Most mammals depend entirely upon their mothers when they are born. In these species, losing a mother at a young age has dramatic consequences for survival. In cases where orphaned individuals do reach adulthood, they often suffer negative effects, like reduced reproductive success or lower social status. But this is not the case for humans. If a child loses their mother, relatives, friends and the wider community can take over. This does not tend to happen in nature. Even our closest relatives, chimpanzees, are much less likely to survive if their mothers die before they reach adolescence.

Although orphan survival is not the norm for mammals, humans may not be entirely unique. Mountain gorillas also live in stable family groups, usually with a dominant male and one or more females who care for their offspring for between 8 and 15 years. It is possible that gorillas may also be able to provide community support to orphans, which could buffer the costs of losing a mother, just as it does in humans.

To answer this question, Morrison et al. examined 53 years of data collected by the Dian Fossey Gorilla Fund to assess the effects of maternal loss in mountain gorillas. The analysis examined survival, reproduction and changes in social relationships. This revealed that, like humans, young gorillas that lose their mothers are not at a greater risk of dying. There is also no clear long-term effect on their ability to reproduce. In fact, gorillas who lost their mothers ended up with stronger social relationships, especially with the dominant male of the group and young gorillas around the same age. It seems that gorilla social groups, like human families, provide support to young group members that lose their mothers.

These findings suggest that the human ability to care for others in times of need may not be unique. It is possible that the tendency to care for orphaned young has its origins in our evolutionary past. Understanding this in more depth could provide clues into the social mechanisms that help to overcome early life adversity, and have a positive impact on future health and survival.

Maternal loss, along with a number of other indicators of early-life adversity, is one of the strongest predictors of lifespan in humans and other social mammals (Snyder-Mackler et al., 2020). In mammals, mothers are vital for the survival of young offspring, providing nutrition, thermoregulation, and protection (Clutton-Brock, 1991). In some species, particularly social species with slow life histories (Mitani et al., 2013), mothers continue to provide benefits to their co-residing offspring throughout immaturity and even into adulthood (Surbeck et al., 2019; Surbeck et al., 2011; Andres et al., 2013; Stanton et al., 2020). The active support of mothers can increase the rank of their offspring (Strauss et al., 2020; East et al., 2009; Maestripieri and Mateo, 2009; Lea et al., 2014) and improve their integration in the group (Tung et al., 2016), both of which are linked with greater survival (Snyder-Mackler et al., 2020; Archie et al., 2014). Maternal presence can also influence nutrition at these later stages of development by buffering against feeding competition (Samuni et al., 2020), providing access to valuable ecological knowledge (Stanton et al., 2020; Foley et al., 2008; Brent et al., 2015) or increasing opportunities for the social learning of complex feeding techniques (Lonsdorf et al., 2004; Estienne et al., 2019).

In social mammals maternal loss can therefore reduce the fitness of offspring across a broad age range through long-term effects on their social environment, negatively influencing their social integration and social status throughout their lives (Snyder-Mackler et al., 2020; Strauss et al., 2020; Tung et al., 2016). Multiple studies have now confirmed effects on survival for individuals orphaned well past the period of nutritional dependency, with these negative changes to their social environment, often termed social adversity, posited to be the key mechanism by which this occurs (Andres et al., 2013; Stanton et al., 2020; Tung et al., 2016; Watts et al., 2009; Foster et al., 2012). In social mammals, the social environment can have extreme consequences for health, fitness, and lifespan, mediated through pathways such as chronic stress, immune function, or environmental exposure (Snyder-Mackler et al., 2020).

The impact of maternal loss varies based on the loss in benefits relative to individuals with mothers present. In species with sex-biased dispersal, the consequences of maternal loss can differ between the sexes due to longer periods for potential investment in non-dispersing offspring (Clutton-Brock, 1991; Fairbanks, 2009; Altmann and Alberts, 2005; Greenwood, 1980). In female-philopatric red deer (Cervus elaphus), maternal loss increases mortality for males and females, but this effect is only detectable in males under 2 years of age, whilst for females, maternal benefits continue throughout their lives (Andres et al., 2013). In male-philopatric chimpanzees (Pan troglodytes), males that suffer maternal loss before reaching 15 years of age have lower survival, whilst females only show reduced survival from maternal loss under the age of 10 (Nakamura et al., 2014; Stanton et al., 2020). In killer whales (Orcinus orca), where neither sex disperses, maternal loss when offspring are over 30 years old reduces survival for both sexes, although considerably more so for males (Foster et al., 2012). However, maternal loss between 15 and 30 years appears to reduce male but not female survival. This is thought to be due to higher maternal investment in males which mate outside the group and whose offspring therefore do not increase within-group feeding competition.

As a result of the numerous benefits mothers can provide, it is not surprising that maternal loss not only influences offspring survival but can also impact other components of their offspring’s fitness, such as reproduction and the survival of grand-offspring. Male bonobos (Pan paniscus) residing in groups with their mothers sire three times the number of offspring (Surbeck et al., 2019), whilst maternal loss before weaning negatively affects antler development in male red deer – a trait found to correlate with reproductive success (Andres et al., 2013). In chimpanzees, females mature faster, first give birth younger (Walker et al., 2018) and enter the dominance hierarchy higher (Foerster et al., 2016) if their mothers are present which is expected to considerably increase their lifetime reproductive success. In savannah baboons (Papio cynocephalus), if mothers had themselves suffered maternal loss in the first 4 years of their life, their offspring had 48% higher mortality throughout the first 4 years of their life, suggesting an intergenerational effect of maternal loss driven by lifelong developmental constraints (Zipple et al., 2019). Maternal loss in social mammals with extended maternal care can therefore have long-term fitness consequences mediated through multiple pathways that detrimentally affect survival and reproduction.

Due to the extended periods of mother–offspring co-residence and the important social support mothers can provide, highly social species often have the most to lose from maternal loss. However, social groups also provide the potential for support from other group members following maternal loss. Both kin and non-kin group members have been suggested to compensate for the loss of close kin to varying extents (Hamilton et al., 1982; Engh et al., 2006; Goldenberg and Wittemyer, 2017; Reddy and Mitani, 2019) and the strengthening of relationships with remaining group members may buffer against changing social environments (Firth et al., 2017). In chacma baboons (Papio ursinus), social support from group members is thought to alleviate the stress of losing a close relative (Engh et al., 2006). Similar social support has been suggested in African savannah elephants (Loxodonta africana) which associate more with group members of a similar age and siblings in response to maternal loss (Goldenberg and Wittemyer, 2017). However, these orphaned elephants interact less with matriarchs which may decrease their access to key knowledge and high-quality resource patches. In chimpanzees, older siblings can ‘adopt’ younger siblings after maternal loss, increasing their social contact and showing heightened vigilance in dangerous situations (Reddy and Mitani, 2019; Hobaiter et al., 2014). But despite these compensatory social behaviours, the negative consequences of maternal loss post-weaning are well documented in all three genera (Stanton et al., 2020; Tung et al., 2016; Samuni et al., 2020; Nakamura et al., 2014; Goldenberg and Wittemyer, 2017; Goldenberg and Wittemyer, 2018).

Humans (Homo sapiens) are a rare example of a group-living mammal in which compensatory social behaviours have been suggested to have the capacity to consistently overcome these negative consequences of maternal loss. In a meta-analysis of historic and contemporary human populations, the death of a mother was associated with increased child mortality in all 28 populations studied (Sear and Mace, 2008). However, this effect appeared to decline substantially with age, disappearing for children that suffered maternal loss over 2 years of age in 5 of the 11 populations in which it was investigated (Sear and Mace, 2008). This reduced mortality was thought to be due to the care provided by other kin, particularly after weaning, suggesting that social buffering from other group members can overcome the negative effect of maternal loss on survival in certain circumstances. Whilst the effects of care from specific kin members varied across populations, at least one kin member significantly impacted child survival in all studies (Sear and Mace, 2008), and there is evidence for the importance of maternal grandmothers (Lahdenperä et al., 2004; Sear et al., 2000) and fathers (Hurtado and Hill, 1992; Hill and Hurtado, 2017) in particular. In killer whales, maternal grandmothers, especially those that are post-reproductive, are also known to improve grand-offspring survival (Nattrass et al., 2019). Whilst the specific effect of killer whale grandmothers on orphan survival has not been investigated, this finding suggests that killer whales may represent a further species in which care from other kin has the capacity to overcome the effects of maternal loss. In humans, there is also evidence for the benefits of care provided by non-kin such as step-mothers (Andersson et al., 1996; Campbell and Lee, 2002) and through the modern practices of non-kin adoption (Bentley and Mace, 2009).

Mountain gorillas (Gorilla beringei beringei) show extended maternal care with offspring remaining in their natal groups at least until sexual maturity and approximately half remaining beyond sexual maturity (48% of females [Robbins et al., 2009a] and 55% of males [Stoinski et al., 2009a]). Females that disperse from their natal group tend to do so earlier (mean age of 7.9 years [Robbins et al., 2009a]) than males (mean age of 15.3 years [Stoinski et al., 2009a]) and therefore have a shorter period of potential maternal investment. The complexity of gorilla social structure with numerous types of differentiated social relationship both within and among groups (Morrison et al., 2019; Mirville et al., 2018; Morrison et al., 2020a; Morrison et al., 2020b) suggests that detrimental long-term effects on individual gorillas’ social environments could have particularly negative fitness consequences. However, these stable, cohesive, social groups also have the potential to provide a social buffer to the negative consequences of maternal loss. Mountain gorilla groups either contain a single adult male (approximately 64% of groups) or multiple adult males (approximately 36% of groups) (Gray, 2010), at least one adult female, and their offspring (Robbins, 1995). Single male groups are polygynous whilst multimale groups have high reproductive skew towards the dominant male who sires the majority of offspring (Nsubuga et al., 2008; Stoinski, 2009b; Bradley et al., 2005). Infants (<4 years of age) are nutritionally dependent on their mothers until being weaned at a mean of 3.3 years (Eckardt et al., 2016) and are reliant on their mothers for thermoregulation and transport, being carried for prolonged periods (Breuer et al., 2009). Juveniles (4–6 years old) are nutritionally independent but remain in close proximity to their mothers the majority of the time (Breuer et al., 2009). Dominant males’ primary form of care is through protection from out-group males and potential predators (Harcourt and Greenberg, 2001). But they also show high levels of affiliative behaviour towards infants, grooming and resting in contact with them, with no evidence that they discriminate between infants based on paternity (Rosenbaum et al., 2018; Rosenbaum et al., 2015).

In this study, we use the long-term demographic records of the Dian Fossey Gorilla Fund’s Karisoke Research Center collected over 53 years (1967–2019) to (A) quantify the effects of maternal loss on multiple fitness measures: survival, female age at first birth, female survival of first offspring through infancy, and male dominance; and (B) investigate the social responses of group members to maternal loss by immature gorillas. We hypothesize that as demonstrated in chimpanzees (Stanton et al., 2020), gorillas may face greater fitness costs if they suffer maternal loss at an earlier age and that males may face greater costs from maternal loss than females due to their longer periods of mother–offspring co-residence. Alternatively, as observed in many human populations, the cohesive, stable social groups of mountain gorillas may enable social buffering from group members to compensate for the social costs of maternal loss with minimal fitness consequences to maternal loss. In particular, dominant males may take on crucial roles in buffering the social adversity faced by maternal orphans (hereafter, orphans), as past research has demonstrated the strong bond between dominant males and young orphans who may regularly share a nest at night (Robbins et al., 2005; Gatesire et al., 2016).

In contrast to many social mammals with extended periods of mother–offspring co-residence (Andres et al., 2013; Stanton et al., 2020; Foster et al., 2012), in mountain gorillas, we found no evidence for higher mortality in immature offspring of either sex following maternal loss. Whilst our sample size of 59 orphans between the ages of 2 and 8 years may limit our ability to detect relatively weak effects on survival, significant effects have been found in other species with comparable sample sizes (Stanton et al., 2020). This suggests that either maternal loss after offspring have reached 2 years of age does not reduce survival in mountain gorillas, or that the reduction in survival is considerably weaker than that observed in other species and therefore undetectable within our sample.

The effect of maternal loss on dispersal decisions differed depending on the age at which maternal loss occurred. Whilst no effect was found for those orphaned as infants, juvenile- or subadult-orphaned gorillas were more than twice as likely to disperse than non-orphans (although for females this effect was not quite significant). This suggests that there may be some benefits to co-residence with mothers for both sexes that do not directly translate to survival, but could influence lifetime reproductive success, like the faster maturation and higher dominance in female chimpanzees (Walker et al., 2018; Foerster et al., 2016) or greater mating opportunities in male bonobos (Surbeck et al., 2019). Alternatively, potential benefits may not be specific to the mother–offspring bond. Instead, the loss of a key social partner close to dispersal age may reduce the social benefits of remaining in a group. Without this strong social bond in the natal group, dispersal to a new group may lead to fewer social costs relative to remaining, whilst also providing considerable benefits for inbreeding avoidance (Vigilant et al., 2015). This might better explain the age-dependent influence of maternal loss, as by the time those suffering maternal loss as infants approach an age at which dispersal could occur, they may have compensated for the loss of such a key social partner through strengthening their relationships with other group members. Our analyses also suggest that the strengthening of relationships with group members post-maternal loss may be greatest for younger individuals, which could further reduce the likelihood that they disperse later in life.

We found no significant effect of maternal loss on the elements of female reproduction we investigated. Female orphans gave birth slightly younger, but despite this, their first offspring was marginally more likely to survive infancy. Whilst neither effect was significant, the direction of the effect, with earlier first birth, is consistent with the stress acceleration hypothesis: that those suffering from early caregiving adversity may show accelerated development as an adaptive strategy to low parental care (Ellis, 2004; Callaghan and Tottenham, 2016). Female dispersal has also not been found to cause any reproductive delays in mountain gorillas, suggesting that the potentially higher likelihood of those suffering maternal loss as juveniles or subadults to disperse is unlikely to reduce their reproductive capacity (Robbins et al., 2009b).

Male reproduction was harder to assess due to limited paternity data and later sexual maturity. However, as dominant males usually sire the majority of offspring, even within multi-male groups (Nsubuga et al., 2008; Stoinski, 2009b; Bradley et al., 2005), analyses of male dominance status provided some insights into the reproductive success of male orphans. Although only around half of males ever reached dominant male status, some males in both orphan age categories were able to do so, demonstrating that this is possible in the absence of maternal support. Small sample sizes limited the extent of analysis possible, but maternal loss appeared to have differing effects depending on the age of maternal loss, with infant-orphaned males more likely and juvenile- or subadult-orphaned males less likely to become the dominant male of a group relative to males that did not suffer maternal loss. This mirrors the effect of maternal loss on dispersal decisions. Modelling has suggested that males that disperse suffer a 50% reduction in lifetime reproductive success (Robbins and Robbins, 2005), as they lose the potential for mating opportunities as a subordinate male within their natal group or for eventually taking over as dominant male of that group and must instead attempt to attract females to form a group of their own (Stoinski et al., 2009a). It is therefore likely that males suffering maternal loss as juveniles or subadults may suffer from reduced siring opportunities throughout their lives due to their increased likelihood of dispersal. As discussed above, it is possible that the greater strengthening of relationships between group members and those orphaned at an earlier age may reduce the likelihood of these infant-orphaned gorillas dispersing relative to those suffering maternal loss as juveniles or subadults, ultimately influencing male orphans’ subsequent reproductive success.

Overall, these findings suggest there are no strong negative fitness consequences for maternal loss in female mountain gorillas over 2 years of age, although we cannot rule out longer-term effects on lifetime reproduction. In males, maternal loss after 2 years does not appear to influence survival but maternal loss as juveniles or subadults (4–8 years) could lower their future reproductive success. This lack of effect on survival reflects patterns found in human populations with natural fertility and mortality, where the negative effect of maternal loss on survival declines substantially with age and in many cases disappears entirely over the age of 2 (Sear and Mace, 2008). However, it is contrary to research in most other social mammals with long periods of mother–offspring co-residency (Snyder-Mackler et al., 2020; Andres et al., 2013; Stanton et al., 2020; East et al., 2009; Tung et al., 2016; Watts et al., 2009; Nakamura et al., 2014; Goldenberg and Wittemyer, 2017; Goldenberg and Wittemyer, 2018). In these species, one of the major mechanisms posited to link maternal loss with increased mortality is through the social adversity caused by mother absence. Specifically, mother absence is found to reduce social integration (Tung et al., 2016; Archie et al., 2014), competitivity (Surbeck et al., 2019; Samuni et al., 2020), dominance rank (Strauss et al., 2020; East et al., 2009; Maestripieri and Mateo, 2009; Lea et al., 2014), and opportunities for social learning (Stanton et al., 2020; Foley et al., 2008; Brent et al., 2015; Estienne et al., 2019). But the lack of increased mortality in gorillas and certain human populations suggests that mother absence does not always lead to social adversity in mammals with extended maternal care.

When immature mountain gorillas suffered maternal loss, we found that their social relationships with other group members estimated through proximity increased in strength (weighted degree), and their social integration within the group (eigenvector centrality) increased considerably. There was no increase in binary degree suggesting that orphans strengthen existing social bonds rather than forming new ones following maternal loss. The increase in orphan eigenvector centrality was especially large (Figure 2), which may be explained by the strengthening of the orphan-dominant male bond in particular, with dominant males typically being extremely well connected within the group network. The increase in proximity-based relationship strength with other group members was actually great enough to outweigh the loss of their mother, although this was not the case for relationships based on contact which did not change significantly more than non-orphans overall. In contrast to fission–fusion social systems such as in chimpanzees, where group composition regularly changes, mountain gorilla orphans remain in stable cohesive social groups in which their social integration is not dependent on their mother – as shown by the strengthening of relationships following maternal loss. Their increased social integration within the larger cohesive group immediately following maternal loss suggests that mountain gorilla orphans are unlikely to have fewer opportunities for social learning as they are regularly in close proximity to multiple group members. Gorillas also do not appear to require the complex feeding techniques such as nut-cracking or termite-fishing, for which close contact with mothers may be most beneficial (Lonsdorf et al., 2004; Estienne et al., 2019). Instead, common group-membership may be sufficient for learning the complex foraging behaviours observed in gorillas (Watts, 1984; Byrne et al., 2001) as groups travel and feed as a cohesive unit.

The greatest increases in relationship strength following maternal loss were found with the dominant male of the group, regardless of whether or not he was the genetic father. This suggests that unlike in elephants where maternal loss leads to weaker relationships with dominant group members, gorillas that suffer maternal loss instead have increased access to the most dominant member of their group. Whilst the cohesion of gorilla social groups already limits the extent to which orphans are likely to suffer from reduced access to resources or knowledge, the strengthening of social relationships, particularly with the dominant male, is likely to further buffer any potential reduction to their competitivity or future dominance rank within the group. Other cohesive social groups in which the effects of maternal loss have been studied have primarily been matriarchal, with groups led by older females, e.g. elephants (Goldenberg and Wittemyer, 2017; Goldenberg and Wittemyer, 2018), or where strong female dominance hierarchies are inherited, e.g. spotted hyenas (East et al., 2009; Watts et al., 2009) and cercopithecine species such as the savannah baboon (Archie et al., 2014). In contrast, males are the dominant sex in gorillas (Wright et al., 2019). Female dominance hierarchies are relatively weak, and the common dispersal of both sexes means maternal support is unlikely to provide considerable benefits for dominance to offspring of either sex. Orphaned gorillas are therefore unlikely to suffer costs in this regard. However, for males that remain in their natal group it is possible that stronger relationships with the dominant male, such as those developed post-maternal loss, could aid dominance acquisition. For males that lose their mothers at particularly early ages and show some of the strongest relationships with the dominant male as a result, it is possible that this could ultimately improve their chances of inheriting dominance of their natal group (Stoinski et al., 2009a; Robbins and Robbins, 2005). Although, due to the rarity of such events (three cases in 53 years) there may never be a large enough sample size to thoroughly investigate such a hypothesis.

The lack of paternity discrimination in the support provided by adult males after maternal loss is consistent with previous findings on paternal care in mountain gorillas, where the highest ranking males sire the majority of offspring and provide the most care, regardless of paternity (Rosenbaum et al., 2018; Rosenbaum et al., 2015). As observed in chimpanzees (Reddy and Mitani, 2019), support from some maternal siblings also appears to occur, with relationships between subordinate adult males and subadult females, and their younger siblings strengthening following maternal loss. In these two classes, caring for siblings may have additional benefits to those of inclusive fitness (Riedman, 1982). Care of infants by adult male mountain gorillas has been found to be linked with dramatically higher reproductive success. Males in the top tertile for showing affiliative behaviour towards infants were found to sire 5.5 times more infants than those in the bottom tertile, even after accounting for rank (Rosenbaum et al., 2018). This suggests that females may prefer males that demonstrate more caring behaviour towards infants, and that subordinate male kin that increase their care of younger maternal siblings following maternal loss may additionally increase their own reproductive success. Pre-reproductive female siblings, particularly subadult females, may also benefit through developing parental experience that may improve their own reproductive success (Riedman, 1982).

Our analyses of social relationship changes used undirected data on pairwise proximity and affiliative contact. Whilst both measures of affiliation indicate at a minimum, high tolerance for the other individual, we cannot determine who was responsible for initiating the relationship changes. Future research could investigate whether it is the orphans themselves that are strengthening their relationships by approaching other group members more often or whether it is the other group members responding to the maternal loss faced by these young gorillas. Our study also only investigates the immediate social response to maternal loss in the 6 months after the mother dies or leaves the group. Whilst this might be expected to be the period where individuals face the greatest social costs from maternal loss, our analyses cannot tell us whether the social buffering we detected during this period is maintained in the longer term. However, previous observations have suggested that the close associations that young gorillas develop following maternal loss continue into subadulthood (Robbins et al., 2005). It is therefore highly likely that the dramatic short-term changes we have detected are part of a longer-term social response to maternal loss with the potential to overcome the long-term fitness costs of maternal loss.

In many human populations, care from other family members is believed to buffer the negative consequences of maternal loss, but the identity of these carers can vary greatly between populations. In rural Gambia, elder sisters and maternal grandmothers increased offspring survival but not fathers, other grandparents, or brothers (Sear et al., 2003). In contrast, in the Ache of Paraguay the loss of fathers significantly impacted offspring survival but the loss of grandparents or adult siblings did not (Hill and Hurtado, 2017). Support from family members in rearing offspring is thought to be a human universal but the composition of those families and the specific family members involved in cooperative care appears to be flexible and responsive to ecological conditions (Sear and Mace, 2008). In killer whales, as observed in many human populations, grandmothers have been found to influence offspring survival and this additional support could in part contribute to the lack of reduced survival for younger female killer whales after maternal loss (Foster et al., 2012; Nattrass et al., 2019). In mountain gorillas, grandparents and their grand-offspring are rarely in the same social group, as females often transfer between groups multiple times within their lives (Robbins et al., 2009a). Instead, fathers (or dominant males with a high likelihood of paternity), siblings, and group members close in age seem to play a key role in buffering the detrimental effects of maternal loss. What appears to set humans, gorillas, and possibly killer whales apart from other species with extended maternal care where high fitness costs to maternal loss are observed is the potential for cooperative care from within the social group.

Demographic data available within the Primate Life Histories Database at https://datadryad.org/stash/dataset/doi:10.5061/dryad.v28t5 Social data available as source data files.

1. 1. Bronikowski
   2. Anne M

   (2017) Dryad Digital Repository

   Data from: Female and male life tables for seven wild primate species.

   https://doi.org/10.5061/dryad.v28t5

1. 1. Albers PCH
   2. de Vries H

   (2001) Elo-rating as a tool in the sequential estimation of dominance strengths

   Animal Behaviour 61:489–495.

   https://doi.org/10.1006/anbe.2000.1571

   • Google Scholar
2. 1. Altmann J
   2. Alberts SC

   (2005) Growth rates in a wild primate population: ecological influences and maternal effects

   Behavioral Ecology and Sociobiology 57:490–501.

   https://doi.org/10.1007/s00265-004-0870-x

   • Google Scholar
3. 1. Andersson T
   2. Hogberg U
   3. Åkerman S

   (1996) Survival of orphans in 19th century Sweden—the importance of remarriages

   Acta Paediatrica 85:981–985.

   https://doi.org/10.1111/j.1651-2227.1996.tb14198.x

   • Google Scholar
4. 1. Andres D
   2. Clutton-Brock TH
   3. Kruuk LEB
   4. Pemberton JM
   5. Stopher KV
   6. Ruckstuhl KE

   (2013) Sex differences in the consequences of maternal loss in a long-lived mammal, the red deer (Cervus elaphus)

   Behavioral Ecology and Sociobiology 67:1249–1258.

   https://doi.org/10.1007/s00265-013-1552-3

   • Google Scholar
5. 1. Archie EA
   2. Tung J
   3. Clark M
   4. Altmann J
   5. Alberts SC

   (2014) Social affiliation matters: both same-sex and opposite-sex relationships predict survival in wild female baboons

   Proceedings of the Royal Society B: Biological Sciences 281:20141261.

   https://doi.org/10.1098/rspb.2014.1261

   • Google Scholar
6. 1. Bentley GR
   2. Mace R

   (2009) Substitute parents: biological and social perspectives on alloparenting across human societies

   Journal of the Royal Anthropological Institute 16:931–932.

   https://doi.org/10.2307/40926215

   • Google Scholar
7. 1. Bradley BJ
   2. Robbins MM
   3. Williamson EA
   4. Steklis HD
   5. Steklis NG
   6. Eckhardt N
   7. Boesch C
   8. Vigilant L

   (2005) Mountain Gorilla tug-of-war: silverbacks have limited control over reproduction in multimale groups

   PNAS 102:9418–9423.

   https://doi.org/10.1073/pnas.0502019102

   • PubMed
   • Google Scholar
8. 1. Brent LJN
   2. Franks DW
   3. Foster EA
   4. Balcomb KC
   5. Cant MA
   6. Croft DP

   (2015) Ecological knowledge, leadership, and the evolution of menopause in killer whales

   Current Biology 25:746–750.

   https://doi.org/10.1016/j.cub.2015.01.037

   • PubMed
   • Google Scholar
9. 1. Breuer T
   2. Hockemba MB
   3. Olejniczak C
   4. Parnell RJ
   5. Stokes EJ

   (2009) Physical maturation, life-history classes and age estimates of free-ranging western gorillas--insights from mbeli bai, republic of congo

   American Journal of Primatology 71:106–119.

   https://doi.org/10.1002/ajp.20628

   • PubMed
   • Google Scholar
10. 1. Byrne RW
    2. Corp N
    3. Byrne JME

    (2001) Estimating the complexity of animal behaviour: how mountain gorillas eat thistles

    Behaviour 138:525–557.

    https://doi.org/10.1163/156853901750382142

    • Google Scholar
11. 1. Callaghan BL
    2. Tottenham N

    (2016) The stress acceleration hypothesis: effects of early-life adversity on emotion circuits and behavior

    Current Opinion in Behavioral Sciences 7:76–81.

    https://doi.org/10.1016/j.cobeha.2015.11.018

    • PubMed
    • Google Scholar
12. Report

    1. Campbell C
    2. Lee JZ

    (2002)

    When Husbands and Parents Die: Widowhood and Orphanhood in Late Imperial Liaoning, 1789-1909, When Dad Died Individ Fam

    Coping with Distress Past Soc.

    • Google Scholar
13. 1. Celeux G
    2. Forbes F
    3. Robert CP
    4. Titterington DM

    (2006) Deviance information criteria for missing data models

    Bayesian Analysis 1:651–673.

    https://doi.org/10.1214/06-BA122

    • Google Scholar
14. Book

    1. Clutton-Brock TH

    (1991) The Evolution of Parental Care

    Princeton University Press.

    https://doi.org/10.1093/acprof:oso/9780199692576.003.0001

    • Google Scholar
15. 1. Colchero F
    2. Jones OR
    3. Rebke M

    (2012) BaSTA: an R package for bayesian estimation of age-specific survival from incomplete mark-recapture/recovery data with covariates

    Methods in Ecology and Evolution 3:466–470.

    https://doi.org/10.1111/j.2041-210X.2012.00186.x

    • Google Scholar
16. 1. Colchero F
    2. Clark JS

    (2012) Bayesian inference on age-specific survival for censored and truncated data

    Journal of Animal Ecology 81:139–149.

    https://doi.org/10.1111/j.1365-2656.2011.01898.x

    • PubMed
    • Google Scholar
17. 1. East ML
    2. Höner OP
    3. Wachter B
    4. Wilhelm K
    5. Burke T
    6. Hofer H

    (2009) Maternal effects on offspring social status in spotted hyenas

    Behavioral Ecology 20:478–483.

    https://doi.org/10.1093/beheco/arp020

    • Google Scholar
18. 1. Eckardt W
    2. Fawcett K
    3. Fletcher AW

    (2016) Weaned age variation in the virunga mountain gorillas (Gorilla beringei beringei): influential factors

    Behavioral Ecology and Sociobiology 70:493–507.

    https://doi.org/10.1007/s00265-016-2066-6

    • Google Scholar
19. 1. Ellis BJ

    (2004) Timing of pubertal maturation in girls: an integrated life history approach

    Psychological Bulletin 130:920–958.

    https://doi.org/10.1037/0033-2909.130.6.920

    • PubMed
    • Google Scholar
20. 1. Engh AL
    2. Beehner JC
    3. Bergman TJ
    4. Whitten PL
    5. Hoffmeier RR
    6. Seyfarth RM
    7. Cheney DL

    (2006) Behavioural and hormonal responses to predation in female chacma baboons ( Papio hamadryas ursinus )

    Proceedings of the Royal Society B: Biological Sciences 273:707–712.

    https://doi.org/10.1098/rspb.2005.3378

    • Google Scholar
21. 1. Estienne V
    2. Cohen H
    3. Wittig RM
    4. Boesch C

    (2019) Maternal influence on the development of nut-cracking skills in the chimpanzees of the taï forest, côte d'ivoire (Pan Troglodytes verus)

    American Journal of Primatology 81:e23022.

    https://doi.org/10.1002/ajp.23022

    • PubMed
    • Google Scholar
22. Book

    1. Fairbanks LA

    (2009) Maternal Investment Throughout the Life Span in Old World Monkeys

    Cambridge University Press.

    https://doi.org/10.1017/cbo9780511542589.014

    • Google Scholar
23. 1. Farine DR
    2. Whitehead H

    (2015) Constructing, conducting and interpreting animal social network analysis

    Journal of Animal Ecology 84:1144–1163.

    https://doi.org/10.1111/1365-2656.12418

    • Google Scholar
24. 1. Firth JA
    2. Voelkl B
    3. Crates RA
    4. Aplin LM
    5. Biro D
    6. Croft DP
    7. Sheldon BC

    (2017) Wild birds respond to flockmate loss by increasing their social network associations to others

    Proceedings of the Royal Society B: Biological Sciences 284:20170299.

    https://doi.org/10.1098/rspb.2017.0299

    • Google Scholar
25. 1. Foerster S
    2. Franz M
    3. Murray CM
    4. Gilby IC
    5. Feldblum JT
    6. Walker KK
    7. Pusey AE

    (2016) Chimpanzee females queue but males compete for social status

    Scientific Reports 6:e35404.

    https://doi.org/10.1038/srep35404

    • Google Scholar
26. 1. Foley C
    2. Pettorelli N
    3. Foley L

    (2008) Severe drought and calf survival in elephants

    Biology Letters 4:541–544.

    https://doi.org/10.1098/rsbl.2008.0370

    • PubMed
    • Google Scholar
27. 1. Foster EA
    2. Franks DW
    3. Mazzi S
    4. Darden SK
    5. Balcomb KC
    6. Ford JK
    7. Croft DP

    (2012) Adaptive prolonged postreproductive life span in killer whales

    Science 337:1313.

    https://doi.org/10.1126/science.1224198

    • PubMed
    • Google Scholar
28. Conference

    1. Gatesire T
    2. Stoinski TS
    3. Caillaud D
    4. Ndagijimana F
    5. Eckardt W

    (2016)

    Going alone? Social bonds of gorilla orphan

    International Primatological Society Congress.

    • Google Scholar
29. 1. Goldenberg SZ
    2. Wittemyer G

    (2017) Orphaned female elephant social bonds reflect lack of access to mature adults

    Scientific Reports 7:e14712-2.

    https://doi.org/10.1038/s41598-017-14712-2

    • Google Scholar
30. 1. Goldenberg SZ
    2. Wittemyer G

    (2018) Orphaning and natal group dispersal are associated with social costs in female elephants

    Animal Behaviour 143:1–8.

    https://doi.org/10.1016/j.anbehav.2018.07.002

    • Google Scholar
31. 1. Gray M

    (2010) Censusing the mountain gorillas in the virunga volcanoes: complete sweep method versus monitoring

    African Journal of Ecology 48:588–599.

    https://doi.org/10.1111/j.1365-2028.2009.01142.x

    • Google Scholar
32. 1. Greenwood PJ

    (1980) Mating systems, philopatry and dispersal in birds and mammals

    Animal Behaviour 28:1140–1162.

    https://doi.org/10.1016/S0003-3472(80)80103-5

    • Google Scholar
33. 1. Hamilton WJ
    2. Busse C
    3. Smith KS

    (1982) Adoption of infant orphan chacma baboons

    Animal Behaviour 30:29–34.

    https://doi.org/10.1016/S0003-3472(82)80233-9

    • Google Scholar
34. 1. Harcourt AH
    2. Greenberg J

    (2001) Do Gorilla females join males to avoid infanticide? A quantitative model

    Animal Behaviour 62:905–915.

    https://doi.org/10.1006/anbe.2001.1835

    • Google Scholar
35. Book

    1. Hill K
    2. Hurtado AM

    (2017) Ache Life History: The Ecology and Demography of a Foraging People

    Routledge.

    https://doi.org/10.2307/2137817

    • Google Scholar
36. 1. Hobaiter C
    2. Schel AM
    3. Langergraber K
    4. Zuberbühler K

    (2014) 'Adoption' by maternal siblings in wild chimpanzees

    PLOS ONE 9:e103777.

    https://doi.org/10.1371/journal.pone.0103777

    • PubMed
    • Google Scholar
37. Book

    1. Hurtado AM
    2. Hill KR

    (1992) Paternal effect on offspring survivorship among ache and hiwi hunter-gatherers: Implications for modeling pair-bond stability. in Father-Child Relations

    In: Hewlett B. S, editors. Cultural and Biosocial Contexts. Elsevier. pp. 1–26.

    https://doi.org/10.4324/9780203792063

    • Google Scholar
38. 1. Lahdenperä M
    2. Lummaa V
    3. Helle S
    4. Tremblay M
    5. Russell AF

    (2004) Fitness benefits of prolonged post-reproductive lifespan in women

    Nature 428:178–181.

    https://doi.org/10.1038/nature02367

    • PubMed
    • Google Scholar
39. 1. Lea AJ
    2. Learn NH
    3. Theus MJ
    4. Altmann J
    5. Alberts SC

    (2014) Complex sources of variance in female dominance rank in a nepotistic society

    Animal Behaviour 94:87–99.

    https://doi.org/10.1016/j.anbehav.2014.05.019

    • PubMed
    • Google Scholar
40. 1. Lonsdorf EV
    2. Eberly LE
    3. Pusey AE

    (2004) Sex differences in learning in chimpanzees

    Nature 428:715–716.

    https://doi.org/10.1038/428715a

    • PubMed
    • Google Scholar
41. Book

    1. Maestripieri D
    2. Mateo JM

    (2009) Maternal Effects in Mammals

    University of Chicago Press.

    https://doi.org/10.7208/chicago/9780226501222.001.0001

    • Google Scholar
42. 1. Mirville MO
    2. Ridley AR
    3. Samedi JPM
    4. Vecellio V
    5. Ndagijimana F
    6. Stoinski TS
    7. Grueter CC

    (2018) Low familiarity and similar ‘group strength’ between opponents increase the intensity of intergroup interactions in mountain gorillas (Gorilla beringei beringei)

    Behavioral Ecology and Sociobiology 72:e2592-5.

    https://doi.org/10.1007/s00265-018-2592-5

    • Google Scholar
43. Book

    1. Mitani JC
    2. Call J
    3. Kappeler PM
    4. Palombit RA
    5. Silk JB

    (2013) The Evolution of Primate Societies

    University of Chicago Press.

    https://doi.org/10.7208/chicago/9780226531731.001.0001

    • Google Scholar
44. 1. Morrison RE
    2. Groenenberg M
    3. Breuer T
    4. Manguette ML
    5. Walsh PD

    (2019) Hierarchical social modularity in gorillas

    Proceedings of the Royal Society B: Biological Sciences 286:20190681.

    https://doi.org/10.1098/rspb.2019.0681

    • Google Scholar
45. 1. Morrison RE
    2. Eckardt W
    3. Stoinski TS
    4. Brent LJN

    (2020a) Comparing measures of social complexity: larger mountain Gorilla groups do not have a greater diversity of relationships

    Proc. R. Soc. B Biol. Sci 287:1026.

    https://doi.org/10.1098/rspb.2020.1026

    • Google Scholar
46. 1. Morrison RE
    2. Hirwa JP
    3. Mucyo JPS
    4. Stoinski TS
    5. Vecellio V
    6. Eckardt W

    (2020b) Inter‐group relationships influence territorial defence in mountain gorillas

    Journal of Animal Ecology 89:2852–2862.

    https://doi.org/10.1111/1365-2656.13355

    • Google Scholar
47. 1. Nakamura M
    2. Hayaki H
    3. Hosaka K
    4. Itoh N
    5. Zamma K

    (2014) Brief communication: orphaned male chimpanzees die young even after weaning

    American Journal of Physical Anthropology 153:139–143.

    https://doi.org/10.1002/ajpa.22411

    • PubMed
    • Google Scholar
48. 1. Nattrass S
    2. Croft DP
    3. Ellis S
    4. Cant MA
    5. Weiss MN
    6. Wright BM
    7. Stredulinsky E
    8. Doniol-Valcroze T
    9. Ford JKB
    10. Balcomb KC
    11. Franks DW

    (2019) Postreproductive killer whale grandmothers improve the survival of their grandoffspring

    PNAS 116:26669–26673.

    https://doi.org/10.1073/pnas.1903844116

    • Google Scholar
49. 1. Neumann C
    2. Duboscq J
    3. Dubuc C
    4. Ginting A
    5. Irwan AM
    6. Agil M
    7. Widdig A
    8. Engelhardt A

    (2011) Assessing dominance hierarchies: validation and advantages of progressive evaluation with Elo-rating

    Animal Behaviour 82:911–921.

    https://doi.org/10.1016/j.anbehav.2011.07.016

    • Google Scholar
50. Software

    1. Neumann C
    2. Lars K

    (2014) EloRating: Animal Dominance Hierarchies by Elo Rating, version 0.43

    R Packag. Version.

    https://rdrr.io/cran/EloRating/
51. 1. Nsubuga AM
    2. Robbins MM
    3. Boesch C
    4. Vigilant L

    (2008) Patterns of paternity and group fission in wild multimale mountain Gorilla groups

    American Journal of Physical Anthropology 135:263–274.

    https://doi.org/10.1002/ajpa.20740

    • PubMed
    • Google Scholar
52. 1. Reddy RB
    2. Mitani JC

    (2019) Social relationships and caregiving behavior between recently orphaned chimpanzee siblings

    Primates 60:389–400.

    https://doi.org/10.1007/s10329-019-00732-1

    • PubMed
    • Google Scholar
53. 1. Riedman ML

    (1982) The evolution of alloparental care and adoption in mammals and birds

    The Quarterly Review of Biology 57:405–435.

    https://doi.org/10.1086/412936

    • Google Scholar
54. 1. Robbins MM

    (1995) A demographic analysis of male life history and social structure of mountain gorillas

    Behaviour 132:21–47.

    https://doi.org/10.1163/156853995X00261

    • Google Scholar
55. Book

    1. Robbins MM
    2. Sicotte P
    3. Stewart KJ

    (2005) Mountain Gorillas: Three Decades of Research at Karisoke

    Cambridge University Press.

    https://doi.org/10.2307/3802725

    • Google Scholar
56. 1. Robbins AM
    2. Stoinski T
    3. Fawcett K
    4. Robbins MM

    (2009a) Leave or conceive: natal dispersal and philopatry of female mountain gorillas in the virunga volcano region

    Animal Behaviour 77:831–838.

    https://doi.org/10.1016/j.anbehav.2008.12.005

    • Google Scholar
57. 1. Robbins AM
    2. Stoinski TS
    3. Fawcett KA
    4. Robbins MM

    (2009b) Does dispersal cause reproductive delays in female mountain gorillas?

    Behaviour 146:426354.

    https://doi.org/10.1163/156853909X426354

    • Google Scholar
58. 1. Robbins AM
    2. Robbins MM

    (2005) Fitness consequences of dispersal decisions for male mountain gorillas (Gorilla beringei beringei)

    Behavioral Ecology and Sociobiology 58:295–309.

    https://doi.org/10.1007/s00265-005-0917-7

    • Google Scholar
59. 1. Rosenbaum S
    2. Hirwa JP
    3. Silk JB
    4. Vigilant L
    5. Stoinski TS

    (2015) Male rank, not paternity, predicts male–immature relationships in mountain gorillas, Gorilla beringei beringei

    Animal Behaviour 104:13–24.

    https://doi.org/10.1016/j.anbehav.2015.02.025

    • Google Scholar
60. 1. Rosenbaum S
    2. Vigilant L
    3. Kuzawa CW
    4. Stoinski TS

    (2018) Caring for infants is associated with increased reproductive success for male mountain gorillas

    Scientific Reports 8:e33380-4.

    https://doi.org/10.1038/s41598-018-33380-4

    • Google Scholar
61. 1. Samuni L
    2. Tkaczynski P
    3. Deschner T
    4. Löhrrich T
    5. Wittig RM
    6. Crockford C

    (2020) Maternal effects on offspring growth indicate post-weaning juvenile dependence in chimpanzees (pan Troglodytes verus)

    Frontiers in Zoology 17:1–12.

    https://doi.org/10.1186/s12983-019-0343-8

    • PubMed
    • Google Scholar
62. 1. Sear R
    2. Mace R
    3. McGregor IA

    (2000) Maternal grandmothers improve nutritional status and survival of children in rural Gambia

    Proceedings of the Royal Society of London. Series B: Biological Sciences 267:1641–1647.

    https://doi.org/10.1098/rspb.2000.1190

    • Google Scholar
63. 1. Sear R
    2. Mace R
    3. McGregor IA

    (2003) The effects of kin on female fertility in rural Gambia

    Evolution and Human Behavior 24:25–42.

    https://doi.org/10.1016/S1090-5138(02)00105-8

    • Google Scholar
64. 1. Sear R
    2. Mace R

    (2008) Who keeps children alive? A review of the effects of kin on child survival

    Evolution and Human Behavior 29:1–18.

    https://doi.org/10.1016/j.evolhumbehav.2007.10.001

    • Google Scholar
65. 1. Siler W

    (1979) A Competing-Risk model for animal mortality

    Ecology 60:750–757.

    https://doi.org/10.2307/1936612

    • Google Scholar
66. 1. Snyder-Mackler N
    2. Burger JR
    3. Gaydosh L
    4. Belsky DW
    5. Noppert GA
    6. Campos FA
    7. Bartolomucci A
    8. Yang YC
    9. Aiello AE
    10. O'Rand A
    11. Harris KM
    12. Shively CA
    13. Alberts SC
    14. Tung J

    (2020) Social determinants of health and survival in humans and other animals

    Science 368:eaax9553.

    https://doi.org/10.1126/science.aax9553

    • PubMed
    • Google Scholar
67. 1. Spiegelhalter DJ
    2. Best NG
    3. Carlin BP
    4. van der Linde A

    (2002) Bayesian measures of model complexity and fit

    Journal of the Royal Statistical Society: Series B 64:583–639.

    https://doi.org/10.1111/1467-9868.00353

    • Google Scholar
68. 1. Stanton MA
    2. Lonsdorf EV
    3. Murray CM
    4. Pusey AE

    (2020) Consequences of maternal loss before and after weaning in male and female wild chimpanzees

    Behavioral Ecology and Sociobiology 74:e2804-7.

    https://doi.org/10.1007/s00265-020-2804-7

    • Google Scholar
69. 1. Stoinski TS
    2. Vecellio V
    3. Ngaboyamahina T
    4. Ndagijimana F
    5. Rosenbaum S
    6. Fawcett KA

    (2009a) Proximate factors influencing dispersal decisions in male mountain gorillas, Gorilla beringei beringei

    Animal Behaviour 77:1155–1164.

    https://doi.org/10.1016/j.anbehav.2008.12.030

    • Google Scholar
70. 1. Stoinski TS

    (2009b) Patterns of male reproductive behaviour in multi-male groups of mountain gorillas: examining theories of reproductive skew

    Behaviour 146:1193–2115.

    https://doi.org/10.1163/156853909X419992

    • Google Scholar
71. 1. Strauss ED
    2. Shizuka D
    3. Holekamp KE

    (2020) Juvenile rank acquisition is associated with fitness independent of adult rank

    Proceedings of the Royal Society B: Biological Sciences 287:20192969.

    https://doi.org/10.1098/rspb.2019.2969

    • Google Scholar
72. 1. Surbeck M
    2. Mundry R
    3. Hohmann G

    (2011) Mothers matter! Maternal support, dominance status and mating success in male bonobos ( Pan paniscus )

    Proceedings of the Royal Society B: Biological Sciences 278:590–598.

    https://doi.org/10.1098/rspb.2010.1572

    • Google Scholar
73. 1. Surbeck M
    2. Boesch C
    3. Crockford C
    4. Thompson ME
    5. Furuichi T
    6. Fruth B
    7. Hohmann G
    8. Ishizuka S
    9. Machanda Z
    10. Muller MN
    11. Pusey A
    12. Sakamaki T
    13. Tokuyama N
    14. Walker K
    15. Wrangham R
    16. Wroblewski E
    17. Zuberbühler K
    18. Vigilant L
    19. Langergraber K

    (2019) Males with a mother living in their group have higher paternity success in bonobos but not chimpanzees

    Current Biology 29:R354–R355.

    https://doi.org/10.1016/j.cub.2019.03.040

    • PubMed
    • Google Scholar
74. 1. Tung J
    2. Archie EA
    3. Altmann J
    4. Alberts SC

    (2016) Cumulative early life adversity predicts longevity in wild baboons

    Nature Communications 7:e11181.

    https://doi.org/10.1038/ncomms11181

    • Google Scholar
75. 1. Vigilant L
    2. Roy J
    3. Bradley BJ
    4. Stoneking CJ
    5. Robbins MM
    6. Stoinski TS

    (2015) Reproductive competition and inbreeding avoidance in a primate species with habitual female dispersal

    Behavioral Ecology and Sociobiology 69:1163–1172.

    https://doi.org/10.1007/s00265-015-1930-0

    • Google Scholar
76. 1. Walker KK
    2. Walker CS
    3. Goodall J
    4. Pusey AE

    (2018) Maturation is prolonged and variable in female chimpanzees

    Journal of Human Evolution 114:131–140.

    https://doi.org/10.1016/j.jhevol.2017.10.010

    • PubMed
    • Google Scholar
77. 1. Watts DP

    (1984) Composition and variability of mountain Gorilla diets in the central virungas

    American Journal of Primatology 7:323–356.

    https://doi.org/10.1002/ajp.1350070403

    • PubMed
    • Google Scholar
78. 1. Watts HE
    2. Tanner JB
    3. Lundrigan BL
    4. Holekamp KE

    (2009) Post-weaning maternal effects and the evolution of female dominance in the spotted hyena

    Proceedings of the Royal Society B: Biological Sciences 276:2291–2298.

    https://doi.org/10.1098/rspb.2009.0268

    • Google Scholar
79. Book

    1. Whitehead H

    (2008) Analyzing Animal Societies: Quantitative Methods for Vertebrate Social Analysis

    University of Chicago Press.

    https://doi.org/10.7208/chicago/9780226895246.001.0001

    • Google Scholar
80. 1. Wright E
    2. Galbany J
    3. McFarlin SC
    4. Ndayishimiye E
    5. Stoinski TS
    6. Robbins MM

    (2019) Male body size, dominance rank and strategic use of aggression in a group-living mammal

    Animal Behaviour 151:87–102.

    https://doi.org/10.1016/j.anbehav.2019.03.011

    • Google Scholar
81. 1. Zipple MN
    2. Archie EA
    3. Tung J
    4. Altmann J
    5. Alberts SC

    (2019) Intergenerational effects of early adversity on survival in wild baboons

    eLife 8:e47433.

    https://doi.org/10.7554/eLife.47433

    • Google Scholar

Author details

1. Robin E Morrison

   1. Dian Fossey Gorilla Fund, Musanze, Rwanda
   2. Centre for Research in Animal Behaviour, University of Exeter, Exeter, United Kingdom

   Contribution

   Data curation, Formal analysis, Visualization, Writing - original draft, Writing - review and editing

   For correspondence

   rmorrison@gorillafund.org

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-9161-4734

2. Winnie Eckardt

   Dian Fossey Gorilla Fund, Musanze, Rwanda

   Contribution

   Conceptualization, Data curation, Formal analysis, Project administration, Writing - review and editing

   Competing interests

   No competing interests declared

3. Fernando Colchero

   1. Department of Mathematics and Computer Science, University of Southern Denmark, Odense, Denmark
   2. Interdisciplinary Center on Population Dynamics, University of Southern Denmark, Odense, Denmark

   Contribution

   Formal analysis, Visualization, Writing - review and editing

   Competing interests

   No competing interests declared

4. Veronica Vecellio

   Dian Fossey Gorilla Fund, Musanze, Rwanda

   Contribution

   Data curation, Project administration

   Competing interests

   No competing interests declared

5. Tara S Stoinski

   Dian Fossey Gorilla Fund, Musanze, Rwanda

   Contribution

   Conceptualization, Funding acquisition, Project administration, Writing - review and editing

   Competing interests

   No competing interests declared

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