The impact of oxytocin administration on social behavior in African lions

Abstract

Sociality is an incredibly complex aspect of mammalian behavior which is regulated by an array of internal and external factors (Ebensperger 2001; Insel & Young, 2000; Kutsukake 2009). African lions are on the extreme end of the social spectrum, displaying in-group egalitarianism, while eliciting fatal levels of out-group territorialism (Packer et al., 2001; Heinsohn 2007; Mosser & Packer, 2009). Many studies have been conducted on social behaviors in the wild, however, as human populations rapidly increase, “wild” territories decline, and naturally free-roaming social species are having to alter their social strategies to survive in closed systems (Magliolo et al., 2023; Miller et al., 2020), which has significant behavioral effects (Clubb & Mason, 2003). Oxytocin, a primary neuropeptide regulating social behavior in the brain (Insel 2010), has been shown to reverse social disturbances, promoting prosocial behavior (Smith & Wang, 2014; Takayanagi & Onaka, 2021; Burkhart et al., 2022). As outlined in the proceeding body of work, we have tested the effects of oxytocin on social behavior in captive African lions. We have investigated its effects on both in-group and out-group relationships, as well as in cooperative vs. competitive contexts. The aim of this work is to develop protocols using oxytocin to manage captive individuals, which can then be translated into a conservation setting. In our first study, we employed a proof-of-concept, testing oxytocin on groups of captive African lions in a sanctuary setting. We investigated whether 10 IUs of intranasal oxytocin administration could increase prosocial behaviors in both within- and between- group contexts. Both scenarios revealed a positive prosocial impact. Familiar, mixed-sex groups all showed increased prosocial behavior and increased tolerance toward group mates in the presence of a non-food play object, as well as decreased vigilance towards an out-group intruder, simulated by the playback of a recorded roar by an unfamiliar lion. Between-group contexts are rarely investigated in the oxytocin literature, and we found a significant prosocial effect when confronted with a stranger’s roar. Not only were we able to confirm that the dosage was appropriate to elicit a positive response, but we found that oxytocin could be a potential tool for behavioral management in carnivores. For our second study, we wanted to further test the effects of oxytocin between out-group members to determine whether oxytocin could be used to facilitate relationships between unfamiliar individuals. This is important because many reserves are fenced, and managers rely on artificial group formation for reintroduction of lions. We developed a protocol in which we implemented intermittent doses of oxytocin either to pairs of unfamiliar individuals for socializations, or to pairs and groups of lions or tigers who were experiencing persistent antagonistic behaviors toward each other. In all 7 scenarios (N=16 lions), positive interaction was either observed for the first time, or restored among members, and in 6 out of 7 groups, stable long-term bonds were maintained. Again, we found oxytocin to be a promising aid for captive management, with serious potential to assist in conservation efforts. For our third study, we took a closer look at oxytocin’s effects on competition between familiar pairs of lions, namely on what appeared to be the development of dominant-subordinate relationships in captivity between females that are ordinarily egalitarian in the wild. Firstly, we had to determine whether dominance hierarchies did, in fact, exist, and secondly, to test whether oxytocin could mitigate these behavioral asymmetries. This study built on our first body of work, which included a food object trial that had not been designed to elicit the specifics of resource possession and the “ownership” rule. We also sought to further investigate the social salience hypothesis of oxytocin, in order to better understand how oxytocin can facilitate reactions across both cooperative, as well as competitive, contexts, so as to provide a more well-rounded understanding of oxytocin’s potential as a management tool. In this work, not only did we determine strong asymmetrical relationships with clear dominance hierarchies between pairs of female lions, but we also found that oxytocin ameliorated these behavioral asymmetries- decreasing submissive behavior by increasing levels of aggression in subordinates as well as increasing their rate of possession of the resource, thus restoring the natural egalitarianism that we expect in African lions. Our complete body of work has helped to elucidate oxytocin’s potential as a management tool in African lions and tigers. Not only will these models apply to additional carnivore species, but we are exploring the implementation of our methods for conservation efforts which will aid an array of endangered social species as they are managed by humans for survival.