Prison construction and guarding behaviour by European honeybees is dependent on inmate small hive beetle density

Increasing small hive beetle (Aethina tumida Murray) density changes prison construction and guarding behaviour in European honeybees (Apis mellifera L.). These changes include more guard bees per imprisoned beetle and the construction of more beetle prisons at the higher beetle density. Despite this, the number of beetles per prison (inmate density) did not change. Beetles solicited food more actively at the higher density and at night. In response, guard bees increased their aggressive behaviour towards beetle prisoners but did not feed beetles more at the higher density. Only 5% of all beetles were found among the combs at the low density but this percentage increased five-fold at the higher one. Successful comb infiltration (and thus reproduction) by beetles is a possible explanation for the significant damage beetles cause to European honeybee colonies in the USA.     

Social encapsulation of beetle parasites by Cape honeybee colonies (Apis mellifera capensis Esch.)

Worker honeybees (Apis mellifera capensis) encapsulate the small hive beetle (Aethina tumida), a nest parasite, in propolis (tree resin collected by the bees). The encapsulation process lasts 1-4 days and the bees have a sophisticated guarding strategy for limiting the escape of beetles during encapsulation. Some encapsulated beetles died (4.9%) and a few escaped (1.6%). Encapsulation has probably evolved because the small hive beetle cannot easily be killed by the bees due to its hard exoskeleton and defensive behaviour.     

The alternative Pharaoh approach: stingless bees mummify beetle parasites alive

Workers from social insect colonies use different defence strategies to combat invaders. Nevertheless, some parasitic species are able to bypass colony defences. In particular, some beetle nest invaders cannot be killed or removed by workers of social bees, thus creating the need for alternative social defence strategies to ensure colony survival. Here we show, using diagnostic radioentomology, that stingless bee workers (Trigona carbonaria) immediately mummify invading adult small hive beetles (Aethina tumida) alive by coating them with a mixture of resin, wax and mud, thereby preventing severe damage to the colony. In sharp contrast to the responses of honeybee and bumblebee colonies, the rapid live mummification strategy of T. carbonaria effectively prevents beetle advancements and removes their ability to reproduce. The convergent evolution of mummification in stingless bees and encapsulation in honeybees is another striking example of co-evolution between insect societies and their parasites.     

Oviposition by small hive beetles elicits hygienic responses from Cape honeybees

Two novel behaviours, both adaptations of small hive beetles (Aethina tumida Murray) and Cape honeybees (Apis mellifera capensis Esch.), are described. Beetles puncture the sides of empty cells and oviposit under the pupae in adjoining cells. However, bees detect this ruse and remove infested brood (hygienic behaviour), even under such well-disguised conditions. Indeed, bees removed 91% of treatment brood (brood cells with punctured walls caused by beetles) but only 2% of control brood (brood not exposed to beetles). Only 91% of treatment brood actually contained beetle eggs; the data therefore suggest that bees remove only that brood containing beetle eggs and leave uninfected brood alone, even if beetles have accessed (but not oviposited on) the brood. Although this unique oviposition strategy by beetles appears both elusive and adaptive, Cape honeybees are able to detect and remove virtually all of the infested brood.     

Ecosystem engineering by leaf-rolling mites enhances arthropod diversity

Bombardier beetles (Coleoptera, Carabidae, Brachininae) possess a remarkable defense mechanism where a hot chemical spray is released from the tip of their abdomen, with an audible explosive sound. To date, the repellent properties of these chemicals have been tested against a limited number of taxa, such as amphibians and insects. To investigate the impact of bombardier beetle defenses on avian predators, feeding trials were conducted using the bombardier beetle (Pheropsophus jessoensis) and the Japanese quail (Coturnix japonica), a sympatric and generalist predator. All naïve, hand-reared quail attacked live beetles, indicating the absence of an innate aversion to them. However, most of the quail rejected consuming the beetles whether or not the beetles sprayed them with chemicals. Naïve quail also rejected dead P. jessoensis individuals. These results support the recent hypothesis that it is not essential for P. jessoensis to spray noxious chemicals to deter predators. We also found that some of the quail exposed to live P. jessoensis remembered to avoid them for up to 5 weeks. Our results provide the first evidence of the repelling effects of bombardier beetle defense mechanisms on avian predators.

     

A behavioral study of the beetle Tenebrio molitor infected with cysticercoids of the rat tapeworm Hymenolepis diminuta

The host–parasite relationship, Tenebrio molitor–Hymenolepis diminuta, was analyzed. The learning behavior of infected and uninfected (control) beetles in a T-maze was compared. The infected beetles moved much slower in the T-maze than the controls. The infected beetles reached the same level of learning as the controls. However, they needed more trials than the controls. The effect of the infection was already distinct after the first week and even higher after the second week. This indicates that the initial phase of infection caused stress in the beetles. Longer infection did not worsen their ability to learn. Thus, the parasites clearly changed the behavior of their intermediate host and probably made them more susceptible to their final host, the rat.     

Microfluidic photomechanic infrared receptors in a pyrophilous flat bug

Infrared (IR) receptors are so far known only in boid and crotalid snakes and in three genera of pyrophilous beetles that seek out forest fires. Pyrophilous insects can also be found in other orders, however, so it can be hypothesised that IR receptors also occur in some of these species. We investigated the pyrophilous Australian flat bug Aradus albicornis and found a small number of dome-shaped sensilla (diameter 13 microm) on the prothorax, which have previously not been described. Ultrastructural investigations revealed that the sensilla are characterised by a fluid-filled inner compartment enclosed in a round cuticular shell. The cuticular apparatus is innervated by the dendrite of a ciliary mechanoreceptor, which is fluidically coupled to the inner compartment. Electrophysiological recordings demonstrated that the sensilla respond to brief warming by red laser light or to broadband IR radiation. Depending on the radiation intensity (4.4-549 mW/cm(2) tested, threshold measured as 11.3 mW/cm(2)), first spike latencies varied between 3.4 and 7.5 ms. Thus, our findings demonstrate that A. albicornis most probably possesses photomechanic IR sensilla resembling the metathoracic IR sensilla of buprestid beetles of the genus Melanophila. In the Melanophila sensillum, IR radiation causes thermal expansion of a fluid, which rapidly deforms the dendritic membrane of a mechanosensory cell. The existence of photomechanic IR receptors in both beetles and bugs demonstrates a remarkable convergent evolution towards this particular biophysical transduction mechanism and suggests that it provides selective advantages over other possible solutions.     

Floral odor learning within the hive affects honeybees’ foraging decisions

Honeybees learn odor cues quickly and efficiently when visiting rewarding flowers. Memorization of these cues facilitates the localization and recognition of food sources during foraging flights. Bees can also use information gained inside the hive during social interactions with successful foragers. An important information cue that can be learned during these interactions is food odor. However, little is known about how floral odors learned in the hive affect later decisions of foragers in the field. We studied the effect of food scent on foraging preferences when this learning is acquired directly inside the hive. By using in-hive feeders that were removed 24 h before the test, we showed that foragers use the odor information acquired during a 3-day stimulation period with a scented solution during a food-choice situation outside the nest. This bias in food preference is maintained even 24 h after the replacement of all the hive combs. Thus, without being previously collected outside by foragers, food odors learned within the hive can be used during short-range foraging flights. Moreover, correct landings at a dual-choice device after replacing the storing combs suggests that long-term memories formed within the colony can be retrieved while bees search for food in the field.     

Plant origin of Okinawan propolis: honeybee behavior observation and phytochemical analysis

Propolis is a natural resinous product collected by honeybees from certain plants. It has gained popularity as a food and alternative medicine. Poplar and Baccharis are well known as the source plants of European and Brazilian propolis, respectively. However, the propolis from Okinawa, Japan, contains some prenylflavonoids not seen in other regions such as Europe and Brazil, suggesting that the plant origin of Okinawan propolis is a particular plant that grows in Okinawa. To identify the plant origin of Okinawan propolis, we observed the behavior of honeybees as they collected material from plants and caulked it inside the hive. Honeybees scraped resinous material from the surface of plant fruits of Macaranga tanarius and brought it back to their hive to use it as propolis. We collected samples of the plant and propolis, and compared their constituents by high-performance liquid chromatography with a photo-diode array detector. We also compared their 1,1-diphenyl-2-picryl-hydrazyl radical scavenging activity. The chemical constituents and biological activity of the ethanol extracts of the plant did not differ from those of propolis. This indicates directly that the plant origin of Okinawan propolis is M. tanarius. S. K. and J. N. contributed equally to this work.     

Recruits of the stingless bee Scaptotrigona pectoralis learn food odors from the nest atmosphere

The ability to learn food odors inside the nest and to associate them with food sources in the field is of essential importance for the recruitment of nestmates in social bees. We investigated odor learning by workers within the hive and the influence of these odors on their food choice in the field in the stingless bee Scaptotrigona pectoralis. During the experiments, recruited bees had to choose between two feeders, one with an odor that was present inside the nest during the recruitment process, and one with an unknown odor. In all experiments with different odor combinations (linalool/phenylacetaldehyde, geraniol/eugenol) a significant majority of bees visited the feeder with the odor they had experienced in their nest (χ ²-tests; p?<?0.05). By contrast, the bees showed no preference for one of two feeders when they were either baited with the same odor (linalool) or contained no odor. Our results clearly show that naïve workers of S. pectoralis can learn the odor of a food source during the recruitment process from the nest atmosphere and that their subsequent food search in the field is influenced by the learned odor.     

Foraging reactivation in the honeybee Apis mellifera L.: factors affecting the return to known nectar sources

This paper addresses, what determines that experienced forager honeybees return to places where they have previously exploited nectar. Although there was already some evidence that dance and trophallaxis can cause bees to return to feed, the fraction of unemployed foragers that follow dance or receive food from employed foragers before revisiting the feeder was unknown. We found that 27% of the experienced foragers had no contact with the returning foragers inside the hive. The most common interactions were dance following (64%) and trophallaxis (21%). The great variability found in the amount of interactions suggests that individual bees require different stimulation before changing to the foraging mode. This broad disparity negatively correlated with the number of days after marking at the feeder, a variable that is closely related to the foraging experience, suggesting that a temporal variable might affect the decision-making in reactivated foragers.     

Reproduction-related interactions and loads induce continuous turn alternation leading to linearity in a terrestrial isopod

The Science of Nature - Red propolis is a substance produced by bees by mixing resins from plants with wax, oils, and other secretions to protect the hive against natural enemies. Dalbergia...     

Do honeybees, Apis mellifera scutellata, regulate humidity in their nest?

Honeybees are highly efficient at regulating the biophysical parameters of their hive according to colony needs. Thermoregulation has been the most extensively studied aspect of nest homeostasis. In contrast, little is known about how humidity is regulated in beehives, if at all. Although high humidity is necessary for brood development, regulation of this parameter by honeybee workers has not yet been demonstrated. In the past, humidity was measured too crudely for a regulation mechanism to be identified. We reassess this issue, using miniaturised data loggers that allow humidity measurements in natural situations and at several places in the nest. We present evidence that workers influence humidity in the hive. However, there are constraints on potential regulation mechanisms because humidity optima may vary in different locations of the nest. Humidity could also depend on variable external factors, such as water availability, which further impair the regulation. Moreover, there are trade-offs with the regulation of temperature and respiratory gas exchanges that can disrupt the establishment of optimal humidity levels. As a result, we argue that workers can only adjust humidity within sub-optimal limits.     

Diet-dependent heat emission reveals costs of post-diapause recovery from different nutritional sources in a carnivorous beetle

Restoration of fat stores is metabolic first priority for many insects that emerge from hibernation with depleted fat bodies. To some extent, the animals must be flexible and use whatever foods available irrespective of their nutrient composition. Previously, the carabid beetles Anchomenus dorsalis have been found to refill their fat stores to the same extent over 9 days irrespective of the nutrient composition of their food. However, a higher cost of fat deposition when the food was rich in sugar or protein rather than lipid was indicated by higher total energy consumption. Here, we test the hypothesis of increased metabolic costs of building fat stores from sugar- or protein-rich food than from lipid-rich food by microcalorimetry. We measured the heat emitted from beetles that had fed on sugar-, protein-, or lipid-rich food for 0 (common control), 2, 5, or 10 days. As predicted, heat emission was increased in beetles getting sugar- and protein-rich food compared with those getting lipid-rich food. However, we did not confirm the beetles’ ability to rebuild fat stores from protein-rich food; instead, they increased in lean mass. Overall, sugar-rich food seems to be optimal for post-winter recovery, because it is better than lipid-rich food that allows concurrent rebuilding of fat stores and lean mass, which may benefit preparation for spring migration and reproduction. We propose that overwintered fruits may be highly preferred post-diapause food for these otherwise mostly carnivorous beetles.     

Maternally inherited architecture in tertiary leaf beetles: paleoichnology of cryptocephaline fecal cases in Dominican and Baltic amber

Complex ethological adaptations and intraspecific interactions leave few fossil traces. We document three Dominican (20 million years old [myo]) and Baltic (45 myo) amber fossils that exhibit firm evidence of highly integrated interactions between mothers and offspring in the diverse camptosomate lineage of beetles (Chrysomelidae, leaf beetles). As in contemporary species, these hard cases were initially constructed by mothers, then inherited and retained by offspring, which then elaborate this protective domicile with an unusual but economical building material, their feces. The three fossils are classified in the Subfamily Cryptocephalinae; two are classified in the tribe Chlamisini based on morphological evidence—the flattened head lacking a sharp keel and long legs with simple recurved untoothed claws. These diagnostic features are not clearly visible in the third specimen to permit more refined identification. These fossils provide more precise paleontological dating of tribal nodes within the cryptocephaline radiation of leaf beetles. These fossils are the first and earliest evidence of mother–offspring interaction, building behavior, and fecal recycling in Camptosomata beetles and of inheritance of architectural structures in beetles.     

Honeybees learn floral odors while receiving nectar from foragers within the hive

Recent studies showed that nectar odors brought back by honeybee foragers can be learned associatively inside the hive. In the present study, we focused on the learning abilities of bees, which directly interact via trophallaxis with the incoming nectar foragers: the workers that perform nectar-receiving tasks inside the hive. Workers that have received food directly from foragers coming back from a feeder offering either unscented or scented sugar solution [phenylacetaldehyde (PHE) or nonanal diluted] were captured from two observational hives, and their olfactory memories were tested using the proboscis extension response paradigm. Bees that have received scented solution from incoming foragers showed significantly increased response frequencies for the corresponding solution odor in comparison with those that have received unscented solution. No differences in the response frequencies were found between food odors and colonies. The results indicate that first-order receivers learn via trophallaxis the association between the scent and the sugar solution transferred by incoming foragers. The implications of these results should be considered at three levels: the operational cohesion of bees involved in foraging-related tasks, the information propagation inside the hive related to the floral type exploited, and the putative effect of these memories on future preferences for resources.     

Keratin decomposition by trogid beetles: evidence from a feeding experiment and stable isotope analysis

The decomposition of vertebrate carcasses is an important ecosystem function. Soft tissues of dead vertebrates are rapidly decomposed by diverse animals. However, decomposition of hard tissues such as hairs and feathers is much slower because only a few animals can digest keratin, a protein that is concentrated in hairs and feathers. Although beetles of the family Trogidae are considered keratin feeders, their ecological function has rarely been explored. Here, we investigated the keratin-decomposition function of trogid beetles in heron-breeding colonies where keratin was frequently supplied as feathers. Three trogid species were collected from the colonies and observed feeding on heron feathers under laboratory conditions. We also measured the nitrogen (δ¹⁵N) and carbon (δ¹³C) stable isotope ratios of two trogid species that were maintained on a constant diet (feathers from one heron individual) during 70 days under laboratory conditions. We compared the isotopic signatures of the trogids with the feathers to investigate isotopic shifts from the feathers to the consumers for δ¹⁵N and δ¹³C. We used mixing models (MixSIR and SIAR) to estimate the main diets of individual field-collected trogid beetles. The analysis indicated that heron feathers were more important as food for trogid beetles than were soft tissues under field conditions. Together, the feeding experiment and stable isotope analysis provided strong evidence of keratin decomposition by trogid beetles.     

Chirality determines pheromone activity for flour beetles

Olfactory perception and orientation behaviour of female and male flour beetles (Tribolium castaneum, T. confusum) to single stereoisomers of their aggregation pheromone revealed maximal receptor potentials and optimal attraction in response to 4R,8R-(?)-dimethyldecanal, whereas its optical antipode 4S,8S-(+)-dimethyldecanal was found to be inactive in this respect. Female flour beetles of both species were ≈ 10³ times less attracted to 4R,8S-(+)- and 4S,8R-(?)-dimethyldecanal than to 4R,8R-(?)-dimethyldecanal, while male flour beetles failed to respond to the R,S-(+)- and S,R-(?)-stereoisomers. Pheromone extracts of prothoracic femora from unmated male flour beetles elicited higher receptor potentials in the antennae of females than in those of males. The results suggest that the aggregation pheromone emitted by maleT. castaneum as well as maleT. confusum has the stereochemical structure of 4R,8R-(?)-dimethyl-decanal, which acts as sex attractant for the females and as aggregant for the males of both species.     

Ant-lepidopteran associations along African forest edges

Working along forest edges, we aimed to determine how some caterpillars can co-exist with territorially dominant arboreal ants (TDAAs) in tropical Africa. We recorded caterpillars from 22 lepidopteran species living in the presence of five TDAA species. Among the defoliator and/or nectarivorous caterpillars that live on tree foliage, the Pyralidae and Nymphalidae use their silk to protect themselves from ant attacks. The Notodontidae and lycaenid Polyommatinae and Theclinae live in direct contact with ants; the Theclinae even reward ants with abundant secretions from their Newcomer gland. Lichen feeders (lycaenid; Poritiinae), protected by long bristles, also live among ants. Some lycaenid Miletinae caterpillars feed on ant-attended membracids, including in the shelters where the ants attend them; Lachnocnema caterpillars use their forelegs to obtain trophallaxis from their host ants. Caterpillars from other species live inside weaver ant nests. Those of the genus Euliphyra (Miletinae) feed on ant prey and brood and can obtain trophallaxis, while those from an Eberidae species only prey on host ant eggs. Eublemma albifascia (Erebidae) caterpillars use their thoracic legs to obtain trophallaxis and trophic eggs from ants. Through transfer bioassays of last instars, we noted that herbivorous caterpillars living in contact with ants were always accepted by alien conspecific ants; this is likely due to an intrinsic appeasing odor. Yet, caterpillars living in ant shelters or ant nests probably acquire cues from their host colonies because they were considered aliens and killed. We conclude that co-evolution with ants occurred similarly in the Heterocera and Rhopalocera.     

Biosynthesis of the defensive alkaloid cicindeloine in Stenus solutus beetles

To protect themselves from predation and microorganismic infestation, rove beetles of the genus Stenus produce and store bioactive alkaloids like stenusine, 3-(2-methyl-1-butenyl)pyridine, and cicindeloine in their pygidial glands. The biosynthesis of stenusine and 3-(2-methyl-1-butenyl)pyridine was previously investigated in Stenus bimaculatus and Stenus similis, respectively. Both molecules follow the same biosynthetic pathway, where the N-heterocyclic ring is derived from l-lysine and the side chain from l-isoleucine. The different alkaloids are finally obtained by slight modifications of shared precursor molecules. The piperideine alkaloid cicindeloine occurs as a main compound additionally to (E)-3-(2-methyl-1-butenyl)pyridine and traces of stenusine in the pygidial gland secretion of Stenus cicindeloides and Stenus solutus. Feeding of S. solutus beetles with [D,¹⁵N]-labeled amino acids followed by GC/MS analysis techniques showed that cicindeloine is synthesized via the identical pathway and precursor molecules as the other two defensive alkaloids.