Biology and oviposition behavior of the phorid Apocephalus attophilus and the response of its host, the leaf-cutting ant Atta laevigata

Atta laevigata (Smith) (Hymenoptera: Formicidae) foragers collected in the field and parasitized by Apocephalus attophilus Borgmeier (Diptera: Phoridae) (1.2% of sampled ants) were larger and had lower survival rates than similar non-parasitized foragers. Moreover, the size of parasitized ants was significantly correlated with the number of A. attophilus puparia and percentage of adult emergence. These results suggest that host size is important for the reproductive success of A. attophilus. Different from most ant-parasitizing phorids, A. attophilus exhibits a pre-oviposition behavior that involves walking towards the host and inspecting it, and this careful approach may be responsible for a relatively low percentage of parasitoid detection by A. laevigata. When an exotic resource (Acalypha sp. leaves) was placed on ants' foraging trails, more foragers were recruited, which resulted in the attraction of A. attophilus. The number and recruiting rates of small workers (minima) were significantly higher on leaves visited by A. attophilus, but larger foragers showed no response to phorids. These results demonstrated that minima react to the presence of A. attophilus and suggest a defensive role of these ants against phorid parasitism.     

A thelytokous lineage of socially parasitic honey bees has retained heterozygosity despite at least 10 years of inbreeding

The honey bee population of South Africa is divided into two subspecies: a northern population in which queenless workers reproduce arrhenotokously and a southern one in which workers reproduce thelytokously. A hybrid zone separates the two, but on at least three occasions the northern population has become infested by reproductive workers derived from the southern population. These parasitic workers lay in host colonies parthenogenetically, resulting in yet more parasites. The current infestation is 20-year old--surprising because an asexual lineage is expected to show a decline in vigor over time due to increasing homozygosity. The decline is expected to be acute in honey bees, where homozygosity at the sex locus is lethal. We surveyed colonies from the zone of infestation and genotyped putative parasites at two sets of linked microsatellite loci. We confirm that there is a single clonal lineage of parasites that shows minor variations arising from recombination events. The lineage shows high levels of heterozygosity, which may be maintained by selection against homozygotes, or by a reduction in recombination frequency within the lineage. We suggest that the clonal lineage can endure the costs of asexual reproduction because of the fitness benefits of its parasitic life history.     

A simple and distinctive microbiota associated with honey bees and bumble bees

Specialized relationships with bacteria often allow animals to exploit a new diet by providing a novel set of metabolic capabilities. Bees are a monophyletic group of Hymenoptera that transitioned to a completely herbivorous diet from the carnivorous diet of their wasp ancestors. Recent culture-independent studies suggest that a set of distinctive bacterial species inhabits the gut of the honey bee, Apis mellifera. Here we survey the gut microbiotae of diverse bee and wasp species to test whether acquisition of these bacteria was associated with the transition to herbivory in bees generally. We found that most bee species lack phylotypes that are the same or similar to those typical of A. mellifera, rejecting the hypothesis that this dietary transition was symbiont-dependent. The most common bacteria in solitary bee species are a widespread phylotype of Burkholderia and the pervasive insect associate, Wolbachia. In contrast, several social representatives of corbiculate bees do possess distinctive bacterial phylotypes. Samples of A. mellifera harboured the same microbiota as in previous surveys, and closely related bacterial phylotypes were identified in two Asian honey bees (Apis andreniformis and Apis dorsata) and several bumble bee (Bombus) species. Potentially, the sociality of Apis and Bombus species facilitates symbiont transmission and thus is key to the maintenance of a more consistent gut microbiota. Phylogenetic analyses provide a more refined taxonomic placement of the A. mellifera symbionts.     

Metabolic response to alarm pheromone in honey bees

Exposure to alarm pheromone elicits increases in oxidative metabolism in Apis mellifera. The following quantitative results are reported: (1) The alarm response, measured by short-term elevated oxygen consumption in each bee, increases with increasing numbers of bees in the test groups. The rate of increase in response per bee shows a group effect which is greatest in small groups (1–100 bees) and remains constant in larger groups (up to 6,700 bees). (2) The pheromone concentration affects the reaction elicited. The greater the dose, the larger is the reaction up to a concentration of 2.4 μg/ml. Greater doses elicit no greater response. (3) Response to the pheromone by winter bees is maximum at 20°C and decreases at air temperatures above or below this value. (4) This metabolic reaction may provide a tool for quantitating temperament of honey bees.     

Methods to estimate breeding values in honey bees

Background

Efficient methodologies based on animal models are widely used to estimate breeding values in farm animals. These methods are not applicable in honey bees because of their mode of reproduction. Observations are recorded on colonies, which consist of a single queen and thousands of workers that descended from the queen mated to 10 to 20 drones. Drones are haploid and sperms are copies of a drone’s genotype. As a consequence, Mendelian sampling terms of full-sibs are correlated, such that the covariance matrix of Mendelian sampling terms is not diagonal.

Results

In this paper, we show how the numerator relationship matrix and its inverse can be obtained for honey bee populations. We present algorithms to derive the covariance matrix of Mendelian sampling terms that accounts for correlated terms. The resulting matrix is a block-diagonal matrix, with a small block for each full-sib family, and is easy to invert numerically. The method allows incorporating the within-colony distribution of progeny from drone-producing queens and drones, such that estimates of breeding values weigh information from relatives appropriately. Simulation shows that the resulting estimated breeding values are unbiased predictors of true breeding values. Benefits for response to selection, compared to an existing approximate method, appear to be limited (~5%). Benefits may however be greater when estimating genetic parameters.

Conclusions

This work shows how the relationship matrix and its inverse can be developed for honey bee populations, and used to estimate breeding values and variance components.     

Regulation of nectar collection in relation to honey storage levels by honey bees, Apis mellifera

Honey bees collect distinct nutrient sources in the form ofnectar (energy) and pollen (nitrogen). We investigated the effectof varying energy stores on nectar and pollen foraging. We foundno significant changes in nectar foraging in response to changesin honey storage levels within colonies. Individual foragersdid not vary activity rates or nectar load sizes in responseto changes in honey stores, and colonies did not increase nectarintake rates when honey stores within the hive were decreased.This result contrasts with pollen foraging behavior, which isextremely sensitive to colony state. Our data show that individualforaging decisions during nectar collection and colony regulationof nectar intake are distincdy different from pollen foraging.The behavior of honey bees illustrates that foraging strategy(and therefore foraging models) can incorporate multiple currencies,including both energy and protein intake.[Behav Ecol 7: 286–291(1996)]     

A modeling approach to swarming in honey bees (Apis mellifera)

Identifying the mechanisms of colony reproduction is essential to understanding the sociobiology of honey bees. Although several proximate causes leading to the initiation of queen rearing – an essential prerequisite to swarming – have been proposed, none have received unequivocal empirical support. Here we model the main proximate hypotheses (colony size, brood comb congestion, and worker age distribution) and show that all proposed swarming triggers occur as a function of the ultimate cause of a colony reaching replacement stability, the point at which the queen has been laying eggs at her maximal rate. We thus present a reproductive optimization model of colony swarming based on evolutionary principles. All models produce results remarkably similar both to each other and to empirically-determined swarming patterns. An examination of the fit between the individual models and swarm-preventing techniques used by beekeepers indicates that the reproductive optimization model has a relatively broad explanatory range. These results suggest that an examination into the behavioral correlates of a queen’s maximum egg laying rate may provide a unified proximate mechanistic trigger leading predictably to colony fission. Generating a predictive model for this very well studied animal is the first step in producing a model of colony fission applicable to other swarm-founding eusocial animals. Received 16 November 2004; revised 31 May 2005; accepted 27 June 2005.     

Taxonomy and preliminary phylogeny of the parasitic genus Apocephalus, subgenus Mesophora (Diptera: Phoridae)

Abstract. The species of Apocephalus , subgenus Mesophora , are revised and twenty-eight species are recognized, including the following twenty-two new to science: from the Nearctic Region A. brunnipes, A. gemursus, A. pristinus, A. setialvus and A. unitarsus , and from the Neotropical Region A. absentis, A. adustus, A. anfractus, A. angustistylus, A. bisetus, A. brevicercus, A. curtus, A. gracilis, A. hansoni, A. leptotarsus, A. longistylus, A. micrepelis, A. moraviensis, A. prolatus, A. trisetus, A. tritarsus and A. truncaticercus. Additionally, three species known only from female specimens are described but not formally named. A lectotype is designated for A. mortifer Borgmeier, and immature stages of A. borealis, A. antennatus and A. mortifer are described. Unlike larvae of other Apocephalus species, all of which are parasites of ants (Hymenoptera: Formicidae), those of Mesophora species are parasites of various other hosts.     

Characterization of development, behavior and neuromuscular physiology in the phorid fly, Megaselia scalaris

The Phoridae is known as 'scuttle flies' because they walk in rapid bursts of movement with short pauses between. In this study, larval locomotive behavior and development was characterized in the phorid, Megaselia scalaris. Comparison was made with the well-characterized fruit fly model, Drosophila melanogaster. Developmentally, the rate of maturation was consistently slower for Megaselia than Drosophila. This disparity was exaggerated at lower temperatures, particularly during larval development. In addition to slower growth, movements in Megaselia were also slower, as evidenced by reduced rates of larval body wall contractions and mouth hook movements. Megaselia larvae also displayed a unique behavior of swallowing air when exposed to a small pool of liquid. This permitted floating upon immersion and, therefore, might prevent drowning in the natural environment. The anatomical and physiological properties of a neuromuscular junction in the phorid larvae were also examined. The innervation of the motor nerve terminals on the ventral abdominal muscle (m6) is innervated by Type Ib and Is axons, similar to Drosophila. As in Drosophila, the Is terminals produce larger excitatory postsynaptic potentials (EPSPs) than the Ib. The amplitudes of the EPSPs in M. scalaris were reduced compared to those of D. melanogaster, but unlike D. melanogaster the EPSPs showed marked facilitation when stimulated with a 20 Hz train. We conclude that there may be differences in synaptic structure of the nerve terminals that could account for the different electrophysiological behaviors.     

Comparing the effects of five naturally occurring monosaccharide and oligosaccharide sugars on longevity and carbohydrate nutrient levels of a parasitic phorid fly, Pseudacteon tricuspis

Abstract.  The longevity and nutrient levels of Pseudacteon tricuspis provided with 1  m solutions of five naturally occurring sugars, fructose, glucose, sucrose, trehalose and melezitose, are compared. All but melezitose, result in significant increases in the longevity of P. tricuspis in comparison with sugar-starved flies (flies provided with water only). Sugar-starved female and male P. tricuspis have an average longevity of 3.3 and 4.1 days, respectively. Provision of free water in addition to sugar solution is necessary for optimum longevity by female and male flies. Longevity is increased by 2.4–2.6-fold by the two monosaccharides, fructose and glucose, and by 2.6–2.8-fold by the disaccharides, sucrose and trehalose. Phorid flies provided with the trisaccharide sugar, melezitose, had a marginal increase in lifespan (approximately 1 day), but this is not significantly different from the longevity of sugar-starved flies. Significantly greater levels of total sugars are detected in P. tricuspis fed the disaccharide sugars (sucrose, trehalose) or the monosaccharide sugars (fructose, glucose), compared with flies provided with melezitose (trisaccharide), or to sugar-starved flies. Fructose is not detected in sugar-starved flies, or in flies fed glucose or trehalose. However, high levels of fructose are detected in flies fed sucrose or fructose, whereas levels of fructose in melezitose-fed flies are intermediate. In general, significantly greater glycogen levels are detected in P. tricuspis fed sucrose, glucose, trehalose or fructose, compared with melezitose-fed or sugar-starved flies. Levels of total sugars and glycogen in sugar-fed flies are positively correlated with wing length, possibly indicating a higher accumulation of storage sugars by larger flies. These results are discussed in relation to the nutritional ecology of the phorid fly.     

Mortality rates of honey bees in the wild

Senescence, defined as an age-specific decrease in physiological performance accompanied by an increase in mortality rate, has been studied in a wide range of animals including social insects. It is not clear, however, whether honey bees in the wild live long enough to exhibit senescent decline. I tested for the effects of senescence on honey bees foraging in natural settings and documented the predicted pattern of exponential increase in mortality rate with forager age. These data indicate that, in spite of high rates of external mortality, senescence is an important factor determining the performance of insects such as honey bees in the wild. Received 16 November 2007; revised 1 February 2008 and 10 March 2008; accepted 18 March 2008.