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Tibetan Macaques with Higher Social Centrality and More Relatives Emit More Frequent Visual Communication in Collective Decision-Making

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Tibetan Macaques with Higher Social Centrality and More Relatives Emit More Frequent Visual Communication in Collective Decision-Making animals Article Tibetan Macaques with Higher Social Centrality and More Relatives Emit More Frequent Visual Communication in Collective Decision-Making Zifei Tang 1,2, Xi Wang 1,2,*, Mingyang Wu 2,3, Shiwang Chen 2,3 and Jinhua Li 1,2,4,* 1 School of Resources and Environmental Engineering, Anhui University, Hefei 230601, China; [email protected] 2 International Collaborative Research Center for Huangshan Biodiversity and Tibetan Macaque Behavior Ecology, Hefei 230601, China; [email protected] (M.W.); [email protected] (S.C.) 3 School of Life Sciences, Anhui University, Hefei 230601, China 4 School of Life Sciences, Hefei Normal University, Hefei 230601, China * Correspondence: [email protected] (X.W.); [email protected] (J.L.) Simple Summary: It is well known that visual communication plays an important role in collective decision-making. However, there is not much research on the influencing factors of visual signals, especially kinship and social relations. In this study, we not only confirmed the function of visual communication in collective decision-making, but also found the effect of kinship and social relations on visual communication. Tibetan macaques with higher social centrality and more relatives emit more frequent visual communication, providing a reference for further research on decision-making. Understanding the link between communication and decision-making can elucidate the powers of group maintenance in animal societies. Citation: Tang, Z.; Wang, X.; Wu, M.; Chen, S.; Li, J. Tibetan Macaques with Abstract: Animals on the move often communicate with each other through some specific postures. Higher Social Centrality and More Previous studies have shown that social interaction plays a role in communication process. However, Relatives Emit More Frequent Visual it is not clear whether the affinity of group members can affect visual communication. We studied Communication in Collective a group of free-ranging Tibetan macaques (Macaca thibetana) at Huangshan Mountain, China, and Decision-Making. Animals 2021, 11, answered whether and how social centrality or relatives matter in visual signals during group 876. https://doi.org/10.3390/ movement using Tobit regression modeling. All individuals emitted the signals of back-glances ani11030876 and pauses in collective movement. The emission of two signals decreased with the number of participants increased. The back-glance and pause signals emitted by the participating individuals Academic Editor: Charles Snowdon were stronger as the position moved backward in the group. Sex, age, and rank had no significant Received: 16 February 2021 influence on back-glance and pause signals. Individuals with higher social centrality would emit Accepted: 14 March 2021 more pause signals, but social centrality had no effect on the back-glance signal. Individuals with Published: 19 March 2021 more relatives in the group had more back-glance signals, but this had no effect on the pause signal. This study verifies that social centrality and the number of relatives have effects on visual signals in Publisher’s Note: MDPI stays neutral Tibetan macaques. We provide insights into the relationship between communication behaviors and with regard to jurisdictional claims in group cooperation in social animals. published maps and institutional affil- iations. Keywords: Tibetan macaques (Macaca thibetana); collective decision-making; visual communication; social centrality; number of relatives Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. 1. Introduction This article is an open access article To maintain group cohesion, social animals need to achieve collective movement distributed under the terms and in a cooperative manner, which facilitates information sharing, benefits reciprocity, and conditions of the Creative Commons collective defense [1,2]. However, members often differ in age, sex, and needs, and then Attribution (CC BY) license (https:// these differences generate divergent interests among individuals, which, in extreme cases, creativecommons.org/licenses/by/ might lead to fragmentation and instability, and even deprive them of the benefits of group 4.0/). Animals 2021, 11, 876. https://doi.org/10.3390/ani11030876 https://www.mdpi.com/journal/animals Animals 2021, 11, 876 2 of 12 living [3,4]. During adaptive evolution, animals employ consensus decision-making to coordinate their actions on the move. Consensus decision-making refers to the process by which members of a group achieve consistency in their activities through information exchange, where they decide when to leave and where to go [5]. To lead a successful collective movement, the initiator must use effective communication to evoke actions and behavioral imitations from other members and attract most of them to participate in the collective movement [6]. Meanwhile, other members of a collective movement can also communicate their preferences of movement direction and time to group mates, either through local communication among neighbors only [7] or through global communication in their group [8], ultimately achieving the consistency of members’ actions [2]. Clearly, the proper use of communication behaviors plays an important role in the success of consensus decision-making and the achievement of a collective movement [9]. Animals can signal departure to group members through visual signals, attracting group members to follow movements they initiate, negotiate the direction and timing of movements, and thus group movement [5]. For example, in group movements of bottlenose dolphins (Tursiops truncatus), the initiators recruit participants a lateral fin-swinging posture prior to group migration [10]. Visual communication in group movements has also been seen in studies of other animals. In domestic geese (Anser domesticus), a higher number of arousal behaviors (flutter wings on both sides) led to a larger number of individuals recruited [11]. European bisons (Bison bonasus) depart in a constant direction (without turning more than 45◦) for at least 20 steps without stopping, with its head horizontal (without grazing) in order to recruit follower [12]; Spotted hyaenas (Crocuta crocuta) view bristled tails as initiation signal of collective movement [13]. Primates are highly cognitive and socially complex, with individuals possessing both local knowledge of the behavior of their neighbors and information about the environ- ment holistically, thus making the functions of communicative behavior more diverse and complex [14]. For example, male barbary macaques (Macaca sylvanus) recruit neighbor- ing individuals and monitor the activities of other group members when leading group movements [9]. At the same time, in primate collective movement, other members of the group may also influence the behavior of the initiator’s behavior. The negotiation process is not only signaling, but also a communicative response between members, that is, when initiators monitor the reluctance of group members to follow the movement, they increase the frequency of recruitment. As the number of participants gradually increases, the recruit- ment signals emitted by initiators decrease [14]. For example, in Tonkean macaques (M. tonkeana), the initiator glances back at other members of the group when leaving the group, pauses briefly while moving, and changes the speed of movement [15]. In addition, the involvement of individual relatives significantly reduces the release of initiator recruitment signals in red-tailed sportive lemurs (Lepilemur ruficaudatus) during travel to a new foraging site or habitat [16]. In recent years, research on communication behavior that occurs during primate consensus decision-making has become increasingly popular [17,18]. We previously conducted some collective decision-making research in Tibetan macaques (M. thibetana). For example, individuals with higher social centrality have a higher success rate of decision-making [19], and they will join group movement earlier. These individ- uals often decide whether to use selective mimetism or quorum [20]. We also found that female Tibetan macaques use their social networks to enhance the speed of collective decision-making, which may have associated fitness benefits [21], but there is no study on the relationship between communication behavior and behavioral decision-making. To clarify the factors that influence visual signals and how visual signals contribute to collective decision-making, we need to explore the potential link between communication and decision-making in Tibetan macaques. We hypothesized that if back-glance and pauses were indeed used as communication signals (Hypothesis 1), then the signals would decrease significantly as the number of followers increases (Prediction 1). Animals 2021, 11, 876 3 of 12 Discrimination in factors, sex, age class, rank, number of relatives within the group, social centrality, and location in the movement queue were known to play an important role in signal transmission in primate groups. We hypothesized that these parameters would influence visual signal emissions (Hypothesis 2). Each factor above corresponds to one prediction, and there were altogether six predictions (Prediction 2–Prediction 7). That is to say, these six factors all have an impact on the release of visual signals. 2. Materials and Methods 2.1. Study Site and Subjects We conducted this study from September 2019 to January 2020 in the Valley of the Wild Monkeys, Mt. Huangshan National Reserve in Anhui, China (30◦290 N, 118◦100 E) [22]. This location
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