Mark J. F. Brown

Disease associations between honeybees and bumblebees as a threat to wild pollinators.

Emerging infectious diseases (EIDs) pose a risk to human welfare, both directly and indirectly, by affecting managed livestock and wildlife that provide valuable resources and ecosystem services, such as the pollination of crops. Honeybees (Apis mellifera), the prevailing managed insect crop pollinator, suffer from a range of emerging and exotic high-impact pathogens, and population maintenance requires active management by beekeepers to control them. Wild pollinators such as bumblebees (Bombus spp.) are in global decline, one cause of which may be pathogen spillover from managed pollinators like honeybees or commercial colonies of bumblebees. Here we use a combination of infection experiments and landscape-scale field data to show that honeybee EIDs are indeed widespread infectious agents within the pollinator assemblage. The prevalence of deformed wing virus (DWV) and the exotic parasite Nosema ceranae in honeybees and bumblebees is linked; as honeybees have higher DWV prevalence, and sympatric bumblebees and honeybees are infected by the same DWV strains, Apis is the likely source of at least one major EID in wild pollinators. Lessons learned from vertebrates highlight the need for increased pathogen control in managed bee species to maintain wild pollinators, as declines in native pollinators may be caused by interspecies pathogen transmission originating from managed pollinators.

The conservation of bees: a global perspective.

Bees are major pollinators of Angiosperms and therefore their apparent decline is of importance for humans and biodiversity. We synthesise results of 12 recent reviews to provide a global picture of the threats they face. Habitat loss is the major threat to bee diversity, whilst invasive species, emerging diseases, pesticide use, and climate change also have the potential to impact bee populations. We suggest that future conservation strategies need to prioritise (i) minimising habitat loss, (ii) making agricultural habitats bee-friendly, (iii) training scientists and the public in bee taxonomy and identification, (iv) basic autecological and population genetic studies to underpin conservation strategies, (v) assessing the value of DNA barcoding for bee conservation, (vi) determining the impact of invasive plants, animals, parasites and pathogens, and (vii) integrating this information to understand the potential impact of climate change on current bee diversity.ZusammenfassungBienen sind die wichtigsten Bestäuber von wildblühenden und landwirtschaftlichen Nutzpflanzen. Das hat zur Konsequenz, dass ihre offensichtliche Abnahme eine bedeutende Sorge um die Ernährung der Menschen und die Erhaltung der Biodiversität im großen Maßstab darstellen sollte. Hier stellen wir die Ergebnisse von 12 neuesten Übersichtsartikeln zusammen, um ein globales Bild der Abnahme der Bienen und von den Bedrohungen, denen die Bienen ausgesetzt sind zu erhalten (Tab. I). Ganz offensichtlich stellt der Verlust an Lebensräumen die hauptsächliche Bedrohung der Vielfalt der Bienen wie der Biodiversität im Allgemeinen dar. Es können aber auch andere Faktoren wie invasive Arten, das Auftauchen neuer Krankheiten, die Verwendung von Pestiziden und der Klimawandel zu bedeutenden Belastungen für die Bienenpopulationen werden. Obwohl es sehr schwierig ist, den Beitrag aller dieser Faktoren zu trennen, ist dies aber eine unabdingbare Aufgabe wenn wir die Bienendiversität erhalten, unterstützen oder wiederherstellen wollen. Es ist offensichtlich, dass die derzeitigen Erhaltungsanstrengungen durch den Mangel an grundlegenden Daten zur Verteilung, Häufigkeit, Ökologie und Populationsgenetik behindert werden. Wir schlagen vor, dass zukünftige Erhaltungsstrategien hauptsächlich auf folgende Punkte ausgerichtet werden sollten: (i) die Minimierung des Verlustes an Lebensraum, (ii) die bienenfreundliche Gestaltung landwirtschaftlicher Habitate, (iii) die Unterweisung von Wissenschaftlern und der Öffentlichkeit in Bienentaxonomie und der Bestimmung der Arten, (iv) der Erstellung von grundlegenden autökologische und populationsgenetische Studien zur Untermauerung der Erhaltungsmassnahmen, (v) der Ermittlung der Nutzbarkeit von DNA Barcoding für die Bienenerhaltung, (vi) der Bestimmung der Auswirkungen invasiver Pflanzen, Tieren, Parasiten und Pathogenen, und (vii) der Zusammenführung dieser Information, um die möglichen Auswirkungen des Klimawechsels auf die verbleibende Bienendiversität verstehen zu können. Zusätzlich zu diesen Prioritäten sollte das vielfältige Angebot an internationalen, nationalen und regionalen Ansätzen und politischen Maßnahmen für die Bienenerhaltung zusammengeführt werden, um Überschneidungen aufzulösen und ein zusammenhängendes Rahmenwerk für die Erhaltungs- und Wiederherstellungsaktivitäten zu schaffen. Während Bienen aller Art über den ganzen Globus hinweg Bedrohungen gegenüberstehen, glauben wir, dass es uns mit abgestimmtem und wissenschaftlich fundiertem Handeln möglich ist die Diversität der Bienen für die zukünftigen Generationen zu erhalten oder wiederherzustellen.

Parasite and host assemblages: embracing the reality will improve our knowledge of parasite transmission and virulence

Interactions involving several parasite species (multi-parasitized hosts) or several host species (multi-host parasites) are the rule in nature. Only a few studies have investigated these realistic, but complex, situations from an evolutionary perspective. Consequently, their impact on the evolution of parasite virulence and transmission remains poorly understood. The mechanisms by which multiple infections may influence virulence and transmission include the dynamics of intrahost competition, mediation by the host immune system and an increase in parasite genetic recombination. Theoretical investigations have yet to be conducted to determine which of these mechanisms are likely to be key factors in the evolution of virulence and transmission. In contrast, the relationship between multi-host parasites and parasite virulence and transmission has seen some theoretical investigation. The key factors in these models are the trade-off between virulence across different host species, variation in host species quality and patterns of transmission. The empirical studies on multi-host parasites suggest that interspecies transmission plays a central role in the evolution of virulence, but as yet no complete picture of the phenomena involved is available. Ultimately, determining how complex host–parasite interactions impact the evolution of host–parasite relationships will require the development of cross-disciplinary studies linking the ecology of quantitative networks with the evolution of virulence.

Effects of Invasive Parasites on Bumble Bee Declines

Bumble bees are a group of pollinators that are both ecologically and economically important and declining worldwide. Numerous mechanisms could be behind this decline, and the spread of parasites from commercial colonies into wild populations has been implicated recently in North America. Commercial breeding may lead to declines because commercial colonies may have high parasite loads, which can lead to colonization of native bumble bee populations; commercial rearing may allow higher parasite virulence to evolve; and global movement of commercial colonies may disrupt spatial patterns in local adaptation between hosts and parasites. We assessed parasite virulence, transmission mode, and infectivity. Microparasites and so-called honey bee viruses may pose the greatest threat to native bumble bee populations because certain risk factors are present; for example, the probability of horizontal transmission of the trypanosome parasite Crithidia bombi is high. The microsporidian parasite Nosema bombi may play a role in declines of bumble bees in the United States. Preliminary indications that C. bombi and the neogregarine Apicystis bombi may not be native in parts of South America. We suggest that the development of molecular screening protocols, thorough sanitation efforts, and cooperation among nongovernmental organizations, governments, and commercial breeders might immediately mitigate these threats.

Harvester ant nests, soil biota and soil chemistry

Many ant species accumulate organic debris in the vicinity of their nests. These organic materials should provide a rich resource base for the soil biota. We examined the effect of harvester ant nests (Pogonomyrmex barbatus) on the soil community and soil chemistry. Ant nest soils supported 30-fold higher densities of microarthropods and 5-fold higher densities of protozoa than surrounding, control soils. The relative abundances of the major groups of protozoa differed as well: amoebae and ciliates were relatively overrepresented, and flagellates underrepresented, in ant nest versus control soils. Densities of bacteria and fungi were similar in the two soil types. Concentrations of nitrate, ammonium, phosphorus, and potassium were significantly higher in ant nest soils, while concentrations of magnesium, calcium, and water were similar in nest and control soils. Ant nest soils were marginally more acidic than controls. The results demonstrate that P. barbatus nests constitute a significant source of spatial heterogeneity in soil biota and soil chemistry in arid grasslands.

Genetic diversity, parasite prevalence and immunity in wild bumblebees

Inbreeding and a consequent loss of genetic diversity threaten small, isolated populations. One mechanism by which genetically impoverished populations may become extinct is through decreased immunocompetence and higher susceptibility to parasites. Here, we investigate the relationship between immunity and inbreeding in bumblebees, using Hebridean island populations of Bombus muscorum. We sampled nine populations and recorded parasite prevalence and measured two aspects of immunity: the encapsulation response and levels of phenoloxidase (PO). We found that prevalence of the gut parasite Crithidia bombi was higher in populations with lower genetic diversity. Neither measure of immune activity was correlated with genetic diversity. However, levels of PO declined with age and were also negatively correlated with parasite abundance. Our results suggest that as insect populations lose heterozygosity, the impact of parasitism will increase, pushing threatened populations closer to extinction.

Task-Related Differences in the Cuticular Hydrocarbon Composition of Harvester Ants, Pogonomyrmex barbatus

Colonies of the harvester ant, Pogonomyrmex barbatus, perform a variety of tasks. The behavior of an individual worker appears to depend on its recent history of brief contacts with ants of the same and other task groups. The purpose of this study was to determine whether task groups differ in cuticular hydrocarbon composition. We compared the cuticular hydrocarbon composition of ants collected under natural conditions as they performed one of three tasks: patrolling (locating food sources), foraging, or nest maintenance. Task groups differed significantly in the relative proportions of classes of hydrocarbon compounds, as well as in individual compounds. Relative to nest maintenance workers, foragers and patrollers had a higher proportion of straight-chain alkanes relative to monomethylalkanes, dimethylalkanes, and alkenes. There was no significant difference in the chain length of n-alkanes among the task groups. Foragers did not differ in hydrocarbon composition from patrollers. Colonies differed significantly from one another in hydrocarbon composition, but task groups differed in consistent ways from colony to colony, suggesting that the mechanism responsible for task-related hydrocarbon composition was the same in all colonies. P. barbatus workers switch tasks during their lifetimes, suggesting that cuticular hydrocarbon composition changes during adulthood as well. Nest maintenance workers are probably younger than foragers and patrollers and perform very little of their work outside of the nest. Task-related hydrocarbon differences detected here may be associated with worker age, and/or the abiotic characteristics (temperature, humidity, and ultraviolet light) of the interior and exterior work environments.

Unveiling cryptic species of the bumblebee subgenus Bombus s. str. worldwide with COI barcodes (Hymenoptera: Apidae)

Bumblebees of the subgenus Bombus s. str. dominate (or used to dominate) many north temperate pollinator assemblages and include most of the commercial bumblebee pollinator species. Several species are now in serious decline, so conservationists need to know precisely which ones are involved. The problem is that many Bombus s. str. species are cryptic, so that species identification from morphology may be impossible for some individuals and is frequently misleading according to recent molecular studies. This is the first review of the entire subgenus to: (1) avoid fixed a priori assumptions concerning the limits of the problematic species; and (2) sample multiple sites from across the entire geographic ranges of all of the principal named taxa worldwide; and (3) fit an explicit model for how characters change within an evolutionary framework; and (4) apply explicit and consistent criteria within this evolutionary framework for recognising species. We analyse easily-obtained DNA (COI-barcode) data for 559 sequences from 279 localities in 33 countries using general mixed Yule-coalescent (GMYC) models, assuming only the morphologically distinctive species B. affinis Cresson, B. franklini (Frison), B. ignitus Smith and B. tunicatus Smith, and then recognise other comparable COI-barcode groups as putative species. These species correspond to modified concepts of the taxa B. cryptarum (Fabricius), B. hypocrita Pérez, B. jacobsoni Skorikov, B. lantschouensis Vogt n. stat., B. longipennis Friese, B. lucorum (Linnaeus), B. magnus Vogt, B. minshanensis Bischoff n. stat., B. occidentalis Greene, B. patagiatus Nylander, B. sporadicus Nylander, B. terrestris (Linnaeus) and B. terricola Kirby (a total of 17 species). Seven lectotypes are designated. Our results allow us for the first time to diagnose all of the putative species throughout their global ranges and to map the extent of these geographic ranges.

A sting in the spit: widespread cross-infection of multiple RNA viruses across wild and managed bees

Summary Declining populations of bee pollinators are a cause of concern, with major repercussions for biodiversity loss and food security. RNA viruses associated with honeybees represent a potential threat to other insect pollinators, but the extent of this threat is poorly understood. This study aims to attain a detailed understanding of the current and ongoing risk of emerging infectious disease (EID) transmission between managed and wild pollinator species across a wide range of RNA viruses. Within a structured large‐scale national survey across 26 independent sites, we quantify the prevalence and pathogen loads of multiple RNA viruses in co‐occurring managed honeybee (Apis mellifera) and wild bumblebee (Bombus spp.) populations. We then construct models that compare virus prevalence between wild and managed pollinators. Multiple RNA viruses associated with honeybees are widespread in sympatric wild bumblebee populations. Virus prevalence in honeybees is a significant predictor of virus prevalence in bumblebees, but we remain cautious in speculating over the principle direction of pathogen transmission. We demonstrate species‐specific differences in prevalence, indicating significant variation in disease susceptibility or tolerance. Pathogen loads within individual bumblebees may be high and in the case of at least one RNA virus, prevalence is higher in wild bumblebees than in managed honeybee populations. Our findings indicate widespread transmission of RNA viruses between managed and wild bee pollinators, pointing to an interconnected network of potential disease pressures within and among pollinator species. In the context of the biodiversity crisis, our study emphasizes the importance of targeting a wide range of pathogens and defining host associations when considering potential drivers of population decline.

The evolution of female multiple mating in social hymenoptera.

Abstract The evolution of female multiple mating is a highly controversial topic, especially in social insects. Here we analyze, using comparative analyses and simulation models, the merits of two major contending hypotheses for the adaptive value of polyandry in this group. The hypotheses maintain that, respectively, the resulting genotypic diversity among offspring within a colony: (1) mitigates against the effects of parasites; or (2) favors adaptive division of labor. Only two of 11 phylogenetically uncontrolled comparative analyses supported an association between polyandry and the complexity of division of labor (measured here using worker caste polymorphism or polyethism) as proposed by hypothesis 2, and after controlling for phylogeny there were no significant associations. In contrast, a previous study demonstrated such an association for parasite load as expected under hypothesis 1. In addition, we used simulation models to track the spread of an initially rare allele for double mating in a population of single‐mating alleles, thus analyzing the crucial first step from monandry to polyandry. We find that double mating evolves consistently under antagonistic coevolution given that parasites exert sufficient selection intensity. In contrast, selection for enhanced division of labor resulted in only an erratic appearance of polyandry in highly (and mostly negatively) autocorrelated environments where no coevolutionary dynamics were allowed. Together, we interpret these results to suggest that parasites, and the antagonistic coevolutionary pressures they exert, may play an important role in the evolution of polyandry in social hymenopteran populations.