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Antidyskinetic action of 3-PPP, a selective dopaminergic autoreceptor agonist, in Cebus monkeys with persistent neuroleptic-induced dyskinesias.

Four Cebus apella monkeys with persistent dyskinetic movements induced by earlier long-term administration of haloperidol were subjected to a trial of the dyskinesia-modifying effects of a novel dopamine autoreceptor agonist 3-PPP (3[3-hydroxyphenyl]-N-n-propyl-piperidine). Three monkeys had choreic dyskinesia involving trunk and extremities whereas one had a buccolingual form including tongue protrusion with choreoathetotic twitching and twisting movements of the tongue. Two monkeys (1 choreic, 1 buccolingual) responded with dose-dependent symptom alleviation to 3-PPP, 1-4 mg/kg, with no signs of concomitant sedation or catalepsy. In the monkey with buccolingual dyskinesia all dyskinetic signs disappeared completely 2 hours after 2 mg/kg of 3-PPP. This animal participated in a separate study where the same doses of 3-PPP but also its enantiomers were given. The (-) enantiomer was a more potent antidyskinetic agent than the (+) enantiomer, the racemate falling between these two. Four mg/kg of the (+) enantiomer precipitated an amphetamine-like excitation and after 4 hours aggravation of dyskinesia was noted. These observations support the notion that the (+) enantiomer has both postsynaptic and presynaptic stimulatory effects, whereas the (-) enantiomer acts as a presynaptic dopamine receptor agonist.

Animals↗

Effect of extended depot fluphenazine treatment and withdrawal on social and other behaviors of Cebus apella monkeys.

To examine whether or not prolonged exposure to a depot neuroleptic has either residual or "tardive pathological" effects on normal behavior, 38 Cebus apella monkeys were observed daily for 108 weeks. The issue of stress influencing such effects was also addressed. During weeks 25-48 half of the monkeys received 0.22 mg/kg fluphenazine decanoate, IM, every 3 weeks, with the dose increased to 0.33 mg/kg during weeks 49-72. Behavioral measures were combined to form composite behavioral variables which quantify four major aspects of behavior: self- and environment-directed behavior, affiliation, aggression, and normal locomotor activity. Mean plasma fluphenazine levels at 48 h post-injection were 0.13 (+/- 0.03) ng/ml for injections 3-8 and 0.24 (+/- 0.07) ng/ml for injections 11-16. The pre-study null hypothesis that the four major aspects of behavior would not be adversely affected by this treatment during the drug-discontinuation phase of the study (weeks 73-108) was not statistically negated. There were highly significant decreases in self- and environment-directed behaviors and affiliation during the treatment periods, implying that treatment may contribute to the negative symptoms of treated schizophrenics. Stress reduced the above effects. Aggression showed some increase during early drug discontinuation, accentuated by stress. Recovery of normal (baseline) behavioral scores began by week 7 after the last treatment. Mild (bucco-lingual) tardive dyskinesias persisted in 30% of the animals for a prolonged time.

Animals↗

Chronic treatment with the D1 receptor antagonist, SCH 23390, and the D2 receptor antagonist, raclopride, in cebus monkeys withdrawn from previous haloperidol treatment. Extrapyramidal syndromes and dopaminergic supersensitivity.

The effects of chronic treatment with dopamine (DA) D1 and D2 receptor antagonists were evaluated in eight cebus apella monkeys with mild oral dyskinesia after previous haloperidol treatment. SCH 23390 (D1 antagonist) was given daily to investigate the direct behavioural effect during long-term treatment and the subsequent supersensitivity to DA agonists. Raclopride (D2 antagonist) was investigated for comparison. All drugs were given subcutaneously. SCH 23390 and raclopride induced dystonic syndromes, catalepsy, sedation and reduced locomotor activity. The monkeys developed marked tolerance to the dystonic effect of SCH 23390, while they showed increased sensibility to the dystonic effect of raclopride. Baseline oral dyskinesia (24 h after injection) remained unchanged during D1 antagonist treatment, while it increased during D2 antagonist treatment. SCH 23390 induced supersensitivity to the oral dyskinesia- and grooming-inducing effects of SKF 81297 (D1 agonist) after 9 weeks, while the subsequent treatment with raclopride induced supersensitivity to the reactivity- and stereotypy-inducing effects of quinpirole (D2 receptor agonist) after 3 weeks. Because of the possibility of a carry-over effect (SKF 81297-induced oral hyperkinesia and grooming), other changes in raclopride-induced behaviours cannot be ruled out. The development of tolerance to the dystonic effect of SCH 23390 and the unchanged baseline oral dyskinesia during SCH 23390 treatment indicate an advantageous profile of side effects of DA D1 receptor blockade.

Animals↗

Behavioral effects of sertindole, risperidone, clozapine and haloperidol in Cebus monkeys.

Extrapyramidal side effects (EPS) are major limitations to neuroleptic treatment of psychoses. To evaluate further the behavioral characteristics of the novel antipsychotic agents, a wide range of single intramuscular doses of sertindole (0.1-2.5 mg/kg IM), risperidone (0.01-0.25 mg/kg IM), clozapine (1.0-25.0 mg/kg IM), and haloperidol (0.01-0.25 mg/kg IM) were blindly evaluated at weekly intervals in Cebus monkeys previously sensitized to neuroleptics. All drugs except clozapine produced dystonia and parkinsonian symptoms, but haloperidol and risperidone were 50-100 times more potent than sertindole in producing EPS. Sertindole, risperidone and haloperidol had no significant sedative effects, whereas clozapine produced dose related sedation. Risperidone, clozapine and haloperidol but not sertindole decreased locomotor activity. Sertindole, risperidone and clozapine had a calming effect at doses below the EPS threshold, unlike haloperidol. Sertindole has many behavioral effects in nonhuman primates that are similar to those seen with the new antipsychotics, risperidone and clozapine, which suggests a favorable antipsychotic benefit/risk ratio in the clinic, especially regarding EPS.

Animals↗

The effects of D1 (NNC 22-0215) and D2 (haloperidol) antagonists in a chronic double-blind placebo controlled trial in cebus monkeys.

The effects of chronic treatment for 28 days with the oral D1 (NNC 22-0215) or D2 (haloperidol) antagonist were evaluated in nonhuman primates in a double blind, placebo controlled crossover trial. Cebus monkeys, 10-18 years old, which were previously sensitized to neuroleptics, were treated in three different groups with NNC 22-0215 2-3 mg/kg PO (n = 6), haloperidol 2-3 mg/kg PO (n = 5), or lactose placebo (n = 7) each day in a banana slice. At the end of 28 days the NNC 22-0215 group crossed over to haloperidol and the haloperidol group crossed over to NNC 22-0215 for 28 more days. The lactose group continued on lactose. Extrapyramidal symptoms (EPS) of dystonia and sedation were scored daily. Initially both NNC 22-0215 and haloperidol produced equal rates of dystonia. However, the NNC 22-0215 group demonstrated nearly full desensitization by day 2 and showed no EPS by day 6, whereas the haloperidol group had increased EPS during the first week, followed by moderate desensitization to EPS, but continued to have symptoms on each of the 28 days of treatment. At crossover, the previously treated haloperidol group rapidly desensitized with NNC 22-0215 by day 4 to show no EPS, whereas the previously treated NNC 22-0215 group showed full EPS on the first day of haloperidol and had EPS continue over the next 28 days of treatment. Sedation from NNC 22-0215 also desensitized within the first week of treatment. Haloperidol produced minimal sedation that did not change. The profound difference in rates of desensitization between repeated D1 and D2 antagonist treatment suggests that D1 antagonists in the clinic may produce EPS side effects for only the first few days, in contrast to the continuous acute EPS associated with chronic neuroleptic treatment.

Administration, Oral↗

Laminar, columnar and topographic aspects of ocular dominance in the primary visual cortex of Cebus monkeys.

The representation of the two eyes in striate cortex (V1) of Cebus monkeys was studied by electrophysiological single-unit recordings in normal animals and by morphometric analysis of the pattern of ocular dominance (OD) stripes, as revealed by cytochrome oxidase histochemistry in V1 flat-mounts of enucleated animals. Single-unit recordings revealed that the large majority of V1 neurons respond to the stimulation of either eye but are more strongly activated by one of them. As in other species of monkey, neurons with preference for the stimulation of the same eye are grouped in columns 300-400 microns wide, spanning all cortical layers. Monocular neurons are clustered in layer IVc, specially in its deeper half (IVc-beta), and constitute less than 10% of the population of other layers. Neurons with equal responses to each eye are more commonly found in layer V than elsewhere in V1. In the supragranular layers and in granular layer IVc-alpha neurons strongly dominated by one of the eyes tend to be broadly tuned for orientation, while binocularly balanced neurons tend to be sharply tuned for this parameter. No such correlation was detected in the infragranular layers, and most neurons in layer IVc-beta responded regardless of stimulus orientation. Ocular dominance stripes are present throughout most of V1 as long, parallel or bifurcating bands alternately dominated by the ipsi- or the contralateral eye. They are absent from the cortical representations of the blind spot and the monocular crescent. The domains of each eye occupy nearly equal portions of the surface of binocular V1, except for the representation of the periphery, where the contralateral eye has a larger domain, and a narrow strip along the border of V1 with V2, where either eye may predominate. The orderliness of the pattern of stripes and the relationship between stripe arrangement and the representation of the visual meridians vary with eccentricity and polar angle but follow the same rules in different animals. These results demonstrate that the laminar, columnar and topographic distribution of neurons with different degrees of OD in V1 is qualitatively similar in New- and Old World monkeys of similar sizes and suggest that common ancestry, rather than parallel evolution, may account for the OD phenotypes of contemporaneous simians.

Animals↗

Evidence for distinct precursor pools for biliary cholesterol and primary bile acids in cebus and cynomolgus monkeys.

The abnormal metabolism and distribution of plasma lipoproteins have been associated with atherosclerosis and gallstones. To better understand the process of cholesterol excretion, a study was designed to determine whether the contribution of lipoprotein free 14C-cholesterol (as LDL or HDL) to biliary cholesterol or primary bile acids differs in two species of nonhuman primates, cebus and cynomolgus monkeys, having opposite plasma LDL/HDL ratios. Since amino acid conjugation might influence bile acid synthesis or secretion, the taurine and glycine conjugates of newly synthesized primary bile acids, cholic acid (CA) and chenodeoxycholic acid (CDCA), were measured in the species capable of conjugating with taurine or glycine (cynomolgus). After total bile acid pool washout, monkeys were infused with human LDL or HDL labeled with free 14C-cholesterol, and the specific activities (SA) of biliary cholesterol and primary bile acid conjugates were determined. In both species, regardless of the lipoprotein infused, the SA of biliary cholesterol and CA were greater than those for total bile acids and CDCA, respectively. In cynomolgus, the SA of glycine conjugates was higher for CA than CDCA, while the SA of taurine conjugates was greater for CDCA than CA. Under these conditions, (i) infused lipoprotein free cholesterol (as either LDL or HDL) contributed more to biliary cholesterol than to bile acids and more to CA than to CDCA; (ii) glycine conjugated preferentially with CA rather than CDCA, while taurine was the preferred conjugate for CDCA.

Animals↗

Benzoquinones from millipedes deter mosquitoes and elicit self-anointing in capuchin monkeys (Cebus spp.).

Neotropical monkeys of the genus Cebus anoint themselves by rubbing arthropods and plants against their pelage. A recent study has shown that free-ranging wedge-capped capuchin monkeys (C. olivaceus) in Venezuela self-anoint with a benzoquinone-secreting millipede, an activity by which they are hypothesized to appropriate chemical deterrents of mosquitoes. To evaluate the plausibility of this hypothesis, female yellow fever mosquitoes (Aedes aegypti) were presented with two millipede secretory compounds, 2-methyl-1,4-benzoquinone and 2-methoxy-3-methyl-1,4-benzoquinone, on nylon-reinforced silicone membranes placed over wells filled with human blood, a highly preferred food. Mosquitoes exhibited fewer landings, fed less frequently, and flew more frequently (a possible indication of repellency) in the presence of membranes treated with benzoquinones than with controls. These compounds also elicit self-anointing in captive male and female tufted (C. apella) and white-faced (C. capucinus) capuchin monkeys.

Aedes↗

Increased incidence of dyskinesias and other behavioral effects of re-exposure to neuroleptic treatment in social colonies of Cebus apella monkeys.

RATIONALE: Typical neuroleptic medications are still administered to as many as 40% of patients receiving antipsychotic treatment in the US. Intermittent administration or interruption of long-term neuroleptic medication for schizophrenia may increase the incidence of human tardive dyskinesias, and similarly may produce increasingly marked motor side-effects, parkinsonism, and other behavioral pathologies in non-human primates. OBJECTIVES AND METHODS: Given these similarities, we addressed the issue of prolonged and intermittent typical neuroleptic treatment and dopaminergic function during a 5-year, multi-phase study with social colonies of Cebus apella monkeys. In the previously reported phase 1, we examined the effects of 48 weeks of exposure to, followed by withdrawal from, fluphenazine decanoate (FPZ). Phase 3 reported here examined the effects of 18 weeks of re-exposure to FPZ in these same monkeys, 91 weeks after discontinuation of their phase 1 FPZ treatment. RESULTS: Analysis of blood plasma FPZ indicated levels of 0.22+/-0.08 ng/ml for the six injections during the re-exposure period (n=54), comparable to the 0.24+/-0.07 ng/ml levels measured during our original treatment with this dose. Acute dyskinesias and dystonias increased by 300% upon re-exposure to FPZ; 15 of 18 FPZ-treated animals exhibited oral-buccal dyskinesias and all exhibited torticollis or retrocollis. Retreatment with FPZ was also associated with highly significant reductions in Self- and Environment-Directed Behavior and Directed Affiliation, effects similar to those seen during the original phase 1 FPZ treatment. Although FPZ re-treatment was associated with a significant reduction in Directed Aggression (an effect that was more robust than that observed during phase 1), in phase 3, we again observed an increase in Directed Aggression during early drug discontinuation when animals were in a stress-inducing situation. CONCLUSIONS: These results both support our phase 1 conclusion that typical neuroleptic medications may contribute to negative symptoms of schizophrenia and provide additional evidence for the possibility of increased aggression in stressful situations when medication is discontinued. Additionally, the results indicate that intermittent treatment with typical neuroleptics may dramatically increase the incidence of dystonias and dyskinesias.

Aggression↗

Evolution of growth hormone in primates: the GH gene clusters of the New World monkeys marmoset (Callithrix jacchus) and white-fronted capuchin (Cebus albifrons).

The GH gene cluster in marmoset, Callithrix jacchus, comprises eight GH-like genes and pseudogenes and appears to have arisen as a consequence of gene duplications occurring independently of those leading to the human GH gene cluster. We report here the complete sequence of the marmoset GH gene locus, including the intergenic regions and 5' and 3' flanking sequence, and a study of the multiple GH-like genes of an additional New World monkey (NWM), the white-fronted capuchin, Cebus albifrons. The marmoset sequence includes 945 nucleotides (nt) of 5' flanking sequence and 1596 nt of 3' flanking sequence that are "unique"; between these are eight repeat units, including the eight GH genes/pseudogenes. The breakpoints between these repeats are very similar, indicating a regular pattern of gene duplication. These breakpoints do not correspond to those found in the much less regular human GH gene cluster. This and phylogenetic analysis of the repeat units within the marmoset gene cluster strongly support the independent origin of these gene clusters, and the idea that the episode of rapid evolution that occurred during GH evolution in primates preceded the gene duplications. The marmoset GH gene cluster also differs from that of human in having fewer and more evenly distributed Alu sequences (a single pair in each repeat unit) and a "P-element" upstream of every gene/pseudogene. In human there is no P-element upstream of the gene encoding pituitary GH, and these elements have been implicated in placental expression of the other genes of the cluster. The GH gene clusters in marmoset and capuchin appear to have arisen as the consequence of a single-gene duplication event, but in capuchin there was then a remarkable expansion of the GH locus, giving at least 40 GH-like genes and pseudogenes. Thus even among NWMs the GH gene cluster is very variable.

Alu Elements↗

Extrapyramidal side effects during chronic combined dopamine D1 and D2 antagonist treatment in Cebus apella monkeys.

Previous studies in non-human primates have shown that tolerance to dystonia occurs during chronic dopamine D1 (D1) but not D2 antagonism and induction/aggravation of oral dyskinesia (TD) during D2 but not D1 antagonism. We were therefore interested in determining the effects of combined chronic D1 + D2 antagonism on dystonia and dyskinesia. To this intent, 8 male Cebus apella monkeys were treated 10 weeks with gradually increasing doses of D1 antagonist (NNC 112) + a D2 antagonist (raclopride), followed by 2 weeks of treatment with the D2 antagonist alone. Due to previous neuroleptic exposure, 5 monkeys had TD and all were sensitized to dystonia. During the combined antagonist treatment, tolerance to dystonia occurred; the tolerance disappearing upon discontinuation of the D1 antagonist and continuation of the D2 antagonist alone. Parallel to these results, improvement of TD was seen during the combined antagonist treatment with worsening during the D2 antagonist alone. Both the combined antagonists and the D2 antagonist alone resulted in moderate/severe bradykinesia, with no tolerance. These findings indicate that supplementation of traditional D2 antagonism with a D1 antagonist would lessen the risk of dystonia and allow alleviation of preexisting TD, though parkinsonian side effects might still occur. The findings further indicate that separate dopaminergic mechanisms control dystonia/dyskinesia and parkinsonism.

Animals↗

The substituted (S)-3-phenylpiperidine (-)-OSU6162 reduces apomorphine- and amphetamine-induced behaviour in Cebus apella monkeys.

Low affinity dopamine (DA) D2 antagonists such as the substituted (S)-3-phenylpiperidine (-)-OSU6162 have been proposed to be putative antipsychotic agents not endowed with extrapyramidal side effects (EPS). In the present study we investigated the effects of (-)-OSU6162 on (-)-apomorphine and d-amphetamine-induced behaviours in EPS sensitised Cebus apella monkeys. (-)-OSU6162 was administered subcutaneously in doses of 1, 3, 6 and 9 mg/kg alone and in combination with (-)-apomorphine (0.25 mg/kg) or d-amphetamine (0.5 mg/kg). (-)-OSU6162 inhibited (-)-apomorphine-(1-9 mg/kg) as well as d-amphetamine (3-9 mg/kg)-induced arousal and stereotypy. EPS did not occur when (-)-OSU6162 was administered in combination with (-)-apomorphine or d-amphetamine. However, when (-)-OSU6162 was administered alone, dystonia was observed at high doses (6 and 9 mg/kg) in two out of six monkeys. The present study shows that (-)-OSU6162 can inhibit (-)-apomorphine-induced behaviours in non-human primates at doses that do not cause EPS. When (-)-OSU6162 was tested against d-amphetamine-induced behaviours a separation between dose levels that inhibit d-amphetamine effects and cause EPS was not observed. The data further substantiate a role for low affinity DA D2 antagonists in the pharmacological treatment of psychosis.

Amphetamine↗

Understanding of the relationship between seeing and knowing by tufted capuchin monkeys (Cebus apella).

The ability of four tufted capuchin monkeys (Cebus apella) to recognize the causal connection between seeing and knowing was investigated. The subjects were trained to follow a suggestion about the location of hidden food provided by a trainer who knew where the food was (the knower) in preference to a trainer who did not (the guesser). The experimenter baited one of three opaque containers behind a cardboard screen so that the subjects could not see which of the containers hid the reward. In experiment 1, the knower appeared first in front of the apparatus and looked into each container; next, the guesser appeared but did not look into any containers. Then the knower touched the correct cup while the guesser touched one of the three randomly. The capuchin monkeys gradually learned to reach toward the cup that the knower suggested. In experiment 2, the subjects adapted to a novel variant of the task, in which the guesser touched but did not look into any of the containers. In experiment 3, the monkeys adapted again when the knower and the guesser appeared in a random order. These results suggest that capuchin monkeys can learn to recognize the relationship between seeing and knowing.

Adaptation, Psychological↗

Tufted capuchins (Cebus apella) attribute value to foods and tools during voluntary exchanges with humans.

This research examined exchange and value attribution in tufted capuchin monkeys ( Cebus apella). We presented subjects with opportunities to obtain various foods and a tool from an experimenter in exchange for the foods or tool in the subjects' possession. The times elapsed before the first chow biscuits were expelled and/or an exchange took place were recorded as the dependent measures. Laboratory chow biscuits, grapes, apples, and a metal bolt (a tool used to probe for syrup) were used as experimental stimuli. The subjects demonstrated the ability to recognize that exchanges could occur when an experimenter was present with a desirable food. Results indicate that subjects exhibited significant variation in their willingness to barter based upon the types of foods that were both in their possession and presented by the experimenter. Subjects more readily traded chow biscuits for fruit, and more readily traded apples for grapes than grapes for apples. During the exchange of tools and food, the subjects preferred the following in descending order when the probing apparatus was baited with sweet syrup: grapes, metal bolts, and chow biscuits. However when the apparatus was not baited, the values changed to the following in descending order: grapes, chow, and metal bolts. These results indicate that tufted capuchins recognize opportunities to exchange and engage in a simple barter system whereby low-valued foods are readily traded for more highly valued food. Furthermore, these capuchins demonstrate that their value for a tool changes depending upon its utility.

Animals↗

A Capuchin monkey (Cebus apella) recognizes when people do and do not know the location of food.

In a previous study, Kuroshima and colleagues demonstrated that capuchin monkeys (Cebus apella) learned to discriminate between a "knower" who inspected a box for food, and a "guesser" who did not. The aim of the present study was to specify whether the subjects learned a simple conditional discrimination or a causal relationship that seeing leads to knowing. In experiment 1, we introduced five types of novel containers to two subjects. Each container was of different shape and color. The subjects gradually learned to reach toward the container the knower suggested. In experiment 2, we diversified the behavior of the knower and the guesser. In experiment 3, in order to eliminate the possibility of discrimination based on differences in the magnitude and the complexity of two trainers, we equated their behaviors. One subject adapted to the novel behaviors of the knower and the guesser, successfully discriminating the two trainers. Thus this monkey clearly learned to use the inspecting action of the knower and the non-inspecting action of the guesser as a discriminative cue to recognize the baited container. This result suggests that one capuchin monkey learned to recognize the relationship between seeing and knowing.

Adaptation, Psychological↗

Do squirrel monkeys (Saimiri sciureus) and capuchin monkeys (Cebus apella) predict that looking leads to touching?

Squirrel monkeys (Saimiri sciureus) and capuchin monkeys (Cebus apella) were tested using an expectancy violation procedure to assess whether they use an actor's gaze direction, signaled by congruent head and eye orientation, to predict subsequent behavior. The monkeys visually habituated to a repeated sequence in which the actor (a familiar human or a puppet) looked at an object and then picked it up, but they did not react strongly when the actor looked at an object but then picked up another object. Capuchin monkeys' responses in the puppet condition were slightly more suggestive of expectancy. There was no differential responding to congruent versus incongruent look-touch sequences when familiarization trials were omitted. The weak findings contrast with a strongly positive result previously reported for tamarin monkeys. Additional evidence is required before concluding that behavior prediction based on gaze cues typifies primates; other approaches for studying how they process attention cues are indicated.

Animals↗

Watching the best nutcrackers: what capuchin monkeys (Cebus apella) know about others' tool-using skills.

The present work is part of a decade-long study on the spontaneous use of stones for cracking hard-shelled nuts by a semi-free-ranging group of brown capuchin monkeys (Cebus apella). Nutcracking events are frequently watched by other individuals--usually younger, less proficient, and that are well tolerated to the point of some scrounging being allowed by the nutcracker. Here we report findings showing that the choice of observational targets is an active, non-random process, and that observers seem to have some understanding of the relative proficiency of their group mates, preferentially watching the more skilled nutcrackers, which enhances not only scrounging payoffs, but also social learning opportunities.

Animals↗

Violent coalitionary attacks and intraspecific killing in wild white-faced capuchin monkeys ( Cebus capucinus).

During 12 years of observation, we have observed three confirmed and two inferred lethal coalitionary attacks on adult male white-faced capuchins ( Cebus capucinus) by members of two habituated social groups at Lomas Barbudal Biological Reserve, Costa Rica. In one case, an alpha male was badly wounded and evicted from his group, and when later found by his former groupmates he was attacked by several of them and died less than 24 h later. In two other cases, lone extra-group males were mobbed by adult and immature males of a bisexual group. One victim's abdomen was torn open and he died less than 24 h later. A second victim was quite badly bitten but may have escaped. The fourth and fifth cases resulted from intergroup encounters. One victim lost the use of both arms but may have survived, whereas the other died of unknown causes within an hour of the attack. The observed death rate from coalitionary aggression at our site is approximately the same as that reported for eastern chimpanzees. Because at least three of the five observed incidents involved large coalitions attacking lone victims, they support the general hypothesis that imbalances of power contribute to intraspecific killing in primates. However, the occurrence of lethal coalitional attacks in a species lacking fission-fusion social organization poses a challenge to the more specific version of the imbalance-of-power hypothesis proposed by Manson and Wrangham in 1991 to explain chimpanzee and human intergroup aggression.

Aggression↗