015). Prior work on B. terrestris has demonstrated detrimental effects on the colony level of these two neonicotinoids (Fauser-Misslin et al, 2014). We ask if and when these two important stresses of neonicotinoids and parasites influence laboratory hibernation survival and weight loss, and whether any detrimental effects are altered, either positively or negatively, when the exposures are combined.…”

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).…”