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

ABSTRACT Compensatory social behavior in nonhuman animals following maternal loss has been documented, but understanding of how orphans allocate bonding to reconstruct their social networks

is limited. Successful social integration may be critical to survival and reproduction for highly social species and, therefore, may be tied to population persistence. We examined the social

partners involved in affiliative interactions of female orphans and non-orphans in an elephant population in Samburu, northern Kenya that experienced heightened adult mortality driven by

drought and intense ivory poaching. We contrasted partners across different competitive contexts to gain insight to the influence of resource availability on social interactions. Though the

number of partners did not differ between orphans and non-orphans, their types of social partners did. Orphans interacted with sisters and matriarchs less while feeding than did non-orphans,

but otherwise their affiliates were similar. While resting under spatially concentrated shade, orphans had markedly less access to mature adults but affiliated instead with sisters, bulls,

and age mates. Orphan propensity to strengthen bonds with non-dominant animals appears to offer routes to social integration following maternal loss, but lack of interaction with adult

females suggests orphans may experience decreased resource access and associated fitness costs in this matriarchal society. SIMILAR CONTENT BEING VIEWED BY OTHERS COOPERATIVE PARTNER CHOICE

IN MULTI-LEVEL MALE DOLPHIN ALLIANCES Article Open access 25 March 2021 SOCIAL SUPPORT CORRELATES WITH GLUCOCORTICOID CONCENTRATIONS IN WILD AFRICAN ELEPHANT ORPHANS Article Open access 14

July 2022 SHARING AND CARING: TESTOSTERONE, FATHERING, AND GENEROSITY AMONG BAYAKA FORAGERS OF THE CONGO BASIN Article Open access 22 September 2020 INTRODUCTION Strong mother-offspring

bonds are widespread in philopatric species1. The importance of these bonds is demonstrated by the adverse consequences documented for orphans across species, including lower life

expectancy2,3, decreased physical condition4,5, and stunted vocal behavior6. Social processes may be especially predictive of the consequences of orphaning. For example, offspring survival

in baboons7 and horses8 is tied to the social relationships of mothers. The absence of those social relationships may therefore be expected to have detrimental effects on orphans, especially

for species highly dependent on social bonds2,9,10. Remaining socially integrated presents a challenge for orphans given the loss of their mothers’ social influence. However, compensatory

behavior has been documented in some species11,12,13,14, and access to important social partners is known to increase survival15,16. Orphans may therefore strive to mitigate the impacts of

maternal loss through compensatory social behavior. Though compensatory bonding is not well studied in nonhuman animals, it may be an important avenue by which sociality influences fitness.

Social behavioral comparisons between orphans and non-orphans provide a powerful framework to explore compensatory bonding. Because the number of strong relationships individuals can

maintain is limited, animals should bond with those that offer the greatest social benefit. In female baboons, preferences follow a hierarchy of availability of relatives: in the absence of

mothers, baboons bond strongly with maternal kin, and in the absence of maternal kin they bond with paternal kin or nonrelatives12. Baboon society is highly nepotistic17, and the prevalence

of these patterns across taxa with different social structures is unknown. In species disproportionately reliant on older individuals18,19, bonding with older conspecifics following maternal

loss may be expected to take precedence over bonding with relatives. Female African savannah elephants (_Loxodonta africana_) form matriarchal societies in which daughters remain with their

mothers and other female relatives in multi-generational groups for life20,21. The disproportionate poaching of older elephants for their larger ivory22,23 removes critical social partners

that offer ecological knowledge and resource access19,24,25. Aberrant behavior has been recorded in male elephant orphans that experienced impoverished social environments10. Recovery of

elephant populations may in part depend on the ability of orphans to remain socially integrated following maternal loss. Because of their decades-long reliance on their mothers and the

relationship of maternal loss to the current ivory poaching crisis26,27, elephants provide a highly relevant wild system in which to investigate orphan bonding patterns. Elephants’ social

patterns are structured by relatedness, as in other species1,21,28, but studies of disrupted populations suggest bonds with nonrelatives may replace those with relatives29,30,31,32. The weak

influence of nepotism in elephants33,34 also indicates a reduced reliance on kin relative to other species17. In this study, we extend previous work on partner preference12 to a different

social system to broaden understanding of the process of orphan social integration. We followed the social behavior of orphan and non-orphan female elephants in the Samburu population in

northern Kenya following drought and during a persistent period of poaching22,26, testing the prediction that orphans shift allocation of bonding effort to maternal relatives. Because

resource access structures social interaction, we separated behaviors during foraging of generally widely distributed resources and resting in spatially concentrated shade. We expected

orphans to interact less with dominant individuals while resting when competition is greater. We discuss the implications of our results for long term orphan social integration and elephant

population recovery. RESULTS Number of affiliative partners per time followed did not significantly differ between orphans and non-orphans at the α = 0.05 level (Kruskal-Wallis Rank Sum

Test: Feeding: χ2 = 0.017, p = 0.897; Resting: χ2 = 0.004, p = 0.949). However, we found a significantly lower age difference between orphans and their adult/older female social partners

(excluding bulls) while resting (Kruskal-Wallis Rank Sum Test: χ2 = 6.259, p = 0.012) but not while feeding (Kruskal-Wallis Rank Sum Test: χ2 = 1.855, p = 0.173) relative to that of

non-orphans. Related to the generally stronger interactions with bulls by orphans relative to non-orphans, we did not find significant differences in the age differences between the two

across all social partners (Feeding: χ2 = 1.603, p = 0.206; Resting: χ2 = 0.483, p = 0.487). While feeding, both orphans and non-orphans preferentially interacted with calves, age mates, and

bulls (Tables 1 and 2; Fig. 1). Non-orphans were more likely to interact with sisters relative to orphans, and demonstrated preference for their mothers. Aunts were unlikely feeding

affiliation partners for both orphans and non-orphans, and orphans were unlikely to affiliate with matriarchs when feeding. Younger orphans demonstrated more feeding affiliation, but orphans

that lost their mothers at an older age had more affiliative interactions while feeding (Table 1). Orphans were more likely to interact with sisters and bulls while resting than were

non-orphans (Tables 1 and 2). Resting non-orphans tended to affiliate more with calves than did orphans, but orphans tended to affiliate more with age mates than did non-orphans. Resting

orphans tended not to affiliate with matriarchs, and resting non-orphans tended to affiliate with their mothers (Fig. 2). In contrast to feeding, resting orphans that lost their mothers at

an earlier age affiliated more (Table 1). DISCUSSION The ability of orphans to adjust to their new circumstances presents a considerable challenge in socially dependent animals. Field

studies of wild populations have demonstrated compensatory behavior of orphans in different taxa11,13, but the process of social integration following maternal loss is not well understood.

Access to more experienced animals is thought to be one of the primary benefits of tight knit elephant social structure19,25, and whether or not orphans are able to compensate for lost

relationships with adults may be consequential for their survival and reproduction. Our comparisons of social behavior in elephant orphans and non-orphans in this wild population offer

insight into the drivers of elephant sociality and the challenges of orphaning in this society. Our models indicated strong differences between orphan and non-orphan interaction partners,

particularly while resting. Interactions while resting suggested that non-orphans affiliate more with young calves and their mothers, while orphans were primarily with younger individuals in

the aggregation, notably sisters, age mates, and bulls. While feeding (behavior focused on widely distributed resources), both orphans and non-orphans exhibited more diverse social

partners. Differences were apparent, however, most notably in avoidance of matriarchs by orphans and the lack of their mother as a social partner. The loss of their mother and apparently

related changes in their social interactions indicate that orphans lack direct access to mature female elephants. By assessing social contexts across activities with different resource

competition, we gained insight to the implications of the observed loss of social access for orphans5. Reducing potential conflicts may be important to orphans when interacting in

potentially competitive circumstances. We did not expect to find support for this during feeding when resources are more widespread, but orphans nonetheless exhibited lower than average

interaction rates with matriarchs while feeding. Despite the widespread nature of foraging resources in this system, elephants exhibit clear preferences among resource patches35. The more

limited social interaction between orphans and matriarchs while foraging indicates that access to high quality resource patches may vary depending on family history. Relatedly, the best

positions during resting are typically secured by older, more dominant animals, when competition for limited shade is common24,33. Anecdotally, non-orphans tended to cluster at the core of

family groups, whereas orphans were observed to occupy peripheral positions external to the group (Fig. 3), often in proximity to lower social status bulls, age mates, or sisters. These

observations may also explain why non-orphans were more likely to interact with young calves while resting, which tend to be at the core of resting groups. Our results are consistent with a

study of reindeer that found greater distances of orphans to adult females than non-orphans to adult females, especially in the context of spatially concentrated resources5. Lost

opportunities to access needed resources may be an important factor for orphan fitness across taxa. The differences apparent between orphans and non-orphans in access to older elephants

suggest disadvantages to being orphaned. Similar to baboons11,12, elephant orphans increase affiliation with sisters in response to maternal loss (at least while resting), which may buffer

them from the costs of orphaning. However, their compensatory bonding largely did not include adults (Fig. 2). Older female elephants confer known fitness advantages to their affiliates via

ecological knowledge36, dominance24, social knowledge19, and calf survival15,16. Loss of access to mature animals, therefore, may lower the fitness of orphans via several mechanisms in this

matriarchal society. Previous work has documented altered association patterns among female elephants in response to mortality, such that core social groups (defined by association patterns)

are sometimes comprised of nonrelatives13,32,37. While this previous work demonstrates their behavioral flexibility in times of disruption, our current study provides finer scale detail on

the social environments they experience. The behavioral flexibility and social processes of orphans are likely critical to population recovery in the face of the recent continental poaching

crisis. Future work should investigate how decreased access to knowledge repositories of adult elephants and compensatory social behavior alter fitness trajectories for this keystone

species. METHODS DATA COLLECTION We conducted near daily transects in Samburu and Buffalo Springs National Reserves in northern Kenya between May 2012 and April 2015 and between August and

September 2017. Aggregations of elephants were encountered randomly along transects. For each aggregation, we recorded the individuals present and whether all breeding females were

observed38. Association indices between pairs of elephants derived from high quality observations39 were used to define core social group membership, the strongest level of bonding in female

elephant society13,38. While female elephants are usually found with their core social group, aggregations of elephants on any given day may consist of any combination of core groups and

independent bulls, such that social context changes frequently38. Co-occurrence in aggregations was used to control for the availability of two elephants to interact in analyses (see below).

To determine the fine scale social patterns of elephants, we conducted focal follows (up to 30 minutes) of non-parous female elephants between six and 17 years old encountered along

transects (Feeding: Norphans = 28, Nmedian (IQR) minutes/orphan = 387.38 (96.75–540.19), Nmedian (IQR) follows/orphan = 20 (4.75–30), Nnon-orphans = 19, Nmedian (IQR) minutes/non-orphan = 

310.5 (119–386.13), Nmedian (IQR) follows/non-orphan = 19 (6–23.5); Resting: Norphans = 30, Nmedian (IQR) minutes/orphan = 57 (30–86.88), Nmedian (IQR) follows/orphan = 3 (2–5), Nnon-orphans

 = 18, Nmedian (IQR) minutes/non-orphan = 57.5 (34.13–86.19), Nmedian (IQR) follows/non-orphan = 2.5 (2–4.75); total sampling hours = 246.12 feeding and 49.14 resting; Supplementary Material

Fig. 1). To control for behavioral autocorrelation, no more than one focal follow in a particular activity was completed on a given animal in a given sampling day, and follows were

terminated before reaching 30 minutes if the animal went out of sight or switched activity. Competition for resources is expected to differ between feeding and resting because shade is a

limited point resource whereas forage is more diffusely distributed. We therefore distinguished between focal follows collected during the two activities (so that a maximum of 60 minutes was

collected on a focal animal in one day: 30 minutes resting and 30 minutes feeding). Sampling spanned both wet and dry seasons, and focal follows were only initiated if elephants appeared

unperturbed by the research vehicle. During focal follows we recorded any interactions with other elephants33,40,41,42. For this study on social bonding, we restricted analysis to

affiliative interactions indicative of bonding including bodily contact, trunk touching, greeting, allomothering, play behavior, and reaching a trunk to another elephant’s mouth40. We

conducted research with permission from the Kenya Wildlife Service, Samburu and Isiolo governments, and Colorado State University (IACUC 12–3414 A), and all methods adhere to relevant

guidelines and regulations. Data used in this study are included as Supplementary Material. DATA ANALYSIS In order to determine general differences between orphans and non-orphans, we

conducted Kruskal-Wallis rank sum tests to assess the number of social partners per time followed and the age differences between social partners and focal animals. We conducted an

additional Kruskal-Wallis rank sum test on age differences including only female partners older than focal animals to more directly assess affiliation with older individuals in female

society. To understand how orphans and non-orphans differ in the categories of their social partners, we constructed four hierarchical Bayesian negative binomial regression models with

uninformative priors predicting affiliative interactions with social partners during different activities (orphans feeding, non-orphans feeding, orphans resting, non-orphans resting). We

used the following process model: $$\mathrm{ln}({\lambda }_{i,j})={\alpha }_{j}+{\boldsymbol{\beta }}{{\boldsymbol{x}}}_{i,j}+\,\mathrm{ln}({\gamma }_{i,j}),$$ (1) where _λ_ _i,j_ is the

expected interaction count for elephant _j_ with social partner _i_ (across all focal follows of elephant _j_ during which social partner _i_ was observed in the same aggregation), _α_ _j_

is the random intercept for elephant _j_, _Β_ represents the vector of fixed effects coefficients associated with covariates _X_, and ln(_γ_ _i,j_ ) is an offset controlling for sampling

effort (the total number of focal minutes for elephant _j_ during which social partner _i_ was observed in the aggregation and therefore available to interact). The conditional probability

was defined as: $$({y}_{i,j}|{\boldsymbol{\beta }},{\alpha }_{j},{\mu }_{\alpha },{\tau }_{\alpha },r)\sim negbinom({p}_{i,j},r)$$ (2) $${\boldsymbol{\beta }}\, \sim normal(0,0.1)$$ (3)

$${\alpha }_{j}\, \sim normal({\mu }_{\alpha },{\tau }_{\alpha })$$ (4) $${\mu }_{\alpha }\, \sim normal(0,0.1)$$ (5) $${\tau }_{\alpha } \sim uniform(0.001,100)$$ (6) $$r\, \sim

uniform(0,100)$$ (7) where _µ_ _α_ and _τ_ _α_ are the mean and precision of _α_ _j_ , respectively, _r_ is the dispersion parameter, and _p_ _i,j_ is the probability that an interaction

occurs. Predictor variables included social partner categories and control variables that might affect interactions using information available from the long-term records of the population

(Table 3). No covariates included in a model were correlated above r = |0.7|. We fit models using JAGS43 and the _rjags_ package in R44,45 with Markov-Chain Monte Carlo by running three

parallel chains of 100,000 iterations each, and discarded the first 10% of iterations as burn-in after assessing convergence indicated by Gelman-Rubin diagnostic values < 1.146.

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from iterative simulation using multiple sequences. _Stat. Sci._ 7, 457–511 (1992). Article  Google Scholar  Download references ACKNOWLEDGEMENTS The Kenyan Office of the President, the

Kenya Wildlife Service, and the Samburu and Isiolo governments gave us permission to work in the national reserves. We thank David Daballen, Jerenimo Lepirei and Iain Douglas-Hamilton for

facilitating data collection. Elizabeth Archie, Kevin Crooks, and Dhruba Naug offered constructive feedback on an earlier version of this manuscript, and Kristin Broms assisted in model

design. This work was funded by National Science Foundation Graduate Research Fellowship DGE-1321845 (S.Z.G.), Save the Elephants, Warner College of Natural Resources and Graduate Degree

Program in Ecology at Colorado State University, and through the generous support of Singer Rankin and WorldWomenWork. AUTHOR INFORMATION AUTHORS AND AFFILIATIONS * Department of Fish,

Wildlife, and Conservation Biology, Fort Collins, CO, 80523, USA Shifra Z. Goldenberg & George Wittemyer * Save the Elephants, Nairobi, 00200, Kenya Shifra Z. Goldenberg & George

Wittemyer Authors * Shifra Z. Goldenberg View author publications You can also search for this author inPubMed Google Scholar * George Wittemyer View author publications You can also search

for this author inPubMed Google Scholar CONTRIBUTIONS S.Z.G. and G.W. designed the study, S.Z.G. collected and analyzed the data, and S.Z.G. and G.W. wrote the manuscript. CORRESPONDING

AUTHOR Correspondence to Shifra Z. Goldenberg. ETHICS DECLARATIONS COMPETING INTERESTS The authors declare that they have no competing interests. ADDITIONAL INFORMATION PUBLISHER'S

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CITE THIS ARTICLE Goldenberg, S.Z., Wittemyer, G. Orphaned female elephant social bonds reflect lack of access to mature adults. _Sci Rep_ 7, 14408 (2017).

https://doi.org/10.1038/s41598-017-14712-2 Download citation * Received: 07 June 2017 * Accepted: 13 October 2017 * Published: 31 October 2017 * DOI:

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