Functional Diversifications of Contact Calls in a Multi-level Primate Society

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However, despite small repertoire sizes, nonhuman primates could use vocalization for social purposes too. Vocal communication could be evolutionarily ancient, and likely evolved hand-in-hand with complex, dynamic social structures. By studying the vocal communication in wild golden snub-nosed monkeys ( Rhinopithecus roxellana ), a species of Asian colobine living in 4-layer multi-level societies with fission-fusion dynamics, we unraveled the complex social functions of contact ‘coo’ calls. Contact calls helped cultivate both within- and between-unit relationships, and depending on the sexes, reproductive states, and social roles of callers and recipients, were also functionally diverse. Within units, calls replaced grooming and were supplementary to social proximity. Males directed more calls to lactating females, who were unavailable for grooming and away from unit centers due to extended foraging and childcare. Higher-ranking males called more frequently but did not receive more calls than lower-ranking ones. Considering their larger social network sizes and leadership roles, contact calls likely facilitated inter-unit proximity and were used for advertising intrasexual affiliation and alliances. By comparing the network of contact call exchange with that of social proximity and grooming, we identified the inter-unit social relationships that were otherwise inconspicuous and, more importantly, the potential mechanisms for maintaining male-male alliances and unit and band cohesion. Together with previous findings, we conclude that contact calls are economical and low-risk social tools for reassuring and advertising affiliation, resolving uncertainties, and promoting cohesion and alliance formation. contact calls functional diversifications social complexity hypothesis convergent evolution multi-level society Rhinopithecus roxellana Figures Figure 1 Figure 2 Significance Statement Large social networks are hard to cultivate, a challenge that concerns both humans and nonhuman primates, including golden snub-nosed monkeys. Living in a four-layer multi-level society, the monkeys maintain various relationships with specific social and ecological values. Through investigating the social functions of contact calls, an acoustically simple but widely used vocalization, we found that the calls are functionally diverse. Depending on the callers’ sexes, reproductive states, and social roles, contact calls were used in different frequencies and exchanged with different correspondences. Both sexes used the call to vocally groom same-unit members and, potentially, to promote unit cohesion by informing locations and coordinating movements. Males, on the other hand, exchanged calls also in between-unit contexts, for cultivating or advertising affiliations and alliances. Together, functional diversifications of contact calls allow economical management of large, multi-layered social networks at a low risk. Introduction Vocal communication is widespread in the animal kingdom (Searcy & Nowicki, 2005 ; Cheney & Seyfarth, 2018 ). In nonhuman primates, through adjustment and combination, small vocal repertoire sizes could convey rich meanings across social contexts (Crockford & Boesch, 2005 ; Cheney & Seyfarth, 2018 ). For recipients, moreover, comprehension sophistication helps decode intentional and motivational content from acoustically simple calls potentially through relational understanding, like by linking calls with sexes, social roles, and recent history (Godfrey-Smith, 2017 ; Cheney & Seyfarth, 2018 ). From the comparative perspective, hence, studying vocal communication in nonhuman primates could inform the evolutionary gradation of socio-cognitive abilities, like the ability to process sequences and understand relations (Cheney & Seyfarth, 2018 ; Wilson & Petkov, 2018 ). Through homoplasy, on the other hand, animals living in large, dynamic societies could have also evolved complex communicative systems comparable to humans, if communication provides solutions to the challenges of social lives and brings fitness advantages (Searcy & Nowicki, 2005 ). In the past decades, vocal communication has been linked with social functions in several primate species characterized as living in large, complex societies (e.g., Pan troglodytes : Crockford & Boesch, 2005 ; Lemur catta : Kulahci et al., 2015 ; Macaca mulatta : Pfefferle et al., 2015 ; Macaca fuscata : Koda et al., 2008 ; Papio ursinus : Bergman et al., 2003 , Silk et al., 2016 ; Pan paniscus : Schamberg et al., 2016 , 2017 ; Papio papio : Dal Pesco & Fischer, 2018 ). Nevertheless, primatologists each have distinct research interests and vocal communication has not been thoroughly studied in many longitudinal field sites. Hence, we are far from having sufficient evidence for studying the homology and homoplasy of human language comparatively. Our understanding of primates’ social networks is mostly based on traditional approaches of social network analysis (using grooming interaction and spatial proximity as indexes). In fact, vocal communication could also help cultivate social relationships, even with greater efficiency and at lower risks (Cheney & Seyfarth, 2018 ). Sound surpasses physical barriers that usually obstruct chemical, tactile, and visual signal transmission, thus allowing efficient distant communication (Koda et al., 2008 ). When being produced, primates need no sacrifice the time and energy that are otherwise worth spending on more important tasks, especially foraging, reproducing, and parenting (Sugiura, 2007 ). In social contexts, certain call types could signal affiliative motivation that facilitates interactions like approaching and grooming or, in certain social contexts, supplant grooming and greeting (Schamberg et al., 2016 , 2017 ; Dal Pesco & Fischer, 2018 ). Theoretically, complex vocal communication systems could have coevolved with large, dynamic primate societies (i.e., the ‘social complexity’ hypothesis: Bouchet et al., 2013 ). In these societies, relationships are cultivated with both kins and nonkins, and depending on their social roles, the size and composition of social networks vary across individuals (Grueter et al., 2020 ). Although large, mixed networks could be adaptive for group cohesion and attaining collecting benefits, due to the risk of aggression, interacting with loosely affiliated others brings uncertainties, stresses, and anxieties (Cheney & Seyfarth, 2008 ). In these contexts, affiliative vocalizations could disambiguate intentions and motivations, thus facilitating social interactions and even reunions (e.g., in groups with fission-fusion dynamics, e.g., Ateles geoffroyi : Ramos-Fernández, 2008 ; Pan paniscus : Schamberg et al., 2016 , 2017 ). Moreover, in multi-level societies, vocal communication should be of greater necessity (Bouchet et al., 2013 ). Conventional approaches of social network analysis identified multi-layered social networks, matching the complexity of social structures (e.g., Papio hamadryas : Patzelt et al., 2014 ; Papio papio : Dal Pesco & Fischer, 2018 ; Theropithecus gelada : Snyder-Mackler et al., 2014 ; and Rhinopithecus roxellana : Qi et al., 2014 ). Depending on individuals’ social parameters, relationship type, strength, and value vary considerably (Grueter et al., 2020 ). With the use of molecular approaches, patterns of group dynamics, like dispersal, fission, and fusion, could be explained from the perspective of kin selection (e.g., Papio hamadryas : Schreier & Swedell, 2009 ; Theropithecus gelada : Snyder-Mackler et al., 2014 ). Nevertheless, the role of vocal communication in cultivating social relationships could have been overlooked. Wild golden snub-nosed monkeys live in large 4-layer societies composed of several one-male multi-female units and shadowing bachelor males. Although residential males maintain rather ‘distant’ relationships with one another (characterized by the absence of direct affiliative interaction like approaching and grooming), between-unit male-male affiliations could exist, with whom they maintain a closer social distance and form alliances (Qi et al., 2017 ). Among females, similarly, grooming and social proximity are restricted, almost exclusively, to unit members. Although the social bonds between females and residential males decay prior to takeovers, females were rarely found engaging in close contact with their future mates (Qi et al., 2009 , 2020 ). It is possible that vocal communication was used. In addition, cultivating large social networks places a heavy demand on time and energy budget. Due to the seasonally changing environment, wild golden snub-nosed monkeys travel distantly for food and other resources (Zhao et al., 2023 ). During their limited time of resting, social interactions should be allocated in favor to more valuable relationships, for residential males and females, within-unit bonds. For the out-unit relationships, in contrast, vocal communication provides an economical solution (i.e., vocal grooming: Dunbar, 2017 ). Alternatively, considering the more uncertain and riskier between-unit relationships, social evolution could have favored vocal communication for cultivating bonds and reassuring affiliation when interacting, potentially as replacements for more ‘stressful’ forms of affiliative interactions (e.g., approaching, greeting, grooming). Based on our impression of two decades of longitudinal study and past research (Fan et al., 2018 , 2019 ), we suspect contact ‘coo’ calls could serve the above functions. In this study, we innovatively incorporated the contact ‘coo’ calls into the traditional social network analysis, and then compared the resulting ‘contact call exchange network’ with the social networks calculated from grooming and proximity data. The contact ‘coo’ call is the most frequently used call type in the wild (Fan et al., 2018 ). Like the calls of other nonhuman primates, it is acoustically simple (‘aye’ or ‘aye-aye’ in English transcript: X.-G. Qi, personal communication), bears clear individuality in acoustic characteristics, and is used across various neutral or affiliative contexts (Fan et al., 2019 ). We ask: (1) whether contact calls help cultivate social networks and (2) whether call uses exhibit context- and role-dependent varieties. Method The study was carried out on the northern slope of the Qinling Mountains (108°14′-108°18′E, 33°45′-33°50′N, 1500-2890m above sea level) Yuhuangmiao village, Zhouzhi National Nature Reserve (ZNNR), Shaanxi Province, China. The subjects were a population of free-ranging but provisioned golden snub-nosed monkeys of the GNG-Breeding band. The GNG herd contained a breeding band composed of 13 one-male multi-female units (hereafter, OMUs) and 13 to 32 bachelor males. Together with the DJF herd, two herds form the West troop (Qi et al. 2014 ). Monkeys were provided with corn and carrots for close observation. The provision site was a frequent foraging and resting site. Provision was provided twice daily, after the band entered the site and before the band left the site. Provision constituted less than 30% of their average daily caloric intake. The climate is semi-humid and seasonal, with spring from March to May, summer from June to August, autumn from September to November, and winter from December to February (Li et al. 2000 ). Average annual rainfall is 894mm. The average annual temperature is 10.7℃ with a maximum of 31.5℃ in July and a minimum of -14.3℃ in January (Qi et al. 2008 ). In the wild, extreme weather conditions and low visibility of dense foliage often impeded data collection; and the study population was very large, motile, hard to approach, and loquacious. Data collection From September 22nd, 2018, to June 4th, 2019, we followed the herd from 0500 to 1900 (Beijing Standard Time) for 186 days, 2232 hours. We studied 70 adult individuals, including 13 males and 57 females. However, because 3 OMUs were not stable and eventually disappeared from the band before the study ended, we excluded the data collected from these units from our analysis. Hence, in our final sample, data from 54 adults including 10 adult males and 44 adult females of ten OMUs are presented. Age categories included adult males (> 7yrs), adult females (> 5yrs), sub-adults (female: 4–5yrs, male: 5–7yrs), juveniles (1–4yrs), and infants (< 1 year) (Qi et al., 2009 ). Before data collection, we first identified each subject based on physical characteristics (including body size, facial features, pelage color, the granulomatous flanges on both sides of their lips, and secondary sexual characteristics: Li & Zhao, 2007). Based on the reproductive history, lactating and nonlactating females were also distinguished. We selected one OMU as the focal unit per day and rotated observations evenly among 10 units. Our data collection concentrated on 4 types of social interactions between dyads, including spatial proximity, grooming, aggressive-submissive behaviors, and contact call exchange. Spatial proximity was recorded by calculating the distance between the focal subject and the nearest neighbor using focal animal sampling and instantaneous scan sampling at five-minute intervals (Altmann, 1974). Grooming interactions were recorded by noting the identities of the groomer and recipient and the start and end time ad libitum. Aggressive-submissive behaviors were also recorded using the ad libitum sampling method with the identities of the aggressor and victim, the start and end time, types of agnostic behavior involved, and the winning party being noted in detail. Agnostic behaviors were defined as behaviors that involve biting, fighting, chasing, threatening, and supplanting, and submissive behaviors as behaviors that include avoiding, crouching, and retreating (Li et al., 2006 ). To estimate the dominance hierarchy, the turnouts of aggressive-submissive interactions were converted into the normalized David score (NDS) following the method standardized by de Vries et al (2006). Finally, contact call exchanges were recorded and defined as the exchange of calls between two individuals within a 5s duration (Fan et al. 2018 ). Data analysis Data analyses were done to investigate the role of contact calls in cultivating social relationships and potential functional diversifications depending on sex, reproductive states, and social roles of callers and recipients. Spatial proximity, grooming, and contact call exchange data were independently converted into matrixes for each OMU and the whole band, using the calculation of HWI in SOCPROG v. 2.4. The matrixes were then cross-compared through the Quadratic Assignment Procedure (QAP) and UCINET to see whether contact call exchanges serve similar or different social functions as grooming and social proximity (Borgatti et al., 2002 ; Johnson et al., 2013 ). QAP compares matrixes by randomly rearranging their rows (and matching columns), performing nonparametric tests on the coefficients through the permutations (we ran 99 999 times), and calculating the correlation coefficient between two matrixes. We chose QAP because it rearranges whole rows and columns rather than individual cells, a default setting that preserves subtle properties of the matrixes (Johnson et al., 2013 ). To see whether dominance hierarchy predicts the initiation and/or response of contact calls, we investigated the relationships between rank with call initiation and reception separately using Spearman's rho correlation tests. To investigate sex differences in contact call uses, we ran two paired t-tests. In the first test, we asked whether males used contact calls more frequently than females. In the second test, we asked whether males directed disproportionally more contact calls to the lactating females than to nonlactating ones. During the study period, a total of 7 females from 7 OMUs were with newborns (who were lactating). Because lactating females were unevenly distributed across units, the frequency and/or proportion of contact calling exchanges with lactating females could be overrepresented in some units. To avoid the influence of unequal data distribution, we compared the expected values and actual values of contact call exchange frequency. Expected values were calculated based on the null hypothesis that contact calls were not given selectively but equally to every unit member (not biased toward lactating females). All statistical tests were two-tailed and performed using SPSS 24.0 (SPSS, Inc., Chicago, IL, USA) with P＜0.05 taken as the significance. Results Data collection was impeded by poor visibility, unpredictable weather conditions, and the noisy study population. In some cases, simultaneous responses from multiple recipients ambiguated the actual correspondences. To avoid mistaking the actual caller and recipient, we conservatively included only the call bouts where both the caller and recipients were unambiguously noted. This yielded a sample of 2135 call exchange bouts. Spatial proximity, grooming, and contact call exchange data were collected from 54 subjects (10 adult males, 44 adult females) on 186 days, and the average observation of each OMU was 15 ± 3d. We generated 22 matrixes based on the association indexes between all within- and between-unit dyads using SOCPROG v. 2.4. The 22 matrixes included 10 spatial proximity association matrixes and 10 contact call exchange matrixes for the 10 study units separately, as well as 1 spatial proximity association matrix and 1 vocal communication association matrix for the breeding band (with each OMU being taken as a focal point). The matrixes can be found in the Appendixes (1–5). Contact call exchange and spatial proximity Contact call exchanges were used differently in between- and within-unit contexts. The QAP correlation analysis revealed significant negative correlations between contact call exchange and spatial proximity matrixes in six OMUs, but a significant positive correlation between OMUs. Across the six units, the correlation coefficients ranged from − 0.671 to -0.335 (low to moderately low) with p-values ranging from 0.011 to 0.041. All units except SQ, SX, XB, and ZD showed significant correlations despite the low to moderately low coefficients (-0.671 to -0.495; see Table 1 for details). Together, our finding suggests that the exchange of contact calls was more frequent between unit members with greater social distances. Among OMUs (or on the band level), in contrast, the association matrixes of spatial proximity and contact call exchange were significantly positively correlated, with a moderate correlation coefficient (the QAP correlation analysis; N = 99999 permutation; r = 0.337, P = 0.004). Because between units, contact calls were exclusively exchanged among residential males, the positive correlation indicates more frequent contact call exchanges among residential males who maintained closer spatial proximity (see Fig. 1 b and c). In addition, we also found that some male-male relationships were more strongly reflected by contact call exchange than by social proximity (see Fig. 1 c: unexpected relationships, in red). Contact call exchange and grooming Grooming was not observed between members of different units (see Fig. 1 a), so we only computed within-unit grooming matrixes. QAP analysis indicated that in 7 out of 10 OMUs, contact call exchange and grooming matrixes were not significantly correlated (r ranged from 0.260 to 0.330, P values ranged from 0.106 to 0.414, see Table 1 for details). In the rest three units, the coefficients were significant, with moderate to moderately high coefficients (SX unit r = 0.372, p = 0.039; LZ unit: r = 0.547, p = 0.017; BF unit: r = 0.545, p = 0.034). Together with the above findings, grooming interaction was not as strongly correlated with contact call exchange as social proximity, although moderately positively correlated. Table 1 Relationships between vocal communication networks and other networks OMU Social proximity Grooming interaction Unit size r P r P BF -0.608 0.033* 0.545 0.034* 5 G3 -0.335 0.029* 0.280 0.130 6 GB -0.588 0.034* 0.297 0.141 5 HL -0.562 0.011* 0.330 0.106 6 LZ -0.412 0.041* 0.547 0.017* 6 SQ -0.560 0.084 0.260 0.184 5 SX -0.435 0.059 0.372 0.039* 6 TB -0.538 0.012* 0.057 0.414 6 XB -0.671 0.166 0.458 0.168 4 ZD -0.495 0.110 0.264 0.186 5 P < 0.05* Contact call exchange and dominance rank Because almost all agnostic interactions were found between dyads of residential males, only between-unit dominance hierarchy was considered. 410 cases of aggression-submission agonistic interactions were recorded, and the turnouts were converted into NDS (see Appendix 6 for details). The dominance hierarchy was linear with a moderately high steepness (steepness K = 0.66, R2 = 0.977). Spearman's rho correlation tests showed that dominance statuses were strongly and positively correlated with contact call initiation (Spearman's rho correlation: r = 0.628, P＜0.05, N = 10) but not with reception (r = 0.468, P＞0.05, N = 10; see Fig. 1 e). Higher-ranking males called more frequently, though received calls in similar frequencies, than the lower-ranking ones. This could be the result of the larger social network sizes of higher-ranking males, their central leading roles on the band level, or the function of contact call exchange for advertising affiliation publicly (see discussion below). Sex differences in contact call exchange Paired Sample t-test revealed a significant sex difference in contact calling frequency (N = 10, P = 0.002). Males on average called two times more frequently than females (38% vs. 15%). Three lines of evidence could explain the sex asymmetry. First, males had more call exchange correspondences than females (see Fig. 1 a-c). Residential males not only exchanged contact calls with same-unit females but also males from other units, while females exchanged calls primarily with same-unit members (also see Fan et al., 2018 , 2019 ). Second, within units, contact call exchange likely served affiliative and mate-securing functions, and helped residential males keep females near and reassure their affiliation. Finally, between units, contact calls helped males cultivate social relationships with other males; especially for high-ranking residential males, the loud and broadcasting call feature functioned potentially for advertising affiliation and reaffirming dominance rank (Fan et al., 2018 ). Functional diversifications in contact call exchange We conducted an additional test to verify the second observation. We hypothesized that if contact calls served affiliative and mate-securing functions, males should be allocated more calls to lactating females than to nonlactating ones, because lactating females were often occupied with childcare and foraging, thus staying distantly from unit centers, and seldomly engaged in grooming interactions. With lactating females, residential males exchanged more contact calls than expected by chance (N = 7, P＜0.05), but not with nonlactating ones (N = 7, P＞0.05). Hence, contact call exchanges could have supplanted social proximity if same-unit correspondences were occupied by other important tasks (see Fig. 2 ). Discussion Our wild golden snub-nosed monkeys used contact calls to cultivate social relationships. The complexity of the multi-level society and the heterogeneity of social relationship types, though brought challenges to our investigation, helped clarify the functions of contact call uses. In most units, contact call exchange was negatively correlated with social proximity but positively correlated with grooming (though not significantly). This indicates that unit members exchanged contact calls for affiliative purposes in parallel with grooming and as replacements for social proximity. The study units were with 4 to 6 members, which likely impeded grooming interactions and caused greater social distances between some unit members. Contact call exchanges likely supplanted social proximity for affiliating with relatively distantly positioned unit members, which in turn, could facilitate unit cohesion by informing locations and coordinating movements. On the other hand, when their grooming partners were occupied, for instance by traveling, foraging, and childcare, contact calls could be used for vocal grooming as replacements for ‘physical’ grooming. Between units, on the other hand, contact calls helped residential males cultivate relatively distant social relationships. Between-unit social distances are often greater than those within units, potentially because of foraging competition and dominance relationships (Qi et al., 2009 ). Social network analysis using grooming and social proximity as inputs has long characterized the relationships among residential males as loose or distant (but see male-male cooperation in Qi et al., 2017 ). Nevertheless, contact call exchanges circumvented the inter-unit barriers of competition and hostility and helped residential males cultivate intrasexual relationships. As our findings revealed, the between-unit networks of contact call exchanges and social proximity were significantly positively correlated. Residential males maintaining closer between-unit social distances also exchanged contact calls more frequently. The units of golden snub-nosed monkeys were often in constant movement towards or away from one another, especially during foraging. Uncertainties about intention could result in fighting and cause stress and anxiety. On the other hand, while resting, some units preferentially maintained closer distances from one another, as our between-unit proximity matrix revealed. These units often shared the same trees with mutual tolerances, while the approaching of other units could bring turmoil and conflict. Hence, in between-unit interactions, contact call exchanges likely facilitated approaching by signaling benign motivation and helped cultivate between-unit relationships as a replacement for grooming. Moreover, the patterns of contact call exchange revealed functional diversifications depending on sexes, reproductive states, and social roles. Compared to females, males on average called two times more frequently because of larger social network sizes (containing both within- and between-unit social relationships). Second, contact calls were directed more to lactating females than to nonlactating ones. Lactating females devoted more time to foraging and childcare (including carrying, feeding, and grooming) than nonlactating ones, hence staying further away from the unit center and having a lower time budget for grooming. This potentially made contact calls economical for cultivating valuable within-unit relationships, but also practical for unit coordination (by informing locations and coordinating movements). Finally, for residential males, contact calls helped cultivate and advertise between-unit relationships. Among residential males, higher-ranking ones gave (but did not receive) more contact calls than lower-ranking ones. High-ranking males maintained larger between-unit social networks than lower-ranking ones (see Fig. 1 ). Larger network sizes predicted greater leadership roles in band movements and more male alliances (Qi et al., 2017 ; Wang et al., 2020 ). The dominance and leading role of some residential males and their units likely provided the priorities to access resources, while having more male alliances could be more effective at deterring bachelor males. In addition, because contact calls are loud and public, with calls being directed and responded to specific individuals (Fan et al., 2018 ), residential males could have used them for advertising affiliation and alliances. Advertising male-male alliances could help maintain dominance hierarchy by forestalling attempts to rank reversals, female alluring, and takeover attempts. Compared with hamadryas baboons, using contact calls for cultivating and advertising intrasexual relationships could be more important to golden snub-nosed monkeys. Among hamadryas leaders, bonds and alliances are often founded on kinship ties (Schreier & Swedell, 2009 ). In contrast, although relatedness predicts social bonds among bachelor males, the residential males of golden snub-nosed monkeys likely form bonds and alliances with both kins and nonkins (Qi et al., 2017 ; Ren et al., 2018 ). Therefore, in this species, uncertainties about male-male relationships and interactions are likely greater, especially in the absence of close affiliative interactions comparable to that in hamadryas males (e.g., grooming and ritualized greeting: Patzelt et al., 2014 ). Hence, the social evolution of the multi-level societies of this species likely selected affiliative calls for easing inter-unit tension and promoting aggregation. On the other hand, the dynamic and multi-layered societies of this species could have also favored the evolution of functional diversity of contact calls. In response to the seasonally changing climate and resource distribution and quality, group size, home range size, and daily travel distance are constantly adjusted, explaining frequent fission and fusions (Qi et al., 2014 ; Zhao et al., 2023 ). During these events, contact call exchanges could help resolve stress and anxiety and facilitate individual recognition and reunions (Yang et al., in preparation; also see in chimpanzees: Crockford & Boesch, 2005 ; bonobos: Schamberg et al., 2016 , 2017 ). Summary Despite its simple acoustic construction, contact calls in golden snub-nosed monkeys exhibited functional diversifications. Within units, for both sexes, contact calls helped cultivate relationships and likely served other practical functions (e.g., informing locations and coordinating movements). For males only, the calls were used for affiliating with lactating females who were unavailable for grooming (due to infant care and prolonged foraging). Between units, on the other hand, contact calls were used for cultivating and, potentially, advertising male-male relationships and alliances. Together, along with grooming and social proximity, golden snub-nosed monkeys incorporated contact calls (and likely other call types) for various affiliative and practical purposes, potentially as an adaptation to the demand of cultivating large, multi-layered social networks. On the other hand, because maintaining and cultivating those relationships could be time- and energetically demanding, the sophistication of call interpretation could be economical and practical for both callers and recipients. By making associations with social knowledge and information, including sexes, reproductive states, dominance ranks, and social roles and histories, interpretations of the calls could be precise. For the callers, similarly, repeated interactions and call exchanges with specific recipients could ritualize the calls by associating them with specific intentions. This is consistent with the ‘social complexity’ hypothesis and in parallel with the vocal communication systems of other primate species, including humans. Our work revealed the social significance of contact calls, and our ongoing studies are investigating that of other call types (e.g., grunting, screaming, and barking). We suggest that the functional diversifications of contact call uses could have coevolved with the multi-level societies of this species. Declarations Acknowledgments We thank Zhouzhi National Nature Reserve (ZNNR) for the permission for the research. Thanks also to editors, reviewers, and all the members of the golden snub-nosed monkey Research Team at the College of Life Science, Northwest University. Funding Information Our research was supported by the National Natural Science Foundation of China (31622053, 31730104), the Promotional Project for Innovation team, the Department of Science and Technology of Shaanxi Prov. China (2018TD-017), the National Key Program of Research and Development, Ministry of Science and Technology of China (2016YFC0503200). Conflict of interest The authors declare no conflict of interest. Compliance with ethical standards We adhered to the American Society of Primatologists (ASP) Principles for the Ethical Treatment of Non-Human Primates, followed the American Society of Primatologists Code of Best Practices for Field Primatology, and adhered to the legal requirements of the People’s Republic of China. Ethical approval Research was permitted by the Chinese Academy of Sciences and the ethics board of the College of Life Sciences, Northwest University. 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Am J Primatol 70:1055–1063. https://doi.org/10.1002/ajp.20597 Kulahci I, Rubenstein D, Ghazanfar A (2015) Lemurs groom-at-a-distance through vocal networks. Anim Behav 110:179–186. https://doi.org/10.1016/j.anbehav.2015.09.016 Li B, Chen C, Ji W, Ren B (2000) Seasonal Home Range Changes of the Sichuan Snub-Nosed Monkey (Rhinopithecus roxellana) in the Qinling Mountains of China. Folia Primatologica; International Journal of Primatology, 71, 375–386. https://doi.org/10.1159/000052734 Li B, Li H, Zhao D, Zhang Y, Qi X-G (2006) Study on dominance hierarchy of the Sichuan snub-nosed monkey (Rhinopithecus roxellana) in Qinling Mountains. Acta Theriol Sinica, 26 Patzelt A, Kopp GH, Ndao I, Kalbitzer U, Zinner D, Fischer J (2014) Male tolerance and male–male bonds in a multilevel primate society. Proceedings of the National Academy of Sciences, 111(41), 14740–14745. https://doi.org/10.1073/pnas.1405811111 Pfefferle D, Ruiz-Lambides A, Widdig A (2015) Male rhesus macaques use vocalizations to distinguish female maternal, but not paternal, kin from non-kin. Behav Ecol Sociobiol 69. https://doi.org/10.1007/s00265-015-1979-9 Qi X-G, Garber P, Ji W, Huang Z-P, Huang K, Zhang P, Guo S, Wang X-W, He G, Zhang P, Li B (2014) Satellite telemetry and social modeling offer new insights into the origin of primate multilevel societies. Nat Commun 5:5296. https://doi.org/10.1038/ncomms6296 Qi X-G, Grueter C, Fang G, Huang P, Zhang J, Duan Y-M, Huang Z-P, Garber P, Li B (2020) Multilevel societies facilitate infanticide avoidance through increased extrapair matings. Anim Behav 161. https://doi.org/10.1016/j.anbehav.2019.12.014 Qi X-G, Huang K, Fang G, Grueter CC, Dunn DW, Li Y-L, Ji W, Wang X-Y, Wang R-T, Garber PA, Li B-G (2017) Male cooperation for breeding opportunities contributes to the evolution of multilevel societies. Proceedings of the Royal Society B: Biological Sciences, 284(1863), 20171480. https://doi.org/10.1098/rspb.2017.1480 Qi X-G, Li B, Garber P, Ji W, Watanabe K (2009) Social dynamics of the golden snub-nosed monkey (Rhinopithecus roxellana): Female transfer and one-male unit succession. Am J Primatol 71:670–679. https://doi.org/10.1002/ajp.20702 Qi X-G, Li B, Ji W (2008) Reproductive Parameters of Wild Female Rhinopithecus roxellana. Am J Primatol 70:311–319. https://doi.org/10.1002/ajp.20480 Ramos-Fernández G (2008) Spider Monkeys: Communication in spider monkeys: The function and mechanisms underlying the use of the whinny. https://api.semanticscholar.org/CorpusID:82094013 Ren Y, Huang K, Guo S, Pan R, Derek DW, Qi X, Wang X, Wang C, Zhao H, Yang B, Li F, Li B (2018) Kinship promotes affiliative behaviors in a monkey. Curr Zool 64(4):441–447. https://doi.org/10.1093/cz/zox046 Schamberg I, Cheney D, Clay Z, Hohmann G, Seyfarth R (2016) Call combinations, vocal exchanges and interparty movement in wild bonobos. Anim Behav 122. https://doi.org/10.1016/j.anbehav.2016.10.003 Schamberg I, Cheney D, Clay Z, Hohmann G, Seyfarth R (2017) Bonobos use call combinations to facilitate inter-party travel recruitment. Behav Ecol Sociobiol 71:75. https://doi.org/10.1007/s00265-017-2301-9 Schreier A, Swedell L (2009) The Fourth Level of Social Structure in a Multi-Level Society: Ecological and Social Functions of Clans in Hamadryas Baboons. Am J Primatol 71:948–955. https://doi.org/10.1002/ajp.20736 Searcy W, Nowicki S (2005) The Evolution of Animal Communication: Reliability and Deception in Signaling Systems. In Bioscience (Vol. 56). https://doi.org/10.1641/0006-3568(2006)56 [849:WAASH]2.0.CO;2 Silk J, Seyfarth R, Cheney D (2016) Strategic Use of Affiliative Vocalizations by Wild Female Baboons. PLoS ONE 11:e0163978. https://doi.org/10.1371/journal.pone.0163978 Snyder-Mackler N, Alberts S, Bergman T (2014) The socio-genetics of a complex society: Female gelada relatedness patterns mirror association patterns in a multilevel society. Mol Ecol 23. https://doi.org/10.1111/mec.12987 Sugiura H (2007) Effects of proximity and behavioral context on acoustic variation in the coo calls of Japanese Macaques. Am J Primatol 69:1412–1424. https://doi.org/10.1002/ajp.20447 Wang C, Pan R, Wang X, Qi X, Zhao H, Guo S, Ren Y, Fu W, Zhu Z, Li B (2020) Decision-making process during collective movement initiation in golden snub-nosed monkeys (Rhinopithecus roxellana). Sci Rep 10(1):480. https://doi.org/10.1038/s41598-019-57191-3 Wilson B, Petkov C (2018) Relational Knowledge and the Origins of Language. In The Social Origins of Language. https://doi.org/10.1515/9781400888146-007 Zhao L, Du JIS-N, Liu X-B, Zhang J-H, Li B-L, Yang P-H, Li Y-J, Guo B-G, Y.-Q., Qi X-G (2023) Dynamic foraging strategy adapted to heterogeneous environment contributes to social aggregation in snub-nosed monkeys. In Zoological Research. https://www.zoores.ac.cn/en/article/id/3d1a26bb-81a 5-40f9-a6db-28ba0c75003d Supplementary Files Appendix.docx Cite Share Download PDF Status: Posted Version 1 posted You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. Also discoverable on Platform About In Review Editorial Policies Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-3687604","acceptedTermsAndConditions":true,"allowDirectSubmit":true,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":257936708,"identity":"4a7a00ca-18e4-4428-b6b5-2199d35964e3","order_by":0,"name":"Yi-Jun Yang","email":"","orcid":"","institution":"Northwest University - Taibai Campus: Northwest University","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Yi-Jun","middleName":"","lastName":"Yang","suffix":""},{"id":257936709,"identity":"50ce891c-4fe9-4458-9367-025ab8701c2b","order_by":1,"name":"Yan Ying","email":"","orcid":"","institution":"Northwest University - Taibai Campus: Northwest University","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Yan","middleName":"","lastName":"Ying","suffix":""},{"id":257936710,"identity":"33138644-c4d3-48e6-b084-759d64358f8e","order_by":2,"name":"Wen-Yong Tian","email":"","orcid":"","institution":"Management Bureau of Shannxi Zhouzhi National Nature Reserve","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Wen-Yong","middleName":"","lastName":"Tian","suffix":""},{"id":257936711,"identity":"ec7202a3-6a4f-42ec-9fe3-3810e5eebe62","order_by":3,"name":"Dai-Bo Zhu","email":"","orcid":"","institution":"Management Bureau of Shannxi Zhouzhi National Nature Reserve","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Dai-Bo","middleName":"","lastName":"Zhu","suffix":""},{"id":257936712,"identity":"78b7b0b7-3ae2-4896-81c1-531959f815d1","order_by":4,"name":"Bao-Guo Li","email":"","orcid":"","institution":"Northwest University - Taibai Campus: Northwest University","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Bao-Guo","middleName":"","lastName":"Li","suffix":""},{"id":257936713,"identity":"55618c6f-8a5b-474a-be14-e31f6fa1720c","order_by":5,"name":"Xiao-guang Qi","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAAAsUlEQVRIiWNgGAWjYDACZiD+AGEaEK+FcQZpWkC6eEjSwnecx/i17Y7DiQ3szdskGGruENYieZgtzTr3DFALz7EyCYZjzwhrMTjMfMw4t+12YoNEjpkEY8NhYrQwthlbgrTIvyFaC/Phx4xgW3iI1ALyC2Nv23/jNp60YouEY0Ro4Tt/xvjDz7Y02X72wxtvfKghQgvDAQY2CRDNBiISiNAA0sL8gSiFo2AUjIJRMHIBAGa7OOHRzSzoAAAAAElFTkSuQmCC","orcid":"https://orcid.org/0009-0009-2811-4388","institution":"Northwest University - Taibai Campus: Northwest University","correspondingAuthor":true,"submittingAuthor":false,"prefix":"","firstName":"Xiao-guang","middleName":"","lastName":"Qi","suffix":""}],"badges":[],"createdAt":"2023-11-30 15:04:25","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-3687604/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-3687604/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":48073267,"identity":"fef8781f-338e-4014-bb0e-99eb8642b76c","added_by":"auto","created_at":"2023-12-12 15:46:59","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":488477,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eGrooming, proximity, and contact call exchange social networks\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe social networks of residential males are presented. Each pyramid represents a one-male unit with the lines that are connected by the joints depicting within-unit relationships. Within-unit bonds are similar across units; however, between-unit bonds differ. Overall, between-unit social proximity correlates positively and significantly with the frequency of contact call exchange. (a) The networks of proximity are presented, illustrating the social distances among units (in black). Some units are clearly core units: ZD, SX, SQ, and G3, among whom social distances are low across the study periods. However, (b) through contact call exchanges, LZ, HL, and GB maintain social bonds that are not captured by social proximity (in red). (c) Illustrations of affiliative contact calls (upper) and agnostic screams (lower). The audiogram of the contact call shows loud initiation and prolonged calling, but the responses are short and repetitive. The call initiator stops the current task, faces the recipient, and calls. The recipients then pause the current task, orientate toward the initiator, and respond. Throughout the calling bout, all callers sit and chew calmly. (d) The contact call initiation (blue bards) and reception (grey bars) frequencies in percentage are listed for each OMU. OMUs are itemized with respect to the decreasing dominant ranks, from the highest (1\u003csup\u003est\u003c/sup\u003e) to the lowest (10\u003csup\u003eth\u003c/sup\u003e). The normalized David scores (NDS) are also presented. Call initiation but not reception correlates significantly positively with dominance hierarchy. The dominance hierarchy is linear with a moderate steepness. Together, residential males who rank higher call more frequently.\u003c/p\u003e","description":"","filename":"floatimage1.png","url":"https://assets-eu.researchsquare.com/files/rs-3687604/v1/b2da918f8b1a6fc9f4595893.png"},{"id":48073219,"identity":"3fca2bd6-e979-4add-9475-2bcf77300d75","added_by":"auto","created_at":"2023-12-12 15:46:08","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":236331,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eExpected and actual contact call exchange frequencies based on reproductive states\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eAmong the six units containing lactating females, contact call exchanges were more frequent between residential males and lactating females than with nonlactating ones, potentially because of the preoccupation with childcare.\u003c/p\u003e","description":"","filename":"floatimage2.png","url":"https://assets-eu.researchsquare.com/files/rs-3687604/v1/fb8257a4b07c2ef7d9a170c1.png"},{"id":49259461,"identity":"cf8f430d-f4ec-4f60-ac9a-d40973565cbf","added_by":"auto","created_at":"2024-01-06 11:50:51","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":981109,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-3687604/v1/2e47ee3c-a6b4-4baa-b05d-4e4c6f80ff8e.pdf"},{"id":48073125,"identity":"a02ff3c4-9cac-46de-bc18-b5c4c6fb5bef","added_by":"auto","created_at":"2023-12-12 15:45:36","extension":"docx","order_by":1,"title":"","display":"","copyAsset":false,"role":"supplement","size":58617,"visible":true,"origin":"","legend":"","description":"","filename":"Appendix.docx","url":"https://assets-eu.researchsquare.com/files/rs-3687604/v1/401aceec30c9f0bd54fa51bc.docx"}],"financialInterests":"","formattedTitle":"Functional Diversifications of Contact Calls in a Multi-level Primate Society","fulltext":[{"header":"Significance Statement","content":"\u003cp\u003eLarge social networks are hard to cultivate, a challenge that concerns both humans and nonhuman primates, including golden snub-nosed monkeys. Living in a four-layer multi-level society, the monkeys maintain various relationships with specific social and ecological values. Through investigating the social functions of contact calls, an acoustically simple but widely used vocalization, we found that the calls are functionally diverse. Depending on the callers\u0026rsquo; sexes, reproductive states, and social roles, contact calls were used in different frequencies and exchanged with different correspondences. Both sexes used the call to vocally groom same-unit members and, potentially, to promote unit cohesion by informing locations and coordinating movements. Males, on the other hand, exchanged calls also in between-unit contexts, for cultivating or advertising affiliations and alliances. Together, functional diversifications of contact calls allow economical management of large, multi-layered social networks at a low risk. \u0026nbsp;\u003c/p\u003e"},{"header":"Introduction","content":"\u003cp\u003eVocal communication is widespread in the animal kingdom (Searcy \u0026amp; Nowicki, \u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e2005\u003c/span\u003e; Cheney \u0026amp; Seyfarth, \u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). In nonhuman primates, through adjustment and combination, small vocal repertoire sizes could convey rich meanings across social contexts (Crockford \u0026amp; Boesch, \u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e2005\u003c/span\u003e; Cheney \u0026amp; Seyfarth, \u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). For recipients, moreover, comprehension sophistication helps decode intentional and motivational content from acoustically simple calls potentially through relational understanding, like by linking calls with sexes, social roles, and recent history (Godfrey-Smith, \u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Cheney \u0026amp; Seyfarth, \u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). From the comparative perspective, hence, studying vocal communication in nonhuman primates could inform the evolutionary gradation of socio-cognitive abilities, like the ability to process sequences and understand relations (Cheney \u0026amp; Seyfarth, \u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e2018\u003c/span\u003e; Wilson \u0026amp; Petkov, \u003cspan citationid=\"CR38\" class=\"CitationRef\"\u003e2018\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eThrough homoplasy, on the other hand, animals living in large, dynamic societies could have also evolved complex communicative systems comparable to humans, if communication provides solutions to the challenges of social lives and brings fitness advantages (Searcy \u0026amp; Nowicki, \u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e2005\u003c/span\u003e). In the past decades, vocal communication has been linked with social functions in several primate species characterized as living in large, complex societies (e.g., \u003cem\u003ePan troglodytes\u003c/em\u003e: Crockford \u0026amp; Boesch, \u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e2005\u003c/span\u003e; \u003cem\u003eLemur catta\u003c/em\u003e: Kulahci et al., \u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e2015\u003c/span\u003e; \u003cem\u003eMacaca mulatta\u003c/em\u003e: Pfefferle et al., \u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e2015\u003c/span\u003e; \u003cem\u003eMacaca fuscata\u003c/em\u003e: Koda et al., \u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e2008\u003c/span\u003e; \u003cem\u003ePapio ursinus\u003c/em\u003e: Bergman et al., \u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e2003\u003c/span\u003e, Silk et al., \u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e2016\u003c/span\u003e; \u003cem\u003ePan paniscus\u003c/em\u003e: Schamberg et al., \u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e2016\u003c/span\u003e, \u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; \u003cem\u003ePapio papio\u003c/em\u003e: Dal Pesco \u0026amp; Fischer, \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). Nevertheless, primatologists each have distinct research interests and vocal communication has not been thoroughly studied in many longitudinal field sites. Hence, we are far from having sufficient evidence for studying the homology and homoplasy of human language comparatively.\u003c/p\u003e \u003cp\u003eOur understanding of primates\u0026rsquo; social networks is mostly based on traditional approaches of social network analysis (using grooming interaction and spatial proximity as indexes). In fact, vocal communication could also help cultivate social relationships, even with greater efficiency and at lower risks (Cheney \u0026amp; Seyfarth, \u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). Sound surpasses physical barriers that usually obstruct chemical, tactile, and visual signal transmission, thus allowing efficient distant communication (Koda et al., \u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e2008\u003c/span\u003e). When being produced, primates need no sacrifice the time and energy that are otherwise worth spending on more important tasks, especially foraging, reproducing, and parenting (Sugiura, \u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e2007\u003c/span\u003e). In social contexts, certain call types could signal affiliative motivation that facilitates interactions like approaching and grooming or, in certain social contexts, supplant grooming and greeting (Schamberg et al., \u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e2016\u003c/span\u003e, \u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Dal Pesco \u0026amp; Fischer, \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e2018\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eTheoretically, complex vocal communication systems could have coevolved with large, dynamic primate societies (i.e., the \u0026lsquo;social complexity\u0026rsquo; hypothesis: Bouchet et al., \u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e2013\u003c/span\u003e). In these societies, relationships are cultivated with both kins and nonkins, and depending on their social roles, the size and composition of social networks vary across individuals (Grueter et al., \u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e2020\u003c/span\u003e). Although large, mixed networks could be adaptive for group cohesion and attaining collecting benefits, due to the risk of aggression, interacting with loosely affiliated others brings uncertainties, stresses, and anxieties (Cheney \u0026amp; Seyfarth, \u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e2008\u003c/span\u003e). In these contexts, affiliative vocalizations could disambiguate intentions and motivations, thus facilitating social interactions and even reunions (e.g., in groups with fission-fusion dynamics, e.g., \u003cem\u003eAteles geoffroyi\u003c/em\u003e: Ramos-Fern\u0026aacute;ndez, \u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e2008\u003c/span\u003e; \u003cem\u003ePan paniscus\u003c/em\u003e: Schamberg et al., \u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e2016\u003c/span\u003e, \u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e2017\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eMoreover, in multi-level societies, vocal communication should be of greater necessity (Bouchet et al., \u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e2013\u003c/span\u003e). Conventional approaches of social network analysis identified multi-layered social networks, matching the complexity of social structures (e.g., \u003cem\u003ePapio hamadryas\u003c/em\u003e: Patzelt et al., \u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e2014\u003c/span\u003e; \u003cem\u003ePapio papio\u003c/em\u003e: Dal Pesco \u0026amp; Fischer, \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e2018\u003c/span\u003e; \u003cem\u003eTheropithecus gelada\u003c/em\u003e: Snyder-Mackler et al., \u003cspan citationid=\"CR35\" class=\"CitationRef\"\u003e2014\u003c/span\u003e; and \u003cem\u003eRhinopithecus roxellana\u003c/em\u003e: Qi et al., \u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e2014\u003c/span\u003e). Depending on individuals\u0026rsquo; social parameters, relationship type, strength, and value vary considerably (Grueter et al., \u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e2020\u003c/span\u003e). With the use of molecular approaches, patterns of group dynamics, like dispersal, fission, and fusion, could be explained from the perspective of kin selection (e.g., \u003cem\u003ePapio hamadryas\u003c/em\u003e: Schreier \u0026amp; Swedell, \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2009\u003c/span\u003e; \u003cem\u003eTheropithecus gelada\u003c/em\u003e: Snyder-Mackler et al., \u003cspan citationid=\"CR35\" class=\"CitationRef\"\u003e2014\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eNevertheless, the role of vocal communication in cultivating social relationships could have been overlooked. Wild golden snub-nosed monkeys live in large 4-layer societies composed of several one-male multi-female units and shadowing bachelor males. Although residential males maintain rather \u0026lsquo;distant\u0026rsquo; relationships with one another (characterized by the absence of direct affiliative interaction like approaching and grooming), between-unit male-male affiliations could exist, with whom they maintain a closer social distance and form alliances (Qi et al., \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). Among females, similarly, grooming and social proximity are restricted, almost exclusively, to unit members. Although the social bonds between females and residential males decay prior to takeovers, females were rarely found engaging in close contact with their future mates (Qi et al., \u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e2009\u003c/span\u003e, \u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e2020\u003c/span\u003e). It is possible that vocal communication was used.\u003c/p\u003e \u003cp\u003eIn addition, cultivating large social networks places a heavy demand on time and energy budget. Due to the seasonally changing environment, wild golden snub-nosed monkeys travel distantly for food and other resources (Zhao et al., \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e2023\u003c/span\u003e). During their limited time of resting, social interactions should be allocated in favor to more valuable relationships, for residential males and females, within-unit bonds. For the out-unit relationships, in contrast, vocal communication provides an economical solution (i.e., vocal grooming: Dunbar, \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). Alternatively, considering the more uncertain and riskier between-unit relationships, social evolution could have favored vocal communication for cultivating bonds and reassuring affiliation when interacting, potentially as replacements for more \u0026lsquo;stressful\u0026rsquo; forms of affiliative interactions (e.g., approaching, greeting, grooming). Based on our impression of two decades of longitudinal study and past research (Fan et al., \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e2018\u003c/span\u003e, \u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e2019\u003c/span\u003e), we suspect contact \u0026lsquo;coo\u0026rsquo; calls could serve the above functions.\u003c/p\u003e \u003cp\u003eIn this study, we innovatively incorporated the contact \u0026lsquo;coo\u0026rsquo; calls into the traditional social network analysis, and then compared the resulting \u0026lsquo;contact call exchange network\u0026rsquo; with the social networks calculated from grooming and proximity data. The contact \u0026lsquo;coo\u0026rsquo; call is the most frequently used call type in the wild (Fan et al., \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). Like the calls of other nonhuman primates, it is acoustically simple (\u0026lsquo;aye\u0026rsquo; or \u0026lsquo;aye-aye\u0026rsquo; in English transcript: X.-G. Qi, personal communication), bears clear individuality in acoustic characteristics, and is used across various neutral or affiliative contexts (Fan et al., \u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). We ask: (1) whether contact calls help cultivate social networks and (2) whether call uses exhibit context- and role-dependent varieties.\u003c/p\u003e"},{"header":"Method","content":"\u003cp\u003eThe study was carried out on the northern slope of the Qinling Mountains (108\u0026deg;14\u0026prime;-108\u0026deg;18\u0026prime;E, 33\u0026deg;45\u0026prime;-33\u0026deg;50\u0026prime;N, 1500-2890m above sea level) Yuhuangmiao village, Zhouzhi National Nature Reserve (ZNNR), Shaanxi Province, China. The subjects were a population of free-ranging but provisioned golden snub-nosed monkeys of the GNG-Breeding band. The GNG herd contained a breeding band composed of 13 one-male multi-female units (hereafter, OMUs) and 13 to 32 bachelor males. Together with the DJF herd, two herds form the West troop (Qi et al. \u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e2014\u003c/span\u003e). Monkeys were provided with corn and carrots for close observation. The provision site was a frequent foraging and resting site. Provision was provided twice daily, after the band entered the site and before the band left the site. Provision constituted less than 30% of their average daily caloric intake.\u003c/p\u003e \u003cp\u003eThe climate is semi-humid and seasonal, with spring from March to May, summer from June to August, autumn from September to November, and winter from December to February (Li et al. \u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e2000\u003c/span\u003e). Average annual rainfall is 894mm. The average annual temperature is 10.7℃ with a maximum of 31.5℃ in July and a minimum of -14.3℃ in January (Qi et al. \u003cspan citationid=\"CR27\" class=\"CitationRef\"\u003e2008\u003c/span\u003e). In the wild, extreme weather conditions and low visibility of dense foliage often impeded data collection; and the study population was very large, motile, hard to approach, and loquacious.\u003c/p\u003e\n\u003ch3\u003eData collection\u003c/h3\u003e\n\u003cp\u003eFrom September 22nd, 2018, to June 4th, 2019, we followed the herd from 0500 to 1900 (Beijing Standard Time) for 186 days, 2232 hours. We studied 70 adult individuals, including 13 males and 57 females. However, because 3 OMUs were not stable and eventually disappeared from the band before the study ended, we excluded the data collected from these units from our analysis. Hence, in our final sample, data from 54 adults including 10 adult males and 44 adult females of ten OMUs are presented.\u003c/p\u003e \u003cp\u003eAge categories included adult males (\u0026gt;\u0026thinsp;7yrs), adult females (\u0026gt;\u0026thinsp;5yrs), sub-adults (female: 4\u0026ndash;5yrs, male: 5\u0026ndash;7yrs), juveniles (1\u0026ndash;4yrs), and infants (\u0026lt;\u0026thinsp;1\u0026nbsp;year) (Qi et al., \u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e2009\u003c/span\u003e). Before data collection, we first identified each subject based on physical characteristics (including body size, facial features, pelage color, the granulomatous flanges on both sides of their lips, and secondary sexual characteristics: Li \u0026amp; Zhao, 2007). Based on the reproductive history, lactating and nonlactating females were also distinguished. We selected one OMU as the focal unit per day and rotated observations evenly among 10 units. Our data collection concentrated on 4 types of social interactions between dyads, including spatial proximity, grooming, aggressive-submissive behaviors, and contact call exchange.\u003c/p\u003e \u003cp\u003eSpatial proximity was recorded by calculating the distance between the focal subject and the nearest neighbor using focal animal sampling and instantaneous scan sampling at five-minute intervals (Altmann, 1974). Grooming interactions were recorded by noting the identities of the groomer and recipient and the start and end time ad libitum. Aggressive-submissive behaviors were also recorded using the ad libitum sampling method with the identities of the aggressor and victim, the start and end time, types of agnostic behavior involved, and the winning party being noted in detail. Agnostic behaviors were defined as behaviors that involve biting, fighting, chasing, threatening, and supplanting, and submissive behaviors as behaviors that include avoiding, crouching, and retreating (Li et al., \u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e2006\u003c/span\u003e). To estimate the dominance hierarchy, the turnouts of aggressive-submissive interactions were converted into the normalized David score (NDS) following the method standardized by de Vries et al (2006). Finally, contact call exchanges were recorded and defined as the exchange of calls between two individuals within a 5s duration (Fan et al. \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e2018\u003c/span\u003e).\u003c/p\u003e \u003cdiv id=\"Sec4\" class=\"Section2\"\u003e \u003ch2\u003eData analysis\u003c/h2\u003e \u003cp\u003eData analyses were done to investigate the role of contact calls in cultivating social relationships and potential functional diversifications depending on sex, reproductive states, and social roles of callers and recipients.\u003c/p\u003e \u003cp\u003eSpatial proximity, grooming, and contact call exchange data were independently converted into matrixes for each OMU and the whole band, using the calculation of HWI in SOCPROG v. 2.4. The matrixes were then cross-compared through the Quadratic Assignment Procedure (QAP) and UCINET to see whether contact call exchanges serve similar or different social functions as grooming and social proximity (Borgatti et al., \u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2002\u003c/span\u003e; Johnson et al., \u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e2013\u003c/span\u003e). QAP compares matrixes by randomly rearranging their rows (and matching columns), performing nonparametric tests on the coefficients through the permutations (we ran 99 999 times), and calculating the correlation coefficient between two matrixes. We chose QAP because it rearranges whole rows and columns rather than individual cells, a default setting that preserves subtle properties of the matrixes (Johnson et al., \u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e2013\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eTo see whether dominance hierarchy predicts the initiation and/or response of contact calls, we investigated the relationships between rank with call initiation and reception separately using Spearman's rho correlation tests. To investigate sex differences in contact call uses, we ran two paired t-tests. In the first test, we asked whether males used contact calls more frequently than females. In the second test, we asked whether males directed disproportionally more contact calls to the lactating females than to nonlactating ones.\u003c/p\u003e \u003cp\u003eDuring the study period, a total of 7 females from 7 OMUs were with newborns (who were lactating). Because lactating females were unevenly distributed across units, the frequency and/or proportion of contact calling exchanges with lactating females could be overrepresented in some units. To avoid the influence of unequal data distribution, we compared the expected values and actual values of contact call exchange frequency. Expected values were calculated based on the null hypothesis that contact calls were not given selectively but equally to every unit member (not biased toward lactating females). All statistical tests were two-tailed and performed using SPSS 24.0 (SPSS, Inc., Chicago, IL, USA) with P＜0.05 taken as the significance.\u003c/p\u003e \u003c/div\u003e"},{"header":"Results","content":"\u003cp\u003eData collection was impeded by poor visibility, unpredictable weather conditions, and the noisy study population. In some cases, simultaneous responses from multiple recipients ambiguated the actual correspondences. To avoid mistaking the actual caller and recipient, we conservatively included only the call bouts where both the caller and recipients were unambiguously noted. This yielded a sample of 2135 call exchange bouts. Spatial proximity, grooming, and contact call exchange data were collected from 54 subjects (10 adult males, 44 adult females) on 186 days, and the average observation of each OMU was 15\u0026thinsp;\u0026plusmn;\u0026thinsp;3d.\u003c/p\u003e \u003cp\u003eWe generated 22 matrixes based on the association indexes between all within- and between-unit dyads using SOCPROG v. 2.4. The 22 matrixes included 10 spatial proximity association matrixes and 10 contact call exchange matrixes for the 10 study units separately, as well as 1 spatial proximity association matrix and 1 vocal communication association matrix for the breeding band (with each OMU being taken as a focal point). The matrixes can be found in the \u003cspan refid=\"Sec14\" class=\"InternalRef\"\u003eAppendixes\u003c/span\u003e (1\u0026ndash;5).\u003c/p\u003e \u003cdiv id=\"Sec6\" class=\"Section2\"\u003e \u003ch2\u003eContact call exchange and spatial proximity\u003c/h2\u003e \u003cp\u003eContact call exchanges were used differently in between- and within-unit contexts. The QAP correlation analysis revealed significant negative correlations between contact call exchange and spatial proximity matrixes in six OMUs, but a significant positive correlation between OMUs. Across the six units, the correlation coefficients ranged from \u0026minus;\u0026thinsp;0.671 to -0.335 (low to moderately low) with p-values ranging from 0.011 to 0.041. All units except SQ, SX, XB, and ZD showed significant correlations despite the low to moderately low coefficients (-0.671 to -0.495; see Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e for details). Together, our finding suggests that the exchange of contact calls was more frequent between unit members with greater social distances.\u003c/p\u003e \u003cp\u003eAmong OMUs (or on the band level), in contrast, the association matrixes of spatial proximity and contact call exchange were significantly positively correlated, with a moderate correlation coefficient (the QAP correlation analysis; N\u0026thinsp;=\u0026thinsp;99999 permutation; r\u0026thinsp;=\u0026thinsp;0.337, P\u0026thinsp;=\u0026thinsp;0.004). Because between units, contact calls were exclusively exchanged among residential males, the positive correlation indicates more frequent contact call exchanges among residential males who maintained closer spatial proximity (see Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e1\u003c/span\u003eb and c). In addition, we also found that some male-male relationships were more strongly reflected by contact call exchange than by social proximity (see Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e1\u003c/span\u003ec: unexpected relationships, in red).\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec7\" class=\"Section2\"\u003e \u003ch2\u003eContact call exchange and grooming\u003c/h2\u003e \u003cp\u003eGrooming was not observed between members of different units (see Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e1\u003c/span\u003ea), so we only computed within-unit grooming matrixes. QAP analysis indicated that in 7 out of 10 OMUs, contact call exchange and grooming matrixes were not significantly correlated (r ranged from 0.260 to 0.330, P values ranged from 0.106 to 0.414, see Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e for details). In the rest three units, the coefficients were significant, with moderate to moderately high coefficients (SX unit r\u0026thinsp;=\u0026thinsp;0.372, p\u0026thinsp;=\u0026thinsp;0.039; LZ unit: r\u0026thinsp;=\u0026thinsp;0.547, p\u0026thinsp;=\u0026thinsp;0.017; BF unit: r\u0026thinsp;=\u0026thinsp;0.545, p\u0026thinsp;=\u0026thinsp;0.034). Together with the above findings, grooming interaction was not as strongly correlated with contact call exchange as social proximity, although moderately positively correlated.\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab1\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 1\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eRelationships between vocal communication networks and other networks\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"7\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c5\" colnum=\"5\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c6\" colnum=\"6\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c7\" colnum=\"7\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eOMU\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colspan=\"2\" nameend=\"c3\" namest=\"c2\"\u003e \u003cp\u003eSocial proximity\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\" morerows=\"1\" rowspan=\"2\"\u003e\u0026nbsp;\u003c/th\u003e \u003cth align=\"left\" colspan=\"2\" nameend=\"c6\" namest=\"c5\"\u003e \u003cp\u003eGrooming interaction\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c7\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eUnit size\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003e\u003cb\u003er\u003c/b\u003e\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003e\u003cb\u003eP\u003c/b\u003e\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c5\"\u003e \u003cp\u003e\u003cb\u003er\u003c/b\u003e\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c6\"\u003e \u003cp\u003e\u003cb\u003eP\u003c/b\u003e\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eBF\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e-0.608\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e\u003cb\u003e0.033*\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e 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colname=\"c5\"\u003e \u003cp\u003e0.547\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e\u003cb\u003e0.017*\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eSQ\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e-0.560\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e0.084\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e0.260\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e0.184\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e5\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eSX\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e-0.435\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e0.059\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e0.372\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e\u003cb\u003e0.039*\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eTB\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e-0.538\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e\u003cb\u003e0.012*\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e0.057\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e0.414\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eXB\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e-0.671\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e0.166\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e0.458\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e0.168\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e4\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eZD\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e-0.495\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e0.110\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e0.264\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e0.186\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e5\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cdiv id=\"Sec8\" class=\"Section3\"\u003e \u003ch2\u003eP\u0026thinsp;\u0026lt;\u0026thinsp;0.05*\u003c/h2\u003e \u003cdiv id=\"Sec9\" class=\"Section4\"\u003e \u003ch2\u003eContact call exchange and dominance rank\u003c/h2\u003e \u003cp\u003eBecause almost all agnostic interactions were found between dyads of residential males, only between-unit dominance hierarchy was considered. 410 cases of aggression-submission agonistic interactions were recorded, and the turnouts were converted into NDS (see Appendix 6 for details). The dominance hierarchy was linear with a moderately high steepness (steepness K\u0026thinsp;=\u0026thinsp;0.66, R2\u0026thinsp;=\u0026thinsp;0.977).\u003c/p\u003e \u003cp\u003eSpearman's rho correlation tests showed that dominance statuses were strongly and positively correlated with contact call initiation (Spearman's rho correlation: r\u0026thinsp;=\u0026thinsp;0.628, P＜0.05, N\u0026thinsp;=\u0026thinsp;10) but not with reception (r\u0026thinsp;=\u0026thinsp;0.468, P＞0.05, N\u0026thinsp;=\u0026thinsp;10; see Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e1\u003c/span\u003ee). Higher-ranking males called more frequently, though received calls in similar frequencies, than the lower-ranking ones. This could be the result of the larger social network sizes of higher-ranking males, their central leading roles on the band level, or the function of contact call exchange for advertising affiliation publicly (see discussion below).\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv id=\"Sec10\" class=\"Section2\"\u003e \u003ch2\u003eSex differences in contact call exchange\u003c/h2\u003e \u003cp\u003ePaired Sample t-test revealed a significant sex difference in contact calling frequency (N\u0026thinsp;=\u0026thinsp;10, P\u0026thinsp;=\u0026thinsp;0.002). Males on average called two times more frequently than females (38% vs. 15%). Three lines of evidence could explain the sex asymmetry. First, males had more call exchange correspondences than females (see Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e1\u003c/span\u003ea-c). Residential males not only exchanged contact calls with same-unit females but also males from other units, while females exchanged calls primarily with same-unit members (also see Fan et al., \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e2018\u003c/span\u003e, \u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). Second, within units, contact call exchange likely served affiliative and mate-securing functions, and helped residential males keep females near and reassure their affiliation. Finally, between units, contact calls helped males cultivate social relationships with other males; especially for high-ranking residential males, the loud and broadcasting call feature functioned potentially for advertising affiliation and reaffirming dominance rank (Fan et al., \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e2018\u003c/span\u003e).\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec11\" class=\"Section2\"\u003e \u003ch2\u003eFunctional diversifications in contact call exchange\u003c/h2\u003e \u003cp\u003eWe conducted an additional test to verify the second observation. We hypothesized that if contact calls served affiliative and mate-securing functions, males should be allocated more calls to lactating females than to nonlactating ones, because lactating females were often occupied with childcare and foraging, thus staying distantly from unit centers, and seldomly engaged in grooming interactions. With lactating females, residential males exchanged more contact calls than expected by chance (N\u0026thinsp;=\u0026thinsp;7, P＜0.05), but not with nonlactating ones (N\u0026thinsp;=\u0026thinsp;7, P＞0.05). Hence, contact call exchanges could have supplanted social proximity if same-unit correspondences were occupied by other important tasks (see Fig.\u0026nbsp;\u003cspan refid=\"Fig4\" class=\"InternalRef\"\u003e2\u003c/span\u003e).\u003c/p\u003e \u003c/div\u003e"},{"header":"Discussion","content":"\u003cp\u003eOur wild golden snub-nosed monkeys used contact calls to cultivate social relationships. The complexity of the multi-level society and the heterogeneity of social relationship types, though brought challenges to our investigation, helped clarify the functions of contact call uses.\u003c/p\u003e \u003cp\u003eIn most units, contact call exchange was negatively correlated with social proximity but positively correlated with grooming (though not significantly). This indicates that unit members exchanged contact calls for affiliative purposes in parallel with grooming and as replacements for social proximity. The study units were with 4 to 6 members, which likely impeded grooming interactions and caused greater social distances between some unit members. Contact call exchanges likely supplanted social proximity for affiliating with relatively distantly positioned unit members, which in turn, could facilitate unit cohesion by informing locations and coordinating movements. On the other hand, when their grooming partners were occupied, for instance by traveling, foraging, and childcare, contact calls could be used for vocal grooming as replacements for \u0026lsquo;physical\u0026rsquo; grooming.\u003c/p\u003e \u003cp\u003e Between units, on the other hand, contact calls helped residential males cultivate relatively distant social relationships. Between-unit social distances are often greater than those within units, potentially because of foraging competition and dominance relationships (Qi et al., \u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e2009\u003c/span\u003e). Social network analysis using grooming and social proximity as inputs has long characterized the relationships among residential males as loose or distant (but see male-male cooperation in Qi et al., \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). Nevertheless, contact call exchanges circumvented the inter-unit barriers of competition and hostility and helped residential males cultivate intrasexual relationships.\u003c/p\u003e \u003cp\u003eAs our findings revealed, the between-unit networks of contact call exchanges and social proximity were significantly positively correlated. Residential males maintaining closer between-unit social distances also exchanged contact calls more frequently. The units of golden snub-nosed monkeys were often in constant movement towards or away from one another, especially during foraging. Uncertainties about intention could result in fighting and cause stress and anxiety. On the other hand, while resting, some units preferentially maintained closer distances from one another, as our between-unit proximity matrix revealed. These units often shared the same trees with mutual tolerances, while the approaching of other units could bring turmoil and conflict. Hence, in between-unit interactions, contact call exchanges likely facilitated approaching by signaling benign motivation and helped cultivate between-unit relationships as a replacement for grooming.\u003c/p\u003e \u003cp\u003eMoreover, the patterns of contact call exchange revealed functional diversifications depending on sexes, reproductive states, and social roles. Compared to females, males on average called two times more frequently because of larger social network sizes (containing both within- and between-unit social relationships). Second, contact calls were directed more to lactating females than to nonlactating ones. Lactating females devoted more time to foraging and childcare (including carrying, feeding, and grooming) than nonlactating ones, hence staying further away from the unit center and having a lower time budget for grooming. This potentially made contact calls economical for cultivating valuable within-unit relationships, but also practical for unit coordination (by informing locations and coordinating movements). Finally, for residential males, contact calls helped cultivate and advertise between-unit relationships.\u003c/p\u003e \u003cp\u003eAmong residential males, higher-ranking ones gave (but did not receive) more contact calls than lower-ranking ones. High-ranking males maintained larger between-unit social networks than lower-ranking ones (see Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e1\u003c/span\u003e). Larger network sizes predicted greater leadership roles in band movements and more male alliances (Qi et al., \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Wang et al., \u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e2020\u003c/span\u003e). The dominance and leading role of some residential males and their units likely provided the priorities to access resources, while having more male alliances could be more effective at deterring bachelor males. In addition, because contact calls are loud and public, with calls being directed and responded to specific individuals (Fan et al., \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e2018\u003c/span\u003e), residential males could have used them for advertising affiliation and alliances. Advertising male-male alliances could help maintain dominance hierarchy by forestalling attempts to rank reversals, female alluring, and takeover attempts.\u003c/p\u003e \u003cp\u003eCompared with hamadryas baboons, using contact calls for cultivating and advertising intrasexual relationships could be more important to golden snub-nosed monkeys. Among hamadryas leaders, bonds and alliances are often founded on kinship ties (Schreier \u0026amp; Swedell, \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2009\u003c/span\u003e). In contrast, although relatedness predicts social bonds among bachelor males, the residential males of golden snub-nosed monkeys likely form bonds and alliances with both kins and nonkins (Qi et al., \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Ren et al., \u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). Therefore, in this species, uncertainties about male-male relationships and interactions are likely greater, especially in the absence of close affiliative interactions comparable to that in hamadryas males (e.g., grooming and ritualized greeting: Patzelt et al., \u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e2014\u003c/span\u003e). Hence, the social evolution of the multi-level societies of this species likely selected affiliative calls for easing inter-unit tension and promoting aggregation.\u003c/p\u003e \u003cp\u003eOn the other hand, the dynamic and multi-layered societies of this species could have also favored the evolution of functional diversity of contact calls. In response to the seasonally changing climate and resource distribution and quality, group size, home range size, and daily travel distance are constantly adjusted, explaining frequent fission and fusions (Qi et al., \u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e2014\u003c/span\u003e; Zhao et al., \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e2023\u003c/span\u003e). During these events, contact call exchanges could help resolve stress and anxiety and facilitate individual recognition and reunions (Yang et al., in preparation; also see in chimpanzees: Crockford \u0026amp; Boesch, \u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e2005\u003c/span\u003e; bonobos: Schamberg et al., \u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e2016\u003c/span\u003e, \u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e2017\u003c/span\u003e).\u003c/p\u003e \u003cdiv id=\"Sec13\" class=\"Section2\"\u003e \u003ch2\u003eSummary\u003c/h2\u003e \u003cp\u003eDespite its simple acoustic construction, contact calls in golden snub-nosed monkeys exhibited functional diversifications. Within units, for both sexes, contact calls helped cultivate relationships and likely served other practical functions (e.g., informing locations and coordinating movements). For males only, the calls were used for affiliating with lactating females who were unavailable for grooming (due to infant care and prolonged foraging). Between units, on the other hand, contact calls were used for cultivating and, potentially, advertising male-male relationships and alliances. Together, along with grooming and social proximity, golden snub-nosed monkeys incorporated contact calls (and likely other call types) for various affiliative and practical purposes, potentially as an adaptation to the demand of cultivating large, multi-layered social networks. On the other hand, because maintaining and cultivating those relationships could be time- and energetically demanding, the sophistication of call interpretation could be economical and practical for both callers and recipients. By making associations with social knowledge and information, including sexes, reproductive states, dominance ranks, and social roles and histories, interpretations of the calls could be precise. For the callers, similarly, repeated interactions and call exchanges with specific recipients could ritualize the calls by associating them with specific intentions. This is consistent with the \u0026lsquo;social complexity\u0026rsquo; hypothesis and in parallel with the vocal communication systems of other primate species, including humans. Our work revealed the social significance of contact calls, and our ongoing studies are investigating that of other call types (e.g., grunting, screaming, and barking). We suggest that the functional diversifications of contact call uses could have coevolved with the multi-level societies of this species.\u003c/p\u003e \u003c/div\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eAcknowledgments\u0026nbsp;\u003c/strong\u003e\u0026nbsp; We thank Zhouzhi National Nature Reserve (ZNNR) for the permission for the research. Thanks also to editors, reviewers, and all the members of the golden snub-nosed monkey Research Team at the College of Life Science, Northwest University.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eFunding Information\u003c/strong\u003e\u0026nbsp; \u0026nbsp;Our research was supported by the National Natural Science Foundation of China (31622053, 31730104), the Promotional Project for Innovation team, the Department of Science and Technology of Shaanxi Prov. China (2018TD-017), the National Key Program of Research and Development, Ministry of Science and Technology of China (2016YFC0503200).\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConflict of interest\u003c/strong\u003e\u0026nbsp; \u0026nbsp;\u003c/p\u003e\n\u003cp\u003eThe authors declare no conflict of interest.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eCompliance with ethical standards\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eWe adhered to the American Society of Primatologists (ASP) Principles for the Ethical Treatment of Non-Human Primates, followed the American Society of Primatologists Code of Best Practices for Field Primatology, and adhered to the legal requirements of the People\u0026rsquo;s Republic of China.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eEthical approval\u003c/strong\u003e\u0026nbsp; \u0026nbsp;\u003c/p\u003e\n\u003cp\u003eResearch was permitted by the Chinese Academy of Sciences and the ethics board of the College of Life Sciences, Northwest University.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eData availability\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eData were uploaded to Dryad and shared through a private link (DOI: 10.5061/dryad.tdz08kq5p) for submission and review. After acceptance, it will be made public.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eContributor Roles\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eXiao-Guang Qi and Bao-Guo Li acquired funding leading to this publication, Wen-Yong Tian and Dai-Bo Zhu supervised and administrated the project, Xiao-Guang Qi designed the research, Yan Ying and Yi-Jun Yang performed the research, Yan Ying and Yi-jun Yang analyzed data, Yi-Jun Yang made the graphs and figures and wrote the manuscript.\u0026nbsp;\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\u003cli\u003e\u003cspan\u003eBergman TJ, Beehner JC, Cheney DL, Seyfarth RM (2003) Hierarchical Classification by Rank and Kinship in Baboons. 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In Zoological Research. \u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttps://www.zoores.ac.cn/en/article/id/3d1a26bb-81a\u003c/span\u003e\u003cspan address=\"https://www.zoores.ac.cn/en/article/id/3d1a26bb-81a\" targettype=\"URL\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e5-40f9-a6db-28ba0c75003d\u003c/span\u003e\u003c/li\u003e\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":true,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true},"keywords":"contact calls, functional diversifications, social complexity hypothesis, convergent evolution, multi-level society, Rhinopithecus roxellana","lastPublishedDoi":"10.21203/rs.3.rs-3687604/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-3687604/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eThe ability to cultivate social relationships through language is human uniqueness. However, despite small repertoire sizes, nonhuman primates could use vocalization for social purposes too. Vocal communication could be evolutionarily ancient, and likely evolved hand-in-hand with complex, dynamic social structures. By studying the vocal communication in wild golden snub-nosed monkeys (\u003cem\u003eRhinopithecus roxellana\u003c/em\u003e), a species of Asian colobine living in 4-layer multi-level societies with fission-fusion dynamics, we unraveled the complex social functions of contact \u0026lsquo;coo\u0026rsquo; calls. Contact calls helped cultivate both within- and between-unit relationships, and depending on the sexes, reproductive states, and social roles of callers and recipients, were also functionally diverse. Within units, calls replaced grooming and were supplementary to social proximity. Males directed more calls to lactating females, who were unavailable for grooming and away from unit centers due to extended foraging and childcare. Higher-ranking males called more frequently but did not receive more calls than lower-ranking ones. Considering their larger social network sizes and leadership roles, contact calls likely facilitated inter-unit proximity and were used for advertising intrasexual affiliation and alliances. By comparing the network of contact call exchange with that of social proximity and grooming, we identified the inter-unit social relationships that were otherwise inconspicuous and, more importantly, the potential mechanisms for maintaining male-male alliances and unit and band cohesion. Together with previous findings, we conclude that contact calls are economical and low-risk social tools for reassuring and advertising affiliation, resolving uncertainties, and promoting cohesion and alliance formation.\u003c/p\u003e","manuscriptTitle":"Functional Diversifications of Contact Calls in a Multi-level Primate Society","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2023-12-12 15:40:07","doi":"10.21203/rs.3.rs-3687604/v1","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"7e0e3300-90e1-4c08-a5be-0e45c642636a","owner":[],"postedDate":"December 12th, 2023","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"posted","subjectAreas":[],"tags":[],"updatedAt":"2024-01-06T11:42:44+00:00","versionOfRecord":[],"versionCreatedAt":"2023-12-12 15:40:07","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-3687604","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-3687604","identity":"rs-3687604","version":["v1"]},"buildId":"Yz8egH4vZwpy0AgOkR8nz","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}