Abstract
The presence of antimicrobial secondary metabolites in nectar suggests that pollinators, which are threatened globally by emergent disease, may benefit from the consumption of nectars rich in these metabolites. We tested whether nicotine, a nectar secondary metabolite common in Solenaceae and Tilia species, is used by parasitized bumblebees as a source of self-medication , using a series of toxicological, microbiological and behavioural experiments. Caged bees infected with Crithidia bombi [TI1]had a slight preference for sucrose solution laced with the alkaloid and behavioural tests showed that the parasite infection induced an increased consumption of nicotine during foraging activity. When ingested, nicotine delayed the progression of a gut infection in bumblebees by a few days, but dietary nicotine did not clear the infection, and after 10 days the parasite load approached that of control bees. Moreover, when pathogens were exposed to the alkaloid prior to host ingestion the protozoan's viability was not directly affected, suggesting that anti-parasite effects were relatively weak. Nicotine consumption in a single dose did not impose any cost even in food-stressed bees (starved) but the alkaloid had detrimental effects on healthy bees if consistently consumed for weeks. These toxic effects disappeared in infected bees suggesting that detoxification costs might have been counterbalanced by the advantages in slowing the progression of the infection. Nonetheless we did not find a benefit of nicotine consumption in terms of life expectancy of infected bees, making these findings difficult to interpret. Our results indicate that caution is warranted in interpreting impacts of plant metabolites on insect parasites and suggest that the conditions under which nicotine consumption provides benefits to either bees or plants remain to be identified. The contention that secondary metabolites in nectar may be under selection from pollinators, or used by plants to enhance their own reproductive success, remains to be confirmed.
Highlights
Parasites can have a dramatic impact on their hosts, and provide a powerful selective force for host defence mechanisms
Infection intensities increased significantly from day 7 to day 10, independently of nicotine treatment. These findings prove the antimicrobial activity of nicotine against the pathogen when ingested by bumblebees, and indicate that when pathogens are exposed to the alkaloid prior to host ingestion the protozoan’s viability is not directly affected
Here we demonstrate that parasitized bumblebees modify their diet preference and foraging behaviour to delay the development of an infection
Summary
Parasites can have a dramatic impact on their hosts, and provide a powerful selective force for host defence mechanisms. Plants are good candidates for prophylactic or therapeutic foods as they often contain metabolites that display a wide range of biological activities (Cowan, 1999) which were originally evolved to combat herbivores or plant-parasites (Hadacek, 2002). This preferential ingestion of “non-nutritive” food and chemicals to self-medicate is known as pharmacophagy or zoopharmacognosy. Exceptions concern self-medication behaviour described in two species of woolly bear caterpillars, which increase their preference for pyrrolizidine alkaloids or iridoid glycosides when parasitized, improving their chances of surviving parasitoid infection (Bernays & Singer, 2005; Singer et al, 2009; Smilanich et al, 2011). Trans-generational medication, but not self-medication, has been described in the monarch butterfly (Lefevre et al, 2010) and self-medication has been hypothesized for honeybees that increase plant resin collection in response to a fungal infection (Simone-Finstrom & Spivak, 2012)
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