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The synthesis of secondary metabolites is a hallmark of plant defence against herbivores. These compounds may be detrimental to consumers, but can also protect herbivores against parasites. Floral nectar commonly contains secondary metabolites, but little is known about the impacts of nectar chemistry on pollinators, including bees. We hypothesized that nectar secondary metabolites could reduce bee parasite infection. We inoculated individual bumblebees with Crithidia bombi, an intestinal parasite, and tested effects of eight naturally occurring nectar chemicals on parasite population growth. Secondary metabolites strongly reduced parasite load, with significant effects of alkaloids, terpenoids and iridoid glycosides ranging from 61 to 81%. Using microcolonies, we also investigated costs and benefits of consuming anabasine, the compound with the strongest effect on parasites, in infected and uninfected bees. Anabasine increased time to egg laying, and Crithidia reduced bee survival. However, anabasine consumption did not mitigate the negative effects of Crithidia, and Crithidia infection did not alter anabasine consumption. Our novel results highlight that although secondary metabolites may not rescue survival in infected bees, they may play a vital role in mediating Crithidia transmission within and between colonies by reducing Crithidia infection intensities. © 2015 The Author(s) Published by the Royal Society. All rights reserved.
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... Actually, C. bombi is known to be a highly prevalent but not too virulent gut parasite [86]. Indeed, previous studies only reported sublethal outcomes (e.g., impeding foraging behaviours and cognitive functions [19]), except under food-limited conditions [21] (but see [87]). While a compensatory feeding behaviour (i.e., increased pollen collection) and reduced survival have been highlighted in infected B. impatiens workers [87], these effects were not observed herein for B. terrestris, suggesting that differences in susceptibility occur among bumble bee species. ...
... Indeed, previous studies only reported sublethal outcomes (e.g., impeding foraging behaviours and cognitive functions [19]), except under food-limited conditions [21] (but see [87]). While a compensatory feeding behaviour (i.e., increased pollen collection) and reduced survival have been highlighted in infected B. impatiens workers [87], these effects were not observed herein for B. terrestris, suggesting that differences in susceptibility occur among bumble bee species. ...
... Although host feeding seems to favour parasite cell growth [47,91], differences in feeding behaviour cannot explain our observations as microcolonies fed a supplemented diet did not display higher pollen collection compared to those fed a control diet. Such a fluctuation in parasite load is then likely related to the occurrence of phenolamides themselves, as already shown for other specialised metabolites [23,87]. Such a parasite-facilitating effect of phenolamides has been already observed in a previous study, though it was less pronounced than herein, probably because of some differences between the experimental designs [32]. ...
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Specific floral resources may help bees to face environmental challenges such as parasite infection, as recently shown for sunflower pollen. Whereas this pollen diet is known to be unsuitable for the larval development of bumble bees, it has been shown to reduce the load of a trypanosomatid parasite (Crithidia bombi) in the bumble bee gut. Recent studies suggested it could be due to phe- nolamides, a group of compounds commonly found in flowering plants. We, therefore, decided to assess separately the impacts of sunflower pollen and its phenolamides on a bumble bee and its gut parasite. We fed Crithidia-infected and -uninfected microcolonies of Bombus terrestris either with a diet of willow pollen (control), a diet of sunflower pollen (natural diet) or a diet of willow pollen supplemented with sunflower phenolamides (supplemented diet). We measured several parameters at both microcolony (i.e., food collection, parasite load, brood development and stress responses) and individual (i.e., fat body content and phenotypic variation) levels. As expected, the natural diet had detrimental effects on bumble bees but surprisingly, we did not observe any reduction in parasite load, probably because of bee species-specific outcomes. The supplemented diet also induced detrimental effects but by contrast to our a priori hypothesis, it led to an increase in parasite load in infected microcolonies. We hypothesised that it could be due to physiological distress or gut microbiota alteration induced by phenolamide bioactivities. We further challenged the definition of medicinal effects and questioned the way to assess them in controlled conditions, underlining the necessity to clearly define the experimental framework in this research field.
... advantage of flowers with pharmacological properties, as when bumble bees self-medicate on sunflower pollen to reduce gut parasite loads (Richardson et al. 2015). By comparing colonies near habitats with or without floral resource enhancements, field studies corroborate benefits of abundant and/or diverse forage on honey bee and bumble bee health and, ultimately, colony growth and overwintering survival (Westphal et al. 2009;Alaux et al. 2017;Schulte et al. 2017;Ricigliano et al. 2019). ...
... Week 2 is the reference week. (Vaudo et al. 2015) and increasing the chances of consuming pollen with pharmaceutical properties (Richardson et al. 2015). Unlike eusocial honey bees and bumble bees, whose offspring feed from a mix of pollen collected by generalist foragers, alfalfa leafcutting bee offspring feed on pollen collected by a single female. ...
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Megachile rotundata (F.) is an important pollinator of alfalfa in the United States. Enhancing landscapes with wildflowers is a primary strategy for conserving pollinators and may improve the sustainability of M. rotundata. Changing cold storage temperatures from a traditionally static thermal regime (STR) to a fluctuating thermal regime (FTR) improves overwintering success and extends M. rotundata’s shelf life and pollination window. Whether floral resources enhance overwintering survival and/or interact with a thermal regime are unknown. We tested the combined effects of enhancing alfalfa fields with wildflowers and thermal regime on survival and macronutrient stores under extended cold storage (i.e., beyond one season). Megachile rotundata adults were released in alfalfa plots with and without wildflower strips. Completed nests were harvested in September and stored in STR. After a year, cells were randomly assigned to remain in STR for 6 months or in FTR for a year of extended cold storage; emergence rates were observed monthly. Macronutrient levels of emerged females were assessed. FTR improved M. rotundata survival but there was no measurable effect of wildflower strips on overwintering success or nutrient stores. Timing of nest establishment emerged as a key factor: offspring produced late in the season had lower winter survival and dry body mass. Sugars and glycogen stores increased under FTR but not STR. Trehalose levels were similar across treatments. Total lipid stores depleted faster under FTR. While wildflowers did not improve M. rotundata survival, our findings provide mechanistic insight into benefits and potential costs of FTR for this important pollinator.
... have been studied intensively in a search for affordable and effective treatments for human infections [5], including exhaustive testing of plant extracts and their components against both mammal-and insect-associated parasite life stages [2,6]. These studies have suggested new treatments for trypanosomatid-associated infections of humans [7] and related parasites of beneficial insects [8,9]. As in humans, antimicrobial phytochemicals can enhance resistance to infection in plants themselves [10] and in other plant-consuming animals, including insects [11]. ...
... The role of nectar chemistry in insect disease ecology has recently been highlighted by work on infections of pollinators. Floral nectar and pollen, their constituent secondary metabolites, and the composition of flowering plant communities can ameliorate trypanosomatid growth and infection in bumble bees [8,9,[29][30][31]. Both nectar and pollen-which may mix with and influence the chemistry of nectar at flowers [32]-contain diverse secondary metabolites that shape plant-pollinator ecology and plant-microbe ecology [33][34][35][36][37]. Flavonoids are one class of antimicrobial and antileishmanial compounds [38,39] that are ubiquitous in both nectar and pollen, with concentrations in pollen often exceeding 1% of total dry matter [40,41]. ...
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Background Insect-vectored Leishmania are responsible for loss of more disability-adjusted life years than any parasite besides malaria. Elucidation of the environmental factors that affect parasite transmission by vectors is essential to develop sustainable methods of parasite control that do not have off-target effects on beneficial insects or environmental health. Many phytochemicals that inhibit growth of sand fly-vectored Leishmania —which have been exhaustively studied in the search for phytochemical-based drugs—are abundant in nectars, which provide sugar-based meals to infected sand flies. Principle findings In a quantitative meta-analysis, we compare inhibitory phytochemical concentrations for Leishmania to concentrations present in floral nectar and pollen. We show that nectar concentrations of several flowering plant species exceed those that inhibit growth of Leishmania cell cultures, suggesting an unexplored, landscape ecology-based approach to reduce Leishmania transmission. Significance If nectar compounds are as effective against parasites in the sand fly gut as predicted from experiments in vitro , strategic planting of antiparasitic phytochemical-rich floral resources or phytochemically enriched baits could reduce Leishmania loads in vectors. Such interventions could provide an environmentally friendly complement to existing means of disease control.
... Although a body of research has accrued to date on the effects of nectar constituents (e.g. secondary metabolites) on pathogen viability and infectivity [102,103], to our knowledge, interactions involving pathogens of pollinators and nectar microbes have received little attention. Circumstantial evidence suggests these interactions can be strong. ...
... However, additional mechanisms may also be at play. As reviewed above, nectar microbe metabolism can modify sugars, amino acids, secondary metabolites, and pH, factors which have been shown to affect C. bombi growth and infectivity [102,104,105]. Many microbe species, including a few that are closely related to common nectar microbes, produce antibiotics [106,107]. ...
Article
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Floral nectar is prone to colonization by nectar-adapted yeasts and bacteria via air-, rain-, and animal-mediated dispersal. Upon colonization, microbes can modify nectar chemical constituents that are plant-provisioned or impart their own through secretion of metabolic by-products or antibiotics into the nectar environment. Such modifications can have consequences for pollinator perception of nectar quality, as microbial metabolism can leave a distinct imprint on olfactory and gustatory cues that inform foraging decisions. Furthermore, direct interactions between pollinators and nectar microbes, as well as consumption of modified nectar, have the potential to affect pollinator health both positively and negatively. Here, we discuss and integrate recent findings from research on plant–microbe–pollinator interactions and their consequences for pollinator health. We then explore future avenues of research that could shed light on the myriad ways in which nectar microbes can affect pollinator health, including the taxonomic diversity of vertebrate and invertebrate pollinators that rely on this reward. This article is part of the theme issue ‘Natural processes influencing pollinator health: from chemistry to landscapes’.
... The health of wild pollinators is under threat from parasites through a variety of anthropogenic factors, including the potential introduction of parasites into new geographical areas by global trade [1,2], spill-over of emerging infectious diseases from managed pollinators like honeybees [3,4] or through additive or synergistic effects between parasites and other man-made stressors like pesticides [5,6]. Dietary secondary plant compounds naturally occurring in nectar or pollen could ameliorate these threats to pollinator health via increased tolerance, prevention or reduction of infections [7][8][9][10][11]. Understanding the role of different foraging plants for pollinator diseases may thus present a promising avenue to promote pollinator health, for example by protecting natural habitats with key plant species [9] or promoting forage plants with health benefits through seed mixes in agricultural environments [11]. ...
... Indeed, the effect of secondary nectar metabolites on parasites in pollinator hosts has, in some cases, been inconsistent or contradictory between studies in the same host-parasite system (e.g. [7,13]) and may be affected by host genotypes or environmental conditions like temperature and food composition [13,14]. In vitro screens of nectar and pollen phytochemicals can provide insights into direct effects on pollinator parasites in culture, for example showing synergistic effects between compounds [15], variation in resistance against compounds between different parasite genotypes [16] or effects on parasite cell morphology [9]. ...
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Antimicrobial nectar secondary metabolites can support pollinator health by preventing or reducing parasite infections. To better understand the outcome of nectar metabolite–parasite interactions in pollinators, we determined whether the antiparasitic activity was altered through chemical modification by the host or resident microbiome during gut passage. We investigated this interaction with linden ( Tilia spp.) and strawberry tree ( Arbutus unedo ) nectar compounds . Unedone from A. unedo nectar inhibited the common bumblebee gut parasite Crithidia bombi in vitro and in Bombus terrestris gynes. A compound in Tilia nectar, 1-[4-(1-hydroxy-1-methylethyl)-1,3-cyclohexadiene-1-carboxylate]-6- O -β- d -glucopyranosyl-β- d -glucopyranose (tiliaside), showed no inhibition in vitro at naturally occurring concentrations but reduced C. bombi infections of B. terrestris workers. Independent of microbiome status, tiliaside was deglycosylated during gut passage, thereby increasing its antiparasitic activity in the hindgut, the site of C. bombi infections . Conversely, unedone was first glycosylated in the midgut without influence of the microbiome to unedone-8- O -β- d -glucoside, rendering it inactive against C. bombi , but subsequently deglycosylated by the microbiome in the hindgut, restoring its activity. We therefore show that conversion of nectar metabolites by either the host or the microbiome modulates antiparasitic activity of nectar metabolites. This article is part of the theme issue ‘Natural processes influencing pollinator health: from chemistry to landscapes’.
... Crithidia bombi inoculum was prepared fresh every day we ran a trial. We prepared inoculum according to a standard protocol (Richardson et al., 2015). We used 5-10 workers from a source colony to prepare inoculum that had a concentration of 1200 cells/μl (details of inoculum preparation are provided in Appendix S1: Section S1). ...
... We prepared fresh inoculum each day to have a concentration of 1200 cells/μl. To ensure the inoculum was infective, we inoculated a control group of 10-12 bees from the same uninfected colony we used for trials (inoculations as in Richardson et al., 2015). For control bees, we prepared the inoculum to have 25% sucrose to encourage consumption. ...
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The spread of parasites is one of the primary drivers of population decline of both managed and wild bees. Several bee parasites are transmitted by the shared use of flowers, turning floral resources into potential disease hotspots. However, we know little about how floral morphology and floral species identity affect different steps of the transmission process. Here, we used the gut parasite Crithidia bombi and its primary host, bumble bees (Bombus spp.), to examine whether floral traits or species identity better predict three basic steps of parasite transmission on flowers: feces deposition on flowers, survival of the parasite on flowers, and acquisition by a new host. We also identified which traits and/or species were most strongly associated with each step in the transmission process. We found that both trait‐ and species‐based models fit the data on deposition of feces and survival of C. bombi on flowers, but that species‐based models provided a better fit than trait‐based ones. However, trait‐based models were better at predicting the acquisition of C. bombi on flowers. While different species tended to support higher fecal deposition or parasite survival, we found that floral shape provided explanatory power for each of the transmission steps. When we assessed overall transmission potential, floral shape had the largest explanatory effect, with wider, shorter flowers promoting higher transmission. Taken together, our results highlight the importance of flower species identity and floral traits in disease transmission dynamics of bee parasites, and floral shape as an important predictor of overall transmission potential. Identifying traits associated with transmission potential may help us create seed mix that presents lower parasite transmission risk for bees for use in pollinator habitat.
... The use of plant secondary metabolites in the fight against diseases caused by parasites has been practiced for so long and it is also used in recent time (Singer et al., 2012). These plants can equally be used to control vectors carrying the parasites causing diseases, including Leishmaniasis and Chagas (Schmidt et al., 2012;Richardson et al., 2015). Mostly, secondary metabolites are known for their numerous biological properties including antiparasitic and antimicrobial, immunosuppressive, antitumor actions, among others (Thirumurugan et al., 2018). ...
... In addition, the existence of parasites in the gut of herbivorous animals like sheep is controlled by secondary metabolites after ingestion of plants. This helps to control the spread of parasites causing diseases such as leishmaniasis and Chagas (Singer et al., 2012;Richardson et al., 2015). Several plants have been tested against the parasites causing malaria and trypanosomiasis. ...
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The treatment of parasitic diseases is multifaceted. The control methods require a complex interplay involving experts in public health, government policies, education, and medical sciences. Several strategies used in the treatment of parasitic diseases are considered and they are based on the availability, effectiveness, affordability, and acceptability of the used drug. Other measures include effective elimination of vector, and animal reservoirs. Interestingly, new strategies and approaches for the treatment of parasitic diseases involve nanomedical encapsulation of drugs and active compounds. Furthermore, genome, cells, and signal pathways targeting have been used for preventing and treating parasitic diseases. These approaches are used for diagnosis, and treatments of disease and to gain increased understanding of underlying disease mechanisms. Phytocompounds such as flavonoids and others are used in nanotherapeutics for treating parasitic diseases as they prevent oxidation of a liable substrate in a system, among other beneficial properties. Therefore, the present review highlights the use of several phytocompounds in nanotherapeutics to treat diseases caused by parasites.
... Pollen (even originating from a single plant species) has a multi-faceted chemical composition that is rich in amino acids, lipids, sugars, secondary metabolite compounds, and other constituents (Roulston & Cane;Palmer-Young et al., 2019). Plant secondary compounds in particular have recently emerged as having beneficial impacts on pollinators Richardson et al., 2015;Stevenson et al., 2017), including protective effects against pesticide exposure (Ardalani et al., 2021a(Ardalani et al., , 2021b. Metabolomic analysis of our pollen diets identified 67 currently-uncharacterized compounds present only in diet 1. ...
Article
A primary goal in biology is to understand the effects of multiple, interacting environmental stressors on organisms. Wild and domesticated bees are exposed to a wide variety of interacting biotic and abiotic stressors, with widespread declines in floral resources and agrochemical exposure being two of the most important. In this study, we used examinations of brain gene expression to explore the sublethal consequences of neonicotinoid pesticide exposure and pollen diet composition in nest-founding bumble bee queens. We demonstrate for the first time that pollen diet composition can influence the strength of bumble bee queen responses to pesticide exposure at the molecular level. Specifically, one pollen mixture in our study appeared to buffer bumble bee queens entirely against the effects of pesticide exposure, with respect to brain gene expression. Additionally, we detected unique effects of pollen diet and sustained (versus more temporary) pesticide exposure on queen gene expression. Our findings support the hypothesis that nutritional status can help buffer animals against the harmful effects of other stressors, including pesticides, and highlight the importance of using molecular approaches to explore sublethal consequences of stressors.
... For example, different plant sugar sources affected malaria (Plasmodium falciparum) infection intensity and transmission potential in mosquitoes (Hien et al., 2016), and feeding of sand flies (Phlebotomus papatasi) on castor bean plants (Ricinus communis) led to the death of intestinal Leishmania major (Schlein and Jacobson, 1994). Among beneficial pollinating insects, specific phytochemicals, pollen diets and plant communities increased resistance to Crithidia bombi infection in bumblebees (Richardson et al., 2015;Giacomini et al., 2018;Adler et al., 2020). Plant secondary compounds can affect plant resistance to insect-vectored Phytomonas parasites of plants as well (Medina et al., 2015). ...
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Gut parasites of plant-eating insects are exposed to antimicrobial phytochemicals that can reduce infection. Trypanosomatid gut parasites infect insects of diverse nutritional ecologies as well as mammals and plants, raising the question of how host diet-associated phytochemicals shape parasite evolution and host specificity. To test the hypothesis that phytochemical tolerance of trypanosomatids reflects the chemical ecology of their hosts, we compared related parasites from honey bees and mosquitoes-hosts that differ in phytochemical consumption-and contrasted our results with previous studies on phylogenetically related, human-parasitic Leishmania. We identified one bacterial and ten plant-derived substances with known antileishmanial activity that also inhibited honey bee parasites associated with colony collapse. Bee parasites exhibited greater tolerance of chrysin-a flavonoid found in nectar, pollen, and plant resin-derived propolis. In contrast, mosquito parasites were more tolerant of cinnamic acid-a product of lignin decomposition present in woody debris-rich larval habitats. Parasites from both hosts tolerated many compounds that inhibit Leishmania, hinting at possible trade-offs between phytochemical tolerance and mammalian infection. Our results implicate the phytochemistry of host diets as a potential driver of insect-trypanosomatid associations, and identify compounds that could be incorporated into colony diets or floral landscapes to ameliorate infection in bees. This article is protected by copyright. All rights reserved.
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Evidence from the last few decades indicates that pollinator abundance and diversity are at risk, with many species in decline. Anthropogenic impacts have been the focus of much recent work on the causes of these declines. However, natural processes, from plant chemistry, nutrition and microbial associations to landscape and habitat change, can also profoundly influence pollinator health. Here, we argue that these natural processes require greater attention and may even provide solutions to the deteriorating outlook for pollinators. Existing studies also focus on the decline of individuals and colonies and only occasionally at population levels. In the light of this we redefine pollinator health and argue that a top-down approach is required focusing at the ecological level of communities. We use examples from the primary research, opinion and review articles published in this special issue to illustrate how natural processes influence pollinator health, from community to individuals, and highlight where some of these processes could mitigate the challenges of anthropogenic and natural drivers of change. This article is part of the theme issue ‘Natural processes influencing pollinator health: from chemistry to landscapes’.
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Nectar and pollen within flowers are usually the primary attractants to floral visitors. Chemical analysis of almond nectar and pollen in this study revealed that they contain the secondary compound amygdalin. Floral display often reflects pollinator characters, and almond flowers are accordingly designated as “bee flowers”. A previous study in Israel showed that when almonds bloom early in the season they attract honeybees, but later in the season the bees shift toward other species that start blooming. In this study, we offered honeybees sugar solutions containing various concentrations of amygdalin. These preference experiments revealed that in mid-summer bees were not selective, whereas early in the summer they were more discriminating, and consumed faster the sugar solutions with the lower amygdalin concentrations. Possible roles of amygdalin in almond nectar and pollen are discussed.
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Parasites infect hosts non-randomly as genotypes of hosts vary in susceptibility to the same genotypes of parasites, but this specificity may be modulated by environmental factors such as nutrition. Nutrition plays an important role for any physiological investment. As immune responses are costly, resource limitation should negatively affect immunity through trade-offs with other physiological requirements. Consequently, nutritional limitation should diminish immune capacity in general, but does it also dampen differences among hosts? We investigated the effect of short-term pollen deprivation on the immune responses of our model host Bombus terrestris when infected with the highly prevalent natural parasite Crithidia bombi. Bumblebees deprived of pollen, their protein source, show reduced immune responses to infection. They failed to upregulate a number of genes, including antimicrobial peptides, in response to infection. In particular, they also showed less specific immune expression patterns across individuals and colonies. These findings provide evidence for how immune responses on the individual-level vary with important elements of the environment and illustrate how nutrition can functionally alter not only general resistance, but also alter the pattern of specific host-parasite interactions.
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Herbivory defence chemicals in plants can affect higher trophic levels such as predators and parasitoids, but the impact on pollinators has been overlooked. We show that defensive plant chemicals can damage pollinator fitness when expressed in pollen. Crop lupins (Lupinus species from Eu-rope and South America) accumulate toxic quinolizidine al-kaloids in vegetative tissues, conferring resistance to herbiv-orous pests such as aphids. We identified the alkaloid lupanine and its derivatives in lupin pollen, and then provided this compound at ecologically-relevant concentrations to queenless microcolonies of bumblebees (Bombus terrestris) in their pollen to determine how foraging on these crops may impact bee colony health and fitness. Fewer males were produced by microcolonies provided with lupanine-treated pollen and they were significantly smaller than controls. This impact on males was not linked to preference as workers willingly fed lupanine-treated pollen to larvae, even though it was deleterious to colony health. Agricultural systems com-prising large monocultures of crops bred for herbivore resis-tance can expose generalist pollinators to deleterious levels of plant compounds, and the broader environmental impacts of crop resistance must thus be considered.
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Honeybees, Apis mellifera, have several prophylactic disease defense strategies, including the foraging of antibiotic, antifungal, and antiviral compounds of plant products. Hence, honey and pollen contain many compounds that prevent fungal and bacterial growth and inhibit viral replication. Since these compounds are also fed to the larvae by nurse bees, they play a central role for colony health inside the hive. Here, we show that honeybee nurse bees, infected with the microsporidian gut parasite Nosema ceranae, show different preferences for various types of honeys in a simultaneous choice test. Infected workers preferred honeys with a higher antibiotic activity that reduced the microsporidian infection after the consumption of the honey. Since nurse bees feed not only the larvae but also other colony members, this behavior might be a highly adaptive form of therapeutic medication at both the individual and the colony level.
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Knowledge of the complete life cycle of a parasite is crucial to understand the epidemiology and population dynamics of a disease. The populations of several social insect pollinators are decreasing, and parasites are often cited as a contributing factor. The exact transmission pathway of the bumblebee parasite Crithidia bombi (Lipa & Triggiani) (Kinetoplastea: Trypanosomatidae) between two hosts is still unknown, although a previous laboratory experiment suggests transmission via the nectar of flowers. Plant species may differentially protect or negatively affect the parasite while it resides in the flower, for instance if plants vary in their floral shape or the compounds present in their nectar. This will lead to differential transmission success and potentially influence disease epidemiology. In the present study we aimed at determining whether the parasite may indeed be transmitted in the nectar by the bumblebee Bombus terrestris (L.) (Hymenoptera: Apidae). We found that parasite survival was significantly decreased in water with higher sugar concentrations. However, none of the field-collected nectar samples contained parasite cells, and no parasite cells were transmitted between two artificial flowers by a foraging worker under laboratory conditions. Our results suggest instead that parasite cells may be deposited on flower surfaces and transported on worker surfaces.
Conference Paper
... compelling but untested hypothesis for the cause of decline in the United States (10) entails the spread of a putatively introduced pathogen , Nosema bombi, which is an obligate intracellular microsporidian parasite found commonly in bumble bees throughout Europe (13–16 ...