Octopaminergic system in the brain controls aggressive motivation in the ant, Formica japonica

The ant, Formica japonica, is polyphagous and workers hunt other insects as foods. In this study, interspecific aggression was examined in the workers and queens. Behavior experiments demonstrated that interspecific aggressiveness was significantly higher in workers than queens. Workers showed predatory aggressive behavior towards crickets, on the other hand, queens elicited threat behavior but they didn't attack crickets. In order to investigate neuronal mechanisms underlying regulation of aggressive motivation, the role of biogenic amine in the brain in evoking aggressive behavior was examined by measuring biogenic amine using high-performance liquid chromatography (HPLC) with electrochemical detection (ECD). No significant difference in the octopamine (OA) level was found between workers and queens, but the level of N-acetyloctopamine (NacOA) in the brain of queens was significantly higher than that of workers. This study suggests that OAergic system in the brain must involve in controlling aggressive motivation in the ants.     

Activity of the parietal associative cortex neurons and aminergic brainstem neurons at the performance of a voluntary movement in cats

Activity of 98 neurons of the parietal associative cortex (PAC) and 189 supposedly aminergic brainstem neurons (dopaminergic in thesubstantia nigra pans compacta, noradrenergic in thelocus coeruleus region, and serotonergic in theraphe nuclei) was recorded in awake cats. The animals were trained to perform a voluntary movement (pressing a pedal) not earlier than at a certain prefixed time moment. More than half of the recorded units modified their activity before the movement initiation. The PAC neurons responded mostly within the interval of planning of the movement, while reactions of aminergic neurons were observed in the course of its initiation, which probably provides facilitation of the responses of cortical neurons. The pattern of responses was rather specific for each of the studied neuronal populations.     

Amines and motivated behaviors: a simpler systems approach to complex behavioral phenomena

Recent investigations in invertebrate neurobiology have opened up new lines of research into the basic roles of behavioral, neurochemical, and physiological effects in complex behavioral phenomena, such as aggression and drug-sensitive reward. This review summarizes a body of quantitative work, which identifies biogenic amines as a pharmacological substrate for motivated behaviors in the crayfish, Orconectes rusticus. Specifically, this paper details progress that has (1) explored links between serotonin and an individuals aggressive state, and (2) demonstrated the existence of crayfish reward systems that are sensitive to human drugs of abuse, such as psychostimulants. First, we summarize a set of experimental approaches that explore aggression in crayfish and the significance of aminergic systems in its control. Agonistic behavior in crustaceans can be characterized within a quantitative framework; different types of behavioral plasticity in aggressive behavior are in need of physiological explanation, and pharmacological intervention involving serotonergic systems bring about characteristic changes in behavior. A second set of experiments demonstrates that psychostimulants (cocaine and D-amphetamine) serve as rewards when an intra-circulatory infusion is coupled to a distinct visual environment. Work in novel model systems such as crayfish constitutes a useful comparative approach to the study of aggression and drug addiction.     

Intercontinental union of Argentine ants: behavioral relationships among introduced populations in Europe, North America, and Asia

Many invasive ants, including the Argentine ant Linepithema humile, form expansive supercolonies, within which intraspecific aggression is absent. The behavioral relationships among introduced Argentine ant populations at within-country or within-continent scales have been studied previously, but the behavioral relationships among intercontinental populations have not been examined. The present study investigated the levels of aggression among intercontinental Argentine ant populations by transporting live ants from Europe and California to Japan and conducting aggression tests against Japanese populations. Workers from the dominant supercolonies of Europe and California did not show aggressive behavior toward workers from the dominant supercolony of Japan, whereas they fought vigorously against workers from minor supercolonies. The three massive supercolonies, together with Argentine ants from Macaronesia, may be the largest non-aggressive unit formed by a social insect species in which intraspecific aggression exists. Absence or low levels of aggression at transcontinental scale, which may have derived from low genetic variation, may help introduced Argentine ants maintain expansive supercolonies. The lack of aggression implies possible frequent exchanges of individuals among the intercontinental populations mediated by human activities.     

The value of the fluorescence histochemistry of biogenic amines in neurotoxicology

Conclusions Acid- and aldehyde-induced fluorescence offers a highly sensitive and specific instrument for the histochemical demonstration of biogenic amines. This technique can be used to advantage for the selective identification of those neuronal structures that contain biogenic amines, namely the peripheral postganglionic sympathetic neurones and the central aminergic neuronal systems.Structural changes of impaired aminergic neurones can be ascertained from their fluorescence microscope image and correlated with light and electron microscopical observations, so that selective neurotoxic changes, such as sympathetic denervation of organs, can be detected and the reversibility of these changes tested.The degree of functional and structural changes occurring in the above neuronal systems can be easily quantified by means of microfluorimetry.The histochemical approach is restricted by the necessity of using fresh and specially fixed tissues. The possibility of numerous pitfalls in the interpretation of histochemical reactions requires the simultaneous use of other optical methods, such as light and electron microscopy, or the testing of the uptake of exogeneous amines or their precursors, whenever the occurrence of neurotoxic effects is to be assessed.     

The aminergic control of cockroach salivary glands

The acinar salivary glands of cockroaches receive a dual innervation from the subesophageal ganglion and the stomatogastric nervous system. Acinar cells are surrounded by a plexus of dopaminergic and serotonergic varicose fibers. In addition, serotonergic terminals lie deep in the extracellular spaces between acinar cells. Excitation-secretion coupling in cockroach salivary glands is stimulated by both dopamine and serotonin. These monoamines cause increases in the intracellular concentrations of cAMP and Ca(2+). Stimulation of the glands by serotonin results in the production of a protein-rich saliva, whereas stimulation by dopamine results in saliva that is protein-free. Thus, two elementary secretory processes, namely electrolyte/water secretion and protein secretion, are triggered by different aminergic transmitters. Because of its simplicity and experimental accessibility, cockroach salivary glands have been used extensively as a model system to study the cellular actions of biogenic amines and to examine the pharmacological properties of biogenic amine receptors. In this review, we summarize current knowledge concerning the aminergic control of cockroach salivary glands and discuss our efforts to characterize Periplaneta biogenic amine receptors molecularly.     

Aminergic cellular organization in the gills of Aplysia species

The constituent elements of the gills of Aplysia kurodai and A. juliana were examined for the presence of biogenic amines using histochemical, immunocytochemical, and HPLC techniques. Aminergic elements were revealed by glyoxylic acid-induced fluorescence in the branchial nerve, branchial ganglion, branchial vessels, and pinnules in both species. Three types of fluorescent cells were found in the neural plexus of the gill in each species. Two of them might be sensory neurons. Although HPLC analysis showed the presence of serotonin and dopamine in all gill structures including fluorescent neural elements, there were regional differences in concentrations of the monoamines. It was noted in the pinnules that there was a much higher concentration of dopamine than serotonin. Serotonin immunocytochemistry revealed neural processes which were immunoreactive to antiserotonin antibody, but serotonin immunoreactivity could not be found in a population of branchioganglionic neuron (BGN) somata. Serotonergic elements in the ganglion may be processes of the central ganglion, while dopaminergic elements may be processes of neurons in the neural plexus, located beyond the branchial ganglion. BGNs were activated by bath-applied dopamine and serotonin. These results suggest that dopaminergic sensory inputs from the neural plexus and serotonergic descending inputs from the abdominal ganglion may be among the inputs received by BGNs. It was found that serotonin depressed excitatory junctional potentials in muscle cells of the efferent branchial vessel, which were induced by an identified neuron of the abdominal ganglion. The aminergic cellular organization of the gill may involve serotonergic presynaptic-inhibitory fibers arising from the abdominal ganglion.     

Reformation process of the neuronal template for nestmate-recognition cues in the carpenter ant <Emphasis Type="Italic">Camponotus floridanus</Emphasis>

Ants use cuticular hydrocarbons (CHC-profiles) as multicomponent recognition cues to identify colony members (nestmates). Recognition cues (label) are thought to be perceived during ant–ant encounters and compared to a neuronal template that represents the colony label. Over time, the CHC-profile may change, and the template is adjusted accordingly. A phenotype mismatch between label and template, as happens with CHC-profiles of foreign workers (non-nestmates), frequently leads to aggressive behavior. We investigated the template reformation in workers of the carpenter ant Camponotus floridanus by masking their antennae with postpharyngeal gland (PPG) extracts from nestmates or non-nestmates. The behavioral response of manipulated workers encountering unmanipulated workers was measured independently after 2 and after 15 h. After 2 h of incubation, workers treated with either of the two PPG-extracts showed low aggression towards nestmates and high aggression towards non-nestmates. In contrast, after 15 h of incubation, workers treated with non-nestmate PPG-extract showed low aggression towards both nestmates and non-nestmates. The slow (>2 h) adjustment of the template indicates a reformation localized in the central nervous system rather than in chemosensory neurons. In addition, our data show that template adjustment to a new CHC-profile does not impair the assessment of the old CHC-profile as nestmate label.     

Changes in the speed of ants as a result of aggressive interactions

Subordinate ant species utilize different tactics to reduce competition with the stronger, larger and more aggressive individuals of a dominant species. In our experimental study, we assessed the behavioral response of individual workers of 4 subordinate ant species during their co‐occurrence with workers of a single dominant species. Contrary to most classical experiments focused on aggressive interactions, we assessed workers’ speed as a crucial factor in the outcome of co‐occurrence. Generally, there was a large intraspecific variation in the speed of the studied species—each had slow and fast individuals. Workers of all studied species moved faster just after interaction, suggesting that contact between 2 hostile workers is a stressful stimulus, generating a behavioral reaction of increasing speed. Also, the number of aggressive contacts experienced by a given individual positively affected its speed. Moreover, workers which were fast when exploring territory were also fast after interspecific interactions. The duration of aggression was significantly reduced by the speed and body size of a subordinate species worker—the more quickly a worker reacted and bigger it was, the shorter was the time of cumulative aggression. To our knowledge, this is the first study of this type to be conducted on ants and we conclude that speed is an overlooked and important characteristic of species and also individuals, therefore it should be considered as a driver of patterns of co‐occurrence in ant assemblages.     

Serotonin and octopamine elicit stereotypical agonistic behaviors in the squat lobster Munida quadrispina (Anomura, Galatheidae)

Serotonin and octopamine have been implicated as modulators of posture and behavior in several crustaceans. Here we characterize the agonistic behaviors of normally interacting squat lobsters Munida quadrispina (Anomura, Galatheidae) and their responses to serotonin and octopamine injected into the ventral hemolymph sinus, in order to evaluate the potential roles of these amines in modulating agonistic behaviors. Normally interacting M. quadrispina do not develop lasting dominance hierarchies, although transient aggressive and submissive displays do occur. Injected serotonin elicits postures and behaviors in isolated individuals similar to those typical of aggressive, normally interacting animals. Injected octopamine can produce postures and behaviors typical of submissive animals, and elicits behaviors which imply a modulatory role for octopamine in tailflipping. The effects of both amines are reversible and dose dependent, and the dose-response curves parallel the normal progression of agonistic interactions. The social behaviors and reactions to injected serotonin and octopamine of M. quadrispina differ from those of lobsters and crayfish, indicating that interspecific differences in neuromodulation of behavior and motor output exist. Such differences have implications for the understanding of aminergic modulation of aggression and the evolution of aminergic modulation in crustaceans. Accepted: 22 June 1997     

Monoaminergic interaction in the central nervous system: a morphological analysis in the locus coeruleus of the rat.

The locus coeruleus of the rat is richly innervated by many aminergic neurons varying in amine content and in site of origin. There are adrenergic and noradrenergic neurons originating in the medulla oblongata, dopaminergic from the hypothalamus, serotonergic from the mesencephalon and also intrinsic noradrenergic neurons in the locus coeruleus complex. Of these, adrenergic and dopaminergic inputs appear relatively specific and powerful.     

Changes in the Content of Brain Biogenic Amine Associated with Early Colony Establishment in the Queen of the Ant, Formica japonica

We examined changes in the content of biogenic amines in the brains of ant queen associated with early colony establishment. In ants, including Formica japonica, winged virgin queens lose their wings following copulation, and then start establishing a colony. Significant changes in brain biogenic amine content in the queen are associated with transition from winged virgin queen to wingless mated queen. The levels of serotonin (5HT), octopamine (OA) and dopamine (DA) decreased significantly in the brain of the queen after starting a colony. On the other hand, tyramine (TA) increased significantly in the brain following colony establishment. Catabolized substances of the biogenic amines in the brain were also measured. The levels of N-acetyloctopamine (Nac-OA) and N-acetyltyramine (Nac-TA) in the brain did not show a significant change after the queen established a colony. However, the levels of N-acetylserotonin (Nac-5HT) in the brain were significantly higher in wingless mated queens than in winged virgin queens, whereas levels of N-acetyldopamine (Nac-DA) in the brain were significantly lower in wingless mated queens than winged virgin queens. These results suggest that serotonergic and octopaminergic systems in the brain of the queen change when the mated queen starts to establish a new colony.     

Serotonin modulates worker responsiveness to trail pheromone in the ant <Emphasis Type="Italic">Pheidole dentata</Emphasis>

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.     

Colony-structure variation and interspecific competitive ability in the invasive Argentine ant

The success of some invasive species may depend on phenotypic changes that occur following introduction. In Argentine ants ( Linepithema humile) introduced populations typically lack intraspecific aggression, but native populations display such behavior commonly. We employ three approaches to examine how this behavioral shift might influence interspecific competitive ability. In a laboratory experiment, we reared colonies of Forelius mccooki with pairs of Argentine ant colonies that either did or did not exhibit intraspecific aggression. F. mccooki reared with intraspecifically non-aggressive pairs of Argentine ants produced fewer eggs, foraged less actively, and supported fewer living workers than those reared with intraspecifically aggressive pairs. At natural contact zones between competing colonies of L. humile and F. mccooki, the introduction of experimental Argentine ant colonies that fought with conspecific field colonies caused L. humile to abandon baits in the presence of F. mccooki, whereas the introduction of colonies that did not fight with field colonies of Argentine ants resulted in L. humile retaining possession of baits. Additional evidence for the potential importance of colony- structure variation comes from the Argentine ants native range. At a site along the Rio de la Plata in Argentina, we found an inverse relationship between ant richness and density of L. humile (apparently a function of local differences in colony structure) in two different years of sampling.     

Dispensable,Redundant, Complementary,and Cooperative Roles of Dopamine,Octopamine, and Serotonin in Drosophila melanogaster

To investigate the regulation of Drosophila melanogaster behavior by biogenic amines, we have exploited the broad requirement of the vesicular monoamine transporter (VMAT) for the vesicular storage and exocytotic release of all monoamine neurotransmitters. We used the Drosophila VMAT (dVMAT) null mutant to globally ablate exocytotic amine release and then restored DVMAT activity in either individual or multiple aminergic systems, using transgenic rescue techniques. We find that larval survival, larval locomotion, and female fertility rely predominantly on octopaminergic circuits with little apparent input from the vesicular release of serotonin or dopamine. In contrast, male courtship and fertility can be rescued by expressing DVMAT in octopaminergic or dopaminergic neurons, suggesting potentially redundant circuits. Rescue of major aspects of adult locomotion and startle behavior required octopamine, but a complementary role was observed for serotonin. Interestingly, adult circadian behavior could not be rescued by expression of DVMAT in a single subtype of aminergic neurons, but required at least two systems, suggesting the possibility of unexpected cooperative interactions. Further experiments using this model will help determine how multiple aminergic systems may contribute to the regulation of other behaviors. Our data also highlight potential differences between behaviors regulated by standard exocytotic release and those regulated by other mechanisms.     

Acute antenatal hypoxia on different stages of embryogenesis changes the offspring behavior patterns and biogenic amine levels

The effects of acute hypobaric hypoxia on the stages of progestation or beginning of organogenesis on biogenic amines levels in brain stem and cerebral cortex of their mature offspring as well as on their behavior, were investigated. It was shown that acute hypoxia applied in the period of embryonic organogenesis resulted in severe delayed changes in offspring spontaneous behavior and led to marked changes of biogenic amine levels, particularly expressed for dopaminergic system. Females subjected to antenatal hypoxia happened to be more sensitive to its influences than males.     

Worker policing limits the number of reproductives in a ponerine ant

Reproductive division of labour is an essential feature of insect sociality, but the regulation of sterility among colony members remains incompletely understood. Ant workers and queens are morphologically divergent and workers are only capable of producing males in a colony, although they usually do not do so. Worker policing is one mechanism proposed for their infertility and it can be expressed as either aggressive inhibition of ovarian activity among workers or destruction of worker-laid eggs. A few studies have shown that workers with developed ovaries are preferentially attacked by nest-mates, but adequate demonstration of worker policing also requires evidence that these attacks result in the suppression of ovarian activity or death. We investigated worker policing in the ponerine ant Harpegnathos saltator in which workers are able to mate and replace the founding queen. Five colonies were each divided into two groups, one of which consisted exclusively of infertile workers. Some individuals in the orphaned groups began laying eggs during the three-week separation and upon reunification these were vigorously attacked by infertile workers of the other groups. The ovarian activity of these new egg layers became inhibited, as revealed by subsequent dissection of marked individuals. Worker policing in H. saltator appears to function primarily in preventing an excess of reproductive workers.     

A Combination of Fertility Signals and Aggression Regulates Reproduction in the Ant <Emphasis Type="Italic">Gnamptogenys striatula</Emphasis>

Approximately 150 ant species are facultatively or obligately queenless whereby mated workers assume the role of the queen. In many of these species a reproductive dominance hierarchy is established by way of aggressive interactions. Top-ranking workers, which are typically the most fecund, acquire a characteristic cuticular hydrocarbon profile. We studied the temporal dynamics of this chemical change and associated interplay with observed aggressive interactions in an experimentally orphaned colony of the facultatively queenless ant Gnamptogenys striatula. Our observations and chemical analyses demonstrate that chemical fertility signals played a major role in the establishment of a dominance hierarchy and aggression settled dominance relationships only when ants had identical hydrocarbon profiles. Moreover, individuals with a higher potential fertility, in this experiment reflected in a higher ovariole number, are shown to have a better chance of becoming a reproductive.     

Contact between supercolonies elevates aggression in Argentine ants

Complex recognition systems underlie the social organization of many organisms. In social insects the acceptance of other individuals as nestmates can involve a variety of different cues, but the relative importance of these cues can change in relation to the fitness costs of accepting or rejecting other individuals. In this study we investigate the mechanisms that underlie recognition behaviour in Argentine ants (Linepithema humile). Introduced populations of Argentine ants are characterized by a social structure known as unicoloniality where intraspecific aggression is absent over large distances resulting in the formation of expansive supercolonies. Recent research has identified sites where multiple, mutually aggressive supercolonies co-occur allowing an examination of Argentine ant behaviour at territorial boundaries. We found that workers from different supercolonies always interact aggressively with one another, but that neighbours from different colonies (i.e., workers from nests located in the immediate vicinity of territory borders) consistently exhibited higher levels of aggression compared to those displayed by non-neighbours from different colonies (i.e., workers from nests located far enough away from a territory border so that interactions are unlikely). This difference in the level of aggression displayed between neighbours and between non-neighbours from different supercolonies cannot be explained by differences in relatedness or genetic similarity. Instead our findings suggest that direct contact between mutually antagonistic colonies is sufficient to elevate aggression. A laboratory experiment in which we manipulated the extent to which colonies with no prior history of contact could interact with one another, revealed that aggression increased after colonies were permitted to interact, but dropped after connections between colonies were severed. Moreover, the mere presence of an aggressive supercolony was sufficient to elicit elevated aggression. Overall these patterns are opposite to the “dear enemy” phenomenon and could be the result of the intense territorial aggression exhibited by established supercolonies of this species. Received 8 January 2007; revised 27 March 2007; accepted 28 March 2007.