DOI 10.1007/s00114-011-0881-1
Jeffery S. Pettis & Dennis vanEngelsdorp &
Josephine Johnson & Galen Dively
Received: 1 May 2011 / Revised: 25 December 2011 / Accepted: 31 December 2011
# The Author(s) 2012. This article is published with open access at Springerlink.com
Abstract Global pollinator declines have been attributed to habitat destruction, pesticide use, and climate change or some combination of these factors, and managed honey bees, Apis
mellifera, are part of worldwide pollinator declines. Here we exposed honey bee colonies during three brood generations to sub-lethal doses of a widely used pesticide, imidacloprid, and then subsequently challenged newly emerged bees with the gut parasite, Nosema spp. The pesticide dosages used were below levels demonstrated to cause effects on longevity or foraging in adult honey bees. Nosema infections increased significantly in the bees from pesticide-treated hives when compared to bees from control hives demonstrating an indirect effect of pesticides on pathogen growth in honey bees. We clearly demonstrate an increase in pathogen growth within
individual bees reared in colonies exposed to one of the most widely used pesticides worldwide, imidacloprid, at below levels considered harmful to bees. The finding that individual
bees with undetectable levels of the target pesticide, after being reared in a sub-lethal pesticide environment within the colony, had higher Nosema is significant. Interactions between pesticides and pathogens could be a major contributor to increased mortality of honey bee colonies, including colony collapse disorder, and other pollinator declines worldwide.
Keywords Apis mellifera . Imidacloprid . Nosema .
Sub-lethal . Pesticides . Pathogens
Introduction
The honey bee, Apis mellifera, is arguably the most important pollinator of agricultural crops (Klein et al. 2007). While worldwide managed honey bee populations have increased over the last 50 years, colony populations have decreased significantly in many European and North American nations (Aizen and Harder 2009) as a result of habitat destruction, pesticide use, pathogens, and climate change (NRC 2007) or some combination of these factors (vanEngelsdorp and
Meixner 2010). At the same time, cultivation of crops that are dependent on insects for pollination (Aizen et al. 2009) has increased. The ability to provide sufficient colonies to meet this anticipated demand is questionable, especially in light of the elevated losses experienced by US beekeepers over the winters of 2006/2007 and 2007/2008 (vanEngelsdorp et al. 2007; vanEngelsdorp et al. 2008). Colonies that die with a condition known as colony collapse disorder (CCD) make up a signifi- cant proportion of recent overwintering losses in the USA
(vanEngelsdorp et al. 2008). While the cause of CCD remains unknown, affected colonies are often infected with a greater variety and higher loads of disease agents than apparently
healthy colonies (Johnson et al. 2009; vanEngelsdorp et al. 2009a; Cox-Foster et al. 2007). This suggests that some factor or combination of factors may be weakening bees by making
them more susceptible to infection (vanEngelsdorp et al. 2009a). A myriad of abiotic and biotic factors can adversely affect the ability of honey bees to fight infection, including interactions between disease agents, mite parasitism, poor nutrition, and sub-lethal exposure to pesticides (Johnson et al. 2009; vanEngelsdorp et al. 2009a). Systemic pesticides such as
imidacloprid pose a new route of exposure in pollen and nectar and have been demonstrated to have negative effects on learning in adult bees (Decourtye et al. 2004).
Here we test the hypothesis that bees exposed to sub-lethal levels of pesticide are more susceptible to disease. We exposed colonies of honey bees to the insecticide imidacloprid at
sub-lethal levels and then challenged newly emerged workers from those colonies with the gut parasite Nosema spp., two species (Nosema apis and Nosema ceranae) of which are
known to adversely affect colony health (Higes et al. 2008; Kauko et al. 2003). The pesticide dosages used were below levels demonstrated to cause effects on longevity or foraging
in adult honey bees (Maus et al. 2003; Bonmatin et al. 2007; Deseneux et al. 2007).
Discussion
We clearly demonstrate an interaction between sub-lethal exposure to imidacloprid at the colony level and the spore production in individual bees of honey bee gut parasite Nosema. Two similar studies have just been published that directly treated individual bees with imidacloprid, fipronil,
or thiacloprid and then challenged them with Nosema with similar synergistic interaction between Nosema and pesticide exposure (Alaux et al. 2010; Vidau et al. 2011). Our study differs in several significant ways; (1) our study employed sub-lethal colony-level pesticide chronic expo-
sure instead of laboratory direct exposure to experimental bees, (2) no imidacloprid residues could be found in the newly emerged worker bees challenged in our study (Table 1),
(3) our test bees could only have received pesticide exposure during larval development, thus (4) pesticide exposure to test bees could only have been indirectly from brood food from
nurse bees (Winston 1987) that were exposed as they fed on imidacloprid-spiked protein. We can only speculate as to why sub-lethal exposure in brood food to larva resulted in in-
creased spore production in adult bees. Since Nosema initiates infection in the mid-gut then perhaps in the larval stages the mid-gut ways altered or weakened in some manner that
resulted in increased Nosema infection in adult bees. Vidau et al. (2011) failed to demonstrate a change in the pesticide detoxification system in adult bees yet still demonstrated an
increase in mortality in adult bees when pesticides and Nosema were combined. Alaux et al. (2010) showed that co-exposure to imidacloprid and Nosema weakened bees but they
also showed a trend toward a slight decrease in spore production with pesticide exposure. Individual bees in our study showed a marked increase in Nosema spore production in
the laboratory but the parent colonies failed to show increased Nosema levels over time. Our understanding of N. ceranae at the colony level is still very limited as colony-level spore counts can be highly variable. Perhaps spore production is not the proper way to measure N. ceranae infection as has always been the case with N. apis? Taken together these three
studies clearly demonstrate synergism between pesticides and Nosema. The current study, with the more robust chronic sublethal pesticide exposure at the colony level, clearly demon-
strates that such interactions are possible in the real world, not just in a laboratory setting. Additional research is needed to understand the underlying mechanisms of pesticide pathogen
interactions. This is especially true in our study in trying to determine how the pesticide moved in the colony, affected nurse bees, and what level of exposure that larvae in these colonies actually received. The pesticide was consumed equally among the two dosages and house bees contained the pesticide but the pharmacokinetics within the colony is yet to be determined.
Past studies have found that chronic, sub-lethal exposure to pesticides can have an adverse effect on colonies (Bendahou et al. 1999) and has been associated with overt disease out-
breaks in honey bees (Morse et al. 1965). Conversely, further infection with the chronic bee paralysis virus can affect honey bee tolerance to agricultural pesticides (Bendahou et al. 1997).
Recent increases in colony losses in the USA and Europe have drawn particular attention to one relatively new class of systemic pesticides, the neonicotinoids, of which imidacloprid is
a member. Beekeeper conviction that imidacloprid is responsible for colony losses in France has resulted in the withdrawal of its registration (under the trade name Gaucho, Bayer, Leverkusen, Germany) as a seed treatment for sunflowers and corn Ministere de l’Agriculture et de la Peche (1999 and 2004). Similar pressure in California has resulted in a reevaluation of four neonicotinoids, including imidacloprid, because of elevated levels of residues in leaves and blossoms of ornamental plants after imidacloprid applications. The published levels of imidacloprid expressing acute and chronic toxicity on bees are variable and conflicting (Nguyen et al. 2009). Most studies suggest that imidacloprid can cause disorientation and associative learning problems in honey bees at exposure levels above 20 ppb (Decourtye et al. 2004; Deseneux et al. 2007). However, crop residue studies have detected imidacloprid at levels of 2–5 ppb in
pollen and >1.5 ppb in nectar of seed-treated corn, sunflowers, and rape (Kauko et al. 2003) well below the 20 ppb level documented to cause acute and chronic toxicity effects. To our knowledge no studies have examined chronic effects of dietary exposure to imidacloprid in functional colonies over multiple brood cycles and potential synergistic effects of pesticide and disease interactions. Our results suggest that the current methods used to evaluate the potential negative effect of pesticides are inadequate. This is not the first study to note a complex and unexpected interaction between low pesticide exposure and pathogen loads. Trem-
atodes levels in amphibian populations are driven by atrazine in the aquatic environment (Rohr et al. 2008). Elevated levels of the fungicide chlorothalonil in honey bees have
been associated with “entombed pollen” which is linked with increased risk of colony mortality (vanEngelsdorp et al. 2009b). The call for a reevaluation of pesticide test protocols required for the registration of products is not new (Colin et al. 2004; Halm et al. 2006). These proposed
new standards utilize the Predicated No Effect Concentration which is determined using chronic and acute toxicity data and not potentially indirect effects of pesticide exposure, such as
increased susceptibility to pathogens. With the wide variety of pesticides that have been documented in failing beehives (Mullen et al. 2010), it is imperative that we understand both
the synergistic effects these compound may have and the interactions with other variables, like pathogens, involved in bee health. We suggest new pesticide testing standards be
devised that incorporate increased pathogen susceptibility into the test protocols. Lastly, we believe that subtle interactions between pesticides and pathogens, such as demonstrated here, could be a major contributor to increased mortality of honey bee colonies worldwide.
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