Immune defense in leaf-cutting ants: a cross-fostering approach

To ameliorate the impact of disease, social insects combine individual innate immune defenses with collective social defenses. This implies that there are different levels of selection acting on investment in immunity, each with their own trade-offs. We present the results of a cross-fostering experiment designed to address the influences of genotype and social rearing environment upon individual and social immune defenses. We used a multiply mating leaf-cutting ant, enabling us to test for patriline effects within a colony, as well as cross-colony matriline effects. The worker's father influenced both individual innate immunity (constitutive antibacterial activity) and the size of the metapleural gland, which secretes antimicrobial compounds and functions in individual and social defense, indicating multiple mating could have important consequences for both defense types. However, the primarily social defense, a Pseudonocardia bacteria that helps to control pathogens in the ants' fungus garden, showed a significant colony of origin by rearing environment interaction, whereby ants that acquired the bacteria of a foster colony obtained a less abundant cover of bacteria: one explanation for this pattern would be co-adaptation between host colonies and their vertically transmitted mutualist. These results illustrate the complexity of the selection pressures that affect the expression of multilevel immune defenses.     

Dynamic Wolbachia prevalence in Acromyrmex leaf-cutting ants: potential for a nutritional symbiosis

Wolbachia are renowned as reproductive parasites, but their phenotypic effects in eusocial insects are not well understood. We used a combination of qrt-PCR, fluorescence in situ hybridization and laser scanning confocal microscopy to evaluate the dynamics of Wolbachia infections in the leaf-cutting ant Acromyrmex octospinosus across developmental stages of sterile workers. We confirm that workers are infected with one or two widespread wsp genotypes of Wolbachia, show that colony prevalence is always 100% and characterize two rare recombinant genotypes. One dominant genotype is always present and most abundant, whereas another only proliferates in adult workers of some colonies and is barely detectable in larvae and pupae. An explanation may be that Wolbachia genotypes compete for host resources in immature stages while adult tissues provide substantially more niche space. Tissue-specific prevalence of the two genotypes differs, with the rarer genotype being over-represented in the adult foregut and thorax muscles. Both genotypes occur extracellularly in the foregut, suggesting an unknown mutualistic function in worker ant nutrition. Both genotypes are also abundant in the faecal fluid of the ants, suggesting that they may have extended functional phenotypes in the fungus garden that the ants manure with their own faeces.     

Trade-offs in group living: transmission and disease resistance in leaf-cutting ants

Sociality can be associated with significant costs due to the increased risk of disease transmission. However, in some organisms the costs may be offset by benefits due to improvements in defences against parasites. To examine this possible trade-off between infection risk and disease resistance, we used Acromyrmex leaf-cutting ants and the entomopathogenic fungus Metarhizium anisopliae as the model system. Ants exposed to the parasite were found to have substantially improved survival when they were kept with nest-mates, while the cost of being in a group in terms of increased disease transmission was very low. The efficiency of transmission is described by the transmission parameter, which decreased with increasing host density showing that transmission rates are inversely density dependent. Both grooming and antibiotic secretions appeared to be important in resistance against the parasite, with the defences of small workers being particularly effective. The results indicate that leaf-cutting ant colonies may have much greater resistance to disease than would be predicted from the high densities of host individuals within them. Unlike most organisms, group living in these ants may actually be associated with a net benefit in terms of disease dynamics.     

Quality control by leaf-cutting ants: evidence from communities of endophytic fungi in foraged and rejected vegetation

Leaf-cutting ants of the genera Acromyrmex and Atta forage vegetation for incorporation into their mutualistic fungal gardens. However, the presence of certain endophytic fungi in this predominantly leaf-based material could affect the fungal garden and thus the choice of material by the ants. The present study was conducted to document the endophytic fungal communities occurring in the vegetation being transported by workers of Atta laevigata into their nests and to compare this community structure with that of the vegetative material subsequently rejected from the nests. We found considerable diversity in the fungi isolated. Acremonium, Cylindrocladium, Drechslera, Epicoccum, Fusarium, Trichoderma, Ulocladium and two unidentified morphospecies were significantly more common in rejected compared with foraged material, and some of these genera include mycoparasites, which could represent a threat to the fungal gardens. Conversely, Colletotrichum, Pestalotiopsis, Phomopsis, Xylaria and an unidentified morphospecies were more common in carried compared with rejected material. The possibility that ants have a ‘quality-control’ mechanism based on the presence of antagonistic fungal endophytes is discussed, as is the potential use of these fungi as biocontrol agents against Attini pests.     

Nonequilibrium dynamics of social groups: insights from foraging Argentine ants

Summary We studied disturbance patterns in groups of feeding Argentine ants, Linepithema humile. All disturbances were caused by the ants themselves, without application of exogenous disturbances. The overall pattern, which consisted of a power law distribution of disturbance avalanche sizes, each of which was initiated by a single wandering ant, is similar to patterns characteristic of self-organized critical systems. In addition, we observed variation among individuals in response to disturbance according to their level of satiation. Ants with distended gasters (indicative of volume of food uptake) resumed feeding less rapidly than their thinner counterparts, and were more likely to leave food sources altogether. Although these disturbances reduce food collection because feeding ants are interrupted, they are minimal and may enable ant groups to balance collectively the advantage of rapid alarm communication with the costs of interrupted foraging from trivial disturbances.Received 18 September 2003; revised 21 November 2003; accepted 4 December 2003.     

High surface temperatures select for individual foraging in ants

Natural selection favors signals, receptors, and signaling behaviorthat maximize the received signal relative to background noiseand that minimize signal degradation. The physical propertiesof the environment affect rates of attenuation and degradationof the signal, and thus temperature may influence the evolutionand maintenance of volatile chemical signals. We tested this hypothesis in ants, where nest mate recruitment to a food sourceby laying trail pheromones on a surface is a common phenomenon.We collected data on maximal soil surface temperatures duringthe ants' activity and mode of foraging (recruitment or solitary).By using two different comparative methodologies, we demonstrateda relationship between maximal soil temperature at which speciesare active and recruitment behavior (which is hypothesized to be related to the presence or absence of chemical signals).The species that were active at lower temperatures proved tobe those that used chemical signals to recruit nest mates duringforaging. This is also the case when comparing sympatric speciesand thereby controlling for other environmental factors. Moreover,all seven nonrecruiter species developed from recruiter ancestries,which is consistent with our hypothesis because ample evidence suggests a forest and tropical origin for ants. Thus, contraryto previous hypotheses, species that forage individually cannotbe categorically considered primitive, but rather appear tobe derived from recruiter species. Therefore, we conclude thattemperature influences the evolution and/or stability of chemicalsignals in ants by determining the recruitment of nest mates.     

A general rule for the dependence of developmental rate on temperature in ectothermic animals

In animals that do not regulate their body temperature by the production of heat, the proportion of the total developmental time spent in a particular developmental stage does not change with temperature. In the quasi-linear region of the relationship between developmental rate and temperature, all of the developmental stages appear to have the same species-specific lower developmental threshold. This trait, which is called developmental isomorphy, constrains developmental adaptations of ectotherms to their environments and facilitates the precise timing of life-history events.     

Fragmentation genetics of rainforest animals: insights from recent studies

Habitat fragmentation is one of the most prominent effects of anthropogenic ecosystem degradation. However, despite the accumulating evidence that anthropogenic habitat fragmentation acts negatively on the dynamics and viability of many species, rainforest fragmentation can occur naturally. The need to disentangle ‘natural’ fragmentation processes from (often) very recent anthropogenic effects poses a methodological challenge in the field of conservation genetics. Additional challenges include sampling schemes that can generate false signals of population size changes or population genetic structure. Finally, limited analytical power often results from restricted sample sizes, numbers of markers, or their informativeness. We reviewed the available literature on the effects of habitat fragmentation in non-aquatic tropical animal species over the last 10 years to ask what has been learned as a result of the increasing attention paid to these methodological issues. Fifty-four studies contained relevant datasets on the question of fragmentation effects in 74 animal species. Primates (n = 18) and passerine birds (n = 17) contributed most species to the survey. Unambiguous signals of fragmentation effects were reported in 33.8 % of species, whereas the remaining species showed either equivocal (36.5 %) or no evidence (29.7 %) of fragmentation effects. Our review further reveals that uneven sampling cannot be ruled out as possible explanation for many of the reported genetic bottleneck signals and genetic structure effects. Based on the reviewed evidence, methodological (e.g. improving sampling schemes, multiple analytical approaches, added value of different markers) and conceptual recommendations offering a better understanding of general and species-specific evolutionary responses to fragmentation are formulated for future studies.     

Functional role of phenylacetic acid from metapleural gland secretions in controlling fungal pathogens in evolutionarily derived leaf-cutting ants

Fungus-farming ant colonies vary four to five orders of magnitude in size. They employ compounds from actinomycete bacteria and exocrine glands as antimicrobial agents. Atta colonies have millions of ants and are particularly relevant for understanding hygienic strategies as they have abandoned their ancestors'' prime dependence on antibiotic-based biological control in favour of using metapleural gland (MG) chemical secretions. Atta MGs are unique in synthesizing large quantities of phenylacetic acid (PAA), a known but little investigated antimicrobial agent. We show that particularly the smallest workers greatly reduce germination rates of Escovopsis and Metarhizium spores after actively applying PAA to experimental infection targets in garden fragments and transferring the spores to the ants'' infrabuccal cavities. In vitro assays further indicated that Escovopsis strains isolated from evolutionarily derived leaf-cutting ants are less sensitive to PAA than strains from phylogenetically more basal fungus-farming ants, consistent with the dynamics of an evolutionary arms race between virulence and control for Escovopsis, but not Metarhizium. Atta ants form larger colonies with more extreme caste differentiation relative to other attines, in societies characterized by an almost complete absence of reproductive conflicts. We hypothesize that these changes are associated with unique evolutionary innovations in chemical pest management that appear robust against selection pressure for resistance by specialized mycopathogens.     

Foraging behaviour of Atta cephalotes (leaf-cutting ants): an examination of two predictions for load selection

Two mechanisms have been proposed to explain how colony-level foraging performance of leaf-cutting ants can be maximized when workers harvest leaf fragments of a size that does not maximize their individual performance. Each mechanism predicts that ants will adjust the size of leaf fragments between starting a foraging bout and establishing full traffic between the nest and foraging site, but the two models predict shifts in opposite directions. I examined fragment sizes at the start of daily foraging in five field colonies of Atta cephalotes in Costa Rica and detected an obvious shift in only one case. More shifts were detected when the small and large ends of the worker body size range were considered separately, but the direction was inconsistent among colonies. I also examined the role of returning laden workers in recruitment of nestmates by intercepting all laden workers for the first 2 h of foraging, and measuring the effect on the arrival of recruits at the foraging site. In two cases, the flow of recruits was not diminished by the interception of returning workers. The results suggest that neither mechanism correctly and consistently accounts for load size selection by leaf-cutting ants. Copyright 2000 The Association for the Study of Animal Behaviour.     

Virus-host interactions: new insights from the small RNA world

RNA silencing has a known role in the antiviral responses of plants and insects. Recent evidence, including the finding that the Tat protein of human immunodeficiency virus (HIV) can suppress the host's RNA-silencing pathway and may thus counteract host antiviral RNAs, suggests that RNA-silencing pathways could also have key roles in mammalian virus-host interactions.     

Global offtake of wild animals from wetlands: critical issues for fish and birds

Hydrobiologia - The global offtake of wild animals is valued at US$400 billion annually and supports the livelihoods of 15% of the global population. Wetlands are amongst the most important...     

Economic damage level for leaf-cutting ants in function of the productivity index of eucalyptus plantations in an Atlantic Forest region

The production and quality of eucalyptus plantations have been studied in areas with different densities of ant nests, being important to estimate losses caused by leaf-cutting ants. The effects of leaf-cutting ant on wood production in differents productivity sites were studied in eucalyptus plantations in the region of Atlantic Forest, Minas Gerais State, Brazil from 2003 to 2006. Data of plots of the continuous forest inventory and data of leaf-cutting ant monitoring in eucalyptus plantations were obtained. Each unitary increment in the area of Atta spp. nests per hectare reduced the wood production of the eucalyptus forest between 0.04 and 0.13 m3.ha(-1), resulting in a level of economic damage for leaf-cutting ants between 13.4 and 39.2 m2.ha(-1), in this region. Moreover, this study innovated when using indices of forest productivity (site index) that promote better adjustment of the models and produce estimate more accurate of the level of economic damage for leaf-cutting ants in cultivated forests, allowing to conclude that the increase of the total area of ant nests reduces the wooden volume of eucalyptus, proportionally to the productive potential of the forest.     

Considerations in the selection and conditioning of Old World monkeys for laboratory research: animals from domestic sources

Nonhuman primates from domestic sources constitute an important resource for the research community. The life history of the Old World monkey species that comprise the bulk of this resource is described, and issues that colony managers and researchers alike should consider regarding animal selection (e.g., species, age, sex, rearing history, temperament, genotype, viral status, geographic origin) are discussed. Preparation of domestically bred animals for research usually involves some combination of social separation, relocation, resocialization, alterations in physical space, photoperiod, and diet, as well as exposure to novel environments. The research literature that has focused on these issues is reviewed, and authors suggest that once animals have been assigned to their project housing situation, a period ranging up to 3 mo (depending on the magnitude of the change in housing) might be warranted before an experimental protocol should begin. Attention to issues of animal selection and conditioning by both researchers and colony managers can lead to the shared goal of high-quality research that utilizes the minimal number of animals.     

Acromyrmex ameliae sp. n. （Hymenoptera： Formicidae）： A new social parasite of leaf-cutting ants in Brazil

The fungus-growing ants （Tribe Attini） are a New World group of〉 200 species, all obligate symbionts with a fungus they use for food. Four attine taxa are known to be social parasites of other attines. Acromyrmex （ Pseudoatta） argentina argentina and Acromyrmex （Pseudoatta） argentina platensis （parasites of Acromyrmex lundi）, and Acromyrmex sp. （a parasite of Acromyrmex rugosus） produce no worker caste. In contrast, the recently discovered Acromyrmex insinuator （a parasite of Acromyrmex echinatior） does produce workers. Here, we describe a new species, Acromyrmex ameliae, a social parasite of Acromyrmex subterraneus subterraneus and Acromyrmex subterraneus brunneus in Minas Gerais, Brasil. Like A. insinuator, it produces workers and appears to be closely related to its hosts. Similar social parasites may be fairly common in the fungus-growing ants, but overlooked due to the close resemblance between parasite and host workers.