Jan Rillich

Assessment strategy of fighting crickets revealed by manipulating information exchange

The assessment strategy used by adult male crickets, Gryllus bimaculatus (de Geer), during conspecific aggression was deduced from the effects of handicaps (disabled mandibles, blackened eyes, size) and altered aggressive motivation (after defeat and flying) on aggressiveness, fight duration and win probability under laboratory conditions. The contestants received either the same (symmetrical) or different (asymmetrical) treatments. Despite handicaps, all crickets showed essentially normal escalating fighting behaviour. In symmetrical contests, fights became even harsher and longer with multiple handicaps. In asymmetrical contests, neither disabling the mandibles nor blackening the eyes significantly influenced win probability. However, ‘blinded’ crickets nearly always defeated opponents with disabled mandibles that could not inflict bites. Furthermore, small crickets and losers showed physical fighting more frequently when prevented from seeing. Handicap effects became more pronounced when both contestants were flown, to maximize aggressive motivation, before fighting. Our findings conform to the cumulative assessment hypothesis. We conclude, first, that contestants need longer to accumulate the cues required to surpass a threshold to flee when visual and physical inputs are reduced. Second, the decision to flee is based solely on the opponents actions. Third, flying enhances aggressiveness by reducing disparities in motivation, making other disparities, such as in weaponry, more decisive. Thus, a crickets aggressiveness is a trade-off between its inherent, experience-dependent agonistic motivation and the accumulated perceived actions of the adversary.

Octopamine and occupancy: an aminergic mechanism for intruder-resident aggression in crickets

Aggression is a behavioural strategy for securing resources (food, mates and territory) and its expression is strongly influenced by their presence and value. While it is known that resource holders are generally highly aggressive towards intruding consexuals and usually defeat them, the underlying neuronal mechanisms are not known. In a novel intruder–resident paradigm for field crickets (Gryllus bimaculatus), we show that otherwise submissive losers of a preceding aggressive encounter readily fight and often defeat aggressive winners after occupying an artificial shelter. This aggression enhancing effect first became evident after 2 min residency, and was maximal after 15 min, but absent 15 min after shelter removal. The residency effect was abolished following non-selective depletion of biogenic amines from the central nervous system using reserpine, or semi-selective depletion of octopamine and dopamine using α-methyl-tyrosine, but not following serotonin depletion using α-methyl-tryptophan. The residency effect was also abolished by the treatment with phentolamine, an α-adrenergic receptor antagonist, or epinastine, a highly selective octopamine receptor blocker, but not by propranolol, a ß-adrenergic receptor antagonist, or by yohimbine, an insect tyramine receptor blocker. We conclude that crickets evaluate residency as a rewarding experience that promotes aggressive motivation via a mechanism involving octopamine, the invertebrate analogue of noradrenaline.

Winning Fights Induces Hyperaggression via the Action of the Biogenic Amine Octopamine in Crickets

Winning an agonistic interaction against a conspecific is known to heighten aggressiveness, but the underlying events and mechanism are poorly understood. We quantified the effect of experiencing successive wins on aggression in adult male crickets (Gryllus bimaculatus) by staging knockout tournaments and investigated its dependence on biogenic amines by treatment with amine receptor antagonists. For an inter-fight interval of 5 min, fights between winners escalated to higher levels of aggression and lasted significantly longer than the preceding round. This winner effect is transient, and no longer evident for an inter-fight interval of 20 min, indicating that it does not result from selecting individuals that were hyper-aggressive from the outset. A winner effect was also evident in crickets that experienced wins without physical exertion, or that engaged in fights that were interrupted before a win was experienced. Finally, the winner effect was abolished by prior treatment with epinastine, a highly selective octopamine receptor blocker, but not by propranolol, a ß-adrenergic receptor antagonist, nor by yohimbine, an insect tyramine receptor blocker nor by fluphenazine an insect dopamine-receptor blocker. Taken together our study in the cricket indicates that the physical exertion of fighting, together with some rewarding aspect of the actual winning experience, leads to a transient increase in aggressive motivation via activation of the octopaminergic system, the invertebrate equivalent to the adrenergic system of vertebrates.

The Decision to Fight or Flee – Insights into Underlying Mechanism in Crickets

Ritualized fighting between conspecifics is an inherently dangerous behavioral strategy, optimized to secure limited resources at minimal cost and risk. To be adaptive, potential rewards, and costs of aggression must be assessed to decide when it would be more opportune to fight or flee. We summarize insights into the proximate mechanisms underlying this decision-making process in field crickets. As in other animals, cricket aggression is enhanced dramatically by motor activity, winning, and the possession of resources. Pharmacological manipulations provide evidence that these cases of experience dependent enhancement of aggression are each mediated by octopamine, the invertebrate counterpart to adrenaline/noradrenaline. The data suggest that both physical exertion and rewarding aspects of experiences can activate the octopaminergic system, which increases the propensity to fight. Octopamine thus represents the motivational component of aggression in insects. For the decision to flee, animals are thought to assess information from agonistic signals exchanged during fighting. Cricket fights conform to the cumulative assessment model, in that they persist in fighting until the sum of their opponent’s actions accumulates to some threshold at which they withdraw. We discuss evidence that serotonin, nitric oxide, and some neuropeptides may promote an insect’s tendency to flee. We propose that the decision to fight or flee in crickets is controlled simply by relative behavioral thresholds. Rewarding experiences increase the propensity to fight to a level determined by the modulatory action of octopamine. The animal will then flee only when the accumulated sum of the opponent’s actions surpasses this level; serotonin and nitric oxide may be involved in this process. This concept is in line with the roles proposed for noradrenaline, serotonin, and nitric oxide in mammals and suggests that basic mechanisms of aggressive modulation may be conserved in phylogeny.

The biphasic NAD(P)H fluorescence response of astrocytes to dopamine reflects the metabolic actions of oxidative phosphorylation and glycolysis.

J. Neurochem. (2010) 115, 483–492.

A fighter's comeback: dopamine is necessary for recovery of aggression after social defeat in crickets.

Social defeat, i.e. losing an agonistic dispute with a conspecific, is followed by a period of suppressed aggressiveness in many animal species, and is generally regarded as a major stressor, which may play a role in psychiatric disorders such as depression and post-traumatic stress disorder. Despite numerous animal models, the mechanisms underlying loser depression and subsequent recovery are largely unknown. This study on crickets is the first to show that a neuromodulator, dopamine (DA), is necessary for recovery of aggression after social defeat. Crickets avoid any conspecific male just after defeat, but regain their aggressiveness over 3 h. This recovery was prohibited after depleting nervous stores of DA and octopamine (OA, the invertebrate analogue of noradrenaline) with α-methyl-tyrosine (AMT). Loser recovery was also prohibited by the insect DA-receptor (DAR) antagonist fluphenazine, but not the OA-receptor (OAR) blocker epinastine, or yohimbine, which blocks receptors for OAs precursor tyramine. Conversely, aggression was restored prematurely in both untreated and amine depleted losers given either chlordimeform (CDM), a tissue permeable OAR-agonist, or the DA-metabolite homovanillyl alcohol (HVA), a component of the honeybee queen mandibular pheromone. As in honeybees, HVA acts in crickets as a DAR-agonist since its aggression promoting effect on losers was selectively blocked by the DAR-antagonist, but not by the OAR-antagonist. Conversely, CDMs aggression promoting effect was selectively blocked by the OAR-antagonist, but not the DAR-antagonist. Hence, only DA is necessary for recovery of aggressiveness after social defeat, although OA can promote loser aggression independently to enable experience dependent adaptive responses.

Isolation Associated Aggression – A Consequence of Recovery from Defeat in a Territorial Animal

Population density has profound influences on the physiology and behaviour of many animal species. Social isolation is generally reported to lead to increased aggressiveness, while grouping lowers it. We evaluated the effects of varying degrees of isolation and grouping on aggression in a territorial insect, the Mediterranean field cricket, Gryllus bimaculatus . Substantiating early observations, we show that dyadic contests between weight-matched, adult male crickets taken from groups rarely escalate beyond threat displays, whereas interactions between pairs of previously isolated crickets typically escalate to physical fights lasting several seconds. No significant differences were found between 1, 2 and 6-day isolates, or between individuals grouped for a few hours or lifelong. Unexpectedly, crickets grouped in immediate proximity within individual mesh cages that precluded fighting while permitting visual, olfactory and mechanical, antennal contact, were as aggressive as free isolates. This suggests that reduced aggression of grouped animals may be an acquired result of fighting. Supporting this notion, isolated crickets initially engage in vigorous fights when first grouped, but fighting intensity and duration rapidly decline to the level of life-long grouped crickets within only 10 min. Furthermore, grouped crickets become as aggressive as life-long isolates after only 3 hours of isolation, and on the same time course required for crickets to regain their aggressiveness after social defeat. We conclude that the reduced aggressiveness of grouped crickets is a manifestation of the loser effect resulting from social subjugation, while isolation allows recovery to a state of heightened aggressiveness, which in crickets can be considered as the default condition. Given the widespread occurrence of the loser effect in the Animal Kingdom, many effects generally attributed to social isolation are likely to be a consequence of recovery from social subjugation.

Female crickets are driven to fight by the male courting and calling songs

Crickets have traditional sex roles, where males compete aggressively for access to selective polyandrous females. However, in a laboratory experiment, we found that normally nonaggressive female Gryllus campestris fought each other vigorously in the presence of a courting male, resulting in a dominant female that gained a greater probability of receiving the spermatophore. Female–female fights included the same series of characteristic actions known from male–male fights, which demonstrates that the females can perform the full repertoire of agonistic actions except for the production of the aggressive rival song. Since females remained nonaggressive towards each other in the vicinity of a muted male, but were induced to fight each other in the complete absence of a male by the auditory experience of the courtship song, this song is both sufficient and necessary to induce female competition for males. Calling song was as effective as courtship song at inducing female aggression, whereas rival song was least effective. We therefore speculate that the calling and courtship songs may signal a males resource value.

Flight and Walking in Locusts–Cholinergic Co-Activation, Temporal Coupling and Its Modulation by Biogenic Amines

Walking and flying in locusts are exemplary rhythmical behaviors generated by central pattern generators (CPG) that are tuned in intact animals by phasic sensory inputs. Although these two behaviors are mutually exclusive and controlled by independent CPGs, leg movements during flight can be coupled to the flight rhythm. To investigate potential central coupling between the underlying CPGs, we used the muscarinic agonist pilocarpine and the amines octopamine and tyramine to initiate fictive flight and walking in deafferented locust preparations. Our data illustrate that fictive walking is readily evoked by comparatively lower concentrations of pilocarpine, whereas higher concentrations are required to elicit fictive flight. Interestingly, fictive flight did not suppress fictive walking so that the two patterns were produced simultaneously. Frequently, leg motor units were temporally coupled to the flight rhythm, so that each spike in a step cycle volley occurred synchronously with wing motor units firing at flight rhythm frequency. Similarly, tyramine also induced fictive walking and flight, but mostly without any coupling between the two rhythms. Octopamine in contrast readily evoked fictive flight but generally failed to elicit fictive walking. Despite this, numerous leg motor units were recruited, whereby each was temporarily coupled to the flight rhythm. Our results support the notion that the CPGs for walking and flight are largely independent, but that coupling can be entrained by aminergic modulation. We speculate that octopamine biases the whole motor machinery of a locust to flight whereas tyramine primarily promotes walking.

Adding up the odds—Nitric oxide signaling underlies the decision to flee and post-conflict depression of aggression

Aversive experiences summated during fighting in crickets activate the NO signaling pathway, which promotes the decision to flee and results in post-conflict depression of aggression. Fighting is dangerous, which is why animals choose to flee once the costs outweigh the benefits, but the mechanisms underlying this decision-making process are unknown. By manipulating aggressive signaling and applying nitrergic drugs, we show that the evolutionarily conserved neuromodulator nitric oxide (NO), which has a suppressing effect on aggression in mammals, can play a decisive role. We found that crickets, which exhibit spectacular fighting behavior, flee once the sum of their opponent’s aversive actions accrued during fighting exceeds a critical amount. This effect of aversive experience is mediated by the NO signaling pathway. Rather than suppressing aggressive motivation, NO increases susceptibility to aversive stimuli and with it the likelihood to flee. NO’s effect is manifested in losers by prolonged avoidance behavior, characteristic for social defeat in numerous species. Intriguingly, fighting experience also induces, via NO, a brief susceptible period to aversive stimuli in winners just after victory. Our findings thus reveal a key role for NO in the mechanism underlying the decision to flee and post-conflict depression in aggressive behavior.