Migration by soaring or flapping: numerical atmospheric simulations reveal that turbulence kinetic energy dictates bee-eater flight mode

Aerial migrants commonly face atmospheric dynamics that may affect their movement and behaviour. Specifically, bird flight mode has been suggested to depend on convective updraught availability and tailwind assistance. However, this has not been tested thus far since both bird tracks and meteorological conditions are difficult to measure in detail throughout extended migratory flyways. Here, we applied, to our knowledge, the first comprehensive numerical atmospheric simulations by mean of the Regional Atmospheric Modeling System (RAMS) to study how meteorological processes affect the flight behaviour of migrating birds. We followed European bee-eaters (Merops apiaster) over southern Israel using radio telemetry and contrasted bird flight mode (flapping, soaring-gliding or mixed flight) against explanatory meteorological variables estimated by RAMS simulations at a spatial grid resolution of 250 × 250 m(2). We found that temperature and especially turbulence kinetic energy (TKE) determine bee-eater flight mode, whereas, unexpectedly, no effect of tailwind assistance was found. TKE during soaring-gliding was significantly higher and distinct from TKE during flapping. We propose that applying detailed atmospheric simulations over extended migratory flyways can elucidate the highly dynamic behaviour of air-borne organisms, help predict the abundance and distribution of migrating birds, and aid in mitigating hazardous implications of bird migration.     

Abdicating power for control: a precision timing strategy to modulate function of flight power muscles

Muscles driving rhythmic locomotion typically show strong dependence of power on the timing or phase of activation. This is particularly true in insects' main flight muscles, canonical examples of muscles thought to have a dedicated power function. However, in the moth (Manduca sexta), these muscles normally activate at a phase where the instantaneous slope of the power-phase curve is steep and well below maximum power. We provide four lines of evidence demonstrating that, contrary to the current paradigm, the moth's nervous system establishes significant control authority in these muscles through precise timing modulation: (i) left-right pairs of flight muscles normally fire precisely, within 0.5-0.6 ms of each other; (ii) during a yawing optomotor response, left-right muscle timing differences shift throughout a wider 8 ms timing window, enabling at least a 50 per cent left-right power differential; (iii) timing differences correlate with turning torque; and (iv) the downstroke power muscles alone causally account for 47 per cent of turning torque. To establish (iv), we altered muscle activation during intact behaviour by stimulating individual muscle potentials to impose left-right timing differences. Because many organisms also have muscles operating with high power-phase gains (Δ(power)/Δ(phase)), this motor control strategy may be ubiquitous in locomotor systems.     

Behavioural mimicry in flight path of Batesian intraspecific polymorphic butterfly Papilio polytes

Batesian mimics that show similar coloration to unpalatable models gain a fitness advantage of reduced predation. Beyond physical similarity, mimics often exhibit behaviour similar to their models, further enhancing their protection against predation by mimicking not only the model''s physical appearance but also activity. In butterflies, there is a strong correlation between palatability and flight velocity, but there is only weak correlation between palatability and flight path. Little is known about how Batesian mimics fly. Here, we explored the flight behaviour of four butterfly species/morphs: unpalatable model Pachliopta aristolochiae, mimetic and non-mimetic females of female-limited mimic Papilio polytes, and palatable control Papilio xuthus. We demonstrated that the directional change (DC) generated by wingbeats and the standard deviation of directional change (SDDC) of mimetic females and their models were smaller than those of non-mimetic females and palatable controls. Furthermore, we found no significant difference in flight velocity among all species/morphs. By showing that DC and SDDC of mimetic females resemble those of models, we provide the first evidence for the existence of behavioural mimicry in flight path by a Batesian mimic butterfly.     

Thermal biology of flight in a butterfly: genotype,flight metabolism,and environmental conditions

Knowledge of the effects of thermal conditions on animal movement and dispersal is necessary for a mechanistic understanding of the consequences of climate change and habitat fragmentation. In particular, the flight of ectothermic insects such as small butterflies is greatly influenced by ambient temperature. Here, variation in body temperature during flight is investigated in an ecological model species, the Glanville fritillary butterfly (Melitaea cinxia). Attention is paid on the effects of flight metabolism, genotypes at candidate loci, and environmental conditions. Measurements were made under a natural range of conditions using infrared thermal imaging. Heating of flight muscles by flight metabolism has been presumed to be negligible in small butterflies. However, the results demonstrate that Glanville fritillary males with high flight metabolic rate maintain elevated body temperature better during flight than males with a low rate of flight metabolism. This effect is likely to have a significant influence on the dispersal performance and fitness of butterflies and demonstrates the possible importance of intraspecific physiological variation on dispersal in other similar ectothermic insects. The results also suggest that individuals having an advantage in low ambient temperatures can be susceptible to overheating at high temperatures. Further, tolerance of high temperatures may be important for flight performance, as indicated by an association of heat‐shock protein (Hsp70) genotype with flight metabolic rate and body temperature at takeoff. The dynamics of body temperature at flight and factors affecting it also differed significantly between female and male butterflies, indicating that thermal dynamics are governed by different mechanisms in the two sexes. This study contributes to knowledge about factors affecting intraspecific variation in dispersal‐related thermal performance in butterflies and other insects. Such information is needed for predictive models of the evolution of dispersal in the face of habitat fragmentation and climate change.     

A new algorithm quantifies the roles of wind and midge flight activity in the bluetongue epizootic in northwest Europe

The 2006 bluetongue (BT) outbreak in northwestern Europe had devastating effects on cattle and sheep in that intensively farmed area. The role of wind in disease spread, through its effect on Culicoides dispersal, is still uncertain, and remains unquantified. We examine here the relationship between farm-level infection dates and wind speed and direction within the framework of a novel model involving both mechanistic and stochastic steps. We consider wind as both a carrier of host semio-chemicals, to which midges might respond by upwind flight, and as a transporter of the midges themselves, in a more or less downwind direction. For completeness, we also consider midge movement independent of wind and various combinations of upwind, downwind and random movements. Using stochastic simulation, we are able to explain infection onset at 94 per cent of the 2025 affected farms. We conclude that 54 per cent of outbreaks occurred through (presumably midge) movement of infections over distances of no more than 5 km, 92 per cent over distances of no more than 31 km and only 2 per cent over any greater distances. The modal value for all infections combined is less than 1 km. Our analysis suggests that previous claims for a higher frequency of long-distance infections are unfounded. We suggest that many apparent long-distance infections resulted from sequences of shorter-range infections; a 'stepping stone' effect. Our analysis also found that downwind movement (the only sort so far considered in explanations of BT epidemics) is responsible for only 39 per cent of all infections, and highlights the effective contribution to disease spread of upwind midge movement, which accounted for 38 per cent of all infections. The importance of midge flight speed is also investigated. Within the same model framework, lower midge active flight speed (of 0.13 rather than 0.5 m s(-1)) reduced virtually to zero the role of upwind movement, mainly because modelled wind speeds in the area concerned were usually greater than such flight speed. Our analysis, therefore, highlights the need to improve our knowledge of midge flight speed in field situations, which is still very poorly understood. Finally, the model returned an intrinsic incubation period of 8 days, in accordance with the values reported in the literature. We argue that better understanding of the movement of infected insect vectors is an important ingredient in the management of future outbreaks of BT in Europe, and other devastating vector-borne diseases elsewhere.     

Ant attendance reduces flight muscle and wing size in the aphid Tuberculatus quercicola

In otherwise mutualistic relationships between aphids and ants, attendance by ants often has negative impacts on aphids. For example, in a previous study using traps in the field, the aphid Tuberculatus quercicola, which exhibits mutualistic interactions with ants, showed extremely low dispersal rates, despite having long wings. This study investigates whether components of the flight apparatus (mesonotum length, flight muscle and wings) differ between aphids attended by ants and not attended by ants. Randomized block analysis of variance, using body length as a covariate, showed that ant attendance has a negative influence on aphid flight apparatus. This result indicates that aphids produce honeydew at the expense of resource investment in flight apparatus. Since the dispersal of T. quercicola is limited under ant attendance, the reduction in flight apparatus could precede a decrease in body size. This study also showed that flight apparatus was more developed in aphids under ant-exclusion conditions. This may imply that T. quercicola fly when ants are not available. The maintenance of flight apparatus in T. quercicola might therefore be partly explained by gene flow on the rare occasions that this aphid species disperses.     

Nocturnal insects use optic flow for flight control

To avoid collisions when navigating through cluttered environments, flying insects must control their flight so that their sensory systems have time to detect obstacles and avoid them. To do this, day-active insects rely primarily on the pattern of apparent motion generated on the retina during flight (optic flow). However, many flying insects are active at night, when obtaining reliable visual information for flight control presents much more of a challenge. To assess whether nocturnal flying insects also rely on optic flow cues to control flight in dim light, we recorded flights of the nocturnal neotropical sweat bee, Megalopta genalis, flying along an experimental tunnel when: (i) the visual texture on each wall generated strong horizontal (front-to-back) optic flow cues, (ii) the texture on only one wall generated these cues, and (iii) horizontal optic flow cues were removed from both walls. We find that Megalopta increase their groundspeed when horizontal motion cues in the tunnel are reduced (conditions (ii) and (iii)). However, differences in the amount of horizontal optic flow on each wall of the tunnel (condition (ii)) do not affect the centred position of the bee within the flight tunnel. To better understand the behavioural response of Megalopta, we repeated the experiments on day-active bumble-bees (Bombus terrestris). Overall, our findings demonstrate that despite the limitations imposed by dim light, Megalopta-like their day-active relatives-rely heavily on vision to control flight, but that they use visual cues in a different manner from diurnal insects.     

Barb geometry of asymmetrical feathers reveals a transitional morphology in the evolution of avian flight

The geometry of feather barbs (barb length and barb angle) determines feather vane asymmetry and vane rigidity, which are both critical to a feather''s aerodynamic performance. Here, we describe the relationship between barb geometry and aerodynamic function across the evolutionary history of asymmetrical flight feathers, from Mesozoic taxa outside of modern avian diversity (Microraptor, Archaeopteryx, Sapeornis, Confuciusornis and the enantiornithine Eopengornis) to an extensive sample of modern birds. Contrary to previous assumptions, we find that barb angle is not related to vane-width asymmetry; instead barb angle varies with vane function, whereas barb length variation determines vane asymmetry. We demonstrate that barb geometry significantly differs among functionally distinct portions of flight feather vanes, and that cutting-edge leading vanes occupy a distinct region of morphospace characterized by small barb angles. This cutting-edge vane morphology is ubiquitous across a phylogenetically and functionally diverse sample of modern birds and Mesozoic stem birds, revealing a fundamental aerodynamic adaptation that has persisted from the Late Jurassic. However, in Mesozoic taxa stemward of Ornithurae and Enantiornithes, trailing vane barb geometry is distinctly different from that of modern birds. In both modern birds and enantiornithines, trailing vanes have larger barb angles than in comparatively stemward taxa like Archaeopteryx, which exhibit small trailing vane barb angles. This discovery reveals a previously unrecognized evolutionary transition in flight feather morphology, which has important implications for the flight capacity of early feathered theropods such as Archaeopteryx and Microraptor. Our findings suggest that the fully modern avian flight feather, and possibly a modern capacity for powered flight, evolved crownward of Confuciusornis, long after the origin of asymmetrical flight feathers, and much later than previously recognized.     

Interaction between Varroa destructor and imidacloprid reduces flight capacity of honeybees

Current high losses of honeybees seriously threaten crop pollination. Whereas parasite exposure is acknowledged as an important cause of these losses, the role of insecticides is controversial. Parasites and neonicotinoid insecticides reduce homing success of foragers (e.g. by reduced orientation), but it is unknown whether they negatively affect flight capacity. We investigated how exposing colonies to the parasitic mite Varroa destructor and the neonicotinoid insecticide imidacloprid affect flight capacity of foragers. Flight distance, time and speed of foragers were measured in flight mills to assess the relative and interactive effects of high V. destructor load and a field-realistic, chronic sub-lethal dose of imidacloprid. Foragers from colonies exposed to high levels of V. destructor flew shorter distances, with a larger effect when also exposed to imidacloprid. Bee body mass partly explained our results as bees were heavier when exposed to these stressors, possibly due to an earlier onset of foraging. Our findings contribute to understanding of interacting stressors that can explain colony losses. Reduced flight capacity decreases the food-collecting ability of honeybees and may hamper the use of precocious foraging as a coping mechanism during colony (nutritional) stress. Ineffective coping mechanisms may lead to destructive cascading effects and subsequent colony collapse.     

Flight of the honey bee VII: metabolic power versus flight speed relation

The existing experimental data on metabolic power P _m of honey bees are critically discussed, partly corrected for real flight conditions and plotted as a function of flight speed v. New wind tunnel measurements of tethered flight under near-natural conditions are added in the range 3.3<v<5.1 m·s^-1, derived from exhaustion flight measurements. Within this small sector the latter measurements can be characterised by a linear correlation: P _m(mW)=6.72v (m·s^-1)+13.83, the slope of which is significantly different from zero. The over-all P _m(v) curve is significantly not a straight line of zero slope but a U-shaped minimum curve and may be approximated by a second-order polynom: P _m=49.2-8.9v+1.5v ². The same is true for relative metabolic power, P _{m rel (e)} related to empty body mass of 76.5 mg: P _{m rel(e)}=630.0-114.0v+19.2v ² (P _m in mW: P _{m rel} in mW·g^-1; v in m·s^-1). The data support the existence of a U-shaped power-versus-speed curve in bees.Abbreviations bm body mass (mg) - f full - e empty - mu muscles - P _m (mJ·s^-1=mW) metabolic power (input) - P _{m rel} (mW·g^-1) relative metabolic power - P _mec (mW) mechanical power (output) - efficiency (of the flight musculature) - t(s) flight time - v (m·s^-1) relative speed between bee and air     

Light,heat, action: neural control of fruit fly behaviour

The fruit fly Drosophila melanogaster has emerged as a popular model to investigate fundamental principles of neural circuit operation. The sophisticated genetics and small brain permit a cellular resolution understanding of innate and learned behavioural processes. Relatively recent genetic and technical advances provide the means to specifically and reproducibly manipulate the function of many fly neurons with temporal resolution. The same cellular precision can also be exploited to express genetically encoded reporters of neural activity and cell-signalling pathways. Combining these approaches in living behaving animals has great potential to generate a holistic view of behavioural control that transcends the usual molecular, cellular and systems boundaries. In this review, we discuss these approaches with particular emphasis on the pioneering studies and those involving learning and memory.     

Differences in pollen viability in relation to different deceptive pollination strategies in Mediterranean orchids

Background and Aims

To date, current research involving pollen viability has been evaluated in a relatively low number of orchid species. In the present study, we focused on five related Mediterranean orchid genera (Anacamptis, Orchis, Dactylorhiza, Ophrys and Serapias) that are characterized by different types of deceptive pollination.

Methods

The in vitro germination ability of increasingly aged pollinaria of eight food-, seven sexually and two shelter-deceptive species was evaluated. Pollination experiments on two food-, one sexually and one shelter-deceptive species were also performed and the percentage of embryonate seeds derived from the increasingly aged pollinaria was checked.

Key Results

All of the examined species showed long-term viabilities (=50 % pollen tube growth) that ranged from 8 to 35 d. Species with the same deceptive pollination strategies exhibited the same pollen viability trends. Interestingly, pollen viabilities of species groups with different deception types have shown significant differences, with sexually and shelter- deceptive species exhibiting a shorter life span than food-deceptive species.

Conclusions

This study confirms the prolonged germination and fertilization capacities of orchid pollinaria, and to our knowledge is the first report demonstrating a clear relationship between pollen viability and pollination system. It is proposed that this relationship is attributed to the different types of reproductive barriers, pre- or post-zygotic, that characterixe Ophrys and Serapias and the food-deceptive species, respectively.     

Using sutures to attach miniature tracking tags to small bats for multimonth movement and behavioral studies

Determining the detailed movements of individual animals often requires them to carry tracking devices, but tracking broad-scale movement of small bats (<30 g) has been limited by transmitter technology and long-term attachment methods. This limitation inhibits our understanding of bat dispersal and migration, particularly in the context of emerging conservation issues such as fatalities at wind turbines and diseases. We tested a novel method of attaching lightweight global positioning system (GPS) tags and geolocating data loggers to small bats. We used monofilament, synthetic, absorbable sutures to secure GPS tags and data loggers to the skin of anesthetized big brown bats (Eptesicus fuscus) in Colorado and hoary bats (Lasiurus cinereus) in California. GPS tags and data loggers were sutured to 17 bats in this study. Three tagged bats were recaptured 7 months after initial deployment, with tags still attached; none of these bats showed ill effects from the tag. No severe injuries were apparent upon recapture of 6 additional bats that carried tags up to 26 days after attachment; however, one of the bats exhibited skin chafing. Use of absorbable sutures to affix small tracking devices seems to be a safe, effective method for studying movements of bats over multiple months, although additional testing is warranted. This new attachment method has the potential to quickly advance our understanding of small bats, particularly as more sophisticated miniature tracking devices (e.g., satellite tags) become available.     

Thermoregulation in male temperate bats depends on habitat characteristics

Several energy-saving strategies have evolved in animals, one example being the short-term reduction of metabolism and body temperature (torpor) in endotherms. For bats, pronounced torpor behaviour has been described. The aim of this study was to assess individual variation in torpor expression of male Myotis daubentonii, and to analyse whether this variation is related to habitat characteristics. For that we measured skin temperatures of bats from different habitats using radio transmitters and also recorded ambient temperature. Skin temperature was corrected for ambient temperature and individual body mass. Cluster analysis of residuals revealed two different thermoregulatory strategies. Males in cluster 1 were more often encountered torpid and reached lower minimum skin temperatures than males in cluster 2. The differences in behaviour were related to environmental variables (water surface area near the roost, roost altitude, precipitation, ambient temperature in the warmest quarter of the year). Males from cluster 1 occupied less favourable habitats (less water surface, higher altitudes, wetter and colder climate) than males from cluster 2. Our data suggest a linkage between torpor behaviour and habitat characteristics. These characteristics could be used to identify favourable and marginal habitats for M. daubentonii.     

Pathophysiology of white-nose syndrome in bats: a mechanistic model linking wing damage to mortality

White-nose syndrome is devastating North American bat populations but we lack basic information on disease mechanisms. Altered blood physiology owing to epidermal invasion by the fungal pathogen Geomyces destructans (Gd) has been hypothesized as a cause of disrupted torpor patterns of affected hibernating bats, leading to mortality. Here, we present data on blood electrolyte concentration, haematology and acid–base balance of hibernating little brown bats, Myotis lucifugus, following experimental inoculation with Gd. Compared with controls, infected bats showed electrolyte depletion (i.e. lower plasma sodium), changes in haematology (i.e. increased haematocrit and decreased glucose) and disrupted acid–base balance (i.e. lower CO₂ partial pressure and bicarbonate). These findings indicate hypotonic dehydration, hypovolaemia and metabolic acidosis. We propose a mechanistic model linking tissue damage to altered homeostasis and morbidity/mortality.     

Flight speeds of swifts (Apus apus): seasonal differences smaller than expected

We have studied the nocturnal flight behaviour of the common swift (Apus apus L.), by the use of a tracking radar. Birds were tracked from Lund University in southern Sweden during spring migration, summer roosting flights and autumn migration. Flight speeds were compared with predictions from flight mechanical and optimal migration theories. During spring, flight speeds were predicted to be higher than during both summer and autumn due to time restriction. In such cases, birds fly at a flight speed that maximizes the overall speed of migration. For summer roosting flights, speeds were predicted to be lower than during both spring and autumn since the predicted flight speed is the minimum power speed that involves the lowest energy consumption per unit time. During autumn, we expected flight speeds to be higher than during summer but lower than during spring since the expected flight speed is the maximum range speed, which involves the lowest energy consumption per unit distance. Flight speeds during spring were indeed higher than during both summer and autumn, which indicates time-selected spring migration. Speeds during autumn migration were very similar to those recorded during summer roosting flights. The general result shows that swifts change their flight speed between different flight behaviours to a smaller extent than expected. Furthermore, the difference between flight speeds during migration and roosting among swifts was found to be less pronounced than previously recorded.     

Successful foraging zones of southern elephant seals from the Kerguelen Islands in relation to oceanographic conditions

Southern elephant seals, Mirounga leonina, undertake large-scale oceanic movements to access favourable foraging areas. Successful foraging areas of elephant seals from the Kerguelen Islands are investigated here in relation to oceanographic parameters. Movements and diving activity of the seals as well as oceanographic data were collected through a new generation of satellite relayed devices measuring and transmitting locations, pressure, temperature and salinity. For the first time, we have associated foraging behaviour, determined by high increased sinuosity in tracks, and dive density (i.e. number of dives performed per kilometre covered), and changes in body condition, determined by variations in drift rate obtained from drift dives, to identify the oceanographic conditions of successful foraging zones for this species. Two main sectors, one close to the Antarctic continent and the other along the Polar Front (PF), where both foraging activity and body condition increase, seem to be of particular interest for the seals. Within these regions, some seals tended to focus their foraging activity on zones with particular temperature signatures. Along the Antarctic continent, some seals targeted colder waters on the sea bottom during benthic dives, while at the PF the favourable zones tended to be warmer. The possible negative effect of colder waters in Antarctic on the swimming performances of potential fish or squid prey could explain the behaviour of elephant seals in these zones, while warmer waters within the PF could correspond to the optimal conditions for potential myctophid prey of elephant seals.     

Hibernation does not affect memory retention in bats

Long-term memory can be critically important for animals in a variety of contexts, and yet the extreme reduction in body temperature in hibernating animals alters neurochemistry and may therefore impair brain function. Behavioural studies on memory impairment associated with hibernation have been almost exclusively conducted on ground squirrels (Rodentia) and provide conflicting results, including clear evidence for memory loss. Here, we for the first time tested memory retention after hibernation for a vertebrate outside rodents—bats (Chiroptera). In the light of the high mobility, ecology and long life of bats, we hypothesized that maintenance of consolidated memory through hibernation is under strong natural selection. We trained bats to find food in one out of three maze arms. After training, the pre-hibernation performance of all individuals was at 100 per cent correct decisions. After this pre-test, one group of bats was kept, with two interruptions, at 7°C for two months, while the other group was kept under conditions that prevented them from going into hibernation. The hibernated bats performed at the same high level as before hibernation and as the non-hibernated controls. Our data suggest that bats benefit from an as yet unknown neuroprotective mechanism to prevent memory loss in the cold brain.