Detouring while foraging up a tree: What bull ants (Myrmecia midas) learn and their reactions to novel sensory cues.

Many animals navigate in a structurally complex environment, which requires them to detour around the physical barriers that they encounter. Although many studies in animal cognition suggest that they are able to adeptly avoid obstacles, it is unclear whether a new route is learned to navigate around these barriers and, if so, what sensory information may be used to do so. We investigated detour learning in traveling up a tree in the Australian bull ant, Myrmecia midas, which primarily uses visual landmarks. We first placed a barrier on the ants' upward path. Initially, 46% of foragers were unsuccessful in detouring the obstacle. On subsequent trips, the ants became more successful and established a new route. We observed up to eight successful foraging trips detouring around the barrier. We then tested the same foragers in a series of manipulations, including changing the position of the barrier, making a new gap in the middle of the obstacle, or removing the barrier altogether. The ants mostly showed the same learned motor routine, detouring with a similar path as in the initial trials, suggesting that foragers were not relying on barrier cues and therefore learned a new route around the obstacle. When foragers encountered new olfactory or tactile cues, or the visual environment was blocked; however, their navigation was profoundly disrupted. These results suggest that changing sensory information drastically affects the foragers' navigational performance. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

Minding the gap: learning and visual scanning behaviour in nocturnal bull ants.

Insects possess small brains but exhibit sophisticated behaviour, specifically their ability to learn to navigate within complex environments. To understand how they learn to navigate in a cluttered environment, we focused on learning and visual scanning behaviour in the Australian nocturnal bull ant, Myrmecia midas, which are exceptional visual navigators. We tested how individual ants learn to detour via a gap and how they cope with substantial spatial changes over trips. Homing M. midas ants encountered a barrier on their foraging route and had to find a 50 cm gap between symmetrical large black screens, at 1 m distance towards the nest direction from the centre of the releasing platform in both familiar (on-route) and semi-familiar (off-route) environments. Foragers were tested for up to 3 learning trips with the changed conditions in both environments. The results showed that on the familiar route, individual foragers learned the gap quickly compared with when they were tested in the semi-familiar environment. When the route was less familiar, and the panorama was changed, foragers were less successful at finding the gap and performed more scans on their way home. Scene familiarity thus played a significant role in visual scanning behaviour. In both on-route and off-route environments, panoramic changes significantly affected learning, initial orientation and scanning behaviour. Nevertheless, over a few trips, success at gap finding increased, visual scans were reduced, the paths became straighter, and individuals took less time to reach the goal.

Vertical Lobes of the Mushroom Bodies Are Essential for View-Based Navigation in Australian Myrmecia Ants.

Prior to leaving home, insects acquire visual landmark information through a series of well-choreographed walks or flights of learning [1-4]. This information allows them to pinpoint goals both when in their vicinity [5-7] and from locations they have not previously visited [8-10]. It is presumed that animals returning home match memorized views to their current view for successful view-based navigation [11]. While view-based navigation strategies have been incorporated into several navigation models [8, 12, 13], we still know little about how this behavior is performed by the insect brain. Mushroom bodies are essential for visual learning and memory [14-16], and therefore we investigated their role in view-based navigation in a visually oriented ant, Myrmecia midas. We injected the local anesthetic procaine [15, 17, 18] into the mushroom body vertical lobes (VLs) to selectively inhibit neural activity in this region. We compared the behavior of VL-procaine-treated ants with three groups: untreated control, VL-saline, and off-target (antennal lobe) procaine. Experienced foragers were collected, treated, and released in their familiar environment where we documented their behavior. Animals with procaine-inactivated VLs had tortuous paths and were unable to find their nest, whereas ants from the untreated and off-target procaine groups were well directed and were the most successful at returning home. Untreated animals walked faster when their gaze was directed toward home, and this behavior was eliminated by anesthetizing the VL region. Our data provide neurobiological evidence that the mushroom body vertical lobes are necessary for retrieving visual memories for successful view-based navigation.

Social Complexity and Brain Evolution: Comparative Analysis of Modularity and Integration in Ant Brain Organization.

The behavioral demands of living in social groups have been linked to the evolution of brain size and structure, but how social organization shapes investment and connectivity within and among functionally specialized brain regions remains unclear. To understand the influence of sociality on brain evolution in ants, a premier clade of eusocial insects, we statistically analyzed patterns of brain region size covariation as a proxy for brain region connectivity. We investigated brain structure covariance in young and old workers of two formicine ants, the Australasian weaver ant Oecophylla smaragdina, a pinnacle of social complexity in insects, and its socially basic sister clade Formica subsericea. As previously identified in other ant species, we predicted that our analysis would recognize in both species an olfaction-related brain module underpinning social information processing in the brain, and a second neuroanatomical cluster involved in nonolfactory sensorimotor processes, thus reflecting conservation of compartmental connectivity. Furthermore, we hypothesized that covariance patterns would reflect divergence in social organization and life histories either within this species pair or compared to other ant species. Contrary to our predictions, our covariance analyses revealed a weakly defined visual, rather than olfactory, sensory processing cluster in both species. This pattern may be linked to the reliance on vision for worker behavioral performance outside of the nest and the correlated expansion of the optic lobes to meet navigational demands in both species. Additionally, we found that colony size and social organization, key measures of social complexity, were only weakly correlated with brain modularity in these formicine ants. Worker age also contributed to variance in brain organization, though in different ways in each species. These findings suggest that brain organization may be shaped by the divergent life histories of the two study species. We compare our findings with patterns of brain organization of other eusocial insects.

Differential investment in brain regions for a diurnal and nocturnal lifestyle in Australian Myrmecia ants.

Animals are active at different times of the day. Each temporal niche offers a unique light environment, which affects the quality of the available visual information. To access reliable visual signals in dim-light environments, insects have evolved several visual adaptations to enhance their optical sensitivity. The extent to which these adaptations reflect on the sensory processing and integration capabilities within the brain of a nocturnal insect is unknown. To address this, we analyzed brain organization in congeneric species of the Australian bull ant, Myrmecia, that rely predominantly on visual information and range from being strictly diurnal to strictly nocturnal. Weighing brains and optic lobes of seven Myrmecia species, showed that after controlling for body mass, the brain mass was not significantly different between diurnal and nocturnal ants. However, the optic lobe mass, after controlling for central brain mass, differed between day- and night-active ants. Detailed volumetric analyses showed that the nocturnal ants invested relatively less in the primary visual processing regions but relatively more in both the primary olfactory processing regions and in the integration centers of visual and olfactory sensory information. We discuss how the temporal niche occupied by each species may affect cognitive demands, thus shaping brain organization among insects active in dim-light conditions.

Origins of Aminergic Regulation of Behavior in Complex Insect Social Systems.

Neuromodulators are conserved across insect taxa, but how biogenic amines and their receptors in ancestral solitary forms have been co-opted to control behaviors in derived socially complex species is largely unknown. Here we explore patterns associated with the functions of octopamine (OA), serotonin (5-HT) and dopamine (DA) in solitary ancestral insects and their derived functions in eusocial ants, bees, wasps and termites. Synthesizing current findings that reveal potential ancestral roles of monoamines in insects, we identify physiological processes and conserved behaviors under aminergic control, consider how biogenic amines may have evolved to modulate complex social behavior, and present focal research areas that warrant further study.

Moving in Dim Light: Behavioral and Visual Adaptations in Nocturnal Ants.

Visual navigation is a benchmark information processing task that can be used to identify the consequence of being active in dim-light environments. Visual navigational information that animals use during the day includes celestial cues such as the sun or the pattern of polarized skylight and terrestrial cues such as the entire panorama, canopy pattern, or significant salient features in the landscape. At night, some of these navigational cues are either unavailable or are significantly dimmer or less conspicuous than during the day. Even under these circumstances, animals navigate between locations of importance. Ants are a tractable system for studying navigation during day and night because the fine scale movement of individual animals can be recorded in high spatial and temporal detail. Ant species range from being strictly diurnal, crepuscular, and nocturnal. In addition, a number of species have the ability to change from a day- to a night-active lifestyle owing to environmental demands. Ants also offer an opportunity to identify the evolution of sensory structures for discrete temporal niches not only between species but also within a single species. Their unique caste system with an exclusive pedestrian mode of locomotion in workers and an exclusive life on the wing in males allows us to disentangle sensory adaptations that cater for different lifestyles. In this article, we review the visual navigational abilities of nocturnal ants and identify the optical and physiological adaptations they have evolved for being efficient visual navigators in dim-light.

Worker brain development and colony organization in ants: Does division of labor influence neuroplasticity?

Brain compartment size allometries may adaptively reflect cognitive needs associated with behavioral development and ecology. Ants provide an informative system to study the relationship of neural architecture and development because worker tasks and sensory inputs may change with age. Additionally, tasks may be divided among morphologically and behaviorally differentiated worker groups (subcastes), reducing repertoire size through specialization and aligning brain structure with task-specific cognitive requirements. We hypothesized that division of labor may decrease developmental neuroplasticity in workers due to the apparently limited behavioral flexibility associated with task specialization. To test this hypothesis, we compared macroscopic and cellular neuroanatomy in two ant sister clades with striking contrasts in worker morphological differentiation and colony-level social organization: Oecophylla smaragdina, a socially complex species with large colonies and behaviorally distinct dimorphic workers, and Formica subsericea, a socially basic species with small colonies containing monomorphic workers. We quantified volumes of functionally distinct brain compartments in newly eclosed and mature workers and measured the effects of visual experience on synaptic complex (microglomeruli) organization in the mushroom bodies-regions of higher-order sensory integration-to determine the extent of experience-dependent neuroplasticity. We demonstrate that, contrary to our hypothesis, O. smaragdina workers have significant age-related volume increases and synaptic reorganization in the mushroom bodies, whereas F. subsericea workers have reduced age-related neuroplasticity. We also found no visual experience-dependent synaptic reorganization in either species. Our findings thus suggest that changes in the mushroom body with age are associated with division of labor, and therefore social complexity, in ants. © 2017 Wiley Periodicals, Inc. Develop Neurobiol 77: 1072-1085, 2017.

Social complexity influences brain investment and neural operation costs in ants.

The metabolic expense of producing and operating neural tissue required for adaptive behaviour is considered a significant selective force in brain evolution. In primates, brain size correlates positively with group size, presumably owing to the greater cognitive demands of complex social relationships in large societies. Social complexity in eusocial insects is also associated with large groups, as well as collective intelligence and division of labour among sterile workers. However, superorganism phenotypes may lower cognitive demands on behaviourally specialized workers resulting in selection for decreased brain size and/or energetic costs of brain metabolism. To test this hypothesis, we compared brain investment patterns and cytochrome oxidase (COX) activity, a proxy for ATP usage, in two ant species contrasting in social organization. Socially complex Oecophylla smaragdina workers had larger brain size and relative investment in the mushroom bodies (MBs)-higher order sensory processing compartments-than the more socially basic Formica subsericea workers. Oecophylla smaragdina workers, however, had reduced COX activity in the MBs. Our results suggest that as in primates, ant group size is associated with large brain size. The elevated costs of investment in metabolically expensive brain tissue in the socially complex O. smaragdina, however, appear to be offset by decreased energetic costs.

Lifespan behavioural and neural resilience in a social insect.

Analyses of senescence in social species are important to understanding how group living influences the evolution of ageing in society members. Social insects exhibit remarkable lifespan polyphenisms and division of labour, presenting excellent opportunities to test hypotheses concerning ageing and behaviour. Senescence patterns in other taxa suggest that behavioural performance in ageing workers would decrease in association with declining brain functions. Using the ant Pheidole dentata as a model, we found that 120-day-old minor workers, having completed 86% of their laboratory lifespan, showed no decrease in sensorimotor functions underscoring complex tasks such as alloparenting and foraging. Collaterally, we found no age-associated increases in apoptosis in functionally specialized brain compartments or decreases in synaptic densities in the mushroom bodies, regions associated with integrative processing. Furthermore, brain titres of serotonin and dopamine--neuromodulators that could negatively impact behaviour through age-related declines--increased in old workers. Unimpaired task performance appears to be based on the maintenance of brain functions supporting olfaction and motor coordination independent of age. Our study is the first to comprehensively assess lifespan task performance and its neurobiological correlates and identify constancy in behavioural performance and the absence of significant age-related neural declines.

Polymorphism and division of labour in a socially complex ant: neuromodulation of aggression in the Australian weaver ant, Oecophylla smaragdina.

Complex social structure in eusocial insects can involve worker morphological and behavioural differentiation. Neuroanatomical variation may underscore worker division of labour, but the regulatory mechanisms of size-based task specialization in polymorphic species are unknown. The Australian weaver ant, Oecophylla smaragdina, exhibits worker polyphenism: larger major workers aggressively defend arboreal territories, whereas smaller minors nurse brood.Here, we demonstrate that octopamine (OA) modulates worker size-related aggression in O. smaragdina. We found that the brains of majors had significantly higher titres of OA than those of minors and that OA was positively and specifically correlated with the frequency of aggressive responses to non-nestmates, a key component of territorial defence. Pharmacological manipulations that effectively switched OA action in major and minor worker brains reversed levels of aggression characteristic of each worker size class. Results suggest that altering OA action is sufficient to produce differences in aggression characteristic of size-related social roles. Neuromodulators therefore may generate variation in responsiveness to task-related stimuli associated with worker size differentiation and collateral behavioural specializations, a significant component of division of labour in complex social systems.

Biogenic amines and collective organization in a superorganism: neuromodulation of social behavior in ants.

The ecological dominance of ants has to a great extent been achieved through their collective action and complex social organization. Ants provide diverse model systems to examine the neural underpinnings of individual behavior and group action that contribute to their evolutionary success. Core elements of ant colony structure such as reproductive and ergonomic division of labor, task specialization, and social integration are beginning to be understood in terms of cellular neuroanatomy and neurochemistry. In this review we discuss the neuroethology of colony organization by focusing on the role of biogenic amines in the control of social behavior in ants. We examine the role of neuromodulation in significant sociobiological characteristics of ants, including reproductive hierarchies, colony foundation, social food flow, nestmate recognition, territoriality, and size- and age-related sensory perception and task performance as well as the involvement of monoamines in collective intelligence, the ultimate key to the global dominance of these remarkable superorganisms. We conclude by suggesting future directions for the analysis of the aminergic regulation of behavior and social complexity in ants.

Serotonin modulates worker responsiveness to trail pheromone in the ant Pheidole dentata.

As social insect workers mature, outside-nest tasks associated with foraging and defense are typically performed at higher frequencies. Foraging in ants is often a pheromonally mediated collective action performed by mature workers; age-dependent differences in olfactory response thresholds may therefore proximately regulate task repertoire development. In the ant Pheidole dentata, foraging activity increases with chronological age in minor workers, and is chemically controlled. The onset of foraging in minor workers is accompanied by marked neuroanatomical and neurochemical changes, including synaptic remodeling in olfactory regions of the brain, proliferation of serotonergic neurons, and increased brain titers of monoamines, notably serotonin. We examined the linkage of serotonin and olfactory responsiveness by assaying trail-following performance in mature P. dentata minor workers with normal serotonin levels, or serotonin levels experimentally lowered by oral administration of the serotonin synthesis inhibitor α-methyltryptophan (AMTP). By assessing responsiveness to standardized pheromone trails, we demonstrate that trail-following behaviors are significantly reduced in serotonin-depleted workers. AMTP-treated individuals were less likely to initiate trail following, and oriented along pheromone trails for significantly shorter distances than untreated, similar-age workers. These results demonstrate for the first time that serotonin modulates olfactory processes and/or motor functions associated with cooperative foraging in ants.

Adult-born hippocampal neurons are more numerous, faster maturing, and more involved in behavior in rats than in mice.

Neurons are born throughout adulthood in the hippocampus and show enhanced plasticity compared with mature neurons. However, there are conflicting reports on whether or not young neurons contribute to performance in behavioral tasks, and there is no clear relationship between the timing of maturation of young neurons and the duration of neurogenesis reduction in studies showing behavioral deficits. We asked whether these discrepancies could reflect differences in the properties of young neurons in mice and rats. We report that young neurons in adult rats show a mature neuronal marker profile and activity-induced immediate early gene expression 1-2 weeks earlier than those in mice. They are also twice as likely to escape cell death, and are 10 times more likely to be recruited into learning circuits. This comparison holds true in two different strains of mice, both of which show high rates of neurogenesis relative to other background strains. Differences in adult neurogenesis are not limited to the hippocampus, as the density of new neocortical neurons was 5 times greater in rats than in mice. Finally, in a test of function, we find that the contribution of young neurons to fear memory is much greater in rats than in mice. These results reveal substantial differences in new neuron plasticity and function between these two commonly studied rodent species.

The effects of exercise and stress on the survival and maturation of adult-generated granule cells.

Stress strongly inhibits proliferation of granule cell precursors in the adult dentate gyrus, whereas voluntary running has the opposite effect. Few studies, however, have examined the possible effects of these environmental manipulations on the maturation and survival of young granule cells. We examined the number of surviving granule cells and the proportion of young neurons that were functionally mature, as defined by seizure-induced immediate-early gene (IEG) expression, in 14- and 21-day-old granule cells in mice that were given access to a running wheel, restrained daily for 2 h, or given no treatment during this period. Treatments began 2 days after BrdU injection, to isolate effects on survival from those on cell proliferation. We found a large increase in granule cell survival in running mice when compared with controls at both time points. In addition, running increased the proportion of granule cells expressing the IEG Arc in response to seizures, suggesting that it speeds incorporation into circuits, i.e., functional maturation. Stressed mice showed no change in Arc expression, compared with control animals, but, surprisingly, showed a transient increase in survival of 14-day-old granule cells, which was gone 7 days later. Examination of cell proliferation, using the endogenous mitotic marker PCNA showed an increase in cell proliferation after 12 days of running but not after 19 days of running. The number of proliferating cells was unchanged 24 h after the 12th or 19th episode of daily restraint stress. These findings demonstrate that running has strong effects on survival and maturation of young granule cells as well as their birth and that stress can have positive but short-lived effects on granule cell survival. Published 2009 Wiley-Liss, Inc.