Supplementary methods (a) Study animals

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(a) Study animals

The Barbary macaque (Macaca sylvanus), currently listed as ‘endangered’ by the IUCN (Red List of Threatened Species. Version 2012.1. . Downloaded on 12th April 2013), has become increasingly vulnerable to human activity. This species is now restricted to the fragmented forests of Morocco and Algeria, due to the effect of de-forestation, over-grazing and human settlement [1,2], at altitudes between 400 and 2300m [3]. As a result, Barbary macaques experience harsh environmental conditions potentially outside of their thermal niche and are thus under strong ecological pressure [1]. Barbary macaques often feed on the ground [4] and thus heavy snow coverage dramatically reduces their opportunities to access food sources.

At the beginning of the study group F consisted of 19 (11 males and 8 females) and group L consisted of 29 (19 males and 10 females) adult/sub-adult individuals (45 adults and 3 sub-adults). Individuals over five years old were considered adults, and those between four and five were considered sub-adults [5,6]. These groups were fully habituated to the presence of human observers and relied on a completely natural diet.

The 2008-2009 winter appeared to be exceptional in terms of snowfall and ground coverage. The road leading to our study site (33° 24’N – 005° 12’W) was closed due to heavy snow for 12 weeks between November 2008 and March 2009. Conversely, that road was closed for an average of only two weeks, for the same months in the following four years (ESM Table 1). We investigated the exceptionality of the 2008-2009 winter with the local people and they confirmed the rarity of that amount and persistence of snow coverage in the winter months. Unfortunately, no detailed, official monthly data on weather conditions are available before we started our study in 2008.

Following the observed absence of 35 individuals from our two study groups between December 2008 and January 2009, we surveyed, for six months, the area and neighbouring groups at least once per week to determine if the missing individuals had emigrated to other groups. Only five of these individuals were observed in neighbouring groups and we found several remains of dead monkeys in the home ranges of our two study groups. The forest patch that our study groups lived was divided from other forest patches by large, open rocky plains. These openings represent important ecological barriers, as we have never observed Barbary macaques crossing these open areas or moving more than 50m away from the forest (personal observation over five years of observations). Therefore, emigration of our study animals to other forest patches was unlikely. As such, we concluded that the 30 missing monkeys were dead and that starvation was the most likely cause of death. The extended period of snow coverage significantly reduced access to food sources as Barbary macaque mostly feed on the ground [4]. One monkey died prior to the cold winter and was excluded from the analysis. Therefore, our analyses are based on data collected from 47 animals.
(b) Data collection

We collected continuous focal sessions, scan samples and ad libitum data [7] from our study animals. Continuous 20min all-occurrences focal sessions were used to collect data on the amount of grooming given to and received from other group members. Focal session were also used to collect data on all exchanges of close-proximity approaches, i.e. ≤1.5 metre approaches that were not followed by aggression or displacement within 30 seconds. The identities of all grooming and approach partners were recorded. During focal sessions we also collected instantaneous scan data from the focal animal, at 5min intervals, on their state activity: (1) Feeding: consuming food, (2) Foraging: searching for food without consuming it, (3) Travelling: locomotion without searching for food, (4) Resting: sitting still without engaging in pro-social or feeding behaviour, (5) Social contact: engaging in grooming or body-contact with another individual, (6) Other: e.g. aggression, mating, vigilance or play with an object. During each scan data were also collected on the presence and identity of other group members within ≤1.5m proximity. Data were collected ad libitum and during focal sessions on the occurrence of aggressive and submissive displays in order to determine the dominance rank of the study animals. Based on the result of dyadic exchanges the relative dominance ranks of each group member were calculated using MatMan 1.0 Software [8]. The order of focal sessions was randomised and an animal was only sampled once in a single day. In total, we collected 661hrs of focal data (mean ± SD = 14 ± 9hrs/subject) and 9536 scans (mean ± SD = 198 ± 125scans/subject) from our study animals.

c) Data analysis

We calculated the percentage of total scans that each individual spent feeding. We used two measures of sociality: 1) the number of social relationships, and 2) the average quality of social relationships an individual had in the group. The number of social relationships an individual had in their group was defined as the number of group members with whom that individual was observed to exchange grooming and/or to be in body contact during focal sessions at least once. We used a composite sociality index (CSI: [9]) to measure the average quality of the social relationships each individual held in their group:

= the dyad’s mean value for each of the three behavioural measures

= the group’s median value for each of the three behavioural measures.

We entered three behavioural variables into the CSI index considered fundamental measures of relationship quality in non-human primates, including the Barbary macaque [10]: (1) Exchange of friendly behaviour – the proportion of scans in which each dyad member was exchanging friendly behaviour (i.e. grooming or body contact), (2) Proximity – the proportion of scans in which dyad members were within ≤1.5m proximity and (3) Tolerance – the proportion close-proximity approaches exchanged during the dyad’s focal sessions that were successful. For each dyad we combined data collected on each of these three measures. The same three variables were used to calculate medians at the group level. We then divided the combined CSI values an animal shared within their group by the total group size to calculate the average CSI (i.e. quality of their social relationships) each individual held within their social group.

d) References

1. Fa, J. E. 1986. On the ecological status of the Barbary macaque Macaca sylvanus L. in north morocco: Habitat influences versus human impact. Biol. Conserv. 35(3), 215-258.

2. Mehlman, P. T. 1989 Comparative density, demography, and ranging behavior of Barbary macaques (Macaca sylvanus) in marginal and prime conifer habitats. Int. J. Primatol. 10(4), 269-292.

3. Fooden, J. 2007 Systematic review of the Barbary macaque, Macaca sylvanus (linnaeus, 1758). Fieldiana Zoology 113, 1-60.

4. Ménard, N. 2002 Ecological plasticity of Barbary macaques (Macaca sylvanus). Evol. Anthropol. 11, 95-100.

5. Ménard, N. & Vallet, D. 1993 Population dynamics of Macaca sylvanus in Algeria: An 8‐year study. Am. J. Primatol. 30, 101-118.

6. Bissonnette, A., de Vries, H. & van Schaik, C. P. 2009 Coalitions in male Barbary macaques (Macaca sylvanus): Strength, success and rules of thumb. Anim. Behav. 78, 329-335.

7. Altmann, J. 1974 Observational study of behavior: Sampling methods. Behaviour 49(3), 227-267.

8. de Vries, H., Netto, W. J. & Hanegraaf, P. L. H. 1993 Matman: A programme for the analysis of sociometric matrices and behavioural transition matrices. Behaviour 125, 157-175.

9. Silk, J. B., Alberts, S. C. & Altmann, J. 2003 Social bonds of female baboons enhance infant survival. Science 302(5648), 1231-1234.

10. McFarland, R. & Majolo, B. 2011 Exploring the components, asymmetry and distribution of relationship quality in wild Barbary macaques (Macaca sylvanus). PLoS ONE 6, e28826. doi:10.1371/journal.pone.0028826.

ESM Table 1 – Weeks of persistent snowfall between the months November and March from 2008 – 2013. * denotes current study period.

Winter years

Weeks of snowfall

2008 – 2009*


2009 – 2010


2010 – 2011


2011 – 2012


2012 – 2013


ESM Table 2 – Variables entered in the logistic regression on survival



Dependent variable


Binary – survived or died during the 2008-2009 winter

Independent variables

Feeding time

Continuous – percentage of scans spent feeding

Number of social relationships

Continuous – total number of social partners in their group

Quality of social relationships

Continuous – composite sociality index


Binary – male or female


Continuous (rank 1 was assigned to the most dominant animal in each group)

Control variable

Group ID

Binary – ‘group F’ or ‘group L’

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