Non-specific association between filamentous bacteria and fungus-growing ants

Fungus-growing ants and their fungal cultivar form a highly evolved mutualism that is negatively affected by the specialized parasitic fungus Escovopsis. Filamentous Pseudonocardia bacteria occurring on the cuticle of attine ants have been proposed to form a mutualistic interaction with these ants in which they are vertically transmitted (i.e. from parent to offspring colonies). Given a strictly vertical transmission of Pseudonocardia, the evolutionary theory predicts a reduced genetic variability of symbionts among ant lineages. The aim of this study was to verify whether actinomycetes, which occur on Acromyrmex octospinosus leaf-cutting ants, meet this expectation by comparing their genotypic variability with restriction fragment length polymorphisms. Multiple actinomycete strains could be isolated from both individual ant workers and colonies (one to seven strains per colony). The colony specificity of actinomycete communities was high: Only 15% of all strains were isolated from more than one colony, and just 5% were present in both populations investigated. Partial sequencing of 16S ribosomal deoxyribonucleic acid of two of the isolated strains assigned both of them to the genus Streptomyces. Actinomycetes could also be isolated from workers of the two non-attine ant species Myrmica rugulosa and Lasius flavus. Sixty-two percent of the strains derived from attine ants and 80% of the strains isolated from non-attine ants inhibited the growth of Escovopsis. Our data suggest that the association between attine ants and their actinomycete symbionts is less specific then previously thought. Soil-dwelling actinomycetes may have been dynamically recruited from the environment (horizontal transmission), probably reflecting an adaptation to a diverse community of microbial pathogens.     

Agro-predation: usurpation of attine fungus gardens by Megalomyrmex ants

 A new ant species of Megalomyrmex conducts mass raids to usurp gardens of the fungus-growing ant Cyphomyrmex longiscapus, then lives in the gardens and consumes the cultivated fungus. Unlike attine ants, however, Megalomyrmex sp. does not forage for substrate to manure the gardens; therefore, when gardens become depleted, Megalomyrmex sp. must locate and usurp new gardens. Megalomyrmex sp. workers feed their larvae with attine brood, but only after removing the fungal mycelium that covers the attine larval integument, suggesting that this fungal coat may provide partial protection against other predators. Unlike other known Megalomyrmex species, which coexist as social parasites in attine colonies, Megalomyrmex sp. expels its attine hosts during the garden raids. Megalomyrmex sp. thus maintains a unique agro-predatory lifestyle that is described here for the first time. Received: 18 August 2000 / Accepted in revised form: 1 November 2000     

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     

<Emphasis Type="Italic">Gnamptogenys hartmani</Emphasis> Wheeler (Ponerinae: Ectatommini): an agro-predator of<Emphasis Type="Italic"> Trachymyrmex</Emphasis> and<Emphasis Type="Italic"> Sericomyrmex</Emphasis> fungus-growing ants

The fungus gardens of fungus-growing ants are a potentially valuable resource for exploitation by natural enemies, but few of these antagonistic interactions have been studied. Here we describe key aspects of the behavioral ecology of Gnamptogenys hartmani (Ponerinae: Ectatommini), a specialized agro-predator of Trachymyrmex and Sericomyrmex fungus-growing ants in Panama. Raiding columns of G. hartmani attack and usurp nests with remarkably little effort: a few intruding workers are sufficient to cause panic among the attine ants and make them abscond from the nest. Both G. hartmani larvae and adults consume the fungus and the host brood, after which the colony migrates to a new fungus-growing ant nest discovered by scouting workers. The morphology of the G. hartmani larval mouthparts is similar to that of Gnamptogenys species with a non-fungal diet. However, we suggest that the presence of long spinules on the larval mandibles in the genus Gnamptogenys, comparable to those found in attine larvae, may have pre-adapted G. hartmani to fungus eating. G. hartmani workers do not actively maintain or modify fungus gardens, which makes them less efficient exploiters than Megalomyrmex, the only other agro-predatory ant species known so far.     

A colony-level response to disease control in a leaf-cutting ant

Parasites and pathogens often impose significant costs on their hosts. This is particularly true for social organisms, where the genetic structure of groups and the accumulation of contaminated waste facilitate disease transmission. In response, hosts have evolved many mechanisms of defence against parasites. Here we present evidence that Atta colombica, a leaf-cutting ant, may combat Escovopsis, a dangerous parasite of Atta's garden fungus, through a colony-level behavioural response. In A. colombica, garden waste is removed from within the colony and transported to the midden - an external waste dump - where it is processed by a group of midden workers. We found that colonies infected with Escovopsis have higher numbers of workers on the midden, where Escovopsis is deposited. Further, midden workers are highly effective in dispersing newly deposited waste away from the dumping site. Thus, the colony-level task allocation strategies of the Atta superorganism may change in response to the threat of disease to a third, essential party.     

The ladybird<Emphasis Type="Italic"> Thalassa saginata</Emphasis>, an obligatory myrmecophile of<Emphasis Type="Italic"> Dolichoderus bidens</Emphasis> ant colonies

The larvae and pupae of the ladybird Thalassa saginata develop inside colonies of the dolichoderine ant Dolichoderus bidens. This association is the first specific and obligatory relationship recorded between ants and ladybirds. The ants provide shelter and protection to the larvae but the diet of the latter remains unclear. The integration of T. saginata larvae into the ant colonies is achieved by mimicking the cuticular patterns of the ants brood. Moreover, the larvae secrete substances from their hairs and anal gland that are likely to enhance their attractiveness.     

Reduced Chitinase Activities in Ant Plants of the Genus Macaranga

Many plant species have evolved mutualistic associations with ants, protecting their host against detrimental influences such as herbivorous insects. Letourneau (1998) reported in the case of Piper that ants defend their plants principally against stem-boring insects and also reduce fungal infections on inflorescences. Macaranga plants that were experimentally deprived of their symbiotic Crematogaster ants suffered heavily from shoot borers and pathogenic fungi (Heil 1998). Here we report that ants seem to reduce fungal infections actively in the obligate myrmecophyte Macaranga triloba (Euphorbiaceae), while ant-free plants can be easily infected. We also found extremely low chitinase activity in Macaranga plants. The plants' own biochemical defense seems to be reduced, and low chitinase activity perhaps may represent a predisposition for the evolution of myrmecophytism. These plants are therefore highly dependent on their ants, which obviously function not only as an antiherbivore defense but also as an effective agent against fungal pathogens. Received: 5 August 1998 / Accepted in revised form: 18 November 1998     

Indirect defense in a highly specific ant–plant mutualism

Although associations between myrmecophytes and their plant ants are recognized as a particularly effective form of protective mutualism, their functioning remains incompletely understood. This field study examined the ant-plant Hirtella physophora and its obligate ant associate Allomerus decemarticulatus. We formulated two hypotheses on the highly specific nature of this association: (1) Ant presence should be correlated with a marked reduction in the amount of herbivory on the plant foliage; (2) ant activity should be consistent with the "optimal defense" theory predicting that the most vulnerable and valuable parts of the plant are the best defended. We validated the first hypothesis by demonstrating that for ant-excluded plants, expanding leaves, but also newly matured ones in the long term, suffered significantly more herbivore damage than ant-inhabited plants. We showed that A. decemarticulatus workers represent both constitutive and inducible defenses for their host, by patrolling its foliage and rapidly recruiting nestmates to foliar wounds. On examining how these activities change according to the leaves’ developmental stage, we found that the number of patrolling ants dramatically decreased as the leaves matured, while leaf wounds induced ant recruitment regardless of the leaf’s age. The resulting level of these indirect defenses was roughly proportional to leaf vulnerability and value during its development, thus validating our second hypothesis predicting optimal protection. This led us to discuss the factors influencing ant activity on the plant’s surface. Our study emphasizes the importance of studying both the constitutive and inducible components of indirect defense when evaluating its efficacy and optimality.     

Low chitinase activity in Acacia myrmecophytes: a potential trade-off between biotic and chemical defences?

 We determined chitinase activity in leaves of four myrmecophytic and four non-myrmecophytic leguminous species at the plants' natural growing sites in Mexico. Myrmecophytic plants (or 'ant plants') have obligate mutualisms with ants protecting them against herbivores and pathogenic fungi. Plant chitinases can be considered a reliable measure of plant resistance to pathogenic fungi. The myrmecophytic Acacia species, which were colonised by mutualistic ants, exhibited at least six-fold lower levels of chitinase activity compared with the non-myrmecophytic Acacia farnesiana and three other non-myrmecophytes. Though belonging to different phylogenetic groups, the myrmecophytic Acacia species formed one distinct group in the data set, which was clearly separated from the non-myrmecophytic species. These findings allowed for comparison between two recent hypotheses that attempt to explain low chitinase activity in ant plants. Most probably, chitinases are reduced in myrmecophytic plant species because these are effectively defended indirectly due to their symbiosis with mutualistic ants. Received: 16 August 2000 / Accepted in revised form: 28 October 2000     

The effect of metapleural gland secretion on the growth of a mutualistic bacterium on the cuticle of leaf-cutting ants

In Acromyrmex octospinosus leaf-cutting ants the metapleural glands produce an array of antibiotic compounds that serve as a general defence against unwanted microbes on the cuticle. Leaf-cutting ants also grow mutualistic Pseudonocardiaceae bacteria on their cuticle that produce antibiotics controlling a microfungal parasite of their fungus gardens. Interaction between this bacterium and gland secretion therefore seems unavoidable. We document the typical development of bacterial growth on the cuticle of young major workers, show that growth starts a few days after eclosion, and that the maximal cover is reached after 2–3 weeks and gradually declines when workers mature. Experimental closure of the metapleural glands had no effect on the initial exponential growth phase of the bacterium, but significantly reduced the cover during the decline phase. The age-dependent abundance of the bacterium and its partial dependence on metapleural gland secretion support the hypothesis that the abundance of this mutualist is actively regulated.     

Ant-lepidopteran associations along African forest edges

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

Olfactive detection of fig wasps as prey by the ant<Emphasis Type="Italic"> Crematogaster scutellaris</Emphasis> (Formicidae; Myrmicinae)

In the species-specific and obligate mutualism between the fig (Ficus carica) and its pollinator (the fig wasps Blastophaga psenes), a third participant, the ant Crematogaster scutellaris, is a predator of the wasps. Here, we ask how ant workers can rapidly localise such prey, whose availability is limited in time and space. Using a Y-tube olfactometer, we tested ant response to odours emitted by different types of figs (receptive female, ripe female or male figs) and by fig wasps (pollinators or non-pollinators). We demonstrate that ants were significantly attracted only to odours emitted by pollinators, either alone or associated with odours of male figs (releasing wasps). Detection of prey odour by ants is an important trait that can explain their observed high rate of predation on pollinators, and could have important implications on the stability of the fig/fig wasp mutualism.     

Vision-independent odometry in the ant Cataglyphis cursor

In contrast to flying insects, in which distance estimation is visually mediated, self-induced image motion and use of familiar landmarks are known to play a minor role in ants. Here we show that strictly diurnal Cataglyphis cursor ants can gauge with accuracy the distance they have travelled even in complete darkness in the absence of any other cues, i.e. chemical or protocounting information. Thus, an ants odometer is a vision-independent system based on proprioceptive cues, implicating some form of step counting, which remain to be elucidated.     

Communal peeing: a new mode of flood control in ants

 The behavioral response of the obligate bamboo-nesting ant Cataulacus muticus to nest flooding was studied in a perhumid tropical rainforest in Malaysia and in the laboratory. The hollow internodes of giant bamboo, in which C. muticus exclusively nests, are prone to flooding by heavy rains. The ants showed a two-graded response to flooding. During heavy rain workers block the nest entrances with their heads to reduce water influx. However, rainwater may still intrude into the nest chamber. The ants respond by drinking the water, leaving the nest and excreting water droplets on the outer stem surface. This cooperative 'peeing' behavior is a new survival mechanism adaptive to the ants' nesting ecology. Laboratory experiments conducted with two other Cataulacus species, C. catuvolcus colonizing small dead twigs and C. horridus inhabiting rotten wood, did not reveal any form of water-bailing behavior. Received: 3 August 2000 / Accepted in revised form: 6 November 2000     

宁东能源化工基地规划产业布局的生态适宜性分析

基于遥感和地理信息系统技术,在宁东地区土壤侵蚀敏感性评价的基础上,对宁东能源化工基地规划的产业布局进行了生态适宜性分析.结果表明,宁东能源化工基地规划的煤炭、电力和煤化工三大主导产业布 局与该区生态环境不相适宜.在规划的12座煤矿、7个电厂和3个煤化工园区中,有3座煤矿、2个电厂和1个化工园区位于土壤侵蚀的高度敏感区内;有2座煤矿、3个电厂和1个化工园区位于土壤侵蚀的中度敏感区内.为更好的促进区域生态环境与经济社会的协调发展,探索性地提出了宁东能源化工基地产业布局规划的优化调整建议.     

Influence of interspecific competition on the recruitment behavior and liquid food transport in the tramp ant species Pheidole megacephala

This study was conducted on the reactions of Pheidole megacephala scouts when finding liquid food sources situated on territories marked by competing dominant ant species or on unmarked, control areas to see if the number of recruited nestmates is affected and if soldiers behave in ways adapted to the situation. We show that scouts recruit more nestmates, particularly soldiers, on marked rather than on unmarked areas. This recruitment allows P. megacephala to organize the defence and rapid depletion of these food sources prior to any contact with competitors. Soldiers can carry liquid foods both (1) in their crops like other Myrmicinae and (2), in a new finding concerning myrmicine ants, under their heads and thoraxes like certain poneromorph genera because the droplets adhere through surface tension strengths. Later, the liquids stored in the crop are distributed to nestmates through regurgitations during trophallaxis and the external droplets are distributed through social buckets, or the mode of liquid food transfer common in poneromorphs. Their flexibility to use or not use the latter technique, based on the situation, corroborates other reports that Pheidole soldiers have a relatively large behavioral repertoire.     

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.     

A new test of random walks in heterogeneous environments

Environmental heterogeneities can change animal movement in two different manners. First, they can modify movement characteristics (move lengths or turning angles), in which case the movement remains of the diffusive kind. Second, they can bias displacement towards a particular direction in which case it becomes non-diffusive. We propose in this paper a simple method that only requires computing the mean length of a sample of trajectories in some bounded area to distinguish between these two kinds of movement. We show through simulations that the method allows to detect the presence of heterogeneities that orient animal movement. We apply it to experimental trajectories of Messor sancta ants engaged in corpse aggregation to show that their displacement is oriented at the contact of the formed corpse piles and that their trajectories become non-diffusive.     

Circadian consequences of social organization in the ant species<Emphasis Type="Italic"> Camponotus compressus</Emphasis>

The locomotor activity rhythm of different castes of the ant species Camponotus compressus was monitored individually under laboratory light/dark (LD) cycles, and under continuous darkness (DD). The colony of this ant species comprises two sexual castes, the queens and the males, and three worker castes, namely the major, media, and minor workers. The virgin males and virgin queens display rhythmic activity patterns, but the mated queens were arrhythmic while laying eggs, with the rhythmicity resuming soon after egg-laying. Under the LD regime, major workers showed nocturnal patterns, while about 75% of the media workers displayed nocturnal patterns and about 25% showed diurnal patterns. Under the DD regime, most major workers exhibited circadian rhythm of activity with a single steady state, whereas media workers displayed two types of activity patterns, with activity patterns changing after 6–9 days in DD (turn-arounds). The pre-turn-around of the ants that showed nocturnal activity patterns during LD entrainment was <24 h after release into DD, which then became >24 h, after 6–9 days. On the other hand, the pre-turn-around of those ants that exhibited diurnal patterns during LD entrainment was first >24 h after release into DD, and then became <24 h, after 6–9 days. The activity of the minor workers neither entrained to LD cycles nor showed any sign of free-run in DD. It appears that the circadian clocks of the ant species C. compressus are flexible, and may perhaps depend upon the tasks assigned to them in the colony.     

Mating behaviour in a slave-making ant, Rossomyrmex minuchae (Hymenoptera, Formicidae)

The mating behaviour of the ant Rossomyrmex minuchae, a rare, protected slave-making species in Spain, seems to be significantly affected by its particular life history and patchy habitat. The mating behaviour of the entire genus Rossomyrmex is virtually unknown. We present here the results of a 3-year study of mating behaviour in R. minuchae.Behavioural observations and limited nest excavations revealed that R. minuchae does not produce sexuals every year, the number of sexuals is low, and the sex ratio tends to be female biased. Females typically exhibit two distinct activity periods. The first, the mating period, takes place in early afternoon: the ants call near the natal nest, mate and then return to their nest. The second, the dispersal period takes place in late afternoon: the mated females exit their nest and fly in search of a new, non-parasitized Proformica longiseta host nest. Males are highly active during the mating period, but will remain inactive in the dispersal period even if experimentally presented with virgin females. It appears that females are monogamous, while males are polygamous. When males are late arriving at the female calling site, the females will frequently congregate presumably calling in chorus.The low reproductive efficiency exhibited by R. minuchae, coupled with the postulated low genetic variation in the population, as sisters may mate with the same male, could result in a low survival rate and risk of eventual extinction. The observed decrease in nest density we observed during the 2004 season may be indicative of such a process.