Fire ant venom alkaloids act as key attractants for the parasitic phorid fly, Pseudacteon tricuspis (Diptera: Phoridae)

The phorid fly, Pseudacteon tricuspis Borgmeier, is an introduced parasitoid of imported fire ants, Solenopsis spp., in the USA. Although the assumption that phorid flies use fire ant alarm pheromones for host location is probably true, we demonstrated in a previous study the possible involvement of other ant semiochemicals in the response of P. tricuspis to fire ants. This study was conducted to determine the glandular sources and identity of the semiochemicals mediating this interaction. First, we tested the electroantennogram response of P. tricuspis to extracts of key body parts and glands of workers of the red imported fire ant, S. invicta Buren. The results confirm that the poison (venom) gland/sac is the key source of compounds which elicited strong antennal activity in P. tricuspis. Follow-up studies were conducted by using a combination of bioassay-guided fractionation and behavioral bioassays to test the hypothesis that attraction of this parasitoid to fire ants is mediated by venom alkaloids. The results confirm the response of P. tricuspis to physiologically relevant amounts of the two venom alkaloid fractions (cis and trans alkaloid fractions) of S. invicta. Further analysis by coupled gas chromatography–electroantennogram detection revealed nine venom alkaloid components including two novel 2,6-dialkylpiperideines that elicited significant antennal activity in P. tricuspis. This is the first demonstration of the role of venom alkaloids of ants as attractants for their natural enemies. We propose a semiochemical-mediated host location mechanism for P. tricuspis involving both alarm pheromones and venom alkaloids. The ecological significance of these findings, including the attraction of male P. tricuspis to fire ant venom alkaloids, possibly for mate location, is discussed.     

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.     

Structural differences in the drone olfactory system of two phylogenetically distant Apis species, A. florea and A. mellifera

Male insects that are attracted by sex pheromones to find their female mates over long distances have specialized olfactory subsystems. Morphologically, these subsystems are characterized by a large number of receptor neurons sensitive to components of the female's pheromones and hypertrophied glomerular subunits ('macroglomeruli' or 'macroglomerular complexes') in the antennal lobes, in which the axons of the receptor neurons converge. The olfactory subsystems are adapted for an increased sensitivity to perceive minute amounts of pheromones. In Apis mellifera, drones have 18,600 olfactory poreplate sensilla per antenna, each equipped with receptor neurons sensitive to the queen's sex pheromone, and four voluminous macroglomeruli (MG1-MG4) in the antennal lobes. In contrast, we show that drones of the phylogenetically distant species, Apis florea, have only 1,200 poreplate sensilla per antenna and only two macroglomeruli in their antennal lobes. These macroglomeruli are homologous in anatomical position to the two most prominent macroglomeruli in A. mellifera, the MG1 and MG2, but they are much smaller in size. The morphological and anatomical differences described here suggest major modifications in the sex-pheromone processing subsystem of both species: (1) less pheromone sensitivity in A. florea and (2) a more complex sex-pheromone processing and thus a more complex sex-pheromone communication in A. mellifera.     

Surface lipids of queen-laid eggs do not regulate queen production in a fission-performing ant

In animal societies, most collective and individual decision making depends on the presence of reproductive individuals. The efficient transmission of information among reproductive and non-reproductive individuals is therefore a determinant of colony organization. In social insects, the presence of a queen modulates multiple colonial activities. In many species, it negatively affects worker reproduction and the development of diploid larvae into future queens. The queen mostly signals her presence through pheromone emission, but the means by which these chemicals are distributed in the colony are still unclear. In several ant species, queen-laid eggs are the vehicle of the queen signal. The aim of this study was to investigate whether queen-laid eggs of the ant Aphaenogaster senilis possess queen-specific cuticular hydrocarbons and/or Dufour or poison gland compounds, and whether the presence of eggs inhibited larval development into queens. Our results show that the queen- and worker-laid eggs shared cuticular and Dufour hydrocarbons with the adults; however, their poison gland compounds were not similar. Queen-laid eggs had more dimethylalkanes and possessed a queen-specific mixture of cuticular hydrocarbons composed of 3,11?+?3,9?+?3,7-dimethylnonacosane, in higher proportions than did worker-laid eggs. Even though the queen-laid eggs were biochemically similar to the queen, their addition to experimentally queenless groups did not prevent the development of new queens. More studies are needed on the means by which queen ant pheromones are transmitted in the colony, and how these mechanisms correlates with life history traits.     

Alternative mating behaviors of the queen polymorphic ant <Emphasis Type="Italic">Temnothorax longispinosus</Emphasis>

Mating behaviors of ants fall into two categories: female calling, in which a female alate releases pheromones that attract males, and male swarming, in which large male aggregations attract females. Female calling is common in species with queens that return to their natal nest to found colonies dependently after mating, while male swarming is common in species with queens that disperse to found independently. In some species that display both founding strategies, a queen-size polymorphism has evolved in which dependent-founding queens are smaller than independent-founding queens. Dependent founding is likely difficult if gynes (virgin queens) are mating in distant swarms. Therefore, a queen may adopt one or the other mating strategy based on its size and founding behavior. We investigated mating behaviors in the queen-polymorphic ant, Temnothorax longispinosus. Observations in laboratory mating arenas indicated that small gynes exhibited significantly lower flight activity than large gynes. Both forms mated in male swarms, and neither form exhibited female calling. The reduced flight activity of the small morph may facilitate returning to the natal nest after mating, provided the mating swarm is located nearby. Therefore, alternative colony-founding behaviors may be possible without the evolution of female-calling behavior; however, the reduced flight activity of small morphs may require that mating swarms are not distant from the natal nest.     

Predicted taxonomic patterns in pheromone production by longhorned beetles

Males of five species of three tribes in the longhorned beetle subfamily Cerambycinae produce volatile pheromones that share a structural motif (hydroxyl or carbonyl groups at carbons two and three in straight-chains of six, eight, or ten carbons). Pheromone gland pores are present on the prothoraces of males, but are absent in females, suggesting that male-specific gland pores could provide a convenient morphological indication that a species uses volatile pheromones. In this article, we assess the taxonomic distribution of gland pores within the Cerambycinae by examining males and females of 65 species in 24 tribes using scanning electron microscopy. Gland pores were present in males and absent in females of 49 species, but absent in both sexes of the remaining 16 species. Pores were confined to indentations in the cuticle. Among the species that had male-specific gland pores were four species already known to produce volatile compounds consistent with the structural motif. These findings support the initial assumption that gland pores are associated with the production of pheromones by males. There were apparently no taxonomic patterns in the presence of gland pores. These findings suggest that volatile pheromones play an important role in reproduction for many species of the Cerambycinae, and that the trait is evolutionarily labile.     

Uncoupling primer and releaser responses to pheromone in honey bees

Pheromones produce dramatic behavioral and physiological responses in a wide variety of species. Releaser pheromones elicit rapid responses within seconds or minutes, while primer pheromones produce long-term changes which may take days to manifest. Honeybee queen mandibular pheromone (QMP) elicits multiple distinct behavioral and physiological responses in worker bees, as both a releaser and primer, and thus produces responses on vastly different time scales. In this study, we demonstrate that releaser and primer responses to QMP can be uncoupled. First, treatment with the juvenile hormone analog methoprene leaves a releaser response (attraction to QMP) intact, but modulates QMP’s primer effects on sucrose responsiveness. Secondly, two components of QMP (9-ODA and 9-HDA) do not elicit a releaser response (attraction) but are as effective as QMP at modulating a primer response, downregulation of foraging-related brain gene expression. These results suggest that different responses to a single pheromone may be produced via distinct pathways.     

Insektenpheromone

Pheromones — semiochemicals used by insects for intraspecific chemical communication — can be isolated and with special analytical techniques their chemical structure elucidated. With stereoselective synthesis methods, presented by the preparation of sex attractants and aggregating pheromones of moths and beetles, respectively, a synthetic access to compounds is given which can be used for behavior manipulation of insects. Aside the importance of these compounds for investigations of the sensoric process the possibility of their application in an integrated and biological pest control is discussed.     

Parasitoids and competitors influence colony-level responses in the red imported fire ant,<Emphasis Type="Italic"> Solenopsis invicta</Emphasis>

Social insect colonies respond to challenges set by a variable environment by reallocating work among colony members. In many social insects, such colony-level task allocation strategies are achieved through individual decisions that produce a self-organized adapting group. We investigated colony responses to parasitoids and native ant competitors in the red imported fire ant (Solenopsis invicta). Parasitoid flies affected fire ants by decreasing the proportion of workers engaged in foraging. Competitors also altered colony-level behaviours by reducing the proportion of foraging ants and by increasing the proportion of roaming majors, whose role is colony defence. Interestingly, the presence of both parasitism and competition almost always had similar effects on task allocation in comparison to each of the biotic factors on its own. Thus, our study uniquely demonstrates that the interactive effect of both parasitism and competition is not necessarily additive, implying that these biotic factors alter colony behaviour in distinct ways. More generally, our work demonstrates the importance of studying the dynamics of species interactions in a broader context.     

Sand-swimming behaviour reduces ectoparasitism in an iguanian lizard

Social interactions may shape brain development. In primitively eusocial insects, the mushroom body (MB), an area of the brain associated with sensory integration and learning, is larger in queens than in workers. This may reflect a strategy of neural investment in queens or it may be a plastic response to social interactions in the nest. Here, we show that nest foundresses—the reproductive females who will become queens but are solitary until their first workers are born—have larger MBs than workers in the primitively eusocial sweat bee Augochlorella aurata. Whole brain size and optic lobe size do not differ between the two groups, but foundresses also have larger antennal lobes than workers. This shows that increased neural investment in MBs precedes social group formation. Larger MBs among foundresses may reflect the increased larval nutrition provisioned to future queens and the lack of social aggression from a dominant queen upon adult emergence.

     

Pathogen Alarm Behavior in a Termite: A New Form of Communication in Social Insects

 Dampwood termites, Zootermopsis angusticollis, show an alarm response after detecting the presence of spores of the pathogenic fungus Metarhizium anisopliae. Termites in direct contact with a high concentration of spores (10⁷ spores/ml) show a striking vibratory display which appears to convey information about the presence of pathogens to nearby unexposed nestmates through substrate vibration. Nestmates not directly in contact with spores that perceive the vibrational signal increase significantly their distance from the spore-exposed vibrating termites, apparently to escape from the source of infection. The fleeing response is not induced by the presence of the spores alone or by pheromones, and requires the perception of the vibrations propagated through the substrate. This "pathogen alarm behavior" appears to be a previously unrecognized communication mechanism that allows termites to reduce disease risks within the nest. Received: 12 May 1999 / Accepted in revised form: 26 August 1999     

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.     

Context dependency and generality of fever in insects

Fever can reduce mortality in infected animals. Yet, despite its fitness-enhancing qualities, fever often varies among animals. We used several approaches to examine this variation in insects. Texas field crickets (Gryllus texensis) exhibited a modest fever (1 °C increase in preferred body temperature, T _pref) after injection of prostaglandin, which putatively mediates fever in both vertebrates and invertebrates, but they did not exhibit fever during chronic exposure to heat-killed bacteria. Further, chronic food limitation and mating status did not affect T _pref or the expression of behavioural fever, suggesting limited context dependency of fever in G. texensis. Our meta-analysis of behavioural fever studies indicated that behavioural fever occurs in many insects, but it is not ubiquitous. Thus, both empirical and meta-analytical results suggest that the fever response in insects ‘is widespread, although certainly not inevitable’ (Moore 2002). We highlight the need for future work focusing on standardizing an experimental protocol to measure behavioural fever, understanding the specific mechanism(s) underlying fever in insects, and examining whether ecological or physiological costs often outweigh the benefits of fever and can explain the sporadic nature of fever in insects.     

Intrinsic worker mortality depends on behavioral caste and the queens’ presence in a social insect

According to the classic life history theory, selection for longevity depends on age-dependant extrinsic mortality and fecundity. In social insects, the common life history trade-off between fecundity and longevity appears to be reversed, as the most fecund individual, the queen, often exceeds workers in lifespan several fold. But does fecundity directly affect intrinsic mortality also in social insect workers? And what is the effect of task on worker mortality? Here, we studied how social environment and behavioral caste affect intrinsic mortality of ant workers. We compared worker survival between queenless and queenright Temnothorax longispinosus nests and demonstrate that workers survive longer under the queens’ absence. Temnothorax ant workers fight over reproduction when the queen is absent and dominant workers lay eggs. Worker fertility might therefore increase lifespan, possibly due to a positive physiological link between fecundity and longevity, or better care for fertile workers. In social insects, division of labor among workers is age-dependant with young workers caring for the brood and old ones going out to forage. We therefore expected nurses to survive longer than foragers, which is what we found. Surprisingly, inactive inside workers showed a lower survival than nurses but comparable to that of foragers. The reduced longevity of inactive workers could be due to them being older than the nurses, or due to a positive effect of activity on lifespan. Overall, our study points to behavioral caste-dependent intrinsic mortality rates and a positive association between fertility and longevity not only in queens but also in ant workers.     

Selective olfactory attention of a specialised predator to intraspecific chemical signals of its prey

Prey-specialised predators have evolved specific cognitive adaptations that increase their prey searching efficiency. In particular, when the prey is social, selection probably favours the use of prey intraspecific chemical signals by predatory arthropods. Using a specialised ant-eating zodariid spider, Zodarion rubidum, which is known to prey on several ant species and possesses capture and venom adaptations more effective on Formicinae ants, we tested its ability to recognise chemical cues produced by several ant species. Using an olfactometer, we tested the response of Z. rubidum towards air with chemical cues from six different ant species: Camponotus ligniperda, Lasius platythorax and Formica rufibarbis (all Formicinae); and Messor structor, Myrmica scabrinodis and Tetramorium caespitum (all Myrmicinae). Z. rubidum was attracted to air carrying chemical cues only from F. rufibarbis and L. platythorax. Then, we identified that the spiders were attracted to airborne cues coming from the F. rufibarbis gaster and Dufour's gland, in particular. Finally, we found that among several synthetic blends, the decyl acetate and undecane mixture produced significant attraction of spiders. These chemicals are produced only by three Formicine genera. Furthermore, we investigated the role of these chemical cues in the communication of F. rufibarbis and found that this blend reduces their movement. This study demonstrates the chemical cognitive capacity of Z. rubidum to locate its ant prey using chemical signals produced by the ants. The innate capacity of Z. rubidum to olfactory detect different ant species is narrow, as it includes only two ant genera, confirming trophic specialisation at lower than subfamily level. The olfactory cue detected by Zodarion spiders is probably a component of the recruitment or trail pheromone.     

Pheromone-modulated behavioral suites influence colony growth in the honey bee (<Emphasis Type="Italic">Apis mellifera</Emphasis>)

The success of a species depends on its ability to assess its environment and to decide accordingly which behaviors are most appropriate. Many animal species, from bacteria to mammals, are able to communicate using interspecies chemicals called pheromones. In addition to exerting physiological effects on individuals, for social species, pheromones communicate group social structure. Communication of social structure is important to social insects for the allocation of its working members into coordinated suites of behaviors. We tested effects of long-term treatment with brood pheromone on suites of honey bee brood rearing and foraging behaviors. Pheromone-treated colonies reared significantly greater brood areas and more adults than controls, while amounts of stored pollen and honey remained statistically similar. Brood pheromone increased the number of pollen foragers and the pollen load weights they returned. It appeared that the pheromone-induced increase in pollen intake was directly canalized into more brood rearing. A two-way pheromone priming effect was observed, such that some workers from the same age cohorts showed an increased and extended capacity to rear larvae, while others were recruited at significantly younger ages into pollen-specific foraging. Brood pheromone affected suites of nursing and foraging behaviors allocating worker and pollen resources associated with an important fitness trait, colony growth.     

Predation and aggressiveness in host plant protection: a generalization using ants from the genus Azteca

In studying the ant genus Azteca, a Neotropical group of arboreal species, we aimed to determine the extent to which the ants use predation and/or aggressiveness to protect their host plants from defoliating insects. We compared a territorially dominant, carton-nester, Azteca chartifex, and three plant-ant species. Azteca alfari and Azteca ovaticeps are associated with the myrmecophyte Cecropia (Cecropiaceae) and their colonies shelter in its hollow branches; whereas Azteca bequaerti is associated with Tococa guianensis (Melastomataceae) and its colonies shelter in leaf pouches situated at the base of the laminas. Whereas A. bequaerti workers react to the vibrations transmitted by the lamina when an alien insect lands on a leaf making it unnecessary for them to patrol their plant, the workers of the three other species rather discover prey by contact. The workers of all four species use a predatory behaviour involving spread-eagling alien insects after recruiting nestmates at short range, and, in some cases, at long range. Because A. alfari and A. ovaticeps discard part of the insects they kill, we deduced that the workers' predatory behaviour and territorial aggressiveness combine in the biotic defence of their host tree.     

Behavioural evidence of male volatile pheromones in the sex-role reversed wolf spiders Allocosa brasiliensis and Allocosa alticeps

The use of chemical signals in a sexual context is widespread in the animal kingdom. Most studies in spiders report the use of female pheromones that attract potential sexual partners. Allocosa brasiliensis and Allocosa alticeps are two burrowing wolf spiders that show sex-role reversal. Females locate male burrows and initiate courtship before males perform any detectable visual or vibratory signal. So, females of these species would be detecting chemical or mechanical cues left by males. Our objective was to explore the potential for male pheromones to play a role in mate detection in A. brasiliensis and A. alticeps. We designed two experiments. In Experiment 1, we tested the occurrence of male contact pheromones by evaluating female courtship when exposed to empty burrows constructed by males or females (control). In Experiment 2, we tested the existence of male volatile pheromones by evaluating female behaviour when exposed to artificial burrows connected to tubes containing males, females or empty tubes (control). Our results suggest the occurrence of male volatile pheromones that trigger female courtship in both Allocosa species. The sex-role reversal postulated for these wolf spiders could be driving the consequent reversal in typical pheromone-emitter and detector roles expected for spiders.     

“You are what you eat”: Diet modifies cuticular hydrocarbons and nestmate recognition in the Argentine ant, Linepithema humile

 Nestmate recognition plays a key role in the behavior and evolution of social insects. We demonstrated that hydrocarbons are the chemical cues used in Argentine ant, Linepithema humile, nestmate recognition, and that these hydrocarbons can be acquired from insect prey. Consequently, Argentine ant cuticular hydrocarbon patterns reveal the same hydrocarbons present in their diet. Diet alters both the recognition cues present on the cuticular surface and the response of nestmates to this new colony odor, resulting in aggression between former nestmates reared on different insect prey. Received: 16 June 2000 / Accepted: 14 August 2000     

A putative octopamine/tyramine receptor mediating appetite in a hungry fly

In the blowfly Phormia regina, experience of simultaneous feeding with d-limonene exposure inhibits proboscis extension reflex (PER) due to decreased tyramine (TA) titer in the brain. To elucidate the molecular mechanism of TA signaling pathway related to the associated feeding behavior, we cloned cDNA encoding the octopamine/TA receptor (PregOAR/TAR). The deduced protein is composed of 607 amino acid residues and has 7 predicted transmembrane domains. Based on homology and phylogenetic analyses, this protein belongs to the OAR/TAR family. The PregOAR/TAR was mainly expressed in head, with low levels of expression in other tissues at adult stages. Gene expression profile is in agreement with a plethora of functions ascribed to TA in various insect tissues. The immunolabeled cell bodies and processes were localized in the medial protocerebrum, outer layer of lobula, antennal lobe, and subesophageal ganglion. These results suggest that decrease of TA level in the brain likely affects neurons expressing PregOAR/TAR, causing mediation of the sensitivity in the sensillum and/or output of motor neurons for PER.