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XU P F, LIU H Y, LI Y P, et al. Seasonal variation of social monitoring behavior of all-male unit for Rhinopithecus bieti[J]. Journal of Sichuan Forestry Science and Technology, 2023, 44(4): 143−148 doi: 10.12172/202209210001
Citation: XU P F, LIU H Y, LI Y P, et al. Seasonal variation of social monitoring behavior of all-male unit for Rhinopithecus bieti[J]. Journal of Sichuan Forestry Science and Technology, 2023, 44(4): 143−148 doi: 10.12172/202209210001

Seasonal Variation of Social Monitoring Behavior of All-male Unit for Rhinopithecus bieti


doi: 10.12172/202209210001
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  • Social monitoring refers to animals cognition of the social environment for adaptation and improving their fitness. In order to understand the frequency and influencing factors of individual social monitoring behavior of all-male unit in black-and-white snub-nosed monkey (Rhinopithecus bieti) under a multi-level social organization, from July 2017 to August 2018, the data of scanning behavior and aggression-submissive behavior of 8 individuals in the all-male unit of R. bieti in Xiangguqing of Baima Snow Mountain National Nature Reserve were collected by using 5-minute focus animal and all-occurrence recording method, and the frequency differences of monitoring behavior in different seasons and grade groups were compared. The results showed that the frequency of scanning behavior was 0.67 ± 0.19 Times /min (n = 8, 0.37-1.01). There was a difference in the frequency of scanning behavior between winter and summer (Z = 7.36, P < 0.001), and the frequency of scanning behavior in summer (0.80 ± 0.24, n = 8) was higher than that in winter (0.50 ± 0.21, n = 8), which may due to high competitive pressure of reproductive and mating in summer. The frequency of scanning behavior in different grade groups was different (H = 62.37, df = 2, P < 0.001). The low grade group (0.85 ± 0.14, n = 3) was higher than the middle grade group (0.68 ± 0.28, n = 2), and the middle grade group was higher than the high grade group (0.49 ± 0.12, n = 3), which indicated that low-grade individual spent more time on social monitoring within all-male unit of R. bieti. Therefore, our finding found that the frequency of social monitoring of R. bieti in all-male unit is affected by the reproductive season and grade group. Adult males can reduce the attack by the resident males of reproductive units through social monitoring, and the social monitoring of young and juvenile males can reduce the direct conflicts within the all-male unit.
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  • [1] Treves A. Theory and method in studies of vigilance and aggregation[J]. Animal Behaviour, 2000, 60(6): 711−722. doi: 10.1006/anbe.2000.1528
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    [17] 王荣涛. 秦岭川金丝猴 (Rhinopithecus roxellana) 全雄群的组成, 亚群体类型及个体间等级关系 [D]. 西北大学, 2014.
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Seasonal Variation of Social Monitoring Behavior of All-male Unit for Rhinopithecus bieti

doi: 10.12172/202209210001
  • 1. Institute of Easter-Himalaya biodiversity Research, Dali University, Dali 671003, China
  • 2. Provincial Innovation Team of Biodiversity Conservation and Utility of the Three Parallel Rivers Region from Dali University, Dali 671003, China
  • 3. Yunling Black-and-White Snub-Nosed Monkey Observation and Research Station of Yunnan Province, Dali 671003, China
  • Corresponding author: liyp@eastern-himalaya.cn huangzp@eastern-himalaya.cn

Abstract: Social monitoring refers to animals cognition of the social environment for adaptation and improving their fitness. In order to understand the frequency and influencing factors of individual social monitoring behavior of all-male unit in black-and-white snub-nosed monkey (Rhinopithecus bieti) under a multi-level social organization, from July 2017 to August 2018, the data of scanning behavior and aggression-submissive behavior of 8 individuals in the all-male unit of R. bieti in Xiangguqing of Baima Snow Mountain National Nature Reserve were collected by using 5-minute focus animal and all-occurrence recording method, and the frequency differences of monitoring behavior in different seasons and grade groups were compared. The results showed that the frequency of scanning behavior was 0.67 ± 0.19 Times /min (n = 8, 0.37-1.01). There was a difference in the frequency of scanning behavior between winter and summer (Z = 7.36, P < 0.001), and the frequency of scanning behavior in summer (0.80 ± 0.24, n = 8) was higher than that in winter (0.50 ± 0.21, n = 8), which may due to high competitive pressure of reproductive and mating in summer. The frequency of scanning behavior in different grade groups was different (H = 62.37, df = 2, P < 0.001). The low grade group (0.85 ± 0.14, n = 3) was higher than the middle grade group (0.68 ± 0.28, n = 2), and the middle grade group was higher than the high grade group (0.49 ± 0.12, n = 3), which indicated that low-grade individual spent more time on social monitoring within all-male unit of R. bieti. Therefore, our finding found that the frequency of social monitoring of R. bieti in all-male unit is affected by the reproductive season and grade group. Adult males can reduce the attack by the resident males of reproductive units through social monitoring, and the social monitoring of young and juvenile males can reduce the direct conflicts within the all-male unit.

  • 社会监视行为 (Social monitoring behavior) 指动物对社会环境的认知,以适应环境提高适合度[1]。社会监视行为研究有助于理解动物资源竞争[2-4]、群体凝聚力[5]、群体成员识别[6]、反捕食防御[7-8]和成员间距离调节[9]等方面的行为策略。因此,社会监视行为是行为生态学和种群稳定维持的重要内容。

    灵长类的社会监视行为发生频次与个体的等级有关。赤猴 (Erythrocebus patas) 和笼养的棕色卷尾猴 (Cebus apella) 社会监视行为中低等级个体注视 (Visual attention) 高等级个体[9],且低等级个体花更多时间投入于社会监视行为 [10]。但相反,Hirsch[7]对棕色卷尾猴研究,高等级的个体比低等级个体花更多的时间保持监视,并且邻居数量的增加,监视行为增强。物种间的比较发现等级森严的松鼠猴 (Saimiri sciureus) 比等级松散的白唇柽柳猴(Saguinus labiatus)花费更多时间监视群内成员[11]

    灵长类的社会监视行为受社群内部个体的繁殖需求影响。绒猴 (Callithrix jacchus) 个体社会监视行为的增加与繁殖竞争的增加有关[4]。雄性红疣猴 (Colobus badius) 和红长尾猴 (Cercopithecus aethiops) 在繁殖期间会提高监视行为[3][12]。但尽管社会监视行为在许多灵长类中已经报道[1],对于复杂的重层社会组织,社会监视行为的关注较少。

    滇金丝猴 (Rhinopithecus bieti) 又称黑白仰鼻猴,为我国特有珍稀濒危灵长类,仅分布于金沙江和澜沧江之间的云岭山系,北至西藏芒康,南至云南云龙[13]。滇金丝猴具有复杂的重层社会组织,主要包括一雄多雌 (One-male unit, OMU) 的繁殖单元和全雄单元 (All-male unit, AMU) 两个部分[14]。全雄单元是由组建过家庭,但又被替换掉的成年雄性和未组建过家庭的成年雄性、青年雄性和未成年雄性等雄性聚集形成的社会单元[15]。全雄群既要靠近寻找繁殖机会或者替换繁殖单元的机会,又要警惕繁殖单元主雄攻击[16];此外,全雄群个体间存在严格等级[17-18],社会监视行为可减少群内的冲突。为了解滇金丝猴全雄群个体如何通过社会监视行为来减少繁殖竞争和避免群内冲突,本研究选择滇金丝猴公园的全雄群开展社会监视行为研究,拟解决2个问题:1) 不同季节全雄个体扫视行为发生频率的差异,预期繁殖季节时全雄群为增加繁殖机会及减少或避免被繁殖单元主雄的攻击会增加扫视行为;2) 不同等级全雄群个体扫视行为的差异,预期高等级个体扫视行为少,低等级个体为减少被攻击社会监视行为频率高。

    • 研究地点位于云南白马雪山国家自然保护区南段的响古箐 (北纬27°36', 东经99°15')。研究地点自然环境复杂,以云南松林、常绿阔叶林、高山硬叶栎树林、针阔叶混交林和高山暗针叶林等植被类型为主。年降水量为1370.7 mm,年平均气温为9.8℃ [19]。研究对象为白马雪山自然保护区响古箐滇金丝猴群中的全雄群,共8只个体,包括2只成年、3只青年和3只青少年 (见表1)。

      个体
      Individual
      年龄
      Age group
      观察时间/h (冬季/夏季)
      Observation time /h (winter/summer)
      状态
      Status
      白脸成年8.33 (4.17/4.17)完全在AMU
      春光成年8.58 (4.17/4.42)2018年5月组建家庭,不稳定
      二戊青年雄性8.42 (4.17/4.25)2019年4月组建家庭
      二己青年雄性8.33 (3.58/4.75)完全在AMU
      二甲青年雄性9.33 (4.67/4.67)完全在AMU
      四乙青少年雄性8.00 (3.33/4.67)完全在AMU
      四庚青少年雄性7.42 (2.50/4.92)2018年4月加入AMU
      五甲青少年雄性7.50 (3.00/4.50)2018年4月加入AMU

      Table 1.  Individuals composition and observation time of AMUs in a group of R. bieti

    • 采用5min焦点动物全事件取样法 (Focal animal all-occurrence sampling)[20],收集焦点个体5分钟内发生的监视行为次数及攻击与屈服行为数据。于2017年7月、2018年1月、2月、7月和8月,9:00至17:30收集数据,有效观察时间共65.92 h,单个个体的平均有效观察时间为8.24 ± 0.6 h (见表1)。

    • 扫视 (Scanning):头部发生45°的转向,并保持3~5 s才恢复头部位置[2]。将攻击行为分为攻击、取代2种类型,屈服行为分为回避、逃跑2种类型。记录的内容包括冲突的时间、发起者、接受者、发起者和接受者所出现的行为类型、冲突的原因和冲突的结果[21]

      攻击 (Aggressive):一个体用嘴或手攻击另一个体。

      取代 (Supplanting):等级高的个体走向等级低个体时,等级低个体离开原位置,由等级高个体占领该位置。

      逃跑 (Retreating):一个体受另一个体攻击时迅速逃跑。

      回避 (Avoiding):低等级个体在高等级过来时,主动离开原位置。

    • 数据分析使用SPSS22.0和Microsoft office Excel 2010软件完成。(1) 统计滇金丝猴全雄群所有个体冬季和夏季发生监视行为频率的平均值、标准偏差。(2) 利用非参数Mann-Whitney U检验,判断不同季节全雄单元个体的社会监视行为发生频率的差异性。(3) 应用优势指数[21]来确定全雄单元成员之间的等级关系。 (4) 统计不同等级个体发生扫视频率的平均值、标准偏差。(5) 利用非参数Kruskal Wallis H检验不同季节全雄群个体和不同等级个体的扫视行为发生频率差异。

    2.   结果
    • 滇金丝猴全雄个体扫视行为发生的频率为 0.67 ± 0.19次·min−1 ( n = 8, 0.37 − 1.01),冬季与夏季扫视频率存在显著差异 (Z = 7.36, P < 0.001),夏季 (0.80 ± 0.24, n = 8) 高于冬季 (0.50 ± 0.21, n = 8)。在冬夏两季,成年雄性白脸扫视频率无差异,春光扫视频率存在季节性差异,夏季高于冬季。青年雄性二甲和二已不同季节扫视频率无差异;二戊发生扫视频率存在季节性差异,夏季高于冬季。青少年雄性四乙、四庚和五甲扫视频率存在季节性差异,夏季高于冬季 (见表2)。

      个体
      Individuality
      冬季/T (Mean ± SD)
      Winter /T
      夏季/T (Mean ± SD)
      Summer /T
      Z, P
      白脸0.34 ± 0.46 (n = 50)0.40 ± 0.39 (n = 50)1.19, 0.235
      春光0.27 ± 0.34 (n = 50)0.94 ± 0.68 (n = 53)5.77, < 0.001
      二戊0.32 ± 0.44 (n = 56)0.68 ± 0.64 (n = 56)3.51, < 0.001
      二甲0.58 ± 0.42 (n = 43)0.72 ± 0.54 (n = 57)1.57, 0.118
      二已0.77 ± 0.51 (n = 50)0.63 ± 0.58 (n = 51)1.31, 0.191
      四乙0.81 ± 0.58 (n = 40)1.16 ± 0.82 (n = 56)2.50, 0.012
      四庚0.40 ± 0.42 (n = 30)1.01 ± 0.63 (n = 59)4.30, < 0.001
      五甲0.54 ± 0.50 (n = 36)0.86 ± 0.55 (n = 54)2.70, 0.007
      总平均0.67 ± 0.19 (n = 8, 0.37 – 1.01)

      Table 2.  Seasonal variation of the frequency of social monitoring behavior of AMUs in a group of R. bieti

    • 总共记录可见成对个体发生49次攻击行为及47次屈服行为 (见表3)。根据优势指数,将白脸、春光和二戊分为高等级组,二己和二甲分为中等级组,四庚、四乙和五甲分为低等级组。

      接受
      白脸春光二己二甲二戊四庚四乙五甲Mean ± SD等级
      发出白脸 6/64/41/11/11/14/41/11.00 ± 0.001
      春光  1/14/42/21/12/21/10.86 ± 0.382
      二戊  4/47/7 1/13/31/10.71 ± 0.493
      二甲  3/3  1/14/41/10.57 ± 0.534
      二己   1/11/21/10.39 ± 0.505
      四庚  1/0  1/1 1/10.32 ± 0.476
      四乙  1/10.14 ± 0.387
      五甲        0.00 ± 0.008
        注:“/”前数字为该个体发出攻击行为的次数,“/”后数字为该个体接受屈服行为的次数;空白为两个体间无攻击-屈服行为。
      Note: The number before "/" refers to the number of times that the individual sends out offensive behavior, and the number after "/" refers to the number of times that the individual accepts yield behavior; Blank is that there is no attack-yield behavior between two individuals.

      Table 3.  Frequencies of aggressive and submission behavior and dominance index of AMUs in a group of R. bieti

      不同等级组的扫视频率存在极显著差异 (H = 62.37, df = 2, P < 0.001),低等级组 (0.85 ± 0.14, n = 3) 高于中等级组 (0.68 ± 0.28, n = 2),中等级组高于高等级组 (0.49 ± 0.12, n = 3)。

    3.   讨论
    • 本研究首次报道滇金丝猴全雄群个体的社会监视行为,发现滇金丝猴全雄群个体的扫视行为受繁殖季节和等级影响。结果符合预期,即繁殖季节时全雄群为增加繁殖机会的同时减少或避免被繁殖单元主雄的攻击会增加扫视频率;低等级个体为减少全雄群内高等级个体的攻击,其扫视频率高于中、高等级个体。

    • 繁殖竞争压力影响个体的社会监视行为。雄性红疣猴和红长尾猴在繁殖期间,竞争压力增大,会提高监视行为发生频率[3,12]。本研究中,滇金丝猴的繁殖具有严格的季节性[22],因此,在繁殖季节,成年雄性个体有望获得成立单元的机会,是繁殖单元主雄繁殖竞争的对手[16,23],通过增加扫视,了解周边的危险,雄性增加繁殖机会[12]

      不同社会状态成年个体扫视行为发生频率不同。成年个体春光的扫视发生频率存在季节性差异,夏季高于冬季,即繁殖季高于非繁殖季。在繁殖季节,基于一雄多雌的繁殖单元决定了其雄性相比全雄单元雄性更易获得与雌性交配机会[23]。全雄单元个体为了繁殖成功,会不断靠近主雄,试探实力,评估能否接管家庭[23],或者避免与主雄的冲突,而花费大量的时间接近雌猴,伺机寻找机会与之交配[16,24]。因此,春光夏季的扫视行为发生频率较高于冬季。但是白脸作为老成年雄性,与繁殖单元主雄的交配竞争行为需求不高,在观察期间白脸独自活动,较少合群,扫视频率不存在季节性差异。

      青年雄性有繁殖需求,但实力不足[18],与主雄斗争将存在高风险,因此,青年二甲和二已在繁殖季不需要增加扫视行为以提高繁殖机会,扫视行为频率无季节性差异性。而青年二戊扫视频率却存在季节性差异,这与二戊在 2019年4月成功组建家庭有关,其较早有能力与繁殖单元主雄争夺雌性,致使其扫视频率的增加。但样本较小,社会监视行为在提升全雄单元青年雄性组建家庭成功率方面,是否发挥重要作用需要深入研究。

      此外,在繁殖季,全雄成员社交频繁,特别是成年雄性受交配竞争,攻击行为频率增加[17],青少年个体需要更多社会监视行为监视群内成员,减少全雄群内其他个体的攻击,以到达更好地适应复杂的社会环境[2][10]。因此,扫视频率存在季节性差异。

    • 低等级个体增加扫视行为避免高等级个体的攻击,而高等级个体因其优势地位无需增加扫视行为[10]。青年和青少年雄性等级低[18],它们通过扫视行为监测群内其他成员,以减少直接冲突[2]。青年雄性处在中间的地位[18],较少被攻击。因此,青年二甲和二已扫视行为频率高于高等级组,低于低等级组个体。在本研究中低等级的四乙、四庚和五甲扫视频率高于其他等级个体的扫视频率,这与赤猴和棕色卷尾猴社会监视行为受等级影响的结论一致,即低等级个体花费更多的时间来监视群体成员,并且更多关注高等级个体以避免冲突[9-10]。因此,滇金丝猴全雄群低等级个体的扫视频率高,其社会监视的目的是关注高等级个体的状态,预先感知即将发生的攻击,以减少群内的直接冲突。

      致谢:感谢白马雪山国家级自然保护区塔城管护所和白马雪山国家级自然保护区野生动物救护站的各位领导给予的支持和帮助,在此表示感谢。

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