Sanitizing the fortress: protection of ant brood and nest material by worker antibiotics

Social groups are at particular risk for parasite infection, which is heightened in eusocial insects by the low genetic diversity of individuals within a colony. To combat this, adult ants have evolved a suite of defenses to protect each other, including the production of antimicrobial secretions. However, it is the brood in a colony that are most vulnerable to parasites because their individual defenses are limited, and the nest material in which ants live is also likely to be prone to colonization by potential parasites. Here, we investigate in two ant species whether adult workers use their antimicrobial secretions not only to protect each other but also to sanitize the vulnerable brood and nest material. We find that, in both leaf-cutting ants and weaver ants, the survival of the brood was reduced and the sporulation of parasitic fungi from them increased, when the workers nursing them lacked functional antimicrobial-producing glands. This was the case for both larvae that were experimentally treated with a fungal parasite (Metarhizium) and control larvae which developed infections of an opportunistic fungal parasite (Aspergillus). Similarly, fungi were more likely to grow on the nest material of both ant species if the glands of attending workers were blocked. The results show that the defense of brood and sanitization of nest material are important functions of the antimicrobial secretions of adult ants and that ubiquitous, opportunistic fungi may be a more important driver of the evolution of these defenses than rarer, specialist parasites

The emergence and spillover of bumblebee parasites

Pollinators and in particular, bumblebees are currently experiencing significant declines. In Britain, bumblebee populations have been declining since the industrial revolution. Modern farming now requires large, monoculture fields to be effectively pollinated, yet the very nature of such large, homogeneous environments prevents many wild pollinators to thrive there. Since the mid-1980s bumblebees have been reared and imported on an industrial scale to aid the pollination of many valuable crops such as tomatoes and raspberry. There is great concern that the intensive rearing and importation of these bumblebees may permit the introduction of exotic parasites to native bumblebees. These concerns follow suggestions that parasite spillover from commercially reared bumblebees may be occurring; with declines of wild bumblebees in North and South America correlated with commercial bumblebee use. It’s believed that around 50, 000 bumblebee hives are imported into the UK every year and whilst they are purported to be disease free, no independent testing is carried out. Here, I assess what risk the use of commercial bumblebees has on native bees. By screening commercially reared and imported bumblebee colonies for a range of bumblebee and honey bee parasites, I identified the majority have infections. The parasites detected include the emerging diseases Apicystis bombi and Nosema ceranae which are found to be lethal to infected bumblebees. Shared flowers between bumblebees and honey bees are shown to be platforms for the dispersal of many of these parasites. The frequent mixing between domesticated and wild bumblebees allows potential transmission of these parasites. The deployment of commercial bumblebees was shown to increase parasite prevalence within local populations of wild bumblebees and when bumblebees have increased competition in the form of domesticated honey bees, they once again have higher parasite prevalence. Here I show that not only are current import regulation inadequate to avoid introducing infected bumblebees into England, but that there are clear opportunities and evidence that transmission is occurring

Toxic temperatures: bee behaviours exhibit divergent pesticide toxicity relationships with warming

Climate change and agricultural intensification are exposing insect pollinators to temperature extremes and increasing pesticide usage. Yet, we lack good quantification of how temperature modulates the sublethal effects of pesticides on behaviours vital for fitness and pollination performance. Consequently, we are uncertain if warming decreases or increases the severity of different pesticide impacts, and whether separate behaviours vary in the direction of response. Quantifying these interactive effects is vital in forecasting pesticide risk across climate regions and informing pesticide application strategies and pollinator conservation. This multi-stressor study investigated the responses of six functional behaviours of bumblebees when exposed to either a neonicotinoid (imidacloprid) or a sulfoximine (sulfoxaflor) across a standardised low, mid, and high temperature. We found the neonicotinoid had a significant effect on five of the six behaviours, with a greater effect at the lower temperature(s) when measuring responsiveness, the likelihood of movement, walking rate, and food consumption rate. In contrast, the neonicotinoid had a greater impact on flight distance at the higher temperature. Our findings show that different organismal functions can exhibit divergent thermal responses, with some pesticide-affected behaviours showing greater impact as temperatures dropped, and others as temperatures rose. We must therefore account for environmental context when determining pesticide risk. Moreover, we found evidence of synergistic effects, with just a 3°C increase causing a sudden drop in flight performance, despite seeing no effect of pesticide at the two lower temperatures. Our findings highlight the importance of multi-stressor studies to quantify threats to insects, which will help to improve dynamic evaluations of population tipping points and spatiotemporal risks to biodiversity across different climate regions

The cost of promiscuity: sexual transmission of Nosema microsporidian parasites in polyandrous honey bees

Multiple mating (and insemination) by females with different males, polyandry, is widespread across animals, due to material and/or genetic benefits for females. It reaches particularly high levels in some social insects, in which queens can produce significantly fitter colonies by being polyandrous. It is therefore a paradox that two thirds of eusocial hymenopteran insects appear to be exclusively monandrous, in spite of the fitness benefits that polyandry could provide. One possible cost of polyandry could be sexually transmitted parasites, but evidence for these in social insects is extremely limited. Here we show that two different species of Nosema microsporidian parasites can transmit sexually in the honey bee Apis mellifera. Honey bee males that are infected by the parasite have Nosema spores in their semen, and queens artificially inseminated with either Nosema spores or the semen of Nosema-infected males became infected by the parasite. The emergent and more virulent N. ceranae achieved much higher rates of infection following insemination than did N. apis. The results provide the first quantitative evidence of a sexually transmitted disease (STD) in social insects, indicating that STDs may represent a potential cost of polyandry in social insects

The relationship between managed bees and the prevalence of parasites in bumblebees

Honey bees and, more recently, bumblebees have been domesticated and are now managed commercially primarily for crop pollination, mixing with wild pollinators during foraging on shared flower resources. There is mounting evidence that managed honey bees or commercially produced bumblebees may affect the health of wild pollinators such as bumblebees by increasing competition for resources and the prevalence of parasites in wild bees. Here we screened 764 bumblebees from around five greenhouses that either used commercially produced bumblebees or did not, as well as bumblebees from 10 colonies placed at two sites either close to or far from a honey bee apiary, for the parasites Apicystis bombi, Crithidia bombi, Nosema bombi, N. ceranae, N. apis and deformed wing virus. We found that A. bombi and C. bombi were more prevalent around greenhouses using commercially produced bumblebees, while C. bombi was 18% more prevalent in bumblebees at the site near to the honey bee apiary than those at the site far from the apiary. Whilst these results are from only a limited number of sites, they support previous reports of parasite spillover from commercially produced bumblebees to wild bumblebees, and suggest that the impact of stress from competing with managed bees or the vectoring of parasites by them on parasite prevalence in wild bees needs further investigation. It appears increasingly likely that the use of managed bees comes at a cost of increased parasites in wild bumblebees, which is not only a concern for bumblebee conservation, but which may impact other pollinators as well

Genetic Variability of the Neogregarine Apicystis bombi, an Etiological Agent of an Emergent Bumblebee Disease

The worldwide spread of diseases is considered a major threat to biodiversity and a possible driver of the decline of pollinator populations, particularly when novel species or strains of parasites emerge. Previous studies have suggested that populations of introduced European honeybee (Apis mellifera) and bumblebee species (Bombus terrestris and Bombus ruderatus) in Argentina share the neogregarine parasite Apicystis bombi with the native bumblebee (Bombus dahlbomii). In this study we investigated whether A. bombi is acting as an emergent parasite in the non-native populations. Specifically, we asked whether A. bombi, recently identified in Argentina, was introduced by European, non-native bees. Using ITS1 and ITS2 to assess the parasite's intraspecific genetic variation in bees from Argentina and Europe, we found a largely unstructured parasite population, with only 15% of the genetic variation being explained by geographic location. The most abundant haplotype in Argentina (found in all 9 specimens of non-native species) was identical to the most abundant haplotype in Europe (found in 6 out of 8 specimens). Similarly, there was no evidence of structuring by host species, with this factor explaining only 17% of the genetic variation. Interestingly, parasites in native Bombus ephippiatus from Mexico were genetically distant from the Argentine and European samples, suggesting that sufficient variability does exist in the ITS region to identify continent-level genetic structure in the parasite. Thus, the data suggest that A. bombi from Argentina and Europe share a common, relatively recent origin. Although our data did not provide information on the direction of transfer, the absence of genetic structure across space and host species suggests that A. bombi may be acting as an emergent infectious disease across bee taxa and continents.Centro de Estudios Parasitológicos y de Vectore

Genetic variability of the neogregarine apicystis bombi, an etiological agent of an emergent bumblebee disease

The worldwide spread of diseases is considered a major threat to biodiversity and a possible driver of the decline of pollinator populations, particularly when novel species or strains of parasites emerge. Previous studies have suggested that populations of introduced European honeybee (Apis mellifera) and bumblebee species (Bombus terrestris and Bombus ruderatus) in Argentina share the neogregarine parasite Apicystis bombi with the native bumblebee (Bombus dahlbomii). In this study we investigated whether A. bombi is acting as an emergent parasite in the non-native populations. Specifically, we asked whether A. bombi, recently identified in Argentina, was introduced by European, non-native bees. Using ITS1 and ITS2 to assess the parasite's intraspecific genetic variation in bees from Argentina and Europe, we found a largely unstructured parasite population, with only 15% of the genetic variation being explained by geographic location. The most abundant haplotype in Argentina (found in all 9 specimens of non-native species) was identical to the most abundant haplotype in Europe (found in 6 out of 8 specimens). Similarly, there was no evidence of structuring by host species, with this factor explaining only 17% of the genetic variation. Interestingly, parasites in native Bombus ephippiatus from Mexico were genetically distant from the Argentine and European samples, suggesting that sufficient variability does exist in the ITS region to identify continent-level genetic structure in the parasite. Thus, the data suggest that A. bombi from Argentina and Europe share a common, relatively recent origin. Although our data did not provide information on the direction of transfer, the absence of genetic structure across space and host species suggests that A. bombi may be acting as an emergent infectious disease across bee taxa and continents

The impacts of predators and parasites on wild bumblebee colonies

1. The study of wild bumblebee nests has been hindered by the difficulty in locating and observing them. Here, 47 wild nests were located using a sniffer dog and volunteers. The entrances to 32 nests were filmed continuously to identify successful nests (those that produced gynes) and observe vertebrate species interactions.   2. Of the 47 nests, 71% and 21% produced gynes in 2010 and 2011, respectively.  3. A total of 39 vertebrate species were filmed at entrances but the majority did not interact with the nests. Great tits (Parus major) depredated or attempted to depredate bees on 32 occasions at the entrances to 10 nests, something that has not previously been described. Small mammals were very often recorded accessing entrances to bumblebee nests, but whether they depredated bees was not known, and frequently visited nests were no less likely to produce gynes. Eight nests were entered by adult wax moths,Aphomia sociella.  4. The faeces of 1179 workers from 29Bombus terrestrisnests were screened microscopically for parasites.Crithidia bombiinfections were apparent in 49% of worker bees, whileNosema bombiandApicystis bombiwere present in 5.5% and 0.68% of bees, respectively. Nests with a high prevalence ofC. bombiinfection were less likely to produce gynes, the first evidence of a direct impact of this common parasite on bumblebee colony reproduction in wild nests.  5. Overall, our data indicate that bumblebee nests are at the heart of a rich web of interactions between many different predator and parasite species