New results from our Cayo Santiago rhesus study at IPS/ASP 2016 in Chicago!

IMG_5715

My collaborators and I have four presentations at the Congress that will feature data from our study in Group S on Cayo Santiago, mostly collected during the unusual tenure of 11Z as alpha (mating season 2013).

On Monday, Megan Petersdorf (NUY) will talk about male facial colour and male-male competitive encounters

On Tuesday, Kevin Rosenfield (Roehampton Uni/Penn State) will talk about how females prefer looking at more masculine-faced males and then on Thursday, he will do a poster on the relationship between male face shape (width-to-height ratio) and male competitive ability and reproduction.

Finally, on Friday, I will have some data on male androgen levels and how they relate (or not) to rank, mating effort and fecundity.

Come and check them out!

 

You can also have a look at some related papers from my work on Cayo below:
(email me for a PDF if you don’t have access)

Breaking the succession rule: The costs and benefits of an alpha-status take-over by an immigrant rhesus macaque on Cayo Santiago

Oxidative stress as an indicator of the costs of reproduction among free-ranging rhesus macaques

Male quality, dominance rank and mating success in free-ranging rhesus macaques

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

(Part I is here)

IMG_5512The 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.

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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.

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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.

All the chimp (and one bonobo) presentations to see at the #AAPA2016 meeting

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More or less in the order in which they appear in the program, here are all the chimpanzee (and the only one bonobo) behavioral ecology talks & posters to watch out for next week in Atlanta.

Research from Kibale (Kanyawara & Ngogo) and Gombe (Uganda and Tanzania, respectively) dominate the program, as usual, but there are also new data from Fongoli (Senegal) and the Goualougo Triangle (Congo)!

There are also some fascinating comparative studies that explicitly compare data on chimpanzee and human physiology and life history variation. Must-see!

(click on title for abstract and other info)

Dominance styles of eight alpha male chimpanzees at Gombe National Park, Tanzania

Relationship of dominance ranks to age and coalition formation among male chimpanzees at Ngogo

Dominance Rank, Male-Female Aggression, and Male Mating Success Among Chimpanzees at Ngogo

Predation by female chimpanzees at Gombe and Kibale: toward an understanding of sex differences in meat acquisition among early hominins

The diet of savanna-woodland chimpanzees (Pan troglodytes schweinfurthii) at Issa, western Tanzania

Chimpanzee laterality redux

Alternative reproductive tactics among male chimpanzees in Gombe National Park, Tanzania

Chimpanzees and the phylogenetic origins of multi-level sociality in humans

Parasite infections reveal costs and benefits of social behavior in a community of wild chimpanzees

Adolescent male chimpanzees do not form a linear dominance hierarchy with their peers

Social bonds in adolescent and young adult male chimpanzees at Ngogo, Kibale National Park, Uganda

Rethinking chimpanzee tool use: Niche construction and developmental bias in maintaining technological traditions among African apes

Comparing the spatial dimensions of gorilla and chimpanzee sleeping sites: Nearest-neighbor nest distances of sympatric apes along a conservation gradient

Paternal age at conception predicts offspring telomere length in chimpanzees to a greater degree than in humans

Dynamics of human-chimpanzee encounters at Fongoli, Senegal, 2006-2014

Nutritional composition of plant foods consumed by the chimpanzees of Gombe National Park, Tanzania

Low Mortality Rates among Ngogo Chimpanzees: Ecological Influences and Evolutionary Implications

Somatic senescence in female chimpanzees (Pan troglodytes) occurs earlier and more rapidly than in women

Hormonal Correlates of Sexual Swellings During Pregnancy in Wild Chimpanzees (Pan troglodytes schweinfurthii) of Kanyawara and Gombe

New data on female maturation milestones indicate longer development in wild chimpanzees

Testosterone, musculature, and development in Kanyawara chimpanzees and Tsimane forager-horticulturalists

Fecal stable isotopes (δ13C:δ15N, %N) used to track infant nutritional development and reveal average weaning age in wild chimpanzees

Infant handling and urinary oxytocin in sub-adult bonobos (Pan paniscus): support for the learning to mother hypothesis

 

Macaques at the AAPA meeting (2016)

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Fan of macaques? Here are all the talks & posters you need to see at the AAPA meeting next week. Clink on titles to go to the abstract (with info on time and location of the presentation).

And follow the conference on Twitter (#AAPA2016)

Rhesus macaques

Social status, seasonality, and stress: Variation in glucocorticoid concentrations of high-ranking male rhesus macaques (Macaca mulatta)

Life in a new world: The Silver River rhesus macaques’ feeding ecology and encounters with humans

Infant weight growth and weaning age in free-ranging rhesus macaques (Macaca mulatta)

Evidence that male face shape in rhesus macaques (Macaca mulatta) is subject to inter-sexual selection

Maternal body composition predicts prepubertal fat mass accrual in female offspring

 

Other macaques 

Social Network Analysis of Stone Handling and Object Manipulation Among Long-Tailed Macaques (Macaca fascicularis) in Bali, Indonesia: A Preliminary Analysis

Network Position and Human Presence in Barbary Macaques of Gibraltar

Social network analysis of Barbary macaque (Macaca sylvanus) dominance structure

Object preferences and the function of object play behavior in a provisioned troop of long-tailed macaques (Macaca fascicularis) at Wat Khao Takieb, Thailand

The Monkeybar Project: Population Density of Long-Tailed Macaques (Macaca fascicularis) in Two Different Forest Types in Kudat District, Sabah, Malaysia

Comparison of the vaginal, fecal, and rectal microbiome in captive Pigtailed Macaques (Macaca nemestrina)

Using ancient DNA from museum specimens for phylogenetic correction to interpret island dwarfing in Macaca fascicularis

 

This month in primatology (Feb 2016)

At the end of February, here’s a non-exhaustive list of papers on primate behavioral ecology from across a variety of journals.

Dominance relations & social competition

The effect of intergroup competition on intragroup affiliation in primates
http://www.sciencedirect.com/science/article/pii/S0003347216000129

Dominance relationships in male Nepal gray langurs (Semnopithecus schistaceus)
http://onlinelibrary.wiley.com/doi/10.1002/ajpa.22958/abstract

The dark side of the red ape: male-mediated lethal female competition in Bornean orangutans
http://link.springer.com.turing.library.northwestern.edu/article/10.1007/s00265-015-2053-3

Breaking the succession rule: the costs and benefits of an alpha-status take-over by an immigrant rhesus macaque on Cayo Santiago
http://booksandjournals.brillonline.com/content/journals/10.1163/1568539x-00003344

Obstacles and catalysts of cooperation in humans, bonobos, and chimpanzees: behavioural reaction norms can help explain variation in sex roles, inequality, war and peace
http://booksandjournals.brillonline.com/content/journals/10.1163/1568539x-00003347

Sex

Promiscuous primates engage in same-sex genital interactions
http://www.sciencedirect.com/science/article/pii/S0376635716300377

 

Communication

Enduring voice recognition in bonobos
http://www.nature.com/articles/srep22046

Bonobos (Pan paniscus) vocally protest against violations of social expectations
http://psycnet.apa.org/index.cfm?fa=buy.optionToBuy&id=2016-07004-003

Social familiarity affects Diana monkey (Cercopithecus diana diana) alarm call responses in habitat-specific ways
http://rsos.royalsocietypublishing.org/content/3/2/150639

Food-Associated Calling in Gorillas (Gorilla g. gorilla) in the Wild
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0144197

Copying hierarchical leaders’ voices? Acoustic plasticity in female Japanese macaques
http://www.nature.com/articles/srep21289

 

Life history & development

Weaned age variation in the Virunga mountain gorillas (Gorilla beringei beringei): influential factors
http://link.springer.com/article/10.1007/s00265-016-2066-6

Male Infanticide in the Golden Snub-Nosed Monkey (Rhinopithecus roxellana), a Seasonally Breeding Primate
http://link.springer.com/article/10.1007/s10764-016-9892-2

Infant Mortality Risk and Paternity Certainty Are Associated with Postnatal Maternal Behavior toward Adult Male Mountain Gorillas (Gorilla beringei beringei)
http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0147441

Early-life social adversity and developmental processes in nonhuman primates
http://www.sciencedirect.com/science/article/pii/S2352154615001448

Non-Maternal Infant Handling in Wild Formosan Macaques of Mount Longevity, Taiwan
http://www.karger.com/Article/Abstract/443307

 

Social networks, sociality, cooperation

Social structure and Escherichia coli sharing in a group-living wild primate, Verreaux’s sifaka
http://bmcecol.biomedcentral.com/articles/10.1186/s12898-016-0059-y

Network centrality and seasonality interact to predict lice load in a social primate
http://www.nature.com/articles/srep22095

Bystanders, parcelling, and an absence of trust in the grooming interactions of wild male chimpanzees
http://www.nature.com/articles/srep20634

The ties that bind: Maternal kin bias in a multilevel primate society despite natal dispersal by both sexes
http://onlinelibrary.wiley.com/doi/10.1002/ajp.22537/abstract

 

Culture & innovation

Chimpanzee accumulative stone throwing
http://www.nature.com/articles/srep22219

The reluctant innovator: orangutans and the phylogeny of creativity
http://rstb.royalsocietypublishing.org/content/371/1690/20150183

The coevolution of innovation and technical intelligence in primates
http://rstb.royalsocietypublishing.org/content/371/1690/20150186

Animal and human innovation: novel problems and novel solutions
http://rstb.royalsocietypublishing.org/content/371/1690/20150182

A multidisciplinary view on cultural primatology: behavioral innovations and traditions in Japanese macaques
http://link.springer.com/article/10.1007/s10329-016-0518-2

 

Ecology, variation & conservation

Nutritional consequences of folivory in a small-bodied lemur (Lepilemur leucopus): Effects of season and reproduction on nutrient balancing
http://onlinelibrary.wiley.com/doi/10.1002/ajpa.22952/abstract

Adapting to Florida’s riverine woodlands: the population status and feeding ecology of the Silver River rhesus macaques and their interface with humans
http://link.springer.com/article/10.1007/s10329-016-0517-3

South to south learning in great ape conservation
http://onlinelibrary.wiley.com/doi/10.1002/ajp.22531/abstract

Is Tickling Torture? Assessing Welfare towards Slow Lorises (Nycticebus spp.) within Web 2.0 Videos
http://www.karger.com/Article/FullText/444231

Chimpanzee research and conservation in Bossou and the Nimba Mountains: a long-term international collaborative effort in West Africa
http://link.springer.com/article/10.1007/s10329-016-0519-1

 

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

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

 

Gorillas in black and white

The BBC breaks new ground (yet again) in a two-part documentary about Grauer’s gorillas and the quest of cameraman Gordon Buchanan to film them in the Democratic Republic of Congo.

For the first time, we see what these rare gorillas do at night in their nests up in the trees. Sensitive night-vision cameras reveal their activity in amazing detail. It’s a delightful programme. The night-time visuals are so good you can actually ‘see’ the breath of the dozing ape –  by the subtle, rhythmic changes in the intensity of the colour of the gorilla’s nostrils -in glorious black-and-white. I recommend watching the clip full-screen.

Gorilla Family & Me starts on BBC 1 Monday (21 December 2015) and it comes with a detailed website presenting a lot of background info on the work of the park guides, scientists, and the TV crew in Kahuzi-Biega National Park. There are also detailed profiles of the gorillas themselves. Well worth a browse.

To find out more about the behavioural ecology of Grauer’s gorillas have a look at the papers below: