Primate Dominance Hierarchies

Cross references:  Dominance Hierarchies in General

The ABC's of Chimpanzee Behavior: Jane Goodall  (Goog) 
Very informative webpage available online for free. 
   
    Hierarchy & Dominance
(from Jane Goodall, above)          "Among the 50 or so members of a chimpanzee community, one adult male is recognized as the highest-ranking or "alpha" male. While several males may exercise dominance over other males, the alpha male is dominant over all the members of the community, male and female. He attains his high-ranking position through intimidation, strength, and intelligence, often exhibited in "dominance displays." "      

    Aggression
(from Jane Goodall, above)           "It is true that chimpanzees, particularly when traveling in small, compatible groups, may maintain peaceful relationships for hours or days. Nevertheless, they can easily be roused to sudden violence, particularly during social excitement. While most fights do not lead to wounding, some certainly do-particularly those directed at individuals of neighboring social groups."      

    Submission (from Jane Goodall, above)      

    "A submissive chimpanzee lets the aggressor know that he or she is not a threat through non-threatening postures such as presenting their back, crouching and bowing in front of the threatening chimpanzee, or bobbing. The submissive chimpanzee will approach the dominant chimpanzee with a fear grin on its face. It is attempting to present itself to the hostile chimpanzee as small and non-threatening. The aggressor will in turn allow the victim to move closer to him. Often he will gently touch the other chimpanzee’s back, arm, or hand. Submissive postures and gestures are often accompanied by vocalizations such as grunts, squeaks, whimpers, or screams depending on the amount of distress the chimpanzee is experiencing."         

    Territoriality
(from Jane Goodall, above)       "As they grow older, male chimpanzees follow along with adult males patrolling the periphery of the community. Members of the patrol look for members of another community that strayed into their area. They move cautiously across the ground in a tight group formation. The ground, leaves, and tree trunks are sniffed for signs of a stranger. They stop frequently to climb tall trees, gaze, listen, and look over the area of a neighboring group. The chance discovery of a fresh night nest causes alarm. The nest is destroyed while making intimidating gestural, vocal, and postural displays. If a stranger is not encountered the patrol party returns to its home territory. If the patrol runs into strangers, with roughly equal numbers of males, a vigorous display with vocal threats such as pant-hooting, roaring pant-hoots, and waa-barks ensues. Most of the time, after making a lot of noise, one party will retreat to their core area. If the patrol encounters a stranger, aggression may occur."      

    War
(from Jane Goodall, above)       "Dr. Jane's once peaceful-seeming chimpanzees were heavily engaged in what amounted to a sort of primitive warfare during the years of 1974-1977. It had begun when the chimpanzee community began to divide. Seven adult males and three mothers and their offspring began spending longer and longer periods of time in the southern part of the range over which the whole community roamed. By 1972, it was obvious that these chimpanzees had formed an entirely new and separate community, which became known as Kahama. When males of the two communities encountered one another in the overlapping zone between the two, they threatened one another in a typical territorial behavior. However, a series of deadly brutal attacks perpetrated by the powerful Kasekela community on individuals of the Kahama community followed. It was known as the Four-Year War at Gombe."  


Male Social Behavior and Dominance Hierarchy in the Sulawesi Crested Black Macaque (Goog) 
www.springerlink.com/index/0npnnp9tyd1wt9j6.pdf
Only abstract available online.  Unable to obtain PDF through the library.   
    "
In a 6-week study of the social behavior of wild Sulawesi crested black macaques (Macaca nigra), we found a linear and transitive dominance hierarchy among the six adult males in one social group. Dominance rank, as determined by the direction of supplantations, correlated strongly with percentage of time near more than four neighbors, frequency of grooming received from adult females, and percentage of time with an adult female as nearest neighbor.

    "
Frequency and intensity of aggression between males are strongly correlated with rank distance ...



Primate models to understand human aggression  (PubMed) 
http://www.ncbi.nlm.nih.gov/pubmed/10418812 
Only abstract available online.  No PDF or HTML available.   
    "
... studies of aggression in rhesus monkeys point to 2 chief categories of aggression--defensive and offensive--and suggest differing underlying neural mechanisms for these types of behaviors. Defensive aggression is fear motivated and related to extreme asymmetric right frontal activity in the brain and high
plasma cortisol concentrations. On the other hand, offensive and/or impulsive aggression is associated with low serotonergic activity in the central nervous system, high levels of testosterone, and lower levels of cortisol.


Asymmetric frontal brain activity, cortisol, and behavior associated with fearful temperament in rhesus monkeys  (PubMed) 
http://www.ncbi.nlm.nih.gov/pubmed/9588478   
Only abstract available online.  I got the PDF from the library. 
from the abstract     
    "The authors first showed that individual differences in asymmetric frontal electrical activity are a stable characteristic. Next, the authors demonstrated that relative right asymmetric frontal activity and cortisol levels are correlated in animals 1 year of age. Additionally, extreme right frontal animals had elevated cortisol concentrations and more intense defensive responses.  
    At 3 years of age, extreme right frontal animals continued to have elevated cortisol concentrations.

 



Plasma testosterone and male dominance in a Japanese macaque (Macaca fuscata) troop compared with repeated measures of testosterone in laboratory males (Goog) 
Only abstract available online.    I got the PDF through the library. 
from the abstract   
    "
Plasma testosterone levels measured by radioimmunoassay did not correlate with dominance rank or aggressive behavior in 21 adult males of a natural troop of Japanese macaques (Macaca fuscata). The data were replicated during two consecutive breeding seasons. Levels of male dominance and aggressive behavior were highly correlated from year to year, but testosterone levels of individual males were not.
"    
My comment
If this was a stable group, then perhaps the dominance hierarchy had already been established.  Endocrine levels seem to correlate with behavior while the dominance hierarchy is being established, but not once it is finalized.   


Styles of dominance and their endocrine correlates among wild olive baboons (Goog) 
Only abstract available online.  I got the PDF from the library. 
from the abstract  
    "
We have studied the relationship between dominance rank and physiology among male olive baboons (Papio anubis) living freely in a national park in Africa. In stable hierarchies, dominant males consistently have lower basal concentrations, than do subordinates, of the adrenal glucocorticoid cortisol. ...
    We find that low basal cortisol concentration is not, in fact, a marker of social dominance; instead, it is only found among dominant males with a certain style of dominance.
    Lower basal cortisol concentrations occurred among males with any of the following behaviors:
    the most marked ability to distinguish between threatening and merely neutral interactions with rivals and, if the former, the greatest likelihood of initiating a fight;
    the most skill at distinguishing between winning and losing a fight and, if the latter, the greatest likelihood of displacing aggression onto a third party.
    Collectively, these behaviors suggest high degrees of social skillfulness, control, and predictability over social contingencies ... Dominant males lacking these behavioral features, in contrast, had as high cortisol concentrations as did subordinate males.
    Finally, low basal cortisol concentrations were also a feature of males with the longest tenures in the dominant cohort, suggesting that this endocrine dichotomy is meaningful in terms of life histories.
"  
My comment
Only those dominant males that had good social skills and/or had been dominant for a long time had low cortisol levels.  The cortisol levels of dominant males with poor social skills and/or who had been dominant for only a short time were no different from the cortisol levels of subordinates. 



Relationship between dominance hierarchy, cerebrospinal fluid levels of amine transmitter metabolites (5-hydroxyindole acetic acid and homovanillic acid) and plasma cortisol in monkeys.
(Goog)  
    
Only abstract available online.  I got the PDF through the library. 
from the abstract   

    "The dominance hierarchy has repercussions for a monkey's sexual behaviour and endocrine state. Here we report on neural mechanisms that are sensitive to a monkey's status in the social hierarchy, and which may regulate not only its endocrine function but its sexual responsiveness to its own hormones.
    During the initial phase of group formation, 5-hydroxyindole acetic acid, the metabolite of serotonin, increases in the cerebrospinal fluid of monkeys which become subordinate (all groups), but decreases in monkeys which become dominant (two out of three groups) and shows no changes in intermediate-ranking animals (five out of seven).
    Homovanillic acid, a metabolite of dopamine, may also increase in the cerebrospinal fluid of monkeys that become subordinate (two out three groups).
    In the initial period of group formation these changes in transmitter metabolites do not parallel changes in cortisol. However, in the established social groups, both 5-hydroxyindole acetic acid and plasma cortisol are related to the social hierarchy, being greater in those monkeys that are subordinate, but homovanillic acid shows no consistent change.
    Although subordinate monkeys receive more aggression than others in their group, fluctuations in 5-hydroxyindole acetic acid do not correlate with aggressive behaviour, and are equally high on days when no aggression occurs.
    Dominant males, however, had higher 5-hydroxyindole acetic acid levels on days when they were involved in agonistic encounters. In the established social hierarchy therefore, elevated levels of the serotonin metabolite in cerebrospinal fluid seem reflect a "state"-dependent consequence of occupying a position of low social status.
"  



Hypercortisolism associated with social subordinance or social isolation among wild baboons.  (Goog)  
Both abstract and PDF available online, but it is possible to copy-and-paste only from the abstract. 
    abstract   
    from the abstract   
    "Our findings indicate that social status and degree of social affilitation can influence adrenocortical profiles; specifically, social subordinance or social isolation were associated in our study with hypercortisolism
"   
    transcribed from the PDF   
    "Hypercortisolism ... occurs in approximately half of the individuals (humans) with affective disroders ..."  
    "In the adrenocortical axis, elevated circulating glucocorticoid concentrations exert a negative feedback effect, inhibiting subsequent secretion.  Repeated stressors can cause glucocorticoid feedback resistance ..."  
    "In stable dominance hierarchies ... subordinance is associated with far more stressors than is dominance ... "    
    "... studies ... demonstrate the power of social proximity or affiliation to blunt the adrenocortical response to various stressors."    
    "... role played by dominance interactions ... in reducing social tension and maintaining cohesion within the social group."    


Serotonergic modulation of behaviour, a phylogenic overview. (PubMed) 
Abstract only.  I got the 35 page PDF from the library.  
from the PDF
   
    "Serotonin also appears to modulate complex social behaviour in primates. Raleigh et al. (1991) explored the role of serotonin on dominance status in vervet monkeys (Cercopithecus aethiops sabaeus).  In these animals, male dominance appears to depend more on the formation of alliances with female group members than on individual fighting ability. 
    At the beginning of the study, stable mixed-sex groups were established; each group contained one dominant and two subordinate males. The dominant male was removed and one of the two remaining males received a drug that affected the serotonergic system. Fenfluramine, which acts as an indirect agonist in the short term but causes serotonin depletion in the long term, or cyproheptadine, a serotonergic receptor antagonist, were used to suppress serotonergic function. Tryptophan, a serotonin precursor, or fluoxetine, a reuptake inhibitor, were used to enhance serotonergic function. 
    Fenfluramine and cyproheptadine decreased affiliative behaviours (approaching, grooming and proximity), while aggressive behaviour increased; animals receiving these treatments invariably remained subordinate. Tryptophan and fluoxetine increased affiliative behaviours and decreased aggression; animals receiving these treatments invariably became dominant. 
    In this example, it appears that serotonergic suppression of aggressive behaviour promotes dominance.  However, the long-term effects of drugs intended to diminish or enhance serotonergic function are not fully understood. For example, fluoxetine is a serotonin reuptake blocker, and in the short term it should increase the amount of serotonin in synaptic clefts or extracellular fluid.  However, this increase in serotonin will enhance activation of autoinhibitory receptors and may cause down regulation of
postsynaptic receptors. In the long term, it is difficult to determine whether serotonergic function will remain elevated.
    Similar arguments could be applied to the other drugs used in this study. Raleigh & McGuire (1991) noted that the effects of tryptophan on aggressive behaviour vary for animals in different social circumstances.  Dominant animals in a social group, subordinate animals in a group, and animals living in isolation differ in the degree and even the direction of their response to tryptophan.  Nonetheless, it is clear that drugs that affect serotonergic function also affect affiliative and aggressive behaviour and can lead to changes in dominance status."  
    "Yodyingyuad et al. (1985) examined the relationship of serotonergic function to dominance status in talapoin monkeys (Miopithecus talapoin). They measured levels of 5-HIAA (5-hydroxyindoleacetic acid, a serotonin metabolite) in the CSF of monkeys before and after the formation of social dominance hierarchies as well as in established hierarchies.
    They found that when a group of monkeys is placed together, 5-HIAA levels fall as a monkey becomes dominant and rise as a monkey becomes subordinate.  Monkeys who assume intermediate positions show no consistent changes in CSF 5-HIAA. 
    In established groups, the top-ranking monkeys have significantly lower 5-HIAA levels than intermediate or low-ranking monkeys, who do not differ significantly from each other. No correlation was found between levels of homovanillic acid (a dopamine metabolite) and position in the dominance hierarchy. 
    As with the work on vervet monkeys, this study clearly supports a link between the central serotonergic system and dominance status.  At first glance, reduced CSF 5-HIAA levels might suggest lowered central serotonin levels and diminished serotonergic function. However, many factors could potentially affect 5-HIAA levels as well as the ratio of serotonin  to 5-HIAA in the brain.
    Decreased release of serotonin, which would diminish serotonergic function, would lower 5-HIAA; reduced serotonin degradation, which would enhance serotonergic function, would also lower 5-HIAA. For example, juvenile mice lacking functional monoamine oxidase type A (MAOA), which degrades serotonin as well as other amines, have increased levels of brain serotonin and reduced levels of 5-HIAA (Cases et al., 1995). Agonistic encounters can raise the ratio of 5-HIAA to serotonin in the amygdalas of inexperienced mice; this observation suggests that situations that result in serotonin release may alter this ratio in the short term (for review see Miczek et al., 1994).  Chronically raised or lowered levels of 5-HIAA indicate alterations in the serotonergic system, but it is difficult to say whether overall serotonergic function is enhanced or diminished."
   
My comment
This is a long (35 page) paper on serotonin as a neurotransmitter throughout evolution.  For discussion of serotonin in non-primates, see:  
Neurotransmitter Evolution  .  



Stress-Induced Suppression of Testicular Function in the Wild Baboon: Role of Glucocorticoids (Goog) 
Full length HTML and PDF available online for free. 

Anabolic steroids and aggressive behavior in cynomolgus monkeys.  Behavior Medicine.  
http://www.ncbi.nlm.nih.gov/pubmed/3367374 
Only abstract available online.  I got the PDF through the library.   
 

CSF testosterone and 5-HIAA correlate with different types of aggressive behaviors.
http://www.biologicalpsychiatryjournal.com/article/PIIS0006322395006753/abstract 
Only abstract available online.  I got the PDF through the library.   

Adolescent impulsivity predicts adult dominance attainment in male vervet monkeys.  
http://www.ncbi.nlm.nih.gov/pubmed/15356854 
Only abstract available online.   
 

Excessive mortality in young free-ranging male nonhuman primates with low cerebrospinal fluid 5-hydroxyindoleacetic acid concentrations. 
http://www.ncbi.nlm.nih.gov/pubmed/8639037 
Only abstract available online.    
 

Urinary testosterone-metabolite levels and dominance rank in male and female bonobos (Pan paniscus).  
http://www.ncbi.nlm.nih.gov/pubmed/14689314 
Only abstract available online.  I got the PDF through the library.    
 

Social parameters and urinary testosterone level in male chimpanzees (Pan troglodytes).
http://www.ncbi.nlm.nih.gov/pubmed/15465534 
Only abstract available online.  I got the PDF through the library.   


Hypercortisolism among socially subordinate wild baboons originates at the CNS level (PubMed) 
Only abstract available online.   No PDF through the library.   



Testosterone predicts future dominance rank and mating activity
among male chacma baboons (Goog) 
Full length PDF available online for free.  Must download to copy-and-paste.   

Mating sequence, dominance and paternity success in captive
male tammar wallabies (Goog) 
Full length PDF available online for free.  Must download to copy-and-paste. 
Full length HTML available online for free. 

 
Dominance, aggression and testosterone in wild chimpanzees:
a test of the ‘challenge hypothesis’ (Goog) 
Full length PDF available online for free.  Must download to copy-and-paste. 
 

Endocrine and behavioral correlates of drought in wild olive baboons (Goog)
Only abstract available online.    I got the PDF from the library.   


Styles of male social behavior and their endocrine correlates among high-ranking wild baboons (Goog) 
Only abstract available online.  I got PDF from the library. 

Styles of Male Social Behavior and Their Endocrine Correlates Among Low-Ranking Baboons (Goog) 
Only abstract available online.  I got PDF from the library.  



CSF testosterone and 5-HIAA correlate with different types of aggressive behaviors.  (PubMed)  - 1996   
Only abstract available online. 
    "
We studied the potential roles of testosterone and serotonin in various forms of aggressive and violent behaviors by measuring each biochemical and behaviour in free-ranging adolescent male nonhuman primates.   Our results showed that  
    (1) CSF free testosterone concentrations were positively correlated with overall aggressiveness, but not with measures of impulsivity.  
    (2) CSF 5-HIAA concentrations were negatively correlated with impulsive behavior, and severe, unrestrained aggression, but not with overall rates of aggression. High rates of impulsive behavior were positively correlated with severe, unrestrained aggression, but not overall rates of aggression.  
    (3) Dimensional analyses showed that while subjects with low CSF 5-HIAA exhibited high rates of aggression, high CSF testosterone further augmented rates and intensity of aggression in subjects with low CSF 5-HIAA.  
    We conclude that high CSF free testosterone concentrations are associated with competitive aggression, while low CSF 5-HIAA concentrations are associated with severe aggression which results from impaired impulse control, and perseverance.
"  
 
   
   
34. Comment on the article: CSF testosterone and 5-HIAA correlate with different types of aggressive behaviors


Comment on the article: CSF testosterone and 5-HIAA correlate with different types of aggressive behaviors Biol Psychiatry 1997;42:305-7)" 

    "Although studies link high levels of testosterone to aggression, this hormone alone does not account for aggressive behavior. In fact, successful athletes and businessmen tend to have high testosterone levels, without being any more violence-prone than their low testosterone counterparts, indicating that testosterone may not act alone in promoting aggression. Rather, aggressive men's behavior may be influenced by high testosterone levels combined with low levels of the brain chemical serotonin.  Testosterone is linked more strongly to dominance in general than to aggression." 
 



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