Production of sexuals in a fission-performing ant: dual effects of queen pheromones and colony size

Models based on the kin selection theory predict that in social hymenopterans, queens may favor a lower investment in the production of sexuals than workers. However, in perennial colonies, this conflict may be tuned down by colony-level selection because of the trade off between colony survival and reproductive allocation. In this study, we present a survey of sexual production in colonies of Aphaenogaster senilis, a common species of ant in the Iberian Peninsula. Similar to most species that reproduce by fission, males were found in large excess compared to gynes (172:1). Sexuals were more likely to be found in queenless than in queenright (QR) field colonies. However, we also found a few gynes and numerous males in very large QR colonies. We compared these data with those available in the literature for A. rudis, a congeneric species from North America that has independent colony founding. The sex ratio in this species was only five males for each female, and sexuals were mostly found in QR nests, irrespective of colony size. We confirmed queen inhibition of sexual production in A. senilis in laboratory experiments and provide evidence that this inhibition is mediated by a nonvolatile pheromone. To seek the potential source of such a queen pheromone, we analyzed the secretions of two conspicuous exocrine glands, the Dufour’s and postpharyngeal glands (DG and PPG, respectively) in both queens and workers. Both secretions were composed of hydrocarbons, but that of DG also contained small quantities of tetradecanal and hexadecanal. The hydrocarbon profile of the DG and PPG showed notable caste specificity suggesting a role in caste-related behavior. The PPG secretions also differed between colonies suggesting its role in colony-level recognition. We suggest that in A. senilis, there are two modes of colony fission: First, in very large colonies, gynes are produced, probably because of the dilution of the queen pheromone, and consequently one or more gynes leave the mother colony with workers and brood to found a new nest. This is beneficial at the colony level because it avoids the production of costly sexuals in small colonies. However, because the queen and workers have different optima for sexual production, we hypothesize that queens tend to overproduce the pheromone to delay their production. This in turn may drive workers to leave the mother colony during nest relocation and to produce sexuals once they are away from the queen’s influence, creating a second mode of colony fission.     

Behavioural evidence for the involvement of Dufour’s gland secretion in nestmate recognition in the social wasp Polistes dominulus (Hymenoptera: Vespidae)

The results of recent studies by our group have suggested that in social wasps of the genus Polistes the Dufour’s gland is involved in kin recognition. In fact, the same hydrocarbons occurring on the cuticle are found in the gland secretion, and in P. dominulus the composition of the glandular secretion is more similar in foundresses belonging to the same colonies than in heterocolonial foundresses. In this study, P. dominulus colonies were experimentally presented with previously treated dead conspecific females. These lures had been deprived of their epicuticular lipids and coated with epicuticular or Dufour’s gland secretion extracts from females hetero- or homocolonial with respect to the tested colonies. The behaviour of the colonies towards these lures indicates that, like the epicuticular lipids, the Dufour’s gland secretion is involved in nestmate recognition. Received: 14 August 1995/Accepted after revision: 5 November 1995     

Predatory behavior and chemical communication in two Metapone species (Hymenoptera:Formicidae)

Summary. Colonies of two species of Metapone (M. madagascarica, M. new species.) were collected in Madagascar and established in laboratory nests. It could be demonstrated that both species are specialist predators of termites (Cryptotermes kirbyi). During hunting the ants sting the termites and thereby paralyze and preserve the prey alive. In this way prey can be stored in the ant nest for extended periods. During foraging and colony emigrations the ants lay chemical trails with poison gland secretions. Among the seven compounds identified in the venom only methyl pyrrole-2-carboxylate elicits trail following behavior in both Metapone species. Received 11 February 2002, accepted 23 February 2002.     

Complex chemical communication in the crazy ant <Emphasis Type="Italic">Paratrechina longicornis</Emphasis> Latreille (Hymenoptera: Formicidae)

Summary. The formicine ant Paratrechina longicornis is known for its extremely opportunistic foraging behaviour. Only a single trail pheromone source, the rectum, was previously described from this ant. Our detailed examination of this ant’s chemical communication system revealed the presence of at least four sources of pheromones. Rectum, poison sac, and Dufour gland contain orientation components with decreasing effectiveness and persistence (in the sequence mentioned) as well as attractants with increasing effectiveness. Furthermore, the mandibular gland contains repellents, and a releaser of defensive behaviour. This set of various signals of different strength and persistence allows an extraordinary degree of flexibility and efficiency in the collective behaviour of P. longicornis, especially food exploitation, and thus may contribute to this insect’s overall ecological success.     

Post-mating odor in females of the solitary bee, Andrena nigroaenea (Apoidea, Andrenidae), inhibits male mating behavior

We investigated odor changes and their behavioral significance in the solitary, ground-nesting bee Andrena nigroaenea. We used gas chromatography with electroantennographic detection and performed behavioral tests with males in the field using natural odor samples and synthetic compounds. We found that only cuticle extracts of young females elicited copulation attempts in the males. We demonstrated that among the 17 compounds which triggered electroantennographic responses, all-trans-farnesyl hexanoate and all-trans-farnesol were significantly more abundant in unattractive cuticle extracts of A. nigroaenea females. Dufour’s gland extracts of these females also contained greater amounts of both compounds. In bioassays using synthetic farnesyl hexanoate and farnesol we found that these compounds inhibit copulation behavior in the males. Farnesyl hexanoate is probably synthesized in Dufour’s gland and used by females for lining brood cells. We interpret the semiochemical function of farnesyl hexanoate and its precursor farnesol to have evolved secondarily. As an outcome of sexual selection, it facilitates the discrimination by males of receptive females from nesting and thus already mated individuals. The dual function of these compounds represents an elegant parsimony in the chemical communication system of this insect. Received: 19 January 2000 / Revised: 29 May 2000 / Accepted: 24 June 2000     

Kin discriminators in the eusocial sweat bee <Emphasis Type="Italic">Lasioglossum malachurum</Emphasis>: the reliability of cuticular and Dufour’s gland odours

The ability to discriminate degrees of relatedness may be expected to evolve if it allows unreciprocated altruism to be preferentially directed towards kin (Hamilton in J Theor Biol 7:1–16, 1964). We explored the possibility of kin recognition in the primitively eusocial halictid bee Lasioglossum malachurum by investigating the reliability of worker odour cues that can be perceived by workers to act as indicators of either nest membership or kinship. Cuticular and Dufour’s gland compounds varied significantly among colonies of L. malachurum, providing the potential for nestmate discrimination. A significant, though weak, negative correlation between chemical distance and genetic relatedness (r = −0.055, p < 0.001) suggests a genetic component to variation in cuticular bouquet, but odour cues were not informative enough to discriminate between different degrees of relatedness within nests. This pattern of variation was similar for Dufour’s gland bouquets. The presence of unrelated individuals within nests that are not chemically different from their nestmates suggests that the discrimination system of L. malachurum is prone to acceptance errors. Compounds produced by colony members are likely combined to generate a gestalt colony chemical signature such that all nestmates have a similar smell. The correlation between odour cues and nest membership was greater for perceived compounds than for non-perceived compounds, suggesting that variability in perceived compounds is a result of positive selection for nestmate recognition despite potentially stabilising selection to reduce variability in odour differences and thereby to reduce costs derived from excessive intracolony nepotistic behaviour.     

Identification of trail pheromone compounds from the labial glands of the stingless bee Geotrigona mombuca

Foragers of several species of stingless bees deposit pheromone spots in the vegetation to guide recruited nestmates to a rich food source. Recent studies have shown that Trigona and Scaptotrigona workers secrete these pheromones from their labial glands. An earlier report stated that species within the genus Geotrigona use citral from their mandibular glands for scent marking. Since convincing experimental proof for this conjecture is lacking, we studied the glandular origin of the trail pheromone of Geotrigona mombuca. In field bioassays, newly recruited bees were diverted by artificial scent trails that branched off from the natural scent trail deposited by their nestmates only when they were baited with extracts from the foragers’ labial glands. Compounds extracted from the mandibular glands, however, did not release trail following behavior. This demonstrates that the trail pheromone of G. mombuca is produced in the labial glands, as in Trigona and Scaptotrigona. Furthermore, in chemical analyses citral was identified exclusively in the foragers’ mandibular glands, which disproves its supposed role as a trail pheromone. The labial glands contained a series of terpene- and wax type esters, with farnesyl butanoate as major constituent. We, therefore, postulate that the trail pheromone of G. mombuca is composed of a blend of esters.     

Trail pheromones and Dufour gland contents in three <Emphasis Type="Italic">Camponotus</Emphasis> species (<Emphasis Type="Italic">C. castaneus,C. balzani,C. sericeiventris</Emphasis>: Formicidae,Hymenoptera)

Summary. By means of gas chromatography, gas chromatographic coupled mass spectrometry and behavioral analysis the major trail pheromone components from the hindgut of the formicine species Camponotus castaneus, C. balzani and C. sericeiventris were identified. The trail pheromone of C. castaneus is 3,5-dimethyl-6-(1-methylpropyl)- tetrahydro-2H-pyran- 2-one, and that of the other two species is 3,4-dihydro-8-hydroxy-3,5,7-trimethylisocoumarin. Although both compounds release precise trail following behavior in the respective species, the major recruitment signal in the three Camponotus species appears to be formic acid discharged from the poison gland. The composition of the Dufour gland secretions of C. castaneus and C. sericeiventris is similar, but that of the hypertrophied Dufour gland of C. balzani is very different from any other Camponotus Dufour gland content described up to date: it contains large amounts of esters, the major compound of which is octyl hexanoate, which makes up 97% a/a of the total volatiles.     

The chemosensory ability of the predatory leech Whitmania laevis (Arhynchobdellida: Haemopidae) for prey searching

Although prey-detecting and searching abilities of predatory leeches of rhynchobdellid or the Erpobdelliformes of arhynchobdellid species have been studied in the past, hirudiniformes leeches are rarely mentioned. In this study, we investigated the chemosensory ability for prey-detecting and searching in Whitmania laevis, a hirudiniformes species that mainly preys on freshwater snails, and examined if such ability aided in their prey selection. Five sympatric snail species, i.e., apple snail Pomacea canaliculata, thiarid snail Thiara tuberculata, viviparid snail Sinotaia quadrata, ear pond snail Radix auricularia swinhoei and tadpole snail Physa acuta were used as prey. Our results showed that W. laevis has the chemosensory ability to detect the waterborne odors of snails. However, they follow the snails by their mucus trails, and not by the odor that the snails leave in the water. Of these five snail species, W. laevis only followed the trails of the thiarid snails, ear pond snails and tadpole snails, and did not show a different response to the trails produced by snails of different sizes. Our results suggest that W. laevis can use waterborne odors to detect the existence of prey. They rely on mucus trails to follow their preferred prey, but do not distinguish between snails of a preferred size by their mucus trails. In addition, when following the trail of a preferred snail, W. laevis exhibits a newly described searching behavior, i.e., head tapping, and may use it to locate a snail trail and increase its probability of finding the trail-laying snail nearby.     

Trail and recruitment pheromones in Camponotus socius (Hymenoptera: Formicidae)

Summary. Worker ants of Camponotus socius employ multicomponent signals during group recruitment to food sources and nest emigrations. The chemical signals consist of trail orientation pheromones that originate from the hindgut. Two components that elicit trail orientation behavior were identified: (2S,4R,5S)-2,4-dimethyl-5-hexanolide and 2,3-dihydro-3,5-dihydroxy-6-methylpyran-4-one. Although both compounds release trail following behavior, in choice tests the former compound is preferred significantly. The major recruitment signal appears to be formic acid discharged from the poison gland. Compounds identified in the Dufour gland secretions do not seem to be involved in the recruitment process.     

Nest separation and the dynamics of the Gestalt odor in the polydomous ant Cataglyphis iberica (Hymenoptera, Formicidae)

In the polydomous ant species Cataglyphis iberica, nests belonging to the same colony are completely separated during hibernation. In order to examine whether this separation induces changes both in the hydrocarbon profile and in recognition ability between adult nestmates, we separated groups of workers for several months under two different conditions: at hibernation temperature and at room temperature. At room temperature, recognition remained unchanged but separation led to longer mutual antennations relative to non-separated controls. When half of a colony was placed under hibernation conditions, antennal interactions also increased in duration and a few aggressive interactions emerged between separated ants. This aggressiveness never reached the intercolonial level observed in this species. In both cases, the hydrocarbon profiles showed differences between individuals after separation while remaining homogeneous within each nest. This chemical modification may induce the longer antennations observed. After separated groups were reunited, individuals recovered their previous antennation pattern and a convergence in hydrocarbon profiles was again observed. These concurrent observations suggest that hydrocarbons are transferred between nestmates. In C. iberica, the formation of the colonial odor seems to follow the “Gestalt” model which allows all satellite nests of a colony to have a common colonial odor. In the field, temporary nest isolation during hibernation may induce divergence between satellites. The role of adult transport in connecting nests during the active season to obtain an efficient Gestalt odor is discussed. Received: 16 June 1997 / Accepted after revision: 25 October 1997     

Reversible royalty in worker honeybees (<Emphasis Type="Italic">Apis mellifera</Emphasis>) under the queen influence

In most social insects, worker sterility is reversible, and in the absence of the queen, at least some workers develop ovaries and lay male-destined eggs. In the honeybee, reproductive workers also produce queen-characteristic mandibular and Dufour’s pheromones. The evolution of worker sterility is still under debate as to whether it is caused by queen manipulation (queen-control hypothesis) or represents worker fitness maximization (worker-control hypothesis). In this study, we investigated whether worker fertility and royal pheromone production are reversible under the queen influence. To that effect, we induced ovary activation and queen pheromone production in workers by rearing them as queenless (QL) groups. These workers were subsequently reintroduced into queenright (QR) microcolonies for 1 week, and their ovary status and queen pheromone levels were monitored. Workers reintroduced into QR, but not QL colonies, showed a clear regression in ovary development and levels of the queen pheromones. This is the first demonstration that worker sterility and/or fertility is reversible and is influenced by the queen. These results also emphasize the robustness of the coupling between ovary activation and royal pheromone production, as well as lending credence to the queen-control hypothesis. The dynamics of queen pheromone production in QL workers supports the role of Dufour’s gland pheromone as a fertility signal and that of the mandibular gland pheromone in dominance hierarchies.The two authors, Osnat Malka and Shiri Shnieor, contributed equally to this work.     

Individual and collective foraging decisions: a field study of worker recruitment in the gypsy ant <Emphasis Type="Italic">Aphaenogaster senilis</Emphasis>

In social insects, the decision to exploit a food source is made both at the individual (e.g., a worker collecting a food item) and colony level (e.g., several workers communicating the existence of a food patch). In group recruitment, the recruiter lays a temporary chemical trail while returning from the food source to the nest and returns to the food guiding a small group of nestmates. We studied how food characteristics influence the decision-making process of workers changing from individual retrieving to group recruitment in the gypsy ant Aphaenogaster senilis. We offered field colonies three types of prey: crickets (cooperatively transportable), shrimps (non-transportable), and different quantities of sesame seeds (individually transportable). Colonies used group recruitment to collect crickets and shrimps, as well as seeds when they were available in large piles, while small seed piles rarely led to recruitment. Foragers were able to “measure” food characteristics (quality, quantity, transportability), deciding whether or not to recruit, accordingly. Social integration of individual information about food emerged as a colony decision to initiate or to continue recruitment when the food patch was rich. In addition, group recruitment allowed a fast colony response over a wide thermal range (up to 45°C ground temperature). Therefore, by combining both advantages of social foraging (group recruitment) and thermal tolerance, A. senilis accurately exploited different types of food sources which procured an advantage against mass-recruiting and behaviorally dominant species such as Tapinoma nigerrimum and Lasius niger.     

Combined use of pheromone trails and visual landmarks by the common garden ant Lasius niger

This study investigated the relative importance of pheromone trails and visual landmarks on the ability of Lasius niger foragers to relocate a previously used food source. Colonies formed foraging trails to a 1-M sucrose feeder. Sections of this trail were then presented back to the same colony after variable time intervals. Individual outgoing foragers were observed to determine if they walked for 15 cm in the direction of the feeder or not. On newly established pheromone trails formed by 500 ant passages, 77% of the foragers walked in the correct direction vs 31% for control foragers (no trail pheromone). Pheromone trails decayed to the control levels in 20–24 h. Trails formed with fewer ant passages (125 or 30) decayed quicker. The use of visual landmarks was investigated by using trails with outgoing foragers from the colony that established the trail, either in the same room or in a different room, with different visual landmarks, to that used during trail establishment. Approximately 20% more ants walked in the correct direction in the same room vs the different room. This difference decreased to around 10% 2 h after trail establishment, indicating that the ants in the different room were learning the new visual cues to navigate by. Our results show that visual landmarks and pheromone trails are approximately equally useful in initially guiding L. niger foragers to food locations and that these two information sources have a complementary function.     

Trail following,speed and fractal dimension of movement in a marine prosobranch,Littorina littorea,during a mating and a non-mating season

We quantitatively studied movement behaviour in the gastropod Littorina littorea in laboratory experiments during periods of their non-mating season (November 1992) and their mating season (April–May 1993). Snails were collected in 1992 and 1993 from one boulder shore on the north west coast of Sweden. In a comparison between the two seasons (one non-mating and one mating) we measured trail complexity of unsexed snails using fractal dimesion, the degree of mucus trail following (coincidence index of marker and tracker trails) and average movement speed of marker and tracker snails. We found no differences in fractal dimension and coincidence index of trails between the two seasons. Tracker snails moved, however, significantly faster than marker snails during both seasons. This could not be explained by trackers, when locomoting, using the mucus trail deposited by the marker to increase their speed, since there was no correlation between coincidence index and tracker speed. During the mating season we also conducted trail complexity, trail following and speed experiments comparing the behaviour of males and females. There was no difference between males and females in the fractal dimension of movement, nor was there any difference between the mean speed of male and female snails, although male marker snails tended to move faster than female marker snails. Males tracking other males, females tracking other females and females tracking males followed trails about equally long distances (i.e., coincidence indices did not differ). In contrast, males following female mucus trails showed a significantly higher degree of trail following than the other sex combinations. This new finding may suggest that females of L. littorea release pheromones in their mucus trails and that males are able to identify them.     

Similar is not the same: Social calls of conspecifics are more effective in attracting wild bats to day roosts than those of other bat species

Many bat species regularly need to find new day roosts as they require numerous shelters each breeding season. It has been shown that bats exchange information about roosts among colony members, and use echolocation and social calls of conspecifics in order to find roosts. However, it is unclear if wild bats discriminate between social calls of conspecifics and other bat species while searching for roosts. Furthermore, the extent that bats are attracted to potential roosts by each of these two call types is unknown. We present a field experiment showing that social calls of conspecifics and other bat species both attract bats to roosts. During two summers, we played back social calls of Bechstein’s bats (Myotis bechsteinii) and Natterer’s bats (Myotis nattereri) from different bat boxes that can serve as roosts for these species. All experimental bat boxes were monitored with infrared video to identify the approaching bat species. Three species (M. bechsteinii, M. nattereri, and Plecotus auritus) approached the boxes significantly more often during nights when bat calls were played compared to nights without playbacks. Bechstein’s bats and Natterer’s bats were both more attracted to social calls of conspecifics than of the other species, whereas P. auritus did not discriminate between calls of either Myotis species. Only Bechstein’s bats entered experimental boxes and only at times when calls from conspecifics were played. Our findings show that wild bats discriminate between social calls of conspecifics and other bat species although they respond to both call types when searching for new roosts.     

Better the nest site you know: decision-making during nest migrations by the Pharaoh’s ant

Animals frequently have to decide between alternative resources and in social insects these individual choices produce a colony-level decision. The choice of nest site is a particularly critical decision for a social insect colony to make, but the decision making process has still only been studied in a few species. In this study, we investigated nest selection by the Pharaoh’s ant, Monomorium pharaonis, a species renowned for its propensity to migrate and its use of multi-component trail pheromones to organise decision-making in other contexts. When presented with the choice of familiar and novel nests of equal quality in a Y set-up, colonies preferentially migrated towards the familiar nest, suggesting a form of colony-level ‘memory’ of potential nest sites. However, if the novel nest was superior to the familiar nest, then colonies began migrating initially to the familiar nest, but then redirected their migration to the superior quality novel nest. This may be an effective method of reducing colony exposure while searching for an optimum nest site. Branches that had previously led to a selected nest were attractive to ants in subsequent migrations, suggesting that trail pheromones mediate the decision making process. The adaptive, pheromone-based organisation of nest-site selection by Pharaoh’s ants matches their ephemeral environment and is likely to contribute to their success as a 'tramp' species.     

Disease resistance in a weaver ant, <Emphasis Type="BoldItalic">Polyrhachis dives</Emphasis>, and the role of antibiotic-producing glands

Parasites represent one of the main threats to all organisms and are likely to be particularly significant for social animals because of the increased potential for intragroup transmission. Social animals must therefore have effective resistance mechanisms against parasites and one of the most important components of disease resistance in ants is thought to be the antibiotic-producing metapleural gland. This gland is ancestral in ants, but has been lost secondarily in a small number of species. It is unknown whether these evolutionary losses are due to a reduction in parasite pressure or the replacement of the gland’s function with other resistance mechanisms. Here we used the generalist entomopathogenic fungus Metarhizium to compare the disease resistance of a species of a weaver ant, Polyrhachis dives, which has lost the metapleural gland, with that of the well-studied leaf-cutting ant Acromyrmex echinatior and two other ant species, Myrmica ruginodis and Formica fusca, all of which have metapleural glands. The P. dives weaver ants had intermediate resistance when kept individually, and similar resistance to A. echinatior leaf-cutting ants when kept in groups, suggesting that the loss of the metapleural gland has not resulted in weaver ants having reduced disease resistance. P. dives weaver ants self-groomed at a significantly higher rate than the other ants examined and apparently use their venom for resistance, as they had reduced resistance when their venom gland was blocked and the venom was shown in vitro to prevent the germination of fungal spores. Unexpectedly, the leaf-cutting ant A. echinatior also had reduced resistance to Metarhizium when its venom gland was blocked. It therefore appears that the evolutionary loss of the metapleural gland does not result in reduced disease resistance in P. dives weaver ants, and that this at least in part may be due to the ants having antimicrobial venom and high self-grooming rates. The results therefore emphasise the importance of multiple, complementary mechanisms in the disease resistance of ant societies.