Predatory spider mimics acquire colony-specific cuticular hydrocarbons from their ant model prey

The integrity of social insect colonies is maintained by members recognising and responding to the chemical cues present on the cuticle of any intruder. Nevertheless, myrmecophiles use chemical mimicry to gain access to these nests, and their mimetic signals may be acquired through biosynthesis or through contact with the hosts or their nest material. The cuticular hydrocarbon profile of the myrmecophilous salticid spider Cosmophasis bitaeniata closely resembles that of its host ant Oecophylla smaragdina. Here, we show that the chemical resemblance of the spider does not arise through physical contact with the adult ants, but instead the spider acquires the cuticular hydrocarbons by eating the ant larvae. More significantly, we show that the variation in the cuticular hydrocarbon profiles of the spider depends upon the colony of origin of the ant larvae prey, rather than the parentage of the spider.     

Nest- and colony-mate recognition in polydomous colonies of meat ants (Iridomyrmex purpureus)

Workers of polydomous colonies of social insects must recognize not only colony-mates residing in the same nest but also those living in other nests. We investigated the impact of a decentralized colony structure on colony- and nestmate recognition in the polydomous Australian meat ant (Iridomyrmex purpureus). Field experiments showed that ants of colonies with many nests were less aggressive toward alien conspecifics than those of colonies with few nests. In addition, while meat ants were almost never aggressive toward nestmates, they were frequently aggressive when confronted with an individual from a different nest within the same colony. Our chemical analysis of the cuticular hydrocarbons of workers using a novel comprehensive two-dimensional gas chromatography technique that increases the number of quantifiable compounds revealed both colony- and nest-specific patterns. Combined, these data indicate an incomplete transfer of colony odor between the nests of polydomous meat ant colonies.     

Nestmate recognition in social wasps: manipulation of hydrocarbon profiles induces aggression in the European hornet

The influence of individual cuticular hydrocarbons on nestmate recognition in the European hornet, Vespa crabro L., was investigated. We observed the behavioural response of workers towards differently treated dead conspecifics in a bioassay. Dummies were extracted with dichloromethane and extracts were spiked with microgram amounts of synthetic hydrocarbons naturally occurring on the cuticle of V. crabro. These modified extracts were reapplied to extracted workers that were subsequently tested in the bioassay. Non-spiked nestmate dummies (negative control) and untreated non-nestmate dummies (positive control) were tested in control experiments. The addition of only heneicosane or a mixture of heneicosane, tricosane, and (Z)-9-tricosene to the extracts led to a significant increase of agonistic behaviour in workers leaving the nest for foraging flights. Returning workers reacted much less aggressively than those leaving. This is one of the first behavioural proofs that manipulation of cuticular hydrocarbon profiles can be perceived by a social insect species. The results support the hypothesis that colony-specific cuticular hydrocarbon profiles are involved in the phenomenon of nestmate recognition among social insects.     

“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     

Knowing your enemies: seasonal dynamics of host–social parasite recognition

Despite its evolutionary significance, behavioural flexibility of social response has rarely been investigated in insects. We studied a host–social parasite system: the slave-making ant Polyergus rufescens and its host Formica rufibarbis. Free-living host workers from parasitized and from unparasitized areas were compared in their level of aggression against the parasite and alien conspecifics. We expected that a seasonal change would occur in the acceptance threshold of F. rufibarbis workers from a parasitized area towards the parasite, whereas F. rufibarbis workers from an unparasitized area would not show substantial changes connected with the parasites peak in activity (raiding and colony-founding season). The results showed a significant adaptive behavioural flexibility of host species workers and are consistent with the acceptance threshold models (Reeve 1989) prediction that recognition systems are not fixed but context-dependent. In particular, host workers from the unparasitized area were highly aggressive towards the parasite regardless of the season, whereas host workers from the parasitized area significantly increased their aggression towards the parasite during its raiding and colony-founding season. Being able to detect and possibly kill a Polyergus scout searching for host nests can be an effective strategy for a Formica colony to avoid being raided or usurped by a parasite queen.     

Reclaiming the crown: queen to worker conflict over reproduction in <Emphasis Type="Italic">Aphaenogaster cockerelli</Emphasis>

In many social taxa, reproductively dominant individuals sometimes use aggression to secure and maintain reproductive status. In the social insects, queen aggression towards subordinate individuals or workers has been documented and is predicted to occur only in species with a small colony size and a low level of queen–worker dimorphism. We report queen aggression towards reproductive workers in the ant species Aphaenogaster cockerelli, a species with a relatively large colony size and a high level of reproductive dimorphism. Through analysis of cuticular hydrocarbon profiles, we show that queens are aggressive only to reproductively active workers. Non-reproductive workers treated with a hydrocarbon typical for reproductives are attacked by workers but not by queens, which suggests different ways of recognition. We provide possible explanations of why queen aggression is observed in this species.     

A unique strategy of host colony exploitation in a parasitic ant: workers of<Emphasis Type="Italic"> Polyrhachis lama</Emphasis> rear their brood in neighbouring host nests

The formicine ant Polyrhachis lama is a social parasite, exploiting its ponerine host ant species Diacamma sp. In most social parasitic associations, the parasitic species are closely related to their host species group, evolving directly from independent ancestors of the host species. However, in the Polyrhachis lama–Diacamma sp. association, the associated species belong to different ant subfamilies. Based on preliminary field surveys, we had presumed that P. lama might have given up its reproductive division of labour, i.e. workers would be able to produce males as well as workers and females parthenogenetically. In this study, this hypothesis was disproved: Polyrhachis lama workers cannot be fertilized and are only able to produce males. In the host–parasite association originating from nests possessing a P. lama queen, workers penetrate surrounding Diacamma sp. nests, carrying brood for rearing within these satellite nests. In this peculiar way, a single P. lama colony is able to exploit several Diacamma sp. colonies simultaneously.     

Effect of time on colony odour stability in the ant <Emphasis Type="Italic">Formica exsecta</Emphasis>

Among social insects, maintaining a distinct colony profile allows individuals to distinguish easily between nest mates and non-nest mates. In ants, colony-specific profiles can be encoded within their cuticular hydrocarbons, and these are influenced by both environmental and genetic factors. Using nine monogynous Formica exsecta ant colonies, we studied the stability of their colony-specific profiles at eight time points over a 4-year period. We found no significant directional change in any colony profile, suggesting that genetic factors are maintaining this stability. However, there were significant short-term effects of season that affected all colony profiles in the same direction. Despite these temporal changes, no significant change in the profile variation within colonies was detected: each colony’s profile responded in similar manner between seasons, with nest mates maintaining closely similar profiles, distinct from other colonies. These findings imply that genetic factors may help maintain the long-term stability of colony profile, but environmental factors can influence the profiles over shorter time periods. However, environmental factors do not contribute significantly to the maintenance of diversity among colonies, since all colonies were affected in a similar way.     

The role of microgynes in the reproductive strategy of the neotropical ant <Emphasis Type="Italic">Ectatomma ruidum</Emphasis>

Miniaturized queens, microgynes, are regarded as an alternative reproductive strategy sparsely present through the ant world. The described roles of miniaturized queens include alternative short-distance dispersal morphs, an adaptation to polygyny and inquiline parasites. Some of these inquiline parasite microgynes have been described as a separate species from their host. In the poneromorph group, miniaturized queens are only reported in two Mexican populations of two Ectatomminae: Ectatomma tuberculatum, in which small queens represent an inquiline species (Ectatomma parasiticum) and Ectatomma ruidum. E. ruidum presents apparently facultative polygyny with microgynes. We used mitochondrial DNA markers and newly developed microsatellite loci to investigate the status as well as the role of microgynes in E. ruidum. We confirmed that microgynes and macrogynes are from the same species. This species is almost exclusively monogynous and monoandrous, supernumerary dealate queens of both types being actually daughters of the mother queen. An apparently polygynous nest was more often headed by a macrogyne than a microgyne. We didn't find any inbreeding or isolation by distance in the studied population, indicating that new gynes are inseminated by unrelated males and can establish a new nest far from their natal nest. However, re-adoption of daughter queens seems to be the rule and rate of microgyny appears to be linked to nest density and environmental factors.     

In-nest environment modulates nestmate recognition in the ant<Emphasis Type="Italic"> Camponotus fellah</Emphasis>

Multiple behavioral and chemical studies indicate that ant nestmate recognition cues are low-volatile substances, in particular hydrocarbons (HCs) located on the cuticular surface. We tested the hypothesis that in the ant Camponotus fellah, nest environment, in particular nest volatile odors, can modulate nestmate-recognition-mediated aggression. Workers were individually confined within their own nest in small cages having either a single mesh (SM = limited physical contact permitted) or a double mesh (DM = exposed to nest volatiles only) screen. Individual workers completely isolated outside their nest (CI) served as control. When reintroduced into a group of 50 nestmates, the CI workers were attacked as alien ants after only 2 weeks of separation, whereas the SM workers were treated as nestmates even after 2 months of separation. Aggression towards DM ants depended on the period of isolation. Only DM workers isolated for over 2 months were aggressed by their nestmates, which did not significantly differ from the CI nestmates. Cuticular HC analyses revealed that the profile of the non-isolated ants (NI) was clearly distinct from that of CI, SM and DM ants. Profile differences matched the aggressive response in the case of CI ants but were uncorrelated in the case of SM or DM ants. This suggests that keeping the ants within the nest environment affected nestmate recognition in additional ways than merely altering their HC profile. Nest environment thus appears to affect label–template mismatch by modulating aggressive behavior, as well as the direction at which cuticular HCs diverged during the separation period.     

Garden sharing and garden stealing in fungus-growing ants

 Fungi cultivated by fungus-growing ants (Attini: Formicidae) are passed on between generations by transfer from maternal to offspring nest (vertical transmission within ant species). However, recent phylogenetic analyses revealed that cultivars are occasionally also transferred between attine species. The reasons for such lateral cultivar transfers are unknown. To investigate whether garden loss may induce ants to obtain a replacement cultivar from a neighboring colony (lateral cultivar transfer), pairs of queenright colonies of two Cyphomyrmex species were set up in two conjoined chambers; the garden of one colony was then removed to simulate the total crop loss that occurs naturally when pathogens devastate gardens. Garden-deprived colonies regained cultivars through one of three mechanisms: joining of a neighboring colony and cooperation in a common garden; stealing of a neighbor's garden; or aggressive usurpation of a neighbor's garden. Because pathogens frequently devastate attine gardens under natural conditions, garden joining, stealing and usurpation emerge as critical behavioral adaptations to survive garden catastrophes. Received: 16 June 2000 / Accepted in revised form: 14 September 2000     

The role of moisture in the nest thermoregulation of social wasps

Paper nests of social wasps are intriguing constructions for both, biologists and engineers. We demonstrate that moisture and latent heat significantly influence the thermal performance of the nest construction. Two colonies of the hornet Vespa crabro were investigated in order to clarify the relation of the temperature and the moisture regime inside the nest. Next to fairly stable nest temperatures the hornets maintain a high relative humidity inside the nest. We found that in consequence a partial vapor-pressure gradient between nest and ambient drives a constant vapor flux through the envelope. The vapor flux is limited by the diffusion resistance of the envelope. The driving force of vapor flux is heat, which is consumed through evaporation inside the nest. The colony has to compensate this loss with metabolic heat production in order to maintain a stable nest temperature. However, humidity fluctuations inside the nest induce circadian adsorption and desorption cycles, which stabilize the nest temperature and thus contribute significantly to temperature homeostasis. Our study demonstrates that both mechanisms influence nest thermoregulation and need to be considered to understand the thermodynamic behavior of nests of wasps and social insects in general.     

Decision rules for egg recognition are related to functional roles and chemical cues in the queenless ant Dinoponera quadriceps

The capacity to distinguish colony members from strangers is a key component in social life. In social insects, this extends to the brood and involves discrimination of queen eggs. Chemical substances communicate colony affiliation for both adults and brood; thus, in theory, all colony members should be able to recognize fellow nestmates. In this study, we investigate the ability of Dinoponera quadriceps workers to discriminate nestmate and non-nestmate eggs based on cuticular hydrocarbon composition. We analyzed whether cuticular hydrocarbons present on the eggs provide cues of discrimination. The results show that egg recognition in D. quadriceps is related to both age and the functional role of workers. Brood care workers were able to distinguish nestmate from non-nestmate eggs, while callow and forager workers were unable to do so. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Deviance partitioning of host factors affecting parasitization in the European brown hare (Lepus europaeus)

Deviance partitioning can provide new insights into the ecology of host-parasite interactions. We studied the host-related factors influencing parasite prevalence, abundance, and species richness in European brown hares (Lepus europaeus) from northern Spain. We defined three groups of explanatory variables: host environment, host population, and individual factors. We hypothesised that parasite infection rates and species richness were determined by different host-related factors depending on the nature of the parasite (endo- or ectoparasite, direct or indirect life cycle). To assess the relative importance of these components, we used deviance partitioning, an innovative approach. The explained deviance (ED) was higher for parasite abundance models, followed by those of prevalence and then by species richness, suggesting that parasite abundance models may best describe the host factors influencing parasitization. Models for parasites with a direct life cycle yielded higher ED values than those for indirect life cycle ones. As a general trend, host individual factors explained the largest proportion of the ED, followed by host environmental factors and, finally, the interaction between host environmental and individual factors. Similar hierarchies were found for parasite prevalence, abundance, and species richness. Individual factors comprised the most relevant group of explanatory variables for both types of parasites. However, host environmental factors were also relevant in models for indirect life-cycle parasites. These findings are consistent with the idea of the host as the main habitat of the parasite; whereas, for indirect life-cycle parasites, transmission would be also modulated by environmental conditions. We suggest that parasitization can be used not only as an indicator of individual fitness but also as an indicator of environmental quality for the host. This research underlines the importance of monitoring parasite rates together with environmental, population, and host factors.     

Fever in honeybee colonies

 Honeybees, Apis spp., maintain elevated temperatures inside their nests to accelerate brood development and to facilitate defense against predators. We present an additional defensive function of elevating nest temperature: honeybees generate a brood-comb fever in response to colonial infection by the heat-sensitive pathogen Ascosphaera apis. This response occurs before larvae are killed, suggesting that either honeybee workers detect the infection before symptoms are visible, or that larvae communicate the ingestion of the pathogen. This response is a striking example of convergent evolution between this "superorganism" and other fever-producing animals. Received: 2 September 1999 / Accepted in revised form: 28 February 2000     

Orientation and navigation during adult transport between nests in the ant Cataglypis iberica

  Cataglyphis iberica is a polydomous ant species in which adult transports between nests are frequently observed. When pairs of workers were captured and released at the same location, the transporters (Ts) fled directly towards their destination nest and reached it in most of the cases. The transportees (Te), on the other hand, fled in the opposite direction and only a third of them eventually reached their nest of departure. Additional experiments suggest that this result may be explained by the fact that the Ts ants have a memory of the compass direction of the nest they are heading to and that they adjust their course by using a sequence of memorised landmarks. As regards to the Te, the reversal of their direction of transport seems to be based essentially on celestial cues. Received: 20 October 1999 / Accepted in revised form: 10 May 2000     

Does contrast between eggshell ground and spot coloration affect egg rejection?

Obligate avian brood parasitic species impose the costs of incubating foreign eggs and raising young upon their unrelated hosts. The most common host defence is the rejection of parasitic eggs from the nest. Both egg colours and spot patterns influence egg rejection decisions in many host species, yet no studies have explicitly examined the role of variation in spot coloration. We studied the American robin Turdus migratorius, a blue-green unspotted egg-laying host of the brown-headed cowbird Molothrus ater, a brood parasite that lays non-mimetic spotted eggs. We examined host responses to model eggs with variable spot coloration against a constant robin-mimetic ground colour to identify patterns of rejection associated with perceived contrast between spot and ground colours. By using avian visual modelling, we found that robins were more likely to reject eggs whose spots had greater chromatic (hue) but not achromatic (brightness) contrast. Therefore, egg rejection decision rules in the American robin may depend on the colour contrast between parasite eggshell spot and host ground coloration. Our study also suggests that egg recognition in relation to spot coloration, like ground colour recognition, is tuned to the natural variation of avian eggshell spot colours but not to unnatural spot colours.     

Olfactory host finding, intermediate memory and its potential ecological adaptation in Nasonia vitripennis

Associative learning of host-associated chemical cues was studied in Nasonia vitripennis, a parasitoid of fly pupae in nests of hole-nesting birds. When females encountered a fly pupa and performed one sequence of host recognition behaviour including drilling the ovipositor into the host in the presence of the artificial odour furfurylheptanoate (FFH), they were afterwards arrested by FFH in olfactometer experiments. The response vanished after 4 days and could be blocked after 3 days by feeding wasps with ethacrynic acid prior and after the training. This indicates the formation of an intermediate form of memory by one host experience in N. vitripennis. Interestingly, the trained wasps avoided odours that were not present during the host encounter, although naive wasps did not react to these odours. This unique behaviour probably causes wasps to focus during host searching on those chemical cues they have experienced in the host environment. Studies in nests of hole-nesting birds revealed that about 30% of all nests contained only one fly pupa, and laboratory studies showed that N. vitripennis females are able to parasitise around 100 fly pupae in their life. It is discussed that under these conditions, the formation of a non-permanent intermediate memory for host-associated odours after one host encounter is adaptive to avoid costs involved with formation and maintenance of memory for misleading cues. The demonstration of associative olfactory learning in N. vitripennis, the first parasitoid species with sequenced genome, opens the gate to study molecular mechanisms of memory formation and its ecological adaptation in parasitoids.     

Resource competition between two fungal parasites in subterranean termites

Subterranean termites live in large groups in underground nests where the pathogenic pressure of the soil environment has led to the evolution of a complex interaction among individual and social immune mechanisms in the colonies. However, groups of termites under stress can show increased susceptibility to opportunistic parasites. In this study, an isolate of Aspergillus nomius Kurtzman, Horn & Hessltine was obtained from a collapsed termite laboratory colony. We determined that it was primarily a saprophyte and, secondarily, a facultative parasite if the termite immunity is undergoing a form of stress. This was determined by stressing individuals of the Formosan subterranean termite Coptotermes formosanus Shiraki via a co-exposure to the virulent fungal parasite Metarhizium anisopliae (Metch.) Sorokin. We also examined the dynamics of a mixed infection of A. nomius and M. anisopliae in a single termite host. The virulent parasite M. anisopliae debilitated the termite immune system, but the facultative, fast growing parasite A. nomius dominated the mixed infection process. The resource utilization strategy of A. nomius during the infection resulted in successful conidia production, while the chance for M. anisopliae to complete its life cycle was reduced. Our results also suggest that the occurrence of opportunistic parasites such as A. nomius in collapsing termite laboratory colonies is the consequence of a previous stress, not the cause of the stress.