(Part I is here)
The mating season of 2013 was on. Monkey faces were turning redder all around. Both male and female rhesus macaques exhibit a reddening of their facial and ano-genital skin areas during this time of the year due to the rising levels of reproductive steroid hormones (androgens and estrogens, respectively).
It is at this time that many young males leave their natal groups and try to join new ones – to find new mates. Usually when they do so they join new groups relatively unobtrusively, at the periphery, without challenging the established dominance hierarchy among the resident males. This is why among rhesus macaques (at least on Cayo Santiago) male dominance rank is established via the seniority (or succession) rule. Males who have been in the group the longest, occupy the highest ranks. New arrivals take up the lowest positions and behave subordinately towards the rest of the males. As males higher-up in the dominance hierarchy die or emigrate to other groups (male may change groups several times during their lifetime), males below them in the hierarchy move up in rank. New arrivals have never been seen to fight for the alpha position on Cayo Santiago – they queue patiently to acquire higher-ranking slots.
This succession-based system of rank acquisition is unusual among primates that live in multi-male multi-female groups. Typically, the highest-ranking males in a group are young males in prime fighting condition. Fighting ability is often the key to get the alpha position because new males need to be able to overcome the incumbent alpha and also dominate all the other males who are already in the group. Unsurprisingly, in many primate species, males who become alphas are in better physical condition and are younger than males who do not become alphas. As they age their fighting ability declines and they are more likely to be challenged by in-coming young males. Rank and age usually show a bell-curve relationship – rank tends to increase as males approach adulthood, peaks in their prime years, after which it gradually (or sometimes, drastically) declines as fitter, stronger males take over.
Among rhesus macaques on Cayo Santiago, however, this is not what happens. Alpha rank is not related to fighting ability but to tenure length – the duration a male has resided in his group. Thus, males who are clearly past their prime can retain their alpha ranking despite the fact that there are many younger males in their group who could beat them in a one-on-one contest.
In the first few months on Cayo Santiago my observations matched what I read about the succession-based ranking system. Then as the mating season began, something odd happened. 11Z, the alpha male from a large, dominant group, Group R, decided it was time to leave his natal group and find new females to mate with elsewhere.
He didn’t travel very far at all. He began making regular and very visible, aggressive incursions into our study group, with which Group R interacts on a daily basis and ranges over in many of the same areas of the island. All the high-ranking males in our Group S were very much intimidated. Some of them tried to put up a fight and show him who’s boss. Given his temperament and domineering presence, however, any attempts to prevent him from settling in the group or to make him acknowledge the seniority of the resident high-rankers failed miserably. Before long he had established himself as the undisputed alpha male of his new group. Such a direct take-over of the alpha position by an immigrant has never before been documented on Cayo Santiago.
The females did not seem to mind this new order one bit. They were very keen on flirting with 11Z and he was the most sexually successful male in the group this mating season. He also sired the most infants of all the males in Group S, even though a rather large number of females got pregnant from males from other groups (ca. 61% of all infants born).
But these reproductive rewards did not come cost-free to the new alpha. By the end of mating season, in July, he was knackered. He had lost a lot of weight. His belly now had wrinkles, with skin hanging where before there was the fat that fueled his sexual marathon. Soon his ribs began to show a bit, too. The energetic costs of mating effort in rhesus are high and they seem to have hit 11Z particularly bad. He was the weakest he had been since immigrating and taking over the alpha position in Group S. If someone was going to make a move on him, this was the time.
The mating season had ended but the resident males still had a problem with their new alpha. For several days after the middle of July we lost track 11Z. Then on 23rd July we found him. Or whatever was left of him and his ego. He looked a shadow of his former self. Creeping on the edges of the group, hiding under bushes, skittish and afraid. He was no longer the alpha of the group. On closer inspection we saw wounds. A gash on the back of his head, a puncture not very far from his scrotum, on his rump, and a big tear on his inner thigh. The blood had already dried, for the most part, but several of the other males were still after him. On several occasions we witnessed prolonged chases, during which he was utterly defeated into retreat. Some of the lowest-ranking males in the group were now on the offensive, repeatedly targeting him for no particular reason. They wanted to really make sure he knew his new place – at the very bottom of the hierarchy of the group, which until a few days ago he dominated so successfully.
To avoid constant harassment, 11Z kept a low profile. He stayed at the fringes of the group, only going in to feed in the feeding corrals, when other higher-ranking males had finished eating and left the area. He didn’t get many social comforts, either. Nobody was grooming him now as he didn’t want to risk approaching the core of the group where most of the females were hanging out during resting times. Over the months after his overthrow, he continued to lose weight. His ribs were now becoming very, very, visible. Compared to his peak form at the start of the mating season, he could hardly have been a more different macaque.
Several months later during the annual trapping season in January 2014 we were able to catch our study subjects and weigh them. 11Z had lost a lot of weight since last year. Of all the males he had the highest relative weight loss, relative to early 2013 (14.7% loss). This was bad news because usually during the birth season (which was now coming to an end), following the energetically exhausting mating season, males try to gain weight so that they have enough energy stored for the next mating season. A month or so from the start of the mating season of 2014, 11Z was at a huge disadvantage – not only he was very low in rank but his energetic condition would not allow him to participate in mating as actively as he did in 2013. His immune system didn’t seem to be doing that well either. When in January 2014 we measured his neopterin concentrations, which are indicative of inflammation, viral or bacterial infections, or other unpleasantness, they were very high – the highest of all males in Group S, in fact.
The gamble that he took when immigrating into Group S by overtaking the alpha position was successful in the short term but a very poor decision in the long term.
On a personal level, watching this highly political drama unfold over several months in 2013 on Cayo Santiago was enthralling. 11Z was a very charismatic, if a little too cocky, monkey. It was difficult not to be drawn in. It was also a rare opportunity for me to try and understand what factors explain the occurrence of the succession-based rank-acquisition system among the males on Cayo. Why is it that males so rarely (if ever) challenge for the top position when they move into a new group? Are the costs higher than the potential benefits?
Having read several papers that discuss the various acquisition strategies of primates a key theme that emerges is that it’s all about relative costs and benefits. If the benefits of acquiring the alpha position quickly are high – i.e. a male can sire most infants in the group – then direct take-overs are more likely (provided the costs of that are not too great). But if the benefits of the alpha position are not that high (i.e. a male cannot monopolize reproduction in his new group) then there’s no pressure for him to challenge for the alpha slot so he doesn’t. In species that have seasonal breeding (like rhesus) it is difficult for one male to monopolize all reproduction, as many females come into estrous at the same time. He just cannot be in multiple places at once, guarding all females that are about to ovulate and conceive. As a result reproductive skew in rhesus groups on Cayo Santiago is low to moderate (typically less than about 30% top male paternity share) and although on average high rank has some advantages, the alpha males are not always the most reproductively successful males in their groups. Female choice also plays a role and many females prefer mating with males other than the alpha, further eroding any reproductive advantages that might come with the top-ranking position.
Yet, despite, this somewhat bleak outlook regarding the benefits of being alpha in rhesus macaques, 11Z seemed rather keen on it. And once he got to be alpha in his new group, he didn’t do too badly. The benefits he obtained were not very high (he sired only 4 infants of 27 born in the group this year) but they were still higher than what the other males got, with only five of the remaining 14 males in Group S siring any offspring at all.
So probably taking over the alpha position was the better option, compared to 11Z joining quietly at the bottom of the hierarchy. Why don’t other males do the same thing, then?
Perhaps it was the character of 11Z. He grew up as the son of a high-ranking female in the large Group R. Early on in his adulthood (in 2009) he participated in a series of revolutionary coalitions that led to the overthrow of the then alpha of that group. 11Z became the new alpha of his natal group and was remarkably successful in siring babies over the next few years. Before joining Group S he had already produced 37 infants, a number that puts him very near the top of the list of the all-time most reproductively successful males on Cayo Santiago. He never knew anything but success. Was there something about his personality, together with his strong physical condition, that made him more likely than other males to take risks?
And if the benefits of the alpha position in rhesus groups were really that low as to make males unwilling to challenge for it, why do they have to challenge for it in the first place? If something is not worth fighting over, why did we see so much resistance to 11Z’s entry to Group S, resistance than continued sporadically throughout the mating season and culminated in his overthrow in late July, by which time his condition had deteriorated significantly.
Seeing the resident males try to oppose 11Z during his tenure as alpha produced some other unexpected observations. On several occasions they seemed to join forces, acting together to attack him. This was another thing that rhesus macaques were not supposed to be doing – forming agonistic coalitions. Many primates have strong male-male bonds and they often act together against rivals. Such behavior was thought to be entirely absent in rhesus macaques, until in 2009 a series of events in Group R showed otherwise. That series of revolutionary coalitions, in which 11Z took part, was the first example of such behavior in this primate. Now several years later, in a different group, we were seeing more coalitions, also in the context of competition for social status, but this time 11Z was on the receiving end. The video below shows one such event from April, the mating season, when a coalition of 5 – 6 males, ganged up on 11Z, but after a few minutes gave up.
Even though we did not witness directly the events that led to his downfall in July, I suspect, on the basis of interactions observed before and after, that some sort of joint action by the other males in Group S played a part. And I think this type of behavior is also the key to understanding the succession-based system on Cayo Santiago. The benefits of the alpha rank are low but still worth fighting for. What dissuades most immigrant males from challenging for the alpha position are not the low benefits but the potential of experiencing high costs, as a result of coalitions of males acting together to keep the new males at the bottom of the hierarchy. The very large groups that form on Cayo Santiago, because of the provisioning, perhaps make this more common. Having more males per group than rhesus have in the wild might be producing a novel social environment and perhaps the succession-based rank-acquisition system is only the norm on this island, where monkeys are fed by people on a daily basis. Observations from Japanese macaques in groups, which are provisioned and from groups, which are not suggest that this might be true. In large, provisioned groups Japanese macaque males mostly queue for rank. All observations of direct take-overs of the alpha position have been observed in the smaller, naturally-foraging groups.
Of course, much of this is speculation. The case of 11Z is a single anecdote. To be able to evaluate some of these ideas we would need many more similar events to establish how the patterning of costs and benefits affect male strategies in groups of various sizes, and crucially also to collect detailed data on smaller, naturally-foraging groups of rhesus in Asia.
The months spent tracking 11Z and watching him succeed and lose provided some of the most interesting observations of animal behavior I’ve ever had the chance to witness. As is often the case, these observations led to more new questions than answers and perhaps that is the beauty of field work: it keeps you wanting to come back for more.
Read our paper describing these events in more detail (and with references to much of the background literature alluded to above) in the journal Behaviour.
New results from our rhesus study will also be presented at the IPS/ASP meeting in Chicago in August 2016. Find out which talks and posters will feature data on 11Z and the other males in Group S here.