This month in primatology (January 2016)

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Gratuitous photo of rhesus macaque juveniles doing a bit of rough-and-tumble play

We are only a month into 2016, and primatologists have been very busy! I’ve compiled a list of the most important/interesting/exciting/cool articles that have been released since the start of the year (in press/early view/advance access etc.). Papers that were released electronically in 2015 and have now been assigned to an actual issue in a journal are not counted. Obviously, this is a subjective list, reflecting my main interests in primatology (behavioural ecology & sociality) so no doubt many excellent studies that deal with topics I do not follow too closely are left out. I’ve organised the studies under several non-mutually exclusive categories – depending on the primary theme of each article.

Now that’s cleared up, here’s my primate-themed January reading list (in almost no particular order):

Sexual selection & reproductive ecology

Sexual Selection and the differences between the sexes in Mandrills (Mandrillus sphinx)

Male endocrine response to seasonally varying environmental and social factors in a neotropical primate, Cebus capucinus

Vocal complexity influences female responses to gelada male calls

Female chimpanzees adjust copulation calls according to reproductive status and level of female competition

Exaggerated sexual swellings in female nonhuman primates are reliable signals of female fertility and body condition

Consequences of a male takeover on mating skew in wild Sanje mangabeys

Maternal effects on offspring stress physiology in wild chimpanzees

Sex or power? The function of male displays in rhesus macaques

Social life

Obstacles and catalysts to peaceful coexistence in chimpanzees and bonobos

Sex and friendship in a multilevel society: behavioural patterns and associations between female and male Guinea baboons

Working the crowd: sociable vervets benefit by reducing exposure to risk

Strong, equitable and long-term social bonds in the dispersing sex in Assamese macaques

Experience-independent sex differences in newborn macaques: Females are more social than males

Adaptations for social cognition in the primate brain

Social behavior shapes the chimpanzee pan-microbiome

Competition

Effects of group size and contest location on the outcome and intensity of intergroup contests in wild blue monkeys

Social power, conflict policing, and the role of subordination signals in rhesus macaque society

Ecology & conservation

Feeding habitat quality and behavioral trade-offs in chimpanzees: a case for species distribution models

Spatio-temporal complexity of chimpanzee food: How cognitive adaptations can counteract the ephemeral nature of ripe fruit

Sympatric Apes in Sacred Forests: Shared Space and Habitat Use by Humans and Endangered Javan Gibbons (Hylobates moloch)

 

 

Journals checked for papers:

  • The discipline journals: American Journal of Primatology, International Journal of Primatology, Primates, American Journal of Physical Anthropology
  • Behavioural journals: Behavioural Ecology, Animal Behaviour, Behavioral Ecology and Sociobiology, Ethology, Behaviour, Hormones and Behavior, Physiology and Behavior
  • Broader journals: Current Biology, Science Advances, Nature Communications, Science, Science Advances, Nature, Scientific Reports, Biology Letters, Proceedings B, Proceedings of the National Academy of Sciences of the USA, Open Science, eLife, PeerJ, PLOSOne, Functional Ecology, Journal of Animal Ecology, Ecology and Evolution, Evolution
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New papers (9 – 16 Jan): crickets, tree frogs, and great tits

Comparing pre- and post-copulatory mate competition using social network analysis in wild crickets (open access article!)

The two types of mating competition – pre- and post-copulatory are usually seen as alternative tactics that male animals can adopt as they try to ensure they sire as many offspring as possible. This study, however, shows this not to be the case, at least in crickets. Using social network analysis, the authors found no trade-off between pre- and post-copulatory competition: males who fought each other more during pre-copulatory competition also interacted indirectly with one another later on, during the post-copulatory phase. The really interesting bit is how post-copulatory social networks were constructed. Males were linked to one another if they successfully mated (by transferring a batch of sperm in a spermatophore, a structure typical of insects) with the same female and were thus considered to be in sperm competition. Fighting off competitors was not an effective means from preventing them from copulating with particular females. The authors conclude their data support the idea that in species where males cannot monopolize mating, the evolution of alternative male phenotypes is unlikely. They also suggest that mating success can be a poor proxy for reproductive success, given that males who mate more often may lose out more paternity via sperm competition. A useful reminder for those of us, studying primate mating behaviour and mating success.

Male treefrogs in low condition resume signaling faster following simulated predator attack

Individuals that have less to loose are expected to take greater risks (especially when the reproductive payoffs of doing so may be significant). This study shows this to be true in male treefrogs as they called to attract mates. The time they took to resume calling (advertising themselves as potential mating partners to nearby females) after a simulated predator attack (grabbing the frog) was shorter in males who were in poor condition – i.e. low-quality males were willing to take greater risks in the face of potential predation. Some caveats apply (condition predicted response in only one of two years; old age did not predict shorter call resumption times, contrary to predictions) but the results provide a nice example of the how individual physical condition may affect risk-taking behavior and thus potentially affect male mating success.

To sing or not to sing: seasonal changes in singing vary with personality in wild great tits

Staying with the topic of signalling, this study adds another dimension to our understanding of what determines how much effort males put into advertising their presence to mates and competitors. Personality matters, too. Male great tits that were determined to be ‘faster explorers’ (i.e. less shy), increased their singing more during the periods their mate was most fertile and during periods of maximum maternal investment (egg laying and incubation). This contrasts with earlier ideas that faster explorers pay less attention to changes in their social environment than slow explorers. The increased singing of fast explorers during key stages of the reproductive cycle was also correlated with more fledged chicks. This finding supports the idea that greater singing activity may reflect the quality of the males or the territory they occupy but the exact mechanism that links male personality and their singing patterns to increased reproductive success remains an open question.

New papers (Jan 1-8, 2016)

In an effort to keep on top of all the exciting papers I want to read (in a perfect world)  or, at least, skim this year, I am starting a weekly-ish round-up of those that catch my eye.

In a descending order, here are my top picks published online (early view) since the start of this year:

The rise and fall of a male rhesus macaque: Part I

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Rhesus macaques are odd. Particularly, if you come to them from studying chimpanzees, which was true for me when, in late 2012, I went to Cayo Santiago, in Puerto Rico, to spend about 1.5 years with these monkeys.

In chimpanzees, males spend their entire lives in the group they were born into. They know each other well and some of them form strong affiliative bonds. In rhesus, males usually leave their natal group shortly after reaching puberty and immigrate into a new group where they will seek mates and reproduction. Unlike chimps, male rhesus macaques don’t seem to care about each other very much and male-male friendships are not known to exist. At best, most of them appear indifferent about their male group-mates. A stark contrast to the strong, cooperative, intense relationships I have seen among chimpanzee males. In both species males form clear linear dominance hierarchies but while among chimps there is intense aggressive competition for the alpha position, this is not the case among rhesus males. Instead, male rhesus macaques are known for an unusual system of rank-acquisition: they queue for rank rather than fight for it. It’s called succession-based rank-acquisition and each male start out at the very bottom when he moves into a new group. With time, as males above him in the hierarchy die or emigrate to other groups, the rank of the newcomer increases, until eventually he may get to the alpha spot. This was the picture I got from all the papers I read about rhesus macaques before travelling to Puerto Rico.

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Cayo Santiago – off the coast of Puerto Rico is home to ca. 1,300 – 1,400 rhesus macaques.

I spent October and November 2012 figuring out who is who in my study group and how they interact with each other. It was the non-mating season. Most females had already given birth in the preceding months and were raising their infants. The males spent most of their time relaxing, feeding and not doing much else. Although the literature had prepared me for what I saw – I was still surprised to see how little they engaged with each other. Very little grooming, little proximity, just a lot of aloofness. If chimpanzee males were like the raucous members of a football team who, most of the time, got along splendidly, enjoyed each other’s company and did things together for the fun of it, rhesus males, on first impressions, were just a bunch of random guys hanging out at the doctors’ waiting room – respectful of each others’ space, polite but somewhat cold and indifferent to one another*.

(*Beware the anthropomorphisms! This is clearly a simplified/exaggerated description of male social relationships but it does convey my subjective impression of the differences between these two species.)

Trying to figure out the male dominance hierarchy in my rhesus study group (Group S) wasn’t as easy as I expected. There were few clear indications of who was the alpha and where each male fitted in the hierarchy. I talked to other researchers and staff of the Caribbean Primate Research Center to get their perspective and I collected data on even the subtlest agonistic (non-friendly) interactions between males that I could discern. One such subtle signal of existing dominance relations is the so-called approach-avoid interaction. One male would be walking in the general direction of another male and the other would actively avoid him by moving to the side and away – even in the absence of any specific threat from the approaching male. The one who avoids is lower down the hierarchy than the one who is approaching. Another good sign of high rank was the way an alpha would ‘carry’ himself around the group. I would have to watch the body language of my male study subjects closely. The alpha would appear confident, strutting casually around, with an air of superiority, his tail curled up in a twirl above his back. I could occasionally notice these telltale signs in the male, who everyone who knew this group of monkeys told me was the alpha – the one called 53N.

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53N – the alpha in Group S at the start of my study

Yet he was surprisingly nonplussed about being alpha. None of the bravado that I came to expect from an alpha male, based on my experience with the Kanyawara chimpanzees that I studied a few years back in Uganda. He did not constantly run around the group, showing off his strength and intimidating rivals. Nor did other males acknowledge his superiority in the ranking by ritualized signals of submission such as a pant-grunt (a common and useful vocal signal for studying chimpanzee dominance relations but completely absent in rhesus). In short – 53N was a very relaxed alpha male.

He had immigrated into Group S about 4.5 years ago. The two other males at the top of the hierarchy had moved into Group S at about the same time – within a month or two at most of each other. All three of them were born in the same group and they were the oldest (at just over 13 years of age) males in their current group – Group S. These three males were at the top of the tenure-based queue of succession – the mean tenure length (the duration of time they had spent in the group) of the remaining 6 immigrant males was 1.7 years (between 0.5 – 3.9 years, calculated as of 1st March 2013). The males of Group S thus presented a textbook example of male dominance relations in rhesus macaques – the males who had been in the group the longest occupied the highest ranks. The males who had joined the group just recently – were the lowest ranking ones.

The three oldest males in the group (53N, 48L, and 03N) had clearly spent most of their lives in each other’s company yet they showed surprisingly little indication of any sort of long-term bonding or friendliness (again, in comparison to the easily observable signs of such bonds among male chimpanzees). Interestingly, there were also very few clear signs of competitiveness or aggression among these three top-ranking males. It was almost as if they existed in parallel realities, barely acknowledging each other’s existence. Perhaps this was because the mating season was still a couple of months away and there was nothing to fight over just yet.

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The mating season on Cayo Santiago. Both sexes develop more intense/redder coloration on their faces and around their genitals – a form of sexual signaling.

By mid-February 2013, ‘love’ was in the air. Mating begins at slightly different times in the different groups of rhesus on Cayo Santiago. I saw my first rhesus macaque copulation sometime in January in one of the groups on the lower parts of the island. Mating in our study group on the top of the hill, however, did not properly get going until the end of February/early March. It was then, at the start of mating season that something quite unexpected happened.

To be continued: Part II