The behavioral responses of a nocturnal burrowing marsupial (Lasiorhinus latifrons) to drone flight

The use of drones in wildlife research and management is increasing. Recent evidence has demonstrated the impact of drones on animal behavior, but the response of nocturnal animals to drone flight remains unknown. Utilizing a lightweight commercial drone, the behavioral response of southern hairy‐nosed wombats (Lasiorhinus latifrons) to drone flights was observed at Kooloola Station, Swan Reach, South Australia. All wombats flown over during both day and night flights responded behaviorally to the presence of drones. The response differed based on time of day. The most common night‐time behavior elicited by drone flight was retreat, compared to stationary alertness behavior observed for daytime drone flights. The behavioral response of the wombats increased as flight altitude decreased. The marked difference of behavior between day and night indicates that this has implications for studies using drones. The behavior observed during flights was altered due to the presence of the drone, and therefore, shrewd study design is important (i.e., acclimation period to drone flight). Considering the sensory adaptations of the target species and how this may impact its behavioral response when flying at night is essential.     

Measuring disturbance at swift breeding colonies due to the visual aspects of a drone: a quasi-experiment study

There is a growing body of research indicating that drones can disturb animals. However, it is usually unclear whether the disturbance is due to visual or auditory cues. Here, we examined the effect of drone flights on the behavior of great dusky swifts Cypseloides senex and white-collared swifts Streptoprocne zonaris in 2 breeding sites where drone noise was obscured by environmental noise from waterfalls and any disturbance must be largely visual. We performed 12 experimental flights with a multirotor drone at different vertical, horizontal, and diagonal distances from the colonies. From all flights, 17% caused <1% of birds to temporarily abandon the breeding site, 50% caused half to abandon, and 33% caused more than half to abandon. We found that the diagonal distance explained 98.9% of the variability of the disturbance percentage and while at distances >50 m the disturbance percentage does not exceed 20%, at <40 m the disturbance percentage increase to > 60%. We recommend that flights with a multirotor drone during the breeding period should be conducted at a distance of >50 m and that recreational flights should be discouraged or conducted at larger distances (e.g. 100 m) in nesting birds areas such as waterfalls, canyons, and caves.     

Pheromonal activity and fine structure of the mandibular glands of honeybee drones (Apis mellifera L.) (Insecta,Hymenoptera, Apidae)

Experiments were conducted to determine the role of drone mandibular gland secretions in attracting flying drones and the effect of age on the secretory activity. Extracts of mandibular glands and of cephalic tissues were applied to cotton lures which were attached below balloons tethered at 8–12 m above the ground. Most flying drones were attracted to extracts of mandibular glands but a few were drawn to other cephalic tissues or to solvent controls. Histological and electron microscope studies showed that the structure of the tiny (0.12 mm long) mandibular gland varied according to age. Its secretory activity in 0–3-day old drones was evident from the abundant rough endoplasmic reticulum. At 7-days the glands were fully developed. After 9 days the glands were no longer active and showed an autolytic process; the product was stored in the gland lumen for further emission during drone mating flights.     

Sex and Caste-Specific Variation in Compound Eye Morphology of Five Honeybee Species

Ranging from dwarfs to giants, the species of honeybees show remarkable differences in body size that have placed evolutionary constrains on the size of sensory organs and the brain. Colonies comprise three adult phenotypes, drones and two female castes, the reproductive queen and sterile workers. The phenotypes differ with respect to tasks and thus selection pressures which additionally constrain the shape of sensory systems. In a first step to explore the variability and interaction between species size-limitations and sex and caste-specific selection pressures in sensory and neural structures in honeybees, we compared eye size, ommatidia number and distribution of facet lens diameters in drones, queens and workers of five species (Apis andreniformis, A. florea, A. dorsata, A. mellifera, A. cerana). In these species, male and female eyes show a consistent sex-specific organization with respect to eye size and regional specialization of facet diameters. Drones possess distinctly enlarged eyes with large dorsal facets. Aside from these general patterns, we found signs of unique adaptations in eyes of A. florea and A. dorsata drones. In both species, drone eyes are disproportionately enlarged. In A. dorsata the increased eye size results from enlarged facets, a likely adaptation to crepuscular mating flights. In contrast, the relative enlargement of A. florea drone eyes results from an increase in ommatidia number, suggesting strong selection for high spatial resolution. Comparison of eye morphology and published mating flight times indicates a correlation between overall light sensitivity and species-specific mating flight times. The correlation suggests an important role of ambient light intensities in the regulation of species-specific mating flight times and the evolution of the visual system. Our study further deepens insights into visual adaptations within the genus Apis and opens up future perspectives for research to better understand the timing mechanisms and sensory physiology of mating related signals.     

Mimicking a Honeybee Queen?Vespa affinis indosinensis Pérez 1910 Hunts Drones of Apis cerana F. 1793

Hornets (Vespa affinis) flying in a drone congregation area attracted drones of Apis cerana. The drones followed the hornet and were ‘manoeuvred’ towards a leaf or a tree. The hornet then rushed at one of the drones. Many attempts by the hornet to catch a drone were unsuccessful and all drones fled. After failing, the hornet returned to centre of the drone congregation area and repeated the behaviour. Only after successfully seizing of a drone did the hornet leave the drone congregation area carrying its prey. In a two-choice test in the centre of the drone congregation area, free-flying A. cerana drones preferred a hornet model to a live A. cerana queen. V. affinis apparently ‘exploits’ the intraspecific communication between queen and drones of A. cerana. Hunting of drones in the drone congregation area by V. affinis may be an example of predatory mimicry.     

Relatedness among honeybees (Apis mellifera) of a drone congregation

The honeybee (Apis mellifera) queen mates during nuptial flights, in the so-called drone congregation area where many males from surrounding colonies gather. Using 20 highly polymorphic microsatellite loci, we studied a sample of 142 drones captured in a congregation close to Oberursel (Germany). A parentage test based on lod score showed that this sample contained one group of four brothers, six groups of three brothers, 20 groups of two brothers and 80 singletons. These values are very close to a Poisson distribution. Therefore, colonies were apparently equally represented in the drone congregation, and calculations showed that the congregation comprised males that originated from about 240 different colonies. This figure is surprisingly high. Considering the density of colonies around the congregation area and the average flight range of males, it suggests that most colonies within the recruitment perimeter delegated drones to the congregation with an equal probability, resulting in an almost perfect panmixis. Consequently, the relatedness between a queen and her mates, and hence the inbreeding coefficient of the progeny, should be minimized. The relatedness among the drones mated to the same queen is also very low, maximizing the genetic diversity among the different patrilines of a colony.     

Determining colony densities in wild honeybee populations (<Emphasis Type="Italic">Apis mellifera</Emphasis>) with linked microsatellite DNA markers

Estimating the population size of social bee colonies in the wild is often difficult because nests are highly cryptic. Because of the honeybee (Apis mellifera) mating behaviour, which is characterized by multiple mating of queens at drone congregation areas (DCA), it is possible to use genotypes of drones caught at these areas to infer the number of colonies in a given region. However, DCAs are difficult to locate and we assess the effectiveness of an alternative sampling technique to determine colony density based on inferring male genotypes from queen offspring. We compare these methods in the same population of wild honeybees, Apis mellifera scutellata. A set of linked microsatellite loci is used to decrease the frequency of recombination among marker loci and therefore increase the precision of the estimates. Estimates of population size obtained through sampling of queen offspring is significantly larger than that obtained by sampling drones at DCAs. This difference may be due to the more extensive flying range of queens compared with drones on mating flights. We estimate that the population size sampled through queen offspring is about double that sampled through drones.     

Drone and Worker Brood Microclimates Are Regulated Differentially in Honey Bees,Apis mellifera

Background

Honey bee (Apis mellifera) drones and workers show differences in morphology, physiology, and behavior. Because the functions of drones are more related to colony reproduction, and those of workers relate to both survival and reproduction, we hypothesize that the microclimate for worker brood is more precisely regulated than that of drone brood.

Methodology/Principal Findings

We assessed temperature and relative humidity (RH) inside honey bee colonies for both drone and worker brood throughout the three-stage development period, using digital HOBO^® Data Loggers. The major findings of this study are that 1) both drone and worker castes show the highest temperature for eggs, followed by larvae and then pupae; 2) temperature in drones are maintained at higher precision (smaller variance) in drone eggs and larvae, but at a lower precision in pupae than the corresponding stages of workers; 3) RH regulation showed higher variance in drone than workers across all brood stages; and 4) RH regulation seems largely due to regulation by workers, as the contribution from empty honey combs are much smaller compared to that from adult workers.

Conclusions/Significance

We conclude that honey bee colonies maintain both temperature and humidity actively; that the microclimate for sealed drone brood is less precisely regulated than worker brood; and that combs with honey contribute very little to the increase of RH in honey bee colonies. These findings increase our understanding of microclimate regulation in honey bees and may have implications for beekeeping practices.     

A Game Theoretical Analysis of the Mating Sign Behavior in the Honey Bee

Queens of the honey bee, Apis mellifera (L.), exhibit extreme polyandry, mating with up to 45 different males (drones). This increases the genetic diversity of their colonies, and consequently their fitness. After copulation, drones leave a mating sign in the genital opening of the queen which has been shown to promote additional mating of the queen. On one hand, this signing behavior is beneficial for the drone because it increases the genetic diversity of the resulting colony that is to perpetuate his genes. On the other hand, it decreases the proportion of the drone??s personal offspring among colony members which is reducing drone fitness. We analyze the adaptiveness and evolutionary stability of this drone??s behavior with a game-theoretical model. We find that theoretically both the strategy of leaving a mating sign and the strategy of not leaving a mating sign can be evolutionary stable, depending on natural parameters. However, the signing strategy is not favored for most scenarios, including the cases that are biologically plausible in reference to empirical data. We conclude that leaving a sign is not in the interest of the drone unless it serves biological functions other than increasing subsequent queen mating chances. Nevertheless, our analysis can also explain the prevalence of such a behavior of honey bee drones by a very low evolutionary pressure for an invasion of the nonsigning strategy.     

Cloning and expression pattern of odorant receptor 11 in Asian honeybee drones,Apis cerana (Hymenoptera,Apidae)

Odorant receptors play a crucial role in the special recognition of scent molecules in the honeybee olfaction system. The odorant receptor 11 (AmOR11) in western honeybee drones (Apis mellifera) has been demonstrated to specifically bind to 9-oxo-2-decenoic acid (9-ODA) of queens. However, little is known regarding the functions of OR11 Asian honeybee drones (Apis cerana) in the context of their mating activities. In this study, the odorant receptor 11 gene (AcOr11) from A. cerana was cloned, and its expression profiles were examined during two developmental stages (immature and sexually mature) and different physiological statuses (flying and crawling). The cDNA sequence of AcOr11 was highly similar to that of AmOr11, and encoded a membrane-coupled protein of 384 amino acids. The results of qRT-PCR indicated that AcOr11 was expressed at higher levels in drone antennae compared to brains, and the expression was significantly up-regulated in sexually mature drone brains compared to immature brains. Interestingly, AcOr11 expression in brains of mature flying drones was dramatically higher than those of mature crawling drones. To our knowledge, this study demonstrate a link between AcOr11 gene expression in the brain of honeybee drones and behavior associated with sexual maturity and mating flight.     

Sex-Specific Differences in Pathogen Susceptibility in Honey Bees (Apis mellifera)

Sex-related differences in susceptibility to pathogens are a common phenomenon in animals. In the eusocial Hymenoptera the two female castes, workers and queens, are diploid and males are haploid. The haploid susceptibility hypothesis predicts that haploid males are more susceptible to pathogen infections compared to females. Here we test this hypothesis using adult male (drone) and female (worker) honey bees (Apis mellifera), inoculated with the gut endoparasite Nosema ceranae and/or black queen cell virus (BQCV). These pathogens were chosen due to previously reported synergistic interactions between Nosema apis and BQCV. Our data do not support synergistic interactions between N. ceranae and BQCV and also suggest that BQCV has limited effect on both drone and worker health, regardless of the infection level. However, the data clearly show that, despite lower levels of N. ceranae spores in drones than in workers, Nosema-infected drones had both a higher mortality and a lower body mass than non-infected drones, across all treatment groups, while the mortality and body mass of worker bees were largely unaffected by N. ceranae infection, suggesting that drones are more susceptible to this pathogen than workers. In conclusion, the data reveal considerable sex-specific differences in pathogen susceptibility in honey bees and highlight the importance of ultimate measures for determining susceptibility, such as mortality and body quality, rather than mere infection levels.     

Drones,automatic counting tools,and artificial neural networks in wildlife population censusing

1. The use of a drone to count the flock sizes of 33 species of waterbirds during the breeding and non‐breeding periods was investigated.
2. In 96% of 343 cases, drone counting was successful. 18.8% of non‐breeding birds and 3.6% of breeding birds exhibited adverse reactions: the former birds were flushed, whereas the latter attempted to attack the drone.
3. The automatic counting of birds was best done with ImageJ/Fiji microbiology software – the average counting rate was 100 birds in 64 s.
4. Machine learning using neural network algorithms proved to be an effective and quick way of counting birds – 100 birds in 7 s. However, the preparation of images and machine learning time is time‐consuming, so this method is recommended only for large data sets and large bird assemblages.
5. The responsible study of wildlife using a drone should only be carried out by persons experienced in the biology and behavior of the target animals.

     

Measuring the influence of unmanned aerial vehicles on Adélie penguins

Unmanned aerial vehicles (UAVs) have become a useful tool in polar research. While their performance is already proven, little is known about their impact on wildlife. To assess the disturbance caused on the penguins, flights with a UAV were conducted over an Adélie penguin (Pygoscelis adeliae) colony. Vertical and horizontal flights were performed between 10 and 50 m in altitude. Penguins’ reactions were video-recorded, and the behavioural response was used to indicate the level of disturbance. During any flight mode, disturbance increased immediately after takeoff and remained elevated at all altitudes between 20 and 50 m. When the UAV descended below 20 m, the disturbance increased further with almost all individuals being vigilant. Only at these low altitudes, vertical flights caused an even higher level of disturbance than horizontal ones. Repetitions of horizontal overflights showed no short-term habituation occurring. Since the results are only valid for the specific UAV model used, we recommend a more extensive approach with different UAV specifications. As the highest flight altitudes already caused detectable but not subjectively visible responses, we also recommend to regard subjective impressions of disturbance with caution.     

The Eye in the Sky: Combined Use of Unmanned Aerial Systems and GPS Data Loggers for Ecological Research and Conservation of Small Birds

Technological advances for wildlife monitoring have expanded our ability to study behavior and space use of many species. But biotelemetry is limited by size, weight, data memory and battery power of the attached devices, especially in animals with light body masses, such as the majority of bird species. In this study, we describe the combined use of GPS data logger information obtained from free-ranging birds, and environmental information recorded by unmanned aerial systems (UASs). As a case study, we studied habitat selection of a small raptorial bird, the lesser kestrel Falco naumanni, foraging in a highly dynamic landscape. After downloading spatio-temporal information from data loggers attached to the birds, we programmed the UASs to fly and take imagery by means of an onboard digital camera documenting the flight paths of those same birds shortly after their recorded flights. This methodology permitted us to extract environmental information at quasi-real time. We demonstrate that UASs are a useful tool for a wide variety of wildlife studies.     

Characterization of HSP70 expression in drones of Apis cerana (Hymenoptera: Apidae)

Heat shock proteins (HSPs) constitute a superfamily of molecular chaperones that are rapidly biosynthesized in response to various biotic and abiotic factors. In this study, we first cloned the full-length HSP70 gene of the Eastern honeybee Apis cerana. Then, using real-time quantitative PCR, we explored HSP70 expression profiles in drones at different developmental stages, ages, and reproductive statuses (with and without semen). The full-length HSP70 cDNA is 2421 bp, including a 1953-bp open reading frame (ORF) that encodes a polypeptide of 650 amino acids. The HSP70 gene consists of one intron and two exons. The phylogenetic analysis revealed that the HSP70 genes of A. cerana and Apis mellifera are the most closely related. We observed HSP70 expression at all selected developmental stages and detected the highest expression in pupae with an unpigmented body cuticle and brown eyes (Pb) and much lower expression in larvae hatched within 72 h. In adult drones of different ages, the highest expression level of HSP70 was observed in 16-day-old drones; significantly lower accumulation of HSP70 mRNA was detected in 4-day-old drones. There was no significant difference in HSP70 expression between drones with and without semen captured at the entrance, while the HSP70 gene expression level strikingly differed between drones captured at the entrance and the drones collected within the hive. Our study suggests that HSP70 might play a critical role in drone development and during reproductive mating events.     

Crossfostered drones ofApis cerana (Fabricius, 1793) andApis koschevnikovi (Buttel-Reepen, 1906) fly at their species specific mating times

Summary Reciprocal transfer of sealed drone brood between colonies ofApis cerana andApis koschevnikovi was successful and resulted in four colonies (two of each species) with a mixed drone population. Flights ofApis cerana drones occurred between 14.00 and 16.15 regardless whether they were in a conspecific or alien colony.Apis koschevnikovi drones also flew at their species specific time from 16.45 to 18.30. A variance estimation revealed that 99.4% of the total variance depended on the species of the drone. In contrast to theApis drone's general biological dependence upon the colony, crossfostered drones ofApis cerana andApis koschevnikovi showed an unexpected autonomy in chosing their mating flight time.     

Behavioural responses of non-breeding waterbirds to drone approach are associated with flock size and habitat

ABSTRACT

Capsule: Non-breeding waterbirds are more likely to respond to drone approach when in larger flocks, and responses are more likely in arable and coastal habitats than at inland lochs.

Aims: To investigate the extent to which drones are a potential source of disturbance to non-breeding waterbirds.

Methods: Using a commercially available quadcopter drone, we approached waterbird flocks of varying sizes in coastal, freshwater, and arable habitats following a standardized protocol.

Results: Waterbirds at coastal sites and in arable fields were more likely to respond to drone approach than those at inland freshwater bodies. Larger flocks were more likely to respond to drone approach and responded at a greater distance than smaller flocks.

Conclusion: Repeated drone use at coastal and arable sites with large aggregations of feeding or roosting waterbirds could cause energetically costly flight responses, increased stress, and effective loss of available habitat. At such sites, it may be beneficial to regulate recreational and commercial drone use to minimize potential disturbance effects.     

Extensive population admixture on drone congregation areas of the giant honeybee,Apis dorsata (Fabricius, 1793)

The giant honeybee Apis dorsata often forms dense colony aggregations which can include up to 200 often closely related nests in the same location, setting the stage for inbred matings. Yet, like in all other Apis species, A. dorsata queens mate in mid‐air on lek like drone congregation areas (DCAs) where large numbers of males gather in flight. We here report how the drone composition of A. dorsata DCAs facilitates outbreeding, taking into the account both spatial (three DCAs) and temporal (subsequent sampling days) dynamics. We compared the drones’ genotypes at ten microsatellite DNA markers with those of the queen genotypes of six drone‐producing colonies located close to the DCAs (Tenom, Sabah, Malaysia). None of 430 sampled drones originated from any of these nearby colonies. Moreover, we estimated that 141 unidentified colonies were contributing to the three DCAs. Most of these colonies were participating multiple times in the different locations and/or during the consecutive days of sampling. The drones sampled in the DCAs could be attributed to six subpopulations. These were all admixed in all DCA samples, increasing the effective population size an order of magnitude and preventing matings between potentially related queens and drones.     

Evaluating success of various restorative interventions through drone‐ and field‐collected data,using six putative framework species in Argentinian Patagonia

Field data and unmanned aerial vehicles, also known as drones, were used to analyze a long‐term experiment in a severely degraded area of the “Monte,” one of the most arid and degraded biomes in Argentina. Field methods and drone orthoimages obtained from flights of a quadcopter at 20 and 40 m were used to compare plantation plots versus natural recovery on scarified sites, and the field performance of six putative framework species under four different treatments was evaluated. After 5 years of recovery in soils with almost no organic matter and mean annual rainfall averaging 145 mm, plantation plots had high survival rates (>65%) for all species as determined through both field survey and drone imagery. Three species were planted with a greater number of seedlings due to their availability in nurseries. For these species experimental treatments were studied statistically. Independently of treatment applied (control; 1/2 L hydrogel; 1 L hydrogel; 1 L of hydrogel + 1/2 kg of organic compost), highest survival rates were found for P. flexuosa var. depressa (88% ± 14.8) and A. lampa (84% ± 14.8). Drone images and field data both showed that these two putative framework species had the highest plant cover. In sharp contrast, mechanical scarification without planting or other treatments induced very low recovery (<2%). We demonstrate that drone imagery provides a new and very valuable tool for evaluating and monitoring restorative interventions in drylands.     

Quantifying honey bee mating range and isolation in semi-isolated valleys by DNA microsatellite paternity analysis

Honey bee males and queens mate in mid air and can fly many kilometres on their nuptial flights. The conservation of native honey bees, such as the European black bee (Apis mellifera mellifera), therefore, requires large isolated areas to prevent hybridisation with other subspecies, such as A. m. ligustica or A. m. carnica, which may have been introduced by beekeepers. This study used DNA microsatellite markers to determine the mating range of A. m. mellifera in two adjacent semi-isolated valleys (Edale and Hope Valley) in the Peak District National Park, England, in order to assess their suitability for native honey bee conservation and as isolated mating locations. Three apiaries were set up in each valley, each containing 12 colonies headed by a virgin queen and 2 queenright drone producing hives. The virgin queens were allowed to mate naturally with drones from the hives we had set up and with drones from hives owned by local beekeepers. After mating, samples of worker larvae were taken from the 41 queens that mated successfully and genotyped at 11 DNA microsatellite loci. Paternity analyses were then carried out to determine mating distances and isolation. An average of 10.2 fathers were detected among the 16 worker progeny. After correction for non-detection and non-sampling errors, the mean effective mating frequency of the test queens was estimated to be 17.2, which is a normal figure for honey bees. Ninety percent of the matings occurred within a distance of 7.5 km, and fifty percent within 2.5 km. The maximal mating distance recorded was 15 km. Queens and drones did occasionally mate across the borders between the two valleys, showing that the dividing mountain ridge Losehill does not provide complete isolation. Nevertheless, in the most isolated part of Edale sixty percent of all matings were to drones from Edale hives. The large majority of observed mating distances fell within the range of Hope Valley, making this site a suitable location for the long term conservation of a breeding population of black bees.