Thermoregulatory morphodynamics of honeybee swarm clusters.

During reproductive swarming, honeybee clusters of more than 10,000 individuals that hang from structures in the environment (e.g. tree branches) are exposed to diurnal variations in ambient temperature for up to a week. Swarm clusters collectively modulate their morphology in response to these variations (i.e. expanding/contracting in response to heating/cooling) to maintain their internal temperature within a tolerable range and to avoid exhausting their honey stores prematurely. To understand the spatiotemporal aspects of thermoregulatory morphing, we measured the change in size, shape and internal temperature profiles of swarm clusters in response to dynamic temperature ramp perturbations. Swarm clusters showed a two-fold variation in their volume/density when heated from 15°C to 30°C. However, they did not reach an equilibrium size or shape when held at 30°C for 5 h, long after the core temperature of the cluster had stabilized. Furthermore, the changes in cluster shape and size were hysteretic, contracting in response to cooling faster than expanding in response to heating. Although the base contact diameter of the cluster increased continuously when the swarm was heated, the change in length of the swarm (base to tip) over time was non-monotonic. Consequently, the aspect ratio of the swarm fluctuated continuously even when held at a constant temperature. Taken together, our results quantify the hysteretic and anisotropic morphological responses of swarm clusters to ambient temperature variations while suggesting that both mechanical constraints and heat transfer govern their thermoregulatory morphodynamics.

Collective ventilation in honeybee nests.

European honey bees ( Apis mellifera) live in large congested nest cavities with a single opening that limits passive ventilation. When the local air temperature exceeds a threshold, the nests are actively ventilated by bees fanning their wings at the nest entrance. Here, we show that colonies with relatively large nest entrances use an emergent ventilation strategy where fanning bees self-organize to form groups, separating regions of continuous inflow and outflow. The observed spatio-temporal patterns correlate the air velocity and air temperature along the entrances to the distribution of fanning bees. A mathematical model that couples these variables to known fanning behaviour of individuals recapitulates their collective dynamics. Additionally, the model makes predictions about the temporal stability of the fanning group as a function of the temperature difference between the environment and the nest. Consistent with these predictions, we observe that the fanning groups drift, cling to the entrance boundaries, break-up and reform as the ambient temperature varies over a period of days. Overall, our study shows how honeybees use flow-mediated communication to self-organize into a steady state in fluctuating environments.

The cues of colony size: how honey bees sense that their colony is large enough to begin to invest in reproduction.

As organisms develop, they first invest resources in survival and growth, but after reaching a certain condition they start to also invest in reproduction. Likewise, superorganisms, such as honey bee colonies, first invest in survival and growth, and later commit resources to reproduction once the number of workers in the colony surpasses a reproductive threshold. The first form of reproductive investment for a honey bee colony is the building of beeswax comb made of special large cells used for rearing males (drones). How do the workers sense that their colony is large enough to start building this 'drone comb'? To address this question, we experimentally increased three possible cues of colony size - worker density, volatile pheromone concentration and nest temperature - and looked for effects on the bees' comb construction. Only the colonies that experienced increased worker density were stimulated to build a higher proportion of drone comb. We then monitored and quantified potential cues in small and large colonies, to determine which cues change with colony size. We found that workers in large colonies, relative to small ones, have increased contact rates, spend more time active and experience less variable worker density. Whereas unicellular and multicellular organisms use mainly chemical cues to sense their sizes, our results suggest that at least one superorganism, a honey bee colony, uses physical cues to sense its size and thus its developmental state.

Wings as impellers: honey bees co-opt flight system to induce nest ventilation and disperse pheromones.

Honey bees (Apis mellifera) are remarkable fliers that regularly carry heavy loads of nectar and pollen, supported by a flight system - the wings, thorax and flight muscles - that one might assume is optimized for aerial locomotion. However, honey bees also use this system to perform other crucial tasks that are unrelated to flight. When ventilating the nest, bees grip the surface of the comb or nest entrance and fan their wings to drive airflow through the nest, and a similar wing-fanning behavior is used to disperse volatile pheromones from the Nasonov gland. In order to understand how the physical demands of these impeller-like behaviors differ from those of flight, we quantified the flapping kinematics and compared the frequency, amplitude and stroke plane angle during these non-flight behaviors with values reported for hovering honey bees. We also used a particle-based flow visualization technique to determine the direction and speed of airflow generated by a bee performing Nasonov scenting behavior. We found that ventilatory fanning behavior is kinematically distinct from both flight and scenting behavior. Both impeller-like behaviors drive flow parallel to the surface to which the bees are clinging, at typical speeds of just under 1 m s-1 We observed that the wings of fanning and scenting bees frequently contact the ground during the ventral stroke reversal, which may lead to wing wear. Finally, we observed that bees performing Nasonov scenting behavior sometimes display 'clap-and-fling' motions, in which the wings contact each other during the dorsal stroke reversal and fling apart at the start of the downstroke. We conclude that the wings and flight motor of honey bees comprise a multifunctional system, which may be subject to competing selective pressures because of its frequent use as both a propeller and an impeller.

Collective Flow Enhancement by Tandem Flapping Wings.

We examine the fluid-mechanical interactions that occur between arrays of flapping wings when operating in close proximity at a moderate Reynolds number (Re≈100-1000). Pairs of flapping wings are oscillated sinusoidally at frequency f, amplitude θ_{M}, phase offset ϕ, and wing separation distance D^{*}, and outflow speed v^{*} is measured. At a fixed separation distance, v^{*} is sensitive to both f and ϕ, and we observe both constructive and destructive interference in airspeed. v^{*} is maximized at an optimum phase offset, ϕ_{max}, which varies with wing separation distance, D^{*}. We propose a model of collective flow interactions between flapping wings based on vortex advection, which reproduces our experimental data.

Effects of trophic level and metamorphosis on discrimination of hydrogen isotopes in a plant-herbivore system.

The use of stable isotopes in ecological studies requires that we know the magnitude of discrimination factors between consumer and element sources. The causes of variation in discrimination factors for carbon and nitrogen have been relatively well studied. In contrast, the discrimination factors for hydrogen have rarely been measured. We grew cabbage looper caterpillars (Trichoplusia ni) on cabbage (Brassica oleracea) plants irrigated with four treatments of deuterium-enriched water (δD = -131, -88, -48, and -2‰, respectively), allowing some of them to reach adulthood as moths. Tissue δD values of plants, caterpillars, and moths were linearly correlated with the isotopic composition of irrigation water. However, the slope of these relationships was less than 1, and hence, discrimination factors depended on the δD value of irrigation water. We hypothesize that this dependence is an artifact of growing plants in an environment with a common atmospheric δD value. Both caterpillars and moths were significantly enriched in deuterium relative to plants by ∼45‰ and 23‰ respectively, but the moths had lower tissue to plant discrimination factors than did the caterpillars. If the trophic enrichment documented here is universal, δD values must be accounted for in geographic assignment studies. The isotopic value of carbon was transferred more or less faithfully across trophic levels, but δ(15)N values increased from plants to insects and we observed significant non-trophic (15)N enrichment in the metamorphosis from larvae to adult.