1. Introduction
In polygynous mammals, male social relationships tend to be competitive as males vie for access to breeding opportunities [
1,
2]. Strong male associations are rare and are most common in species with male philopatry [
2]. However, most polygynous mammals also exhibit sexual segregation which allows all-male groups to form for portions of the year [
2,
3,
4,
5,
6,
7]. Associating in all-male groups may offer various benefits to males including protection from predators [
2,
8,
9], group defense of high-value resources or female groups [
2,
3,
5,
7,
10], and shared ecological knowledge of foraging opportunities [
2,
11].
Historically, mature bull elephants were considered completely solitary except when they were associating with female herds for breeding purposes [
12,
13,
14]. However, recent research provides clear evidence that bull elephants are more social than previously reported and that they often spend time in all-male groups [
4,
11,
15,
16,
17,
18]. Bull African elephants form all-male groups ranging from 2–40 individuals [
17], with the size of these groups varying seasonally, often in relation to resource abundance [
19]. Additionally, there is some evidence that bull Asian elephants form all-male groups in high-risk environments, including human-dominated landscapes, or to undertake high-risk activities such as crop-raiding or crossing roadways [
16,
18,
20]. This collaboration may reduce individual risk and increase survival [
18,
20].
Additional research indicates that the amount of time bulls spend alone, with female herds, and in bull groups varies throughout their lifetime [
4,
21,
22]. Young bulls are forced out of their natal herds between the ages of 9 and 15 years (African elephants 10–15 years, [
23]; Asian elephants 9–15 years, [
15]). These bulls often continue to occasionally associate with their natal herds as well as with all-male groups [
23,
24,
25]. Adolescent bulls (ages 11–20 years) spend more time alone and in all-male groups as they reach sexual maturity with the onset of musth and become completely independent from their natal herds [
24,
26,
27]. These adolescent bulls often preferentially associate with older males to learn important social and ecological information [
25,
27,
28], and with similarly-aged conspecifics as they practice sparring and other social interactions through play [
25,
28,
29,
30]. In African elephants, younger males follow older bulls to observe reproductive behaviors, explore novel foraging grounds, and undertake risky behaviors, especially in human-dominated landscapes [
11,
28]. Bull Asian elephant sociality is understudied due to many challenges including locating and following animals in forest habitats [
14,
31]. However, groups of Asian bulls who raid crops are often led by an older male, indicating that some behaviors are passed down to younger males through social learning [
18,
20,
32].
Mature male elephants undergo an annual musth cycle marked by increased testosterone production, decreased foraging, and increased roaming and aggression [
24,
27,
28,
29,
33,
34]. Musth appears to reduce direct competition with other males and increase mating opportunities [
35]. Musth is asynchronous in elephant populations, and in African elephants the presence of an older musth bull can suppress musth in younger males [
34,
35,
36,
37]. In South Africa, introducing mature bulls suppressed musth in adolescent males and decreased adolescent aggression towards white rhinos [
37]. Musth also directly affects bull elephant social groups; most often, musth bulls are solitary or associate with female herds instead of with other bulls [
27,
29].
Beyond patterns of association based on age and reproductive status, males may be more likely to associate with closely related conspecifics with whom they share a social history [
3,
4,
10,
38]. In many species, bachelor groups consist of closely related males and the increased survival of any individual is a form of kin selection (e.g., lions, [
3]; chimpanzees, [
38]; and bottlenose dolphins, [
7]). In elephants, younger bulls may socialize with more closely related bulls as they disperse from the same natal herd, and these associations can last throughout their lifetimes [
4]. Additionally, in long-lived species, older males may pass knowledge on to related males through association in a form of kin selection, similar to the role of grandmothers in both elephant and orca whale societies [
4,
39,
40,
41].
Elephant groups engage in both affiliative and agonistic social interactions, and all-male groups likely exhibit more agonistic behaviors than female herds [
42]. Affiliative behaviors in elephants include maintaining body contact, extending their trunk towards conspecifics, and playing, while agonistic behaviors can include both contact (e.g., sparring, kicking, pushing) and non-contact interactions (e.g., displaying, supplanting, charging) [
16,
43]. Agonistic interactions are rare even between bulls [
16] and often decrease over time after the introduction of a novel animal into an established group [
44]. Generally, animal managers consider high amounts of affiliative behavior and low amounts of agonistic behaviors indicators of good animal welfare [
45,
46,
47].
Historically, male elephants in managed care were housed alone except when they were temporarily placed with females for breeding purposes [
23,
48,
49]. However, with the growing body of evidence for male elephant sociality, institutions increasingly house their bull elephants in social groups [
23,
48,
49]. While some studies have documented the process of introducing a novel bull into an existing group [
44,
50,
51,
52], no studies that we are aware of have examined how individual bulls’ age or social history impact social interactions with other bulls during the process of social integration. As more institutions house bulls together, these shifts in management practice require a deeper understanding of the effects of individual bulls’ age and social histories to support management decisions.
We hypothesize that age impacts bull elephants’ social behavior. Specifically, we predict that adolescent bulls will engage in less contact and non-contact agonistic behaviors and spend more time engaging in affiliative and submissive behaviors, and less time in proximity, with mature conspecifics compared to other adolescents with whom they compete for similar positions in the social network. We expect that mature bulls will engage in more contact and non-contact agonistic behaviors and spend less time on affiliative and submissive behaviors, and less time in proximity, with adolescent conspecifics than with mature conspecifics in order to establish dominance.
We also hypothesize that previous social experience influences bull behavior. We predict that bulls will exhibit more affiliative behavior, spend more time in proximity, and engage in fewer contact agonistic, non-contact agonistic, and submissive behaviors with known conspecifics from previous social groups than with novel social partners as they establish a new social network.
4. Discussion
Overall, bull elephants’ age and social history impacted their social behavior and time in proximity, but not always in ways we predicted. With respect to our first hypothesis that age impacts bull elephants’ social behavior, the presence of a mature bull significantly affected adolescent bulls’ behavior, and the presence of adolescent bulls significantly altered mature bulls’ affiliative and contact agonistic behavior. As expected, adolescent bulls engaged in fewer agonistic behaviors and more affiliative and submissive behaviors with mature conspecifics than with only adolescent conspecifics. This pattern of increased affiliative behaviors and decreased submissive behaviors remained when focal adolescent bulls were in mixed-age groups consisting of mature and adolescent conspecifics, but there was no significant difference in the focal adolescents’ agonistic behavior in mixed-age groups. Including at least one mature male in social groups may temporarily reduce competition between adolescents, resulting in the increased affiliative behaviors that we observed in groups containing at least one mature bull. As more institutions house bull elephants together, animal managers can use this understanding of expected amounts of affiliative, agonistic, and submissive behaviors to inform which individuals to include in social groupings, especially during the introductory period. Specifically, managers might begin the introduction process by focusing on combining mature and adolescent bulls in small social groupings to promote low levels of agonism, while delaying housing groups together that only contain adolescent bulls as these groupings displayed the highest levels of agonism in our study. Further, empirically measuring rates of affiliative, agonistic, and submissive behavior in different social groupings empowers animal managers to choose to house bulls together based on specific measurements which could be compared to this study of the successful integration of two bull groups.
Mature bulls altered their behavior in different social groups, but the shifts were mostly contrary to our predictions. Interestingly, there was a significant increase in mature bulls’ affiliative behavior when they were housed with only adolescent bulls, and a similar increase in contact agonistic behavior in mixed-age groups, which had both mature and adolescent conspecifics, compared to groups with only the mature bulls. Unexpectedly, mature bulls spent more time in proximity with conspecifics when they were housed with at least one adolescent bull, compared to with the other mature male. Overall, the consistency of mature bulls’ behavior across social groups could indicate that bulls who reliably undergo musth hold more stable positions in bull social networks. For example, in wild African elephant populations older males held more central positions in social networks [
4]. Furthering our understanding of this social stability allows animal managers to anticipate bulls’ interactions and may indicate that mature bulls can mediate agonistic interactions between younger conspecifics.
For this study, we considered mature bulls to be animals who consistently underwent an annual musth period, which included Individual 2 (14 years old at the beginning of this study) and Individual 3 (49 years old at the beginning of this study). Both mature individuals were physically larger than the adolescent bulls; however, Individual 2 was still growing and while he underwent a musth period annually, the duration and timing of that period varied from year to year. The “mature bull” category covered a very large age range, and it is possible that our analysis did not capture more nuanced social interactions due to the discrepancy in age between the two mature males. Few institutions currently house Asian elephant bull groups, so it is difficult to ensure that bachelor groups include more than one mature adult of similar ages [
48,
49]. We are hopeful that as more facilities house multiple bulls, opportunities for socializing diverse age groups will increase, allowing for more bull groups that consist of multiple mature adults as well as multiple adolescent bulls. Anecdotally, the presence of the oldest bull (Individual 3) exerted a much larger influence on the adolescent bulls’ behavior than the presence of the newly mature male (Individual 2); the eldest bull directly interrupted sparring matches between adolescents on several occasions while we never observed the newly mature male actively intervening (Davis pers. comm.). Further investigation into the effects of a newly mature male versus a fully mature or geriatric male would elucidate the influence of older, dominant bulls on adolescent conspecifics.
Regarding our second hypothesis that bull elephants’ social history affects social behaviors, and as we expected, an established social history resulted in significant decreases in the odds of agonistic and submissive behaviors and a significant increase in the odds of being in proximity to a conspecific compared to when bulls were interacting in novel social combinations. These results indicate that at this stage of social integration, bulls may experience more social stress with new partners compared to established social partners. This difference may also represent a preference for engaging in more social interactions with novel bulls as the group establishes new social bonds and individuals vie for positions within the social network, which is further supported by the unexpected increase in affiliative behaviors that we observed in new social groups. As more facilities house bull Asian elephants together, animal managers can build upon previously established social bonds between bulls, especially during the stressful introductory period. For example, animal managers could group two bulls with an established positive social history together with a novel individual, especially when the newcomer is older or physically larger than the two established bulls.
This study ended approximately 11 months after Individuals 4 and 5 were first physically introduced to Individuals 1, 2, and 3. It is possible that it takes longer than that for such long-lived mammals to establish stable social relationships especially when socialization of mature bulls is decreased due to separation during periods of musth. For example, a study investigating the integration of a new adolescent bull into a bachelor group at Heidelberg Zoo found that the new bull engaged in more play and participated in more friendly interactions one year after introductions compared to the four months after his initial introduction [
44]. Future studies should compare groups’ social behaviors close to introduction and a few years later to expand our understanding of longer-term social dynamics between bull Asian elephants.
In range countries, adolescent bull elephants often associate with their natal herds and with other closely related young bulls [
4,
25,
28]. These social preferences can continue throughout the bulls’ lives, and some studies indicate that bulls are more likely to associate with closely related bulls throughout their lifetimes [
4]. These patterns of preferential association may support the kin selection hypothesis, whereby animals share ecological knowledge with closely related conspecifics to increase overall fitness [
58]. However, it is important to note that we cannot empirically separate a long social history and genetic relatedness in these cases. This study indicated that bull Asian elephants engaged in fewer agonistic and submissive behaviors with, and spent more time in proximity to, bulls with whom they had an established social history compared to novel social partners. We hypothesize that a long social history may support the close social bonds observed between related individuals in wild populations and serve to benefit the inclusive fitness of both animals by reducing conflict between related individuals.
Other variables in our models that significantly affected the bulls’ social interactions included time of day, access inside or outside, and introductory period. Bulls engaged in all social behaviors more often during the morning observation period compared to the afternoon or nighttime observation periods (
Appendix B). Bulls were also more socially active when they had access to both inside stalls and outdoor yards than when they were housed only indoors (
Appendix B). Previous studies indicated that more than exhibit size, social management and complexity can influence elephant welfare, and the enrichment provided from social interaction may improve animal welfare at institutions where exhibit size is limited [
48,
59,
60]. The bulls’ social behavior differed during the introductory period (the first 5 months after introductions began) compared to later in our study; generally, the bulls engaged in less social behavior during the introduction period compared to after the first five months (
Appendix B). Previous studies of both bull and cow introductions indicated that the initial introductory period is a time of increased stress, but that this stress decreases over time after introductions [
44,
61], which may account for the increased social behavior we observed once the bulls had at least five months of social interaction.
During this study we did not house the mature bulls socially when they were in musth or the adolescent bulls when they showed signs of moto-musth (e.g., temporal gland drainage; unprompted aggression towards facilities, conspecifics, or staff). However, musth bulls were still housed in the same building and in neighboring outdoor yards, so all bulls had auditory and olfactory access to an animal during musth. There is strong evidence for musth suppression of adolescent bulls in African elephants [
28,
34,
37], but much less is understood about the effects of musth in Asian elephant bull groups [
24,
35,
36]. The potential for concurrent or overlapping musth periods with Asian elephant bulls further complicates housing multiple bulls at one facility. Opportunities for future studies on the effects of Asian elephant sociality on musth continue to increase as more institutions house bulls together, and as some institutions focus on solely housing bull elephants.
While this study only included five Asian elephants at one facility, we provide an initial investigation into the effects of age and social history on bulls’ social interactions. As more institutions house bulls socially, we hope our results provide insights into some of the demographic and life-history factors that may affect bull social interactions during the introductory period and beyond. Improving animal welfare is our “duty of care” [
62] and as animal managers we can no longer disregard the evidence of bull elephant sociality [
48,
49,
63]. Bull elephants often exhibit more agonistic behaviors than females [
42], leading to common, and well-founded, concerns about socializing bulls in managed care. This study and similar investigations into bull elephant sociality prepare animal managers to plan species-appropriate social housing and support positive animal welfare, especially as populations of elephants in range countries face unprecedented changes and ex situ populations become increasingly valuable for conservation [
64].