New kind of polarotaxis governed by degree of polarization: attraction of tabanid flies to differently polarizing host animals and water surfaces

Aquatic insects find their habitat from a remote distance by means of horizontal polarization of light reflected from the water surface. This kind of positive polarotaxis is governed by the horizontal direction of polarization (E-vector). Tabanid flies also detect water by this kind of polarotaxis. The host choice of blood-sucking female tabanids is partly governed by the linear polarization of light reflected from the host’s coat. Since the coat-reflected light is not always horizontally polarized, host finding by female tabanids may be different from the established horizontal E-vector polarotaxis. To reveal the optical cue of the former polarotaxis, we performed choice experiments in the field with tabanid flies using aerial and ground-based visual targets with different degrees and directions of polarization. We observed a new kind of polarotaxis being governed by the degree of polarization rather than the E-vector direction of reflected light. We show here that female and male tabanids use polarotaxis governed by the horizontal E-vector to find water, while polarotaxis based on the degree of polarization serves host finding by female tabanids. As a practical by-product of our studies, we explain the enigmatic attractiveness of shiny black spheres used in canopy traps to catch tabanids.     

Glass buildings on river banks as “polarized light traps” for mass-swarming polarotactic caddis flies

The caddis flies Hydropsyche pellucidula emerge at dusk from the river Danube and swarm around trees and bushes on the river bank. We document here that these aquatic insects can also be attracted en masse to the vertical glass surfaces of buildings on the river bank. The individuals lured to dark, vertical glass panes land, copulate, and remain on the glass for hours. Many of them are trapped by the partly open, tiltable windows. In laboratory choice experiments, we showed that ovipositing H. pellucidula are attracted to highly and horizontally polarized light stimulating their ventral eye region and, thus, have positive polarotaxis. In the field, we documented that highly polarizing vertical black glass surfaces are significantly more attractive to both female and male H. pellucidula than weakly polarizing white ones. Using video polarimetry, we measured the reflection-polarization characteristics of vertical glass surfaces of buildings where caddis flies swarmed. We propose that after its emergence from the river, H. pellucidula is attracted to buildings by their dark silhouettes and the glass-reflected, horizontally polarized light. After sunset, this attraction may be strengthened by positive phototaxis elicited by the buildings' lights. The novelty of this visual-ecological phenomenon is that the attraction of caddis flies to vertical glass surfaces has not been expected because vertical glass panes do not resemble the horizontal surface of waters from which these insects emerge and to which they must return to oviposit.     

Phototaxis and polarotaxis hand in hand: night dispersal flight of aquatic insects distracted synergistically by light intensity and reflection polarization

Based on an earlier observation in the field, we hypothesized that light intensity and horizontally polarized reflected light may strongly influence the flight behaviour of night-active aquatic insects. We assumed that phototaxis and polarotaxis together have a more harmful effect on the dispersal flight of these insects than they would have separately. We tested this hypothesis in a multiple-choice field experiment using horizontal test surfaces laid on the ground. We offered simultaneously the following visual stimuli for aerial aquatic insects: (1) lamplit matte black canvas inducing phototaxis alone, (2) unlit shiny black plastic sheet eliciting polarotaxis alone, (3) lamplit shiny black plastic sheet inducing simultaneously phototaxis and polarotaxis, and (4) unlit matte black canvas as a visually unattractive control. The unlit matte black canvas trapped only a negligible number (13) of water insects. The sum (16,432) of the total numbers of water beetles and bugs captured on the lamplit matte black canvas (7,922) and the unlit shiny black plastic sheet (8,510) was much smaller than the total catch (29,682) caught on the lamplit shiny black plastic sheet. This provides experimental evidence for the synergistic interaction of phototaxis (elicited by the unpolarized direct lamplight) and polarotaxis (induced by the strongly and horizontally polarized plastic-reflected light) in the investigated aquatic insects. Thus, horizontally polarizing artificial lamplit surfaces can function as an effective ecological trap due to this synergism of optical cues, especially in the urban environment.     

Positive polarotaxis in a mayfly that never leaves the water surface: polarotactic water detection in Palingenia longicauda (Ephemeroptera)

Tisza mayflies, Palingenia longicauda (Olivier 1791), swarm exclusively over the river Tisza (from which the name of the mayfly was derived). This river is bordered by a high vertical wall of trees and bushes, which hinder P. longicauda to move away horizontally from the water. During swarming, Tisza mayflies fly immediately above the river in such a way that their cerci touch the water frequently or sweep its surface. This continuous close connection with water and the vertical wall of the shore and riparian vegetation result in that Tisza mayflies never leave the water surface; consequently, they need not search for water. Several Ephemeroptera species move away far from water and return to it guided by the horizontal polarization of water-reflected light. To reveal whether also P. longicauda is or is not polarotactic, we performed a field experiment during the very short swarming period of Tisza mayflies. We show here that also P. longicauda has positive polarotaxis, which, however, can be observed only under unnatural conditions, when the animals are displaced from the water and then released above artificial test surfaces. P. longicauda is the first species in which polarotactic water detection is demonstrated albeit it never leaves the water surface, and thus, a polarotactic water detection seems unnecessary for it. The polarotactic behaviour of Tisza mayflies explains the earlier observation that these insects swarm above wet asphalt roads running next to river Tisza.     

Light-mimicking cockroaches indicate Tertiary origin of recent terrestrial luminescence

Bioluminescence is a common feature of the communication and defence of marine organisms, but this phenomenon is highly restricted in the terrestrial biota. Here, we present a geographical distribution of only the third order of luminescent insects—luminescent cockroaches, with all 13 known and/or herein reported new living species (based on deposited specimens). We show that, for the first time, photo-characteristics of three examined species are nearly identical with those of toxic luminescent click beetles, which they mimic. These observations are the evidence for the mimicry by light—a new type of defensive, Batesian and interordinal mimicry. Our analysis surprisingly reveals an evolutionary novelty of all living luminescent insects, while in the sea (and possibly in the soil) luminescence is present also phylogenetically in very primitive organisms.     

Discovery of mycangia and the associated xylose-fermenting yeasts in stag beetles (Coleoptera: Lucanidae)

Most wood-feeding insects need an association with microbes to utilize wood as food, and some have special organs to store and convey the microbes. We report here the discovery of the microbe-storage organ (mycangium) in stag beetles (Coleoptera: Lucanidae), which develop in decayed wood. The mycangium, which was discovered in the abdomen, is present in all adult females of 22 lucanid species examined in this study, but absent in adult males. By contrast, adult insects of both sexes of selected Passalidae, Geotrupidae, and Scarabaeidae, which are related to Lucanidae, lacked mycangia similar to those of the lucanid species. Yeast-like microbes were isolated from the mycangium of five lucanid species. DNA sequence analyses indicate that the microbes are closely related to the xylose-fermenting yeasts Pichia stipitis, Pichia segobiensis, or Pichia sp. known from the gut of a passalid species.     

Pre- and post-hatch trophic egg production in the subsocial burrower bug, Canthophorus niveimarginatus (Heteroptera: Cydnidae)

In recent years, three terrestrial bugs, Adomerus triguttulus and Sehirus cinctus (Cydnidae) and the closely related Parastrachia japonensis (Parastrachiidae), have been the focus of several fascinating studies because of the remarkable, extensive parental care they were found to display. This care includes egg and nymph guarding, production of trophic eggs, unfertilized, low cost eggs that are used as food by newly hatched nymphs, and progressive provisioning of the host seed. In this study, we have investigated yet a third related Asian cydnid, Canthophorus niveimarginatus, with regard to the possible occurrence of some or all of these complex traits in order to assess how widespread these maternal investment patterns are in this group of insects and to better understand the implications of their manifestations from an evolutionary context. Manipulative experiments were carried out in the lab to determine whether females provision nests. Observational and egg removal studies were carried out to determine whether trophic eggs are produced, and, if they are, their possible impact on nymphal success. The findings revealed that C. niveimarginatus does, in fact, progressively provision young, and this species also displays all of the other behaviors associated with extended parental care in subsocial insects. Moreover, unlike the other two related species, which place trophic eggs on the surface of the original egg mass, C. niveimarginatus produces both pre- and post-hatch trophic eggs. Nymphs deprived of access to post-hatch trophic eggs had significantly lower body weight and survival rate than those that fed on them. To our knowledge, this is the first time the production of both pre- and post-hatch trophic eggs has been demonstrated in insects outside the Hymenoptera. In this paper, we qualitatively and quantitatively demonstrate the provisioning behavior and patterns of trophic egg production in C. niveimarginatus. When and how trophic eggs are produced and delivered to young should have important correlations with the ecological and life history constraints under which a species has evolved. Thus, we also discuss the possible ecological and life history factors that favor the evolution of post-hatch trophic eggs.     

Associative learning for danger avoidance nullifies innate positive chemotaxis to host olfactory stimuli in a parasitic wasp

Animals rely on associative learning for a wide range of purposes, including danger avoidance. This has been demonstrated for several insects, including cockroaches, mosquitoes, drosophilid flies, paper wasps, stingless bees, bumblebees and honeybees, but less is known for parasitic wasps. We tested the ability of Psyttalia concolor (Hymenoptera: Braconidae) females to associate different dosages of two innately attractive host-induced plant volatiles (HIPVs), ethyl octanoate and decanal, with danger (electric shocks). We conducted an associative treatment involving odours and shocks and two non-associative controls involving shocks but not odours and odours but not shocks. In shock-only and odour-only trained wasps, females preferred on HIPV-treated than on blank discs. In associative-trained wasps, however, P. concolor’s innate positive chemotaxis for HIPVs was nullified (lowest HIPV dosage tested) or reversed (highest HIPV dosage tested). This is the first report of associative learning of olfactory cues for danger avoidance in parasitic wasps, showing that the effects of learning can override innate positive chemotaxes.     

A male gift to its partner? Cyanogenic glycosides in the spermatophore of longwing butterflies (<Emphasis Type="Italic">Heliconius</Emphasis>)

Males of several insect species transfer nuptial gifts to females during mating, typically in the form of a protein-rich spermatophore. In chemically defended species, males could potentially enhance such a gift with chemicals that help protect the female, her eggs, or both. This was shown for lepidopteran species that accumulate pyrrolizidine alkaloids. Most Heliconius butterflies are presumably protected from predators by virtue of de novo synthesized and/or sequestered cyanogenic glycosides. Males of Heliconius species are known to transfer nutritional gifts to the females but whether defensive chemicals could also be transferred is not known. To ascertain whether transfer of cyanogens occurs, we dissected freshly mated females from nine different Heliconius species and analyzed spermatophores for cyanogenic glycosides. We found cyanogens in the spermatophores of all nine species. This is the first time cyanogenic glycosides are reported in the spermatophores of arthropods. We discuss the implications of these findings for Heliconius biology and for other cyanogenic insects as well. We suggest that chemically defended species commonly lace their nuptial gifts with defensive chemicals to improve gift quality.     

Divergent mating patterns and a unique mode of external sperm transfer in Zoraptera: an enigmatic group of pterygote insects

A remarkable external sperm transfer is described for the first time in a species of a group of winged insects (Pterygota), the enigmatic Zoraptera. Mating and sperm transfer of two species of the order were examined in detail, documented, and compared with each other and with patterns described for other species belonging to the order. The behavior differs strikingly in Zorotypus impolitus and Zorotypus magnicaudelli. A copula is performed by males and females of the latter, as it is also the case in other zorapteran species and generally in pterygote insects. In striking contrast to this, males of Z. impolitus do not copulate but deposit small (100 μm in diameter) spermatophores externally on the abdomen of the female. Each spermatophore contains only one giant spermatozoon (3 mm long and 3 μm wide), a unique feature in the entire Hexapoda. External sperm transfer in Pterygota is a highly unusual case of evolutionary reversal. The very small relict group Zoraptera displays a uniform general morphology but exhibits very different reproductive structures and patterns of mating behavior. This may be an extreme form of a more general situation in insects, with a specific form of selection resulting in an accelerated rate of evolution in the reproductive system.     

Codling moth males do not discriminate between pheromone and a pheromone/antagonist blend during upwind flight

Discrimination between conspecific and heterospecific signals is a key element in the evolution of pheromone-mediated communication in insects. Pheromone antagonists prevent heterospecific attraction. They are typically pheromone synergists in other species and enable specific communication in closely related species, using partly the same chemicals. In codling moth, Cydia pomonella, as in other moths, upwind flights to a pheromone/antagonist blend were slower and more convoluted than to pheromone. However, this deteriorated flight behaviour did not account for the strong decrease in male attraction. The pheromone/antagonist blend blocked instead the onset of upwind flight. This was corroborated by placing a separate source of pheromone close by, which restored male attraction. Males flying upwind did not discriminate between pheromone and the adjacent pheromone/antagonist blend, and landed on either source. This indicates differences in the neural regulation for initiating and maintaining a behavioural response to pheromone.     

Diel periodicity of pheromone release by females of Planococcus citri and Planococcus ficus and the temporal flight activity of their conspecific males

The diel periodicity of sex pheromone release was monitored in two mealybug species, Planococcus citri and Planococcus ficus (Hemiptera; Pseudococcidae), using sequential SPME/GCMS analysis. A maximal release of 2 ng/h pheromone by 9–12-day-old P. citri females occurred 1–2 h before the beginning of photophase. The highest release of pheromone by P. ficus females was 1–2 ng/2 h of 10–20-day-old females, approximately 2 h after the beginning of photophase. Mating resulted in termination of the pheromone release in both mealybug species. The temporal flight activity of the males was monitored in rearing chambers using pheromone baited delta traps. Males of both P. citri and P. ficus displayed the same flight pattern and began flying at 06:00 hours when the light was turned on, reaching a peak during the first and second hour of the photophase. Our results suggest that other biparental mealybug species display also diel periodicities of maximal pheromone release and response. Direct evaluation of the diel periodicity of the pheromone release by the automatic sequential analysis is convenient and will be very helpful in optimizing the airborne collection and identification of other unknown mealybug pheromones and to study the calling behavior of females. Considering this behavior pattern may help to develop more effective pheromone-based management strategies against mealybugs.     

On the success of a swindle: pollination by deception in orchids

A standing enigma in pollination ecology is the evolution of pollinator attraction without offering reward in about one third of all orchid species. Here I review concepts of pollination by deception, and in particular recent findings in the pollination syndromes of food deception and sexual deception in orchids. Deceptive orchids mimic floral signals of rewarding plants (food deception) or mating signals of receptive females (sexual deception) to attract pollen vectors. In some food deceptive orchids, similarities in the spectral reflectance visible to the pollinator in a model plant and its mimic, and increased reproductive success of the mimic in the presence of the model have been demonstrated. Other species do not mimic specific model plants but attract pollinators with general attractive floral signals. In sexually deceptive orchids, floral odor is the key trait for pollinator attraction, and behaviorally active compounds in the orchids are identical to the sex pheromone of the pollinator species. Deceptive orchids often show high variability in floral signals, which may be maintained by negative frequency-dependent selection, since pollinators can learn and subsequently avoid common deceptive morphs more quickly than rare ones. The evolution of obligate deception in orchids seems paradoxical in the light of the typically lower fruit set than in rewarding species. Pollination by deception, however, can reduce self-pollination and encourage pollen flow over longer distances, thus promoting outbreeding. Although some food deceptive orchids are isolated through postzygotic reproductive barriers, sexually deceptive orchids lack post-mating barriers and species isolation is achieved via specific pollinator attraction. Recent population genetic and phylogenetic investigations suggest gene-flow within subgeneric clades, but pollinator-mediated selection may maintain species-specific floral traits.     

Sex pheromone component ratios and mating isolation among three Lygus plant bug species of North America

The plant bugs Lygus hesperus, Lygus lineolaris, and Lygus elisus (Hemiptera: Miridae) are major pests of many agricultural crops in North America. Previous studies suggested that females release a sex pheromone attractive to males. Other studies showed that males and females contain microgram amounts of (E)-4-oxo-2-hexenal, hexyl butyrate, and (E)-2-hexenyl butyrate that are emitted as a defense against predators. Using gas chromatography–mass spectrometry, we found that female L. lineolaris and L. elisus have a 4:10 ratio of hexyl butyrate to (E)-2-hexenyl butyrate that is reversed from the 10:1 ratio in female L. hesperus (males of the three species have ~10:1 ratio). These reversed ratios among females of the species suggest a behavioral role. Because both sexes have nearly equal amounts of the major volatiles, females should release more to attract males. This expectation was supported because L. hesperus females released more hexyl butyrate (mean of 86 ng/h) during the night (1800–0700 hours) than did males (<1 ng/h). We used slow-rotating pairs of traps to test the attraction of species to blends of the volatiles with a subtractive method to detect synergism. Each species’ major butyrate ester was released at 3 μg/h, the minor butyrate according to its ratio, and (E)-4-oxo-2-hexenal at 2 μg/h. The resulting catches of only Lygus males suggest that (E)-4-oxo-2-hexenal is an essential sex pheromone component for all three species, (E)-2-hexenyl butyrate is essential for L. elisus and L. lineolaris, and hexyl butyrate is essential for L. hesperus. However, all three components are recognized by each species since ratios of the butyrate esters are critical for conspecific attraction and heterospecific avoidance by males and thus play a role in reproductive isolation among the three species. Because L. hesperus males and females are known to emit these major volatiles for repelling ant predators, our study links defensive allomones in Lygus bugs with an additional use as sex pheromones.     

Silk wrapping of nuptial gifts as visual signal for female attraction in a crepuscular spider

An extensive diversity of nuptial gifts is known in invertebrates, but prey wrapped in silk is a unique type of gift present in few insects and spiders. Females from spider species prefer males offering a gift accepting more and longer matings than when males offered no gift. Silk wrapping of the gift is not essential to obtain a mating, but appears to increase the chance of a mating evidencing a particularly intriguing function of this trait. Consequently, as other secondary sexual traits, silk wrapping may be an important trait under sexual selection, if it is used by females as a signal providing information on male quality. We aimed to understand whether the white color of wrapped gifts is used as visual signal during courtship in the spider Paratrechalea ornata. We studied if a patch of white paint on the males’ chelicerae is attractive to females by exposing females to males: with their chelicerae painted white; without paint; and with the sternum painted white (paint control). Females contacted males with white chelicerae more often and those males obtained higher mating success than other males. Thereafter, we explored whether silk wrapping is a condition-dependent trait and drives female visual attraction. We exposed good and poor condition males, carrying a prey, to the female silk. Males in poor condition added less silk to the prey than males in good condition, indicating that gift wrapping is an indicator of male quality and may be used by females to acquire information of the potential mate.     

Sexual contact influences orientation to plant attractant in Colorado potato beetle, Leptinotarsa decemlineata Say (Coleoptera: Chrysomelidae)

Chemical signals emitted by insects and their hosts are important for sexual communication and host selection. Plant volatiles facilitate the location of suitable hosts for feeding and oviposition, and may moderate responses to sex and aggregation pheromones. While mating has been shown to moderate behavioral responses to pheromones in a number of insects, little is known about the effects of mating on behavioral responses of insects to plant attractants, and even less is known about the mechanisms involved. In this study, mating was shown to decrease behavioral responses of the Colorado potato beetle to a host kairomone within 24 h, and attraction to the kairomone recovers only after 72 h. This decrease in responsiveness also occurs when only contact with the opposite sex is allowed; the effect is not observed with contact among individuals of the same sex. Peripheral olfactory responses to a component of the kairomone correlate with the observed behavioral responses and suggest involvement of antennal receptors in the behavioral change.     

Empirical corroboration of an earlier theoretical resolution to the UV paradox of insect polarized skylight orientation

It is surprising that many insect species use only the ultraviolet (UV) component of the polarized skylight for orientation and navigation purposes, while both the intensity and the degree of polarization of light from the clear sky are lower in the UV than at longer (blue, green, red) wavelengths. Why have these insects chosen the UV part of the polarized skylight? This strange phenomenon is called the "UV-sky-pol paradox". Although earlier several speculations tried to resolve this paradox, they did this without any quantitative data. A theoretical and computational model has convincingly explained why it is advantageous for certain animals to detect celestial polarization in the UV. We performed a sky-polarimetric approach and built a polarized skylight sensor that models the processing of polarization signals by insect photoreceptors. Using this model sensor, we carried out measurements under clear and cloudy sky conditions. Our results showed that light from the cloudy sky has maximal degree of polarization in the UV. Furthermore, under both clear and cloudy skies the angle of polarization of skylight can be detected with a higher accuracy. By this, we corroborated empirically the soundness of the earlier computational resolution of the UV-sky-pol paradox.     

In search of the sky compass in the insect brain

Like many vertebrate species, insects rely on a sun compass for spatial orientation and long- range navigation. In addition to the sun, however, insects can also use the polarization pattern of the sky as a reference for estimating navigational directions. Recent analysis of polarization vision pathways in the brain of orthopteroid insects sheds some light onto brain areas that might act as internal navigation centers. Here I review the significance, peripheral mechanisms, and central processing stages for polarization vision in insects with special reference to the locust Schistocerca gregaria. As in other insect species, polarization vision in locusts relies on specialized photoreceptor cells in a small dorsal rim area of the compound eye. Stages in the brain involved in polarized light signaling include specific areas in the lamina, medulla and lobula of the optic lobe and, in the midbrain, the anterior optic tubercle, the lateral accessory lobe, and the central complex. Integration of polarized-light signals with information on solar position appears to start in the optic lobe. In the central complex, polarization-opponent interneurons form a network of interconnected neurons. The organization of the central complex, its connections to thoracic motor centers, and its involvement in the spatial control of locomotion strongly suggest that it serves as a spatial organizer within the insect brain, including the functions of compass orientation and path integration. Time compensation in compass orientation is possibly achieved through a neural pathway from the internal circadian clock in the accessory medulla to the protocerebral bridge of the central complex.     

Sexual differences in food preferences in the white stork: an experimental study

Sex differences in the foraging ecology of monomorphic species are poorly understood, due to problems with gender identification in field studies. In the current study, we used experimental conditions to investigate the food preferences of the white stork Ciconia ciconia, an opportunistic species in terms of food, but characterised by a low level of sexual dimorphism. During a 10-day experiment, 29 individuals (20 females and 9 males) were studied by means of a ‘cafeteria test’ in which the storks’ diet consisted of mammals, birds, fish, amphibians, insects and earthworms. The storks preferred food characterised by high calorific and protein values such as mammals, birds and fish. Sexes differed strongly in their preferences; males preferred mammals, whereas females preferred birds. Moreover, females consumed insects and earthworms less often than males. Interestingly, males spent significantly less time foraging than females. We have demonstrated that the white stork exhibits clear sexual differences in food preferences which are mostly attributable to differences in parental duties, physiology and anatomy.