Primate Mothers

I am going to take a little trip back in time here to talk a bit about the research I did for my thesis for my Masters of Research. In 2011/2012 I undertook the MRes Primate Biology, Behaviour and Conservation degree with the University of Roehampton under the wonderful supervisor Dr. Stuart Semple. This fascinating course taught me so much about all areas of primatology and allowed me to spend 3 months carrying out my own research project on the Puerto Rican island of Cayo Santiago.

View from Cayo Santiago (2012)

Cayo Santiago is a 16ha island about 1km off the coast of Puerto Rico and is inhabitated only by 1000 rhesus macaques (Macaca mulata). Starting in March 2012 I carried out a study of the effects of the weaning process on the stress levels of the macaque mothers. Rhesus macaques live in large multi-male/multi-female groups. Rhesus macaques social groups are female–bonded and male dispersal. The females remain in their family group and their dominance hierarchies are based on their matrilineal kinship  (Melnick et al. 1984). Female rhesus macaques very rarely leave their natal groups (Fooden 2000). I hypothesised that weaning would be a stressful period for the mother as if, her newly weaned offspring dies before it can reproduce itself, her investment has been wasted.

I started my study at the beginning of the mating season, when the female macaques were beginning to wean their infants. I looked at levels of self-scratching, a well known behavioural indicator of stress in primates, normally (to determine a baseline frequency of scratching) compared to the frequency of self-scratching in the minute following a rejection of the infant when it tried to nurse. There were three distinct types of rejection: passive rejection involved the mother turning her back or gently blocking her nipple; active rejection where the infant was pushed away or restrained from reaching the mother and violent rejection in which the infant was attacked when attempting to nurse. I also looked at the type of reaction that the infant displayed when it was blocked from weaning. Some infant displayed completely hysterical tantrums that seemed very likely to draw negative attention from other group members, especially adult males.

Female relationships are very important to rhesus macaques.

 In addition to this I looked at whether the stress reaction to rejecting the infant was affected by the dominance rank of the female, how many female relatives she had in the group (and therefore, likely level of support), how many previous infants she had raised, whether the infant was male or female and how socially connected the female was within the group.

Adult female's older offspring trying to steal her new baby.

I found that there is a significant increase in self-scratching directly following the rejection of an infant and that this is effected by whether the infant is male or female. In rhesus macaques, the structure of their society means that dominant males have a huge monopoly on mating opportunities. If the female macaques want to ensure their genes pass to the next generation they have to invest a lot more in a male to give him the best chance of becoming big enough to become dominant. Females have a lot more to lose if a male infant dies between weaning and mating.

In capuchins, things are a bit different. On average, female capuchins give birth every 19.4 months (Janson et al. 2012). Birth season varies by area and is dependant on rainfall, food availability and photoperiod of the habitat (Carosi et al. 2005). In Laguna Blanca, I have only recorded once instance of mating (captured on a camera trap in July 2015) and most of the new babies I have seen have appeared in late December, although both F Group and N Group currently have babies that are less than a month old. As the groups become more habituated to researcher presence I aim to modify my masters research methodology in order to investigate whether weaning causes stress to the mother in the hooded capuchin.

 

Adult female grooming a juvenile.

Adult female carrying a juvenile as another young capuchin approaches her.

Capuchin Remedies

Zoopharmacognosy, or self-medication, is the use of specific plants (or in some cases arthropods) by wild animals to combat parasitic infection or disease. Self-medication has been widely documented in the great apes. One particularly interesting example has been documented in chimpanzees (Pan troglodytes) and gorillas (Gorilla gorilla) and bonobos (Pan paniscus) ingesting and defecating whole leaves in order to purge intestinal parasites (Huffman et al. 1996; Huffman 1997; Huffman & Caton 2001). Rough leaves are folded between the tongue and pass through the gastrointestinal tract intact (Huffman & Caton 2001). These leaves not only scour the gut, forcing expulsion of parasites and eggs but also stimulate diarrhoea, expelling the worms and possibly toxins from the body (Jain et al. 2008). Not pleasant, but effective. White-bellied spider monkeys (Ateles belzebuth) and red howler monkeys (Alouatta seniculus) in Ecuador engage in geophagy – the eating of soil – which is believed to provide them with a variety of nutritional and health benefits (Link et al. 2011).

Chimpanzees eating rough leaves to get rid of parasites. Nigel Swales/wikimedia, CC BY-SA (http://theconversation.com/how-other-primates-self-medicate-and-what-they-could-teach-us-59869)

In capuchin monkeys, the most commonly reported method of self-medication is fur-rubbing or anointing. Anointing can be a solitary or social behaviour and involves a monkey rubbing a foreign substance (e.g. leaves, insects etc.) into it’s fur. In white-faced capuchins (Cebus capucinus) this behaviour is highly social and results in a writhing, drooling ball of very excited monkeys rubbing a variety of plants including Citrus fruits, Piper leaves, Sloanea terniflora fruit and insects (Lynch Alfaro et al. 2011). A review of the variation in anointing behaviours between Cebus and Sapajus species found that Cebus species – the nontufted capuchins – anoint at higher frequencies than Sapajus species – the tufted capuchins, but do not anoint with a higher diversity of materials. This review also found that Cebus uses more plants for anointing and Sapajus more commonly use insects. This behaviour is a type of self-medication as the plants and insects used contain , often very strong, secondary compounds with healing and insect-repelling properties (Jain et al. 2008).

Self-medication in wild primates is certainly a fascinating topic. In Laguna Blanca, I have only seen two incidences of fur rubbing by the hooded capuchins. Both occurred in rather strange circumstances. The first happened back in 2014 (and is described in a natural history note currently under review). During an observer directed threat display, a large adult male in F Group seized a handful of leaves from a Citrus tree and furiously rubbed them all over his fur and then threw them into the air. During the entire display he was loudly alarm calling and threatening me. The second occurred just this week. Two juvenile capuchins came within a few metres of the primate team before settling in the branches of the tree and chewing leaves before rubbing them into their fur. Two individuals engaged in this behaviour separately at first and then together – though the social rubbing only lasted for a couple of second. The unusual thing about both these sightings was that they occurred during observer directed displays.

Young capuchin during solitary fur rubbing bout (Photograph: Anna O'Riordan)

Another suspected case of self-medication is the bark eating behaviour that both groups of capuchins at Laguna Blanca engage in. They only eat the bark of a single tree species and, though little information is available on the exact species, the genus is well known to have various medicinal properties, including anti-parasitic properties!! Parasitological analysis planned for the future will help shed more light on this interesting behaviour!

Adult capuchin eating bark while a juvenile watches (Photograph: Carter Payne)

A Quick Update: Second publication from the PLT Primate Project available to read online!

The second publication from the PLT Primate Project has now been published in Acta Ethologica and is available to read online. "Preliminary Observations of Complex Object Manipulation in a Wild Population of Sapajus cay Illiger 1815 (Primates: Cebidae) in a Fragment of Upper Paraná Atlantic Forest, Rancho Laguna Blanca, eastern Paraguay" describes the different techniques used by the O Group capuchins of Laguna Blanca to access the seeds of the Ka'i Ka'gua tree. 

Please have a read at this link!

http://rdcu.be/ml5x

in a wild population of Sapajus cay Illiger 1815 (primates:

Cebidae) in a fragment of upper Paraná Atlantic Forest, Rancho

Laguna Blanca, eastern Paraguay