Dynamics and drivers of fungal communities in a multipartite ant-plant association.

BACKGROUND: Fungi and ants belong to the most important organisms in terrestrial ecosystems on Earth. In nutrient-poor niches of tropical rainforests, they have developed steady ecological relationships as a successful survival strategy. In tropical ant-plant mutualisms worldwide, where resident ants provide the host plants with defense and nutrients in exchange for shelter and food, fungi are regularly found in the ant nesting space, inhabiting ant-made dark-colored piles ("patches"). Unlike the extensively investigated fungus-growing insects, where the fungi serve as the primary food source, the purpose of this ant-fungi association is less clear. To decipher the roles of fungi in these structures within ant nests, it is crucial to first understand the dynamics and drivers that influence fungal patch communities during ant colony development. RESULTS: In this study, we investigated how the ant colony age and the ant-plant species affect the fungal community in the patches. As model we selected one of the most common mutualisms in the Tropics of America, the Azteca-Cecropia complex. By amplicon sequencing of the internal transcribed spacer 2 (ITS2) region, we analyzed the patch fungal communities of 93 Azteca spp. colonies inhabiting Cecropia spp. trees. Our study demonstrates that the fungal diversity in patches increases as the ant colony grows and that a change in the prevalent fungal taxa occurs between initial and established patches. In addition, the ant species significantly influences the composition of the fungal community in established ant colonies, rather than the host plant species. CONCLUSIONS: The fungal patch communities become more complex as the ant colony develops, due to an acquisition of fungi from the environment and a substrate diversification. Our results suggest a successional progression of the fungal communities in the patches during ant colony growth and place the ant colony as the main driver shaping such communities. The findings of this study demonstrate the unexpectedly complex nature of ant-plant mutualisms in tropical regions at a micro scale.

Collective search in ants: Movement determines footprints, and footprints influence movement.

Collectively searching animals might be expected to coordinate with their groupmates to cover ground more evenly or efficiently than uncoordinated groups. Communication can lead to coordination in many ways. Previous work in ants suggests that chemical 'footprints', left behind by individuals as they walk, might serve this function by modulating the movement patterns of following ants. Here, we test this hypothesis by considering the two predictions that, first, ants may turn away from sites with higher footprint concentrations (klinotaxis), or, second, that they may change their turning patterns depending on the presence of footprints (klinokinesis). We tracked 5 whole colonies of Temnothorax rugatulus ants in a large arena over 5h. We approximated the footprint concentration by summing ant visitations for each point in the arena and calculated the speed and local path straightness for each point of the ant trajectories. We counterintuitively find that ants walk slightly faster and straighter in areas with fewer footprints. This is partially explained by the effect that ants who start out from the nest walking straighter move on average further away from the nest, where there are naturally fewer footprints, leading to an apparent relationship between footprint density and straightness However, ants walk slightly faster and straighter off footprints even when controlling for this effect. We tested for klinotaxis by calculating the footprint concentrations perceived by the left and right antennae of ants and found no evidence for a turning-away (nor turning-towards) behavior. Instead, we found noticeable effects of environmental idiosyncrasies on the behavior of ants which are likely to overpower any reactions to pheromones. Our results indicate that search density around an ant colony is affected by several independent processes, including individual differences in movement pattern, local spatial heterogeneities, and ants' reactions to chemical footprints. The multitude of effects illustrates that non-communicative coordination, individual biases and interactions with the environment might have a greater impact on group search efficiency and exploratory movements than pheromone communication.

Ant evolution: Amber revelations of extinction, survival and recovery.

Ant fossils from the Cretaceous are rare but critical for understanding the early evolution of this incredibly successful group of animals. New amber fossils fill important gaps, revealing patterns of death, survival, and radiation around the end Cretaceous extinction.

Catch bond kinetics are instrumental to cohesion of fire ant rafts under load.

Dynamic networks composed of constituents that break and reform bonds reversibly are ubiquitous in nature owing to their modular architectures that enable functions like energy dissipation, self-healing, and even activity. While bond breaking depends only on the current configuration of attachment in these networks, reattachment depends also on the proximity of constituents. Therefore, dynamic networks composed of macroscale constituents (not benefited by the secondary interactions cohering analogous networks composed of molecular-scale constituents) must rely on primary bonds for cohesion and self-repair. Toward understanding how such macroscale networks might adaptively achieve this, we explore the uniaxial tensile response of 2D rafts composed of interlinked fire ants (S. invicta). Through experiments and discrete numerical modeling, we find that ant rafts adaptively stabilize their bonded ant-to-ant interactions in response to tensile strains, indicating catch bond dynamics. Consequently, low-strain rates that should theoretically induce creep mechanics of these rafts instead induce elastic-like response. Our results suggest that this force-stabilization delays dissolution of the rafts and improves toughness. Nevertheless, above 35[Formula: see text] strain low cohesion and stress localization cause nucleation and growth of voids whose coalescence patterns result from force-stabilization. These voids mitigate structural repair until initial raft densities are restored and ants can reconnect across defects. However mechanical recovery of ant rafts during cyclic loading suggests that-even upon reinstatement of initial densities-ants exhibit slower repair kinetics if they were recently loaded at faster strain rates. These results exemplify fire ants' status as active agents capable of memory-driven, stimuli-response for potential inspiration of adaptive structural materials.

Plant-ant interactions mediate herbivore-induced conspecific negative density dependence in a subtropical forest.

The early growth stage of plants is vital to community diversity and community regeneration. The Janzen-Connell hypothesis predicts that conspecific density dependence lowers the survival of conspecific seedlings by attracting specialist natural enemies, promoting the recruitment and performance of heterospecific neighbors. Recent work has underscored how this conspecific negative density dependence may be mediated by mutualists - such as how mycorrhizal fungi may mediate the accrual of host-specific pathogens beneath the crown of conspecific adult trees. Aboveground mutualist and enemy interactions exist as well, however, and may provide useful insight into density dependence that are as of yet unexplored. Using a long-term seedling demographic dataset in a subtropical forest plot in central China, we confirmed that conspecific neighborhoods had a significant negative effect on seedling survival in this subtropical forest. Furthermore, although we detected more leaf damage in species that were closely related to ants, we found that the presence of ants had significant positive effects on seedling survival. Beside this, we also found a negative effect of ant appearance on seedling growth which may reflect a trade-off between survival and growth. Overall, our findings suggested that ants and conspecific neighborhoods played important but inverse roles on seedling survival and growth. Our results suggest ants may mediate the influence of conspecific negative density dependence on seedling survival at community level.

Foraging behaviour of Pheidole latinoda: An impetus for employing a heuristic approach to address optimization challenges.

The primary goal of the binary model in this study was to understand the convergence pattern of the Pheidole latinoda ants. Forager and scout ants on the hunt for food use path integration. When they find a food source, they leave a trail pheromone to alert other nest mates. Every ant starts following that trail and reinforces it on their way back home. To investigate the ant convergence pattern, binary and ternary bridges of varying lengths are used. Each bridge is built in such a way that one end is connected to a food source whilst the other end is connected to the nest. The food source is surrounded by water-filled islands. The Pheidole latinoda ant's convergence pattern has been observed following the successful installation of a bridge near the ants' nest. This species took between 1 and 3 and 3-4 min to find the shortest possible path. Numerous studies looking for optimal solutions, such as those addressing the challenges of travelling salesmen, routing in communication networks, etc., may use this convergence or path optimization as their new starting point.

Trail pheromone identification in the ant Crematogaster scutellaris.

In this work, we identified the trail pheromone of the ant Crematogaster scutellaris. We combined gas chromatography-mass spectrometry analysis of extracts from the hind tibia, the location of the respective glands, with automated trail following assays. The study found tridecan-2-ol to be the strongest discriminator between hind tibia and other body part extracts. Tridecan-2-ol elicited trail-following behaviour at concentrations of 1 ng/µL. A separation of the enantiomers showed responses to (R)-tridecan-2-ol already at 0.001 ng/µL and only at a 1000-fold higher concentration for (S)-tridecan-2-ol, suggesting that only the R enantiomer is used by C. scutellaris in its natural environment. We also found strong behavioural responses to 2-dodecanol, a substance that was not detectable in the hind tibia extract of C. scutellaris, but which has been reported to be the trail pheromone of the related species C. castanea. We discuss the contribution of these results to the 'dissection and reconstruction' of strategies and mechanisms underlying the social organization of ants.

Impact of Aphis pomi-tending Formica rufa (Hymenoptera: Formicidae) on biological parameters of Hippodamia variegata (Coleoptera: Coccinellidae).

One of the key reasons for the poor performance of natural enemies of honeydew-producing insect pests is mutualism between ants and some aphid species. The findings demonstrated that red wood ant, Formica rufa Linnaeus (Hymenoptera: Formicidae) had a deleterious impact on different biological parameters of the lady beetle, Hippodamia variegata Goeze (Coleoptera: Coccinellidae). H. variegata laid far fewer eggs in ant-tended aphid colonies, laying nearly 2.5 times more eggs in ant absence. Ants antennated and bit the lady beetle eggs, resulting in significantly low egg hatching of 66 per cent over 85 per cent in ant absent treatments. The presence of ants significantly reduced the development of all larval instars. The highest reduction was found in the fourth larval instar (31.33% reduction), and the lowest in the first larval instar (20% reduction). Later larval instars were more aggressively attacked by ants than earlier instars. The first and second larval instars stopped their feeding and movement in response to ant aggression. The third and fourth larval instars modified their mobility, resulting in increased ant aggression towards them. Adult lady beetles were shown to be more vulnerable to ant attacks than larvae. However, H. variegata adults demonstrated counterattacks in the form of diverse defensive reaction behaviours in response to F. rufa aggression.

Temperature-driven homogenization of an ant community over 60 years in a montane ecosystem.

Identifying the mechanisms underlying the changes in the distribution of species is critical to accurately predict how species have responded and will respond to climate change. Here, we take advantage of a late-1950s study on ant assemblages in a canyon near Boulder, Colorado, USA, to understand how and why species distributions have changed over a 60-year period. Community composition changed over 60 years with increasing compositional similarity among ant assemblages. Community composition differed significantly between the periods, with aspect and tree cover influencing composition. Species that foraged in broader temperature ranges became more widespread over the 60-year period. Our work highlights that shifts in community composition and biotic homogenization can occur even in undisturbed areas without strong habitat degradation. We also show the power of pairing historical and contemporary data and encourage more mechanistic studies to predict species changes under climate change.

Different feeding preferences for macronutrients across seasons and sites indicate temporal and spatial nutrient limitation in the black bog ant.

How the resource use by consumers vary in different environments and time scales is one of the fundamental ecological questions. Replicated field studies are rare, however; so the extent to which nutrient use varies and why is uncertain. We studied an endangered tyrphobiotic species, the black bog ant (Formica picea), and its feeding preferences in temperate peatlands. We conducted a baiting experiment at three different sites with high nest densities, repeated over three years and three periods of growing season. Preferences for three main macronutrients (carbohydrates, proteins and lipids) were assessed. We hypothesised that if nutrient limitation plays a role, ants will have an increased need for proteins and lipids in early seasons when brood is raised, while carbohydrates use will increase in late seasons. We also expected that site identity would influence nutrient preferences, but not year. Our results supported the nutrient limitation hypothesis for proteins that were consumed more in the early season. In contrast, preference for carbohydrates was rather high and did not increase consistently through season. Although the occupancy of lipid baits was low overall, it increased at colder temperatures, in contrast to carbohydrate and protein baits. Nutrient preferences varied more among sites than years, with the lowest nutrient use observed in a diverse fen-meadow, consistent with the nutrient limitation hypothesis. Year affected ant abundance, but not bait occupancy. Our results suggest that black bog ants flexibly adapt their diet to environmental conditions and that an interplay between nutrient limitation and climate determines their feeding behaviour.

Unraveling the forces shaping foraging dynamics in harvester ant colonies: Recruitment efficiency and environmental variability.

The collective foraging behavior of ant colonies is a central focus in behavioral ecology. This paper enhances the classical model of foraging dynamics in harvester ant colonies by introducing a nonlinear recruitment rate and considering environmental variability. Initially, we analyze the existence and stability of steady states in the deterministic model. The results suggest that an increase in mean recruitment time can reduce the foraging threshold, leading to both forward and backward bifurcations. Furthermore, both average recruitment time and the interference intensity of recruiters impact the number of workers in each subgroup. Subsequently, we conduct an analysis of the long-term and transient dynamics of collective foraging in random environments, providing sufficient conditions for the colony to sustain foraging activity. The findings emphasize the scene-dependent impact of environmental stochasticity on foraging dynamics. When ant colonies deterministically cease foraging, environmental stochasticity may unexpectedly prolong the foraging state. Conversely, when colonies deterministically persist in foraging, environmental stochasticity may disrupt this continuity. Additionally, the effect of environmental stochasticity on foraging status varies with the initial worker size. Sizes near the boundary of the basin of attraction between non-foraging and foraging states exhibit greater sensitivity to environmental stochasticity, and sufficiently large stochasticity can impact foraging dynamics across a broader range of initial worker sizes. These findings underscore the intricate interplay between intrinsic factors (e.g., recruitment efficiency and interference intensity) and extrinsic factors (e.g., environmental stochasticity) in shaping the collective foraging dynamics of ant colonies.

Immune response in paper wasp workers: Task matters more than age.

Workers of social hymenopterans (ants, bees and wasps) display specific tasks depending on whether they are younger or older. The relative importance of behavior and age in modulating immune function has seldom been addressed. We compared the strength of encapsulation-melanization immune response (hereafter melanotic encapsulation) in paper wasps displaying age polyethism or experimentally prevented from behavioral specialization. Foragers of Polybia paulista had higher melanotic encapsulation than guards, regardless of their age. Nevertheless, melanotic encapsulation decreased with age when wasps were prevented from behavioral specialization. Thus, in this species, worker melanotic encapsulation seems more sensitive to task than age. Foraging is considered one of the riskier behaviors in terms of pathogen exposure, so upregulating melanotic encapsulation in foragers can possibly improve both individual and colony-level resistance against infections.

Prolonged faunal turnover in earliest ants revealed by North American Cretaceous amber.

All ∼14,000 extant ant species descended from the same common ancestor, which lived ∼140-120 million years ago (Ma).1,2 While modern ants began to diversify in the Cretaceous, recent fossil evidence has demonstrated that older lineages concomitantly occupied the same ancient ecosystems.3 These early-diverging ant lineages, or stem ants, left no modern descendants; however, they dominated the fossil record throughout the Cretaceous until their ultimate extinction sometime around the K-Pg boundary. Even as stem ant lineages appear to be diverse and abundant throughout the Cretaceous, the extent of their longevity in the fossil record and circumstances contributing to their extinction remain unknown.3 Here we report the youngest stem ants, preserved in ∼77 Ma Cretaceous amber from North Carolina, which illustrate unexpected morphological stability and lineage persistence in this enigmatic group, rivaling the longevity of contemporary ants. Through phylogenetic reconstruction and morphometric analyses, we find evidence that total taxic turnover in ants was not accompanied by a fundamental morphological shift, in contrast to other analogous stem extinctions such as theropod dinosaurs. While stem taxa showed broad morphological variation, high-density ant morphospace remained relatively constant through the last 100 million years, detailing a parallel, but temporally staggered, evolutionary history of modern and stem ants.

Effects of macro- and micro-nutrients on momentary and season-long feeding responses by select species of ants.

Few studies have investigated the relative contribution of specific nutrients to momentary and season-long foraging responses by ants. Using western carpenter ants, Camponotus modoc, and European fire ants, Myrmica rubra, as model species, we: (1) tested preferential consumption of various macro- and micro-nutrients; (2) compared consumption of preferred macro-nutrients; (3) investigated seasonal shifts (late May to mid-September) in nutrient preferences; and (4) tested whether nutrient preferences of C. modoc and M. rubra pertain to black garden ants, Lasius niger, and thatching ants, Formica aserva. In laboratory and field experiments, we measured nutrient consumption by weighing Eppendorf tubes containing aqueous nutrient solutions before and after feeding by ants. Laboratory colonies of C. modoc favored nitrogenous urea and essential amino acids (EAAs), whereas M. rubra colonies favored sucrose. Field colonies of C. modoc and M. rubra preferentially consumed EAAs and sucrose, respectively, with no sustained shift in preferred macro-nutrient over the course of the foraging season. The presence of a less preferred macro-nutrient in a nutrient blend did not diminish the blend's 'appeal' to foraging ants. Sucrose and EAAs singly and in combination were equally consumed by L. niger, whereas F. aserva preferred EAAs. Baits containing both sucrose and EAAs were consistently consumed by the ants studied in this project and should be considered for pest ant control.

Interspecific insect relationships on Terminalia argentea (Myrtales: Combretaceae) trees in the Cerrado biome.

Terminalia argentea Mart. (Combretaceae), native to Brazil, is used in habitat restoration programs. Arthropods are bioindicators because their populations reflect changes in the environment. We evaluated the recovery of a degraded area by using ecological indices and analyzing arthropod interactions on T. argentea plants. The richness and diversity of sap-sucking Hemiptera and the abundance of tending ants and Sternorrhyncha predators increased with the number of T. argentea leaves. The correlation of the abundance of tending ants and Sternorrhyncha predators was positive with that of the sap-sucking Hemiptera, and the abundance of Sternorrhyncha predators was negative with that of tending ants and sap-sucking Hemiptera. The positive correlation between the abundance, richness, and diversity of insect groups and numbers of T. argentea leaves is an example of the bottom-up regulation mechanism, with the population dynamics of the lower trophic levels dictating those of higher trophic levels. The contribution of T. argentea, a host plant of many arthropods, to the recovery of ecological relationships between organisms in degraded ecosystems is important.

Fungal infection alters collective nutritional intake of ant colonies.

In animals, parasitic infections impose significant fitness costs.1,2,3,4,5,6 Infected animals can alter their feeding behavior to resist infection,7,8,9,10,11,12 but parasites can manipulate animal foraging behavior to their own benefits.13,14,15,16 How nutrition influences host-parasite interactions is not well understood, as studies have mainly focused on the host and less on the parasite.9,12,17,18,19,20,21,22,23 We used the nutritional geometry framework24 to investigate the role of amino acids (AA) and carbohydrates (C) in a host-parasite system: the Argentine ant, Linepithema humile, and the entomopathogenic fungus, Metarhizium brunneum. First, using 18 diets varying in AA:C composition, we established that the fungus performed best on the high-amino-acid diet 1:4. Second, we found that the fungus reached this optimal diet when given various diet pairings, revealing its ability to cope with nutritional challenges. Third, we showed that the optimal fungal diet reduced the lifespan of healthy ants when compared with a high-carbohydrate diet but had no effect on infected ants. Fourth, we revealed that infected ant colonies, given a choice between the optimal fungal diet and a high-carbohydrate diet, chose the optimal fungal diet, whereas healthy colonies avoided it. Lastly, by disentangling fungal infection from host immune response, we demonstrated that infected ants foraged on the optimal fungal diet in response to immune activation and not as a result of parasite manipulation. Therefore, we revealed that infected ant colonies chose a diet that is costly for survival in the long term but beneficial in the short term-a form of collective self-medication.

Understanding the ant's unique biting system can improve surgical needle holders.

Mechanical grasping and holding devices depend upon a firm and controlled grip. The possibility to improve this gripping performance is severely limited by the need for miniaturization in many applications, such as robotics, microassembly, or surgery. In this paper, we show how this gripping can be improved in one application (the endoscopic needle holder) by understanding and imitating the design principles that evolution has selected to make the mandibles of an ant a powerful natural gripping device. State-of-the-art kinematic, morphological, and engineering approaches show that the ant, in contrast to other insects, has considerable movement within the articulation and the jaw´s rotational axis. We derived three major evolutionary design principles from the ant's biting apparatus: 1) a mobile joint axis, 2) a tilted orientation of the mandibular axis, and 3) force transmission of the adductor muscle to the tip of the mandible. Application of these three principles to a commercially available endoscopic needle holder resulted in calculated force amplification up to 296% and an experimentally measured one up to 433%. This reduced the amount of translations and rotations of the needle, compared to the needle's original design, while retaining its size or outer shape. This study serves as just one example showing how bioengineers might find elegant solutions to their design problems by closely observing the natural world.

Importance of magnetic information for neuronal plasticity in desert ants.

Many animal species rely on the Earth's magnetic field during navigation, but where in the brain magnetic information is processed is still unknown. To unravel this, we manipulated the natural magnetic field at the nest entrance of Cataglyphis desert ants and investigated how this affects relevant brain regions during early compass calibration. We found that manipulating the Earth's magnetic field has profound effects on neuronal plasticity in two sensory integration centers. Magnetic field manipulations interfere with a typical look-back behavior during learning walks of naive ants. Most importantly, structural analyses in the ants' neuronal compass (central complex) and memory centers (mushroom bodies) demonstrate that magnetic information affects neuronal plasticity during early visual learning. This suggests that magnetic information does not only serve as a compass cue for navigation but also as a global reference system crucial for spatial memory formation. We propose a neural circuit for integration of magnetic information into visual guidance networks in the ant brain. Taken together, our results provide an insight into the neural substrate for magnetic navigation in insects.

Daniel Kronauer.

Daniel Kronauer explores the behavioral genetics and neurobiology of ants, tracing their evolution from solitary ancestors to supremely social insects. In this interview with Neuron, he discusses his lab's efforts to develop a new ant model species and describes how his passion for natural history inspires his research.

Effect of Solenopsis invicta virus 3 on brood mortality and egg hatch in Solenopsis invicta.

Solenopsis invicta virus 3 (SINV-3) has been shown to cause significant mortality among all stages of its host, Solenopsis invicta. One impact of the virus is alteration of worker ant foraging behavior, which results in colony starvation and collapse over time. Additionally, it has been hypothesized that SINV-3 infection of S. invicta may disrupt worker ant brood care behavior. To investigate this possibility, various combinations of SINV-3-infected and -uninfected adult (worker) and immature (brood) stages were placed together and monitored using the response variables, mortality, egg hatch, and virus load. While significant differences in percent cumulative S. invicta worker ant mortality among six combinations of SINV-3-infected and -uninfected stages were observed, no significant differences in percent cumulative mortality of S. invicta larvae or pupae were observed. No significant differences in egg hatch were observed among SINV-3-uninfected, SINV-3-infected (colony-treated and queen-treated), and starved colonies. Eggs hatched normally in 10-12 days for all treatments indicating that egg care by worker ants was unaffected by SINV-3 infection status. The study further clarifies SINV-3 pathogenesis in its host, S. invicta. Larval mortality in SINV-3-infected colonies does not appear to be caused by worker ant neglect. S. invicta brood under the care of SINV-3-infected worker ants did not exhibit higher mortality rates compared with those tended by SINV-3-uninfected worker ants.