1. Ecology
  2. Evolutionary Biology
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Social groups buffer maternal loss in mountain gorillas

  1. Robin E Morrison  Is a corresponding author
  2. Winnie Eckardt
  3. Fernando Colchero
  4. Veronica Vecellio
  5. Tara S Stoinski
  1. Dian Fossey Gorilla Fund, Rwanda
  2. Centre for Research in Animal Behaviour, University of Exeter, United Kingdom
  3. Department of Mathematics and Computer Science, University of Southern Denmark, Denmark
  4. Interdisciplinary Center on Population Dynamics, University of Southern Denmark, Denmark
Research Article
Cite this article as: eLife 2021;10:e62939 doi: 10.7554/eLife.62939
3 figures, 5 tables and 2 additional files

Figures

Figure 1 with 1 supplement
Survivorship curves for each of the four maternal loss categories for each sex.

Plots show the proportion of surviving (a) females (n = 98) and (b) males (n = 102) that suffered maternal loss as infants, juveniles, and subadults compared to non-orphans that did not suffer maternal loss under the age of 8 years. Figure 1—figure supplement 1 shows survivorship curves of each orphan age and sex class plotted separately against non-orphans for further clarity. Grey dashed line indicates the age from which orphan and non-orphan survival are modelled separately.

Figure 1—figure supplement 1
Orphan survivorship curves separated by age and sex class.
Figure 2 with 1 supplement
The change in proximity-based social network position (eigenvector centrality, weighted degree, and binary degree) for orphaned (n = 28) and non-orphaned immature gorillas (n = 108) within the same group in the 6 months before an incident of maternal loss and the 6 months after.

Weighted degree and binary degree values are calculated as proportions of the greatest value observed within their specific network to enable comparison across multiple networks (multiple incidents of maternal loss). Networks include only individuals that were present both before and after maternal loss and therefore exclude the mothers of orphans. Blue lines and shading indicate mean and 95% confidence interval. Figure 2—figure supplement 1 shows the change in affiliative contact-based social network position. Source data available in file: ‘Figure 2—source data 1’.

Figure 2—source data 1

Changes in the network position of orphaned and non-orphaned immature gorillas following an incident of maternal loss.

https://cdn.elifesciences.org/articles/62939/elife-62939-fig2-data1-v1.xlsx
Figure 2—figure supplement 1
The change in affiliative contact-based social network position (eigenvector centrality, proportional weighted degree, and proportional binary degree) for orphaned and non-orphaned immature gorillas within the same group in the 6 months before an incident of maternal loss and the 6 months after. Blue lines and shading indicate mean and 95% confidence interval.
Figure 3 with 2 supplements
The change in relationship strength (SRI) between immature gorillas and other group members in both affiliative contact and proximity, between the 6 months prior to an incident of maternal loss and the 6 months post-maternal loss (n relationships = 3592, orphaned immature gorillas = 31, non-orphaned immature gorillas = 51).

Black points show values for orphans, and grey points show values for immature gorillas within the same group that did not suffer maternal loss. Error bars indicate the standard error. Dashed red line indicates no change in relationship strength. NS indicates no significant difference between orphan and non-orphan changes in relationship strength, * indicates significance at <0.05, ** indicates significance at <0.01, and *** indicates significance at <0.001. Exact p-values (L to R), contact: <0.001, 0.001, 0.997, 0.280, 0.122, 0.021, 0.941, 0.019; proximity: 0.006, 0.009, 0.004, 0.265, 0.680, <0.001, <0.001, 0.328. Source data available in file: ‘Figure 3—source data 1’. Figure 3—figure supplement 1 shows the change in relationship strength between orphans and group members that were their maternal siblings (dark blue) and those that were not (light blue) after maternal loss based on (A) affiliative contact and (B) proximity. Figure 3—figure supplement 2 shows the change in relationship strength between orphans and dominant and subordinate adult male group members by kinship after maternal loss based on (A) affiliative contact and (B) proximity.

Figure 3—source data 1

Changes in dyadic relationship strengths following an incident of maternal loss within a gorilla group.

https://cdn.elifesciences.org/articles/62939/elife-62939-fig3-data1-v1.xlsx
Figure 3—figure supplement 1
The change in relationship strength between orphans and group members that were their maternal siblings (dark blue) and those that were not (light blue) after maternal loss based on (A) affiliative contact and (B) proximity.

DSB: dominant silverback male, SB: subordinate silverback male, AF: adult female, BB: blackback male, SAM: subadult male, SAF: subadult female, JUV: juvenile, INF: infant.

Figure 3—figure supplement 2
Change in relationship strength between orphans and dominant and subordinate adult male group members by kinship after maternal loss based on (A) affiliative contact and (B) proximity.

Tables

Table 1
Cox-proportional hazards models showing the effects of the four maternal loss categories: infants, juveniles, subadults, and non-orphans, for each sex (98 females and 102 males), on survival.

All results are relative to the non-orphan class.

FemalesMales
Age-classEst ± SEpEst ± SEp
Infants0.73 ± 0.5920.218−0.34 ± 0.5510.540
Juveniles1.22 ± 1.1700.2980.05 ± 1.0600.959
Subadults1.77 ± 1.2400.1520.59 ± 1.1100.591
Table 2
Deviance information criterion (DIC) for the three models tested.

(a) No covariates (i.e. null model where all individuals have the same hazard rate); (b) proportional hazards (where mortality differs proportionally between orphan classes); (c) covariates modifying all Siler mortality parameters (where each orphan class has a different age-specific mortality), for each sex (98 females and 102 males). The delta DIC shows the difference in DIC from the model with lowest DIC.

FemalesMales
ModelDICΔ DICDICΔ DIC
No covariates371.460486.080
Prop. hazards374.162.71486.440.36
All mortality parameters377.045.59499.4613.38
Table 3
The influence of age at maternal loss (infant or juvenile/subadult (J/SA)) relative to non-orphans on a female’s decision to disperse from their natal group prior to their first birth and a male’s decision to disperse prior to the age of 16, modelled using binomial generalized linear models.
Females (n = 51)Males (n = 53)
Est ± SETPEst ± SETp
Intercept−0.511 ± 0.365−1.3990.162−0.511 ± 0.327−1.5640.118
Infant0.693 ± 0.7070.9800.327---
J/SA1.609 ± 0.8941.7990.0722.216 ± 0.8352.6530.008
Table 4
The percentage of gorilla orphans for which their mother was their closest social partner prior to maternal loss based on affiliative contact and proximity within 2 m.
ContactProximity
Infants (n = 9)89%78%
Juveniles (n = 14)86%79%
Subadults (n = 8)25%75%
Table 5
GAMMs predicting the change in dyadic relationship strength (SRI values for affiliative contact and proximity) between orphans (O) and other group members (GM) following maternal loss (n = 755).
Affiliative contactProximity
Est ± SEZpEst ± SEZp
Intercept0.028 ± 0.0055.508<0.0010.058 ± 0.0183.1800.002
Orphan
Age (years)−0.001 ± 0.000−1.6400.101−0.004 ± 0.002−2.0330.042
Sex (male)0.000 ± 0.002−0.0340.973−0.003 ± 0.006−0.5030.615
Group member
Age-mate (within 2 years)−0.001 ± 0.002−0.6230.5340.020 ± 0.0072.8850.004
Maternal sibling−0.014 ± 0.011−1.3050.1920.010 ± 0.0370.2840.777
Group member age/sex class (relative to a dominant male)
Adult male (subordinate)−0.023 ± 0.005−4.911<0.001−0.033 ± 0.017−1.9730.049
Adult female−0.024 ± 0.005−5.083<0.001−0.016 ± 0.017−0.9590.338
Blackback male−0.023 ± 0.005−4.731<0.001−0.032 ± 0.018−1.7820.075
Subadult male−0.026 ± 0.005−4.801<0.001−0.021 ± 0.020−1.0380.299
Subadult female−0.018 ± 0.005−3.2050.001−0.003 ± 0.020−0.1510.880
Juvenile−0.021 ± 0.005−3.930<0.001−0.002 ± 0.019−0.1240.902
Infant−0.021 ± 0.005−4.224<0.001−0.006 ± 0.018−0.3340.738
Age/sex class–sibling interaction (relative to a non-sibling dominant male)
Adult male (sub.) sibling0.041 ± 0.0133.2100.0010.052 ± 0.0431.2310.219
Adult female sibling0.015 ± 0.0141.0160.310−0.048 ± 0.048−0.9860.324
Blackback male sibling0.004 ± 0.0150.2430.808−0.044 ± 0.049−0.8960.371
Subadult male sibling0.001 ± 0.0170.0420.966−0.107 ± 0.057−1.8760.061
Subadult female sibling0.058 ± 0.0173.3870.0010.011 ± 0.0580.1970.844
Juvenile sibling−0.020 ± 0.021−0.9550.340−0.118 ± 0.072−1.6430.101
Infant sibling−0.004 ± 0.015−0.2820.778−0.096 ± 0.052−1.8500.065
  1. Smooth term: s(mean focal scans) Contact: F = 6.955, p=0.008; Proximity: F = 7.288, p<0.001.

Table 5—source data 1

Model: relationship change ~ age_O + sex_O + age mate + age sex class_GM * sibling + s(MeanDen), random = ~(Group|ID_O) + (1|ID_GM).

https://cdn.elifesciences.org/articles/62939/elife-62939-table5-data1-v1.xlsx

Additional files

Supplementary file 1

Supplementary Tables 1–7 including analyses with merged juvenile and subadult orphan classes, information on group composition, and sampling at each incident of maternal loss and GAMMs predicting the change in both orphan and non-orphan network position and social relationships.

https://cdn.elifesciences.org/articles/62939/elife-62939-supp1-v1.docx
Transparent reporting form
https://cdn.elifesciences.org/articles/62939/elife-62939-transrepform-v1.docx

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