大熊猫母兽可根据幼仔的尖叫声辨别自己的后代

doi:10.17520/biods.2022362

生物多样性 ›› 2023, Vol. 31 ›› Issue (1): 22362. DOI: 10.17520/biods.2022362

• 中国野生脊椎动物鸣声监测与生物声学研究专题 • 上一篇下一篇

大熊猫母兽可根据幼仔的尖叫声辨别自己的后代

赵琳¹, 程建斌², 曾文², 李果², 龚海兵², 张贵权²^,^*(), 刘定震¹^,^*()

1.北京师范大学生命科学学院, 生物多样性与生态工程教育部重点实验室, 北京 100875
2.中国大熊猫保护研究中心, 四川都江堰 611830

收稿日期:2022-06-29 接受日期:2023-01-16 出版日期:2023-01-20 发布日期:2023-01-18
通讯作者: *张贵权, E-mail: zguiquan@126.com;刘定震 dzliu@bnu.edu.cn
基金资助:
国家林业和草原局项目(2018-018);国家自然科学基金(31772466)

Giant panda mothers can discriminate own neonates from others based on their squalls

Lin Zhao¹, Jianbin Cheng², Wen Zeng², Guo Li², Haibing Gong², Guiquan Zhang²^,^*(), Dingzhen Liu¹^,^*()

1. Ministry of Education Key Laboratory of Biodiversity Science and Ecological Engineering, College of Life Sciences, Beijing Normal University, Beijing 100875
2. China Conservation and Research Center for the Giant Panda, Dujiangyan, Sichuan 611830

Received:2022-06-29 Accepted:2023-01-16 Online:2023-01-20 Published:2023-01-18
Contact: *Guiquan Zhang, E-mail: zguiquan@126.com;Dingzhen Liu dzliu@bnu.edu.cn

摘要/Abstract

摘要：

研究表明, 群居哺乳动物具备通过叫声进行母幼识别的机制, 而有关独栖动物的母幼识别机制鲜有研究。大熊猫(Ailuropoda melanoleuca)是典型的独栖动物, 原始森林是保持野生大熊猫种群数量可持续发展的必要条件, 其中的大型古树提供的育幼巢穴对大熊猫幼仔的存活至关重要。但是, 近年来大型古树因受人为干扰而急剧减少, 致使野生成年雌性大熊猫活动领域的重叠增大, 在育幼期产仔大熊猫母兽对育幼巢穴的利用产生了竞争。大熊猫幼仔的体重约为成年大熊猫的0.1%, 幼仔需要母兽高度关怀才能存活和成长。叫声是0‒45日龄大熊猫幼仔向其母兽传递生理需求或所处状态的主要方式。然而, 母兽能否根据幼仔的叫声识别自己的后代, 目前尚无定论。本研究以274条大熊猫幼仔的尖叫声为例, 首先对其进行个体独特性分析, 然后通过叫声回放以及母兽对所回放的两种叫声的行为反应, 验证大熊猫母兽能否辨别出其亲生幼仔。结果发现, 尖叫声的17个声学参数中有14个具有潜在的个体判别能力(PIC > 1); 进一步的判别分析结果显示, 基于这17个声学参数, 78.5%的尖叫声被正确分配到对应的幼仔; 叫声回放实验的结果显示, 母兽在行为上更倾向其亲生幼仔的尖叫声(P = 0.008)。我们的结果表明尖叫声可以编码大熊猫幼仔的身份信息, 且圈养大熊猫母兽通过该叫声能辨别亲生和非亲生后代。本研究结果为大熊猫的迁地保护和圈养大熊猫繁育工作提供了理论依据, 对人工繁育大熊猫幼仔存活率具有重要意义。

关键词: 大熊猫, 幼仔, 叫声, 个体声学签名

Abstract

Background & Aim: In many group-living mammal species, mothers can recognize calls from their own offspring, but little research has been done in solitary species. The giant panda (Ailuropoda melanoleuca) is a solitary species, yet there is high competition for breeding dens and an overlap in giant panda territory. Competition between pregnant giant panda females for denning becomes strained in the wild because the availability of old tree caves has decreased in recent years. Giant panda neonates are highly altricial, weighing little more than 0.1% of the adult weight, and rely on constant maternal care for growth and survival. To elicit maternal care, 0‒45-day old neonates use vocalizations to express distress and their physiological needs. Here, we use the giant panda as a model to investigate if mothers can discriminate calls of their own cubs from those of other cubs.

Methods: In this study, we first investigated if neonate squalls have the potential of encoding an individual-specific acoustic signature, and then examined whether mothers can discriminate squalls of their own from all other neonates by playing the audio recordings of their squalls to the mothers.

Results: Analyzing results based on 274 call samples from six cubs revealed that 14 out of 17 analyzed acoustic parameters of squalls have the potential for individual identity coding (PIC > 1), indicating a potential of an individual acoustic signature. Further discriminant analysis revealed that 78.5% of the squalls were correctly paired to the calling individual. The playback experiments demonstrated that mothers responded to squalls of their own neonates significantly more frequently than to squalls of other neonates (P = 0.008), indicating that mothers can identify their own offspring from their squalls.

Conclusions: The squall calls of newborn pandas likely encode an individual acoustic signature, and panda mothers can distinguish the acoustic structure of squalls of their own neonates from that of other cubs. The results of this study provide valuable insights for the ex-situ conservation and breeding management of giant pandas in captivity and are conducive to improving the survival rate of giant panda cubs in captivity.

Key words: Ailuropoda melanoleuca, neonates, vocalization, individual acoustic signature

赵琳, 程建斌, 曾文, 李果, 龚海兵, 张贵权, 刘定震 (2023) 大熊猫母兽可根据幼仔的尖叫声辨别自己的后代. 生物多样性, 31, 22362. DOI: 10.17520/biods.2022362.

Lin Zhao, Jianbin Cheng, Wen Zeng, Guo Li, Haibing Gong, Guiquan Zhang, Dingzhen Liu (2023) Giant panda mothers can discriminate own neonates from others based on their squalls. Biodiversity Science, 31, 22362. DOI: 10.17520/biods.2022362.

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https://www.biodiversity-science.net/CN/Y2023/V31/I1/22362

图/表 11

参考文献 44

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幼仔编号 Neonates ID	母兽呼名 Name of mother	出生日期 Date of birth	性别 Gender
Cub_a	汪佳 Wangjia	2020/7/31	雄 Male
Cub_f	小白兔 Xiaobaitu	2020/8/19	雄 Male
Cub_g	小白兔 Xiaobaitu	2020/8/19	雌 Female
Cub_j	绅宾 Shenbin	2020/8/27	雌 Female
Cub_p	华美 Huamei	2019/10/17	雌 Female
Cub_s	知春 Zhichun	2019/10/20	雄 Male

幼仔编号 Neonates ID	母兽呼名 Name of mother	出生日期 Date of birth	性别 Gender
Cub_a	汪佳 Wangjia	2020/7/31	雄 Male
Cub_f	小白兔 Xiaobaitu	2020/8/19	雄 Male
Cub_g	小白兔 Xiaobaitu	2020/8/19	雌 Female
Cub_j	绅宾 Shenbin	2020/8/27	雌 Female
Cub_p	华美 Huamei	2019/10/17	雌 Female
Cub_s	知春 Zhichun	2019/10/20	雄 Male

母兽呼名 Name of mother	谱系号 Studbook number	出生日期 Date of birth	产幼仔时间 Date of postpartum	健康状况 Health state
汪佳 Wangjia	702	2007/9/1	2020/7/30	良好 In good health
娜娜 Nana	568	2003/8/20	2020/8/9	良好 In good health
姚蔓 Yaoman	759	2009/8/27	2020/8/10	良好 In good health
小白兔 Xiaobaitu	784	2010/8/13	2020/8/19	贫血 Anemic
绅宾 Shenbin	755	2009/8/20	2020/8/27	良好 In good health
汉媛 Hanyuan	708	2008/7/21	2020/8/27	良好 In good health

母兽呼名 Name of mother	谱系号 Studbook number	出生日期 Date of birth	产幼仔时间 Date of postpartum	健康状况 Health state
汪佳 Wangjia	702	2007/9/1	2020/7/30	良好 In good health
娜娜 Nana	568	2003/8/20	2020/8/9	良好 In good health
姚蔓 Yaoman	759	2009/8/27	2020/8/10	良好 In good health
小白兔 Xiaobaitu	784	2010/8/13	2020/8/19	贫血 Anemic
绅宾 Shenbin	755	2009/8/20	2020/8/27	良好 In good health
汉媛 Hanyuan	708	2008/7/21	2020/8/27	良好 In good health

声学参数 Acoustic parameters	幼仔a Cub_a	幼仔f Cub_f	幼仔g Cub_g	幼仔j Cub_j	幼仔p Cub_p	幼仔s Cub_s
时长 Duration (D, s)	0.59 ± 0.16	0.45 ± 0.10	0.33 ± 0.10	0.40 ± 0.11	0.38 ± 0.10	0.47 ± 0.13
基频 Fundamental frequency (f₀, kHz)	1.72 ± 0.70	2.39 ± 0.70	2.30 ± 1.04	1.03 ± 0.53	2.79 ± 0.84	1.93 ± 0.62
基频的最小值 Minimum fundamental frequency (f_0min, kHz)	0.37 ± 0.10	0.73 ± 0.40	0.44 ± 0.21	0.32 ± 0.16	0.80 ± 0.73	0.56 ± 0.25
基频的最大值 Maximum fundamental frequency (f_0max,kHz)	3.64 ± 2.36	3.91 ± 1.15	4.46 ± 2.00	2.13 ± 1.35	4.11 ± 0.70	4.06 ± 1.22
基频的范围 Range of fundamental frequency (Rangef₀, kHz)	3.26 ± 2.36	3.18 ± 1.25	4.01 ± 1.98	1.81 ± 1.33	3.92 ± 1.74	3.38 ± 0.99
主频 Dominant frequency (DF, kHz)	2.95 ± 1.20	2.71 ± 0.81	3.35 ± 1.25	1.67 ± 0.81	3.20 ± 0.68	3.69 ± 0.81
主频的最大值 Maximum dominant frequency (DF_max, kHz)	6.12 ± 2.06	4.57 ± 1.80	6.28 ± 2.65	3.62 ± 1.71	5.47 ± 2.12	6.47 ± 2.33
最小频率 Minimum frequency (MINF, kHz)	1.58 ± 0.50	1.12 ± 1.14	1.66 ± 0.94	1.08 ± 0.36	2.24 ± 0.67	2.10 ± 0.74
最小频率的最小值 Minimum value of minimum frequency (MINF_min,kHz)	0.61 ± 0.38	0.19 ± 0.65	0.62 ± 0.70	0.42 ± 0.26	1.21 ± 3.00	1.06 ± 0.48
最小频率的最大值 Maximum value of minimum frequency (MINF_max, kHz)	3.28 ± 1.42	2.36 ± 1.59	3.33 ± 1.49	1.79 ± 0.52	3.80 ± 0.82	3.76 ± 1.43
最大频率 Maximum frequency (MAXF, kHz)	8.80 ± 3.69	6.19 ± 2.06	10.22 ± 4.03	4.00 ± 2.84	7.81 ± 1.25	8.27 ± 2.28
最大频率的最小值 Minimum value of maximum frequency (MAXF_min,kHz)	1.90 ± 1.04	1.46 ± 1.80	2.19 ± 1.79	0.79 ± 0.65	3.66 ± 0.80	3.16 ± 1.05
最大频率的最大值 Maximum value of maximum frequency (MAXF_max, kHz)	17.27 ± 3.54	12.51 ± 4.03	15.62 ± 4.27	7.08 ± 3.59	12.27 ± 2.00	12.78 ± 3.20
带宽 Bandwidth (BW, kHz)	16.07 ± 3.69	11.77 ± 4.01	14.36 ± 4.16	6.11 ± 3.67	10.75 ± 1.77	11.27 ± 3.30
维纳熵 Wiener entropy (E)	0.50 ± 0.10	0.47 ± 0.10	0.57 ± 0.13	0.32 ± 0.10	0.49 ± 0.04	0.49 ± 0.08
维纳熵的最小值 Minimum of Wiener entropy (E_min)	0.34 ± 0.12	0.30 ± 0.11	0.36 ± 0.14	0.18 ± 0.09	0.37 ± 0.06	0.33 ± 0.08
维纳熵的最大值 Maximum of Wiener entropy (E_max)	0.70 ± 0.10	0.60 ± 0.10	0.72 ± 0.10	0.46 ± 0.10	0.60 ± 0.05	0.63 ± 0.09

大熊猫母兽可根据幼仔的尖叫声辨别自己的后代

Giant panda mothers can discriminate own neonates from others based on their squalls

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参考文献 44

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声学参数 Acoustic Parameters	个体间变异系数 Coefficient of variation between individuals	个体内变异系数的均值Coefficient of variation intra-individuals	个体身份编码的潜力 Potential for individual identity coding
时长 Duration (D, s)	30.20	25.78	1.13
基频 Fundamental frequency (f₀, kHz)	44.14	37.86	1.11
基频的最小值 Minimum fundamental frequency (f_0min, kHz)	65.00	51.58	2.57
基频的最大值 Maximum fundamental frequency (f_0max,kHz)	41.68	41.15	0.65
基频的范围 Range of fundamental frequency (Rangef₀, kHz)	47.68	50.89	0.67
主频 Dominant frequency (DF, kHz)	35.73	32.43	0.90
主频的最大值 Maximum dominant frequency (DF_max, kHz)	42.65	39.16	1.29
最小频率 Minimum frequency (MINF, kHz)	47.93	47.52	1.56
最小频率的最小值 Minimum value of minimum frequency (MINF_min,kHz)	71.15	107.7	1.19
最小频率的最大值 Maximum value of minimum frequency (MINF_max, kHz)	45.55	40.24	1.07
最大频率 Maximum frequency (MAXF, kHz)	42.19	37.88	1.02
最大频率的最小值 Minimum value of maximum frequency (MAXF_min,kHz)	60.51	65.59	1.12
最大频率的最大值 Maximum value of maximum frequency (MAXF_max, kHz)	34.70	28.43	1.73
带宽 Bandwidth (BW, kHz)	38.59	31.8	1.71
维纳熵 Wiener entropy (E)	24.58	19.52	1.11
维纳熵的最小值 Minimum of Wiener entropy (E_min)	36.08	33.67	1.04
维纳熵的最大值 Maximum of Wiener entropy (E_max)	18.8	14.83	1.25

声学参数 Acoustic Parameters	函数1 Function 1	函数2 Function 2
时长 Duration (D, s)	0.292	?0.193
基频 Fundamental frequency (f₀, kHz)	0.060	0.187
基频的最小值 Minimum fundamental frequency (f_0min, kHz)	0.339	0.308
基频的最大值 Maximum fundamental frequency (f_0max,kHz)	0.405	0.229
基频的范围 Range of fundamental frequency (Rangef₀, kHz)	0.751	0.057
主频 Dominant frequency (DF, kHz)	0.080	?0.110
主频的最大值 Maximum dominant frequency (DF_max, kHz)	0.071	0.157
带宽 Bandwidth (BW, kHz)	0.380	?0.838
最小频率 Minimum frequency (MINF, kHz)	?0.249	0.306
最小频率的最小值 Minimum value of minimum frequency (MINF_min,kHz)	0.579	0.290
最小频率的最大值 Maximum value of minimum frequency (MINF_max, kHz)	?1.182	0.426
最大频率 Maximum frequency (MAXF, kHz)	0.406	?0.473
最大频率的最小值 Minimum value of maximum frequency (MAXF_min,kHz)	?0.060	?1.102
最大频率的最大值 Maximum value of maximum frequency (MAXF_max, kHz)	?0.602	0.315
维纳熵 Wiener entropy (E)	0.273	?0.093
维纳熵的最小值 Minimum of Winer entropy (E_min)	?0.339	1.533
维纳熵的最大值 Maximum of Wiener entropy (E_max)	?0.043	0.327

对象 Subject	用于分析的叫声样本量 Sample size of vocalizations used for acoustic analysis	正确分类的百分率 Corrective assignment rate (%)
Cub_a	13	46.20
Cub_f	17	82.40
Cub_g	43	65.10
Cub_j	42	90.50
Cub_p	26	57.70
Cub_s	133	91.70

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