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

doi:10.17520/biods.2022362

Abstract

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

Lin Zhao, Jianbin Cheng, Wen Zeng, Guo Li, Haibing Gong, Guiquan Zhang, Dingzhen Liu. Giant panda mothers can discriminate own neonates from others based on their squalls[J]. Biodiv Sci, 2023, 31(1): 22362.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.biodiversity-science.net/EN/10.17520/biods.2022362

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

Figures/Tables 11

References 44

[1]	Balcombe JP, McCracken GF (1992) Vocal recognition in Mexican free-tailed bats: Do pups recognize mothers? Animal Behaviour, 43, 79-87. DOI URL
[2]	Baotic A, Stoeger AS, Li DS, Tang CX, Charlton BD (2014) The vocal repertoire of infant giant pandas (Ailuropoda melanoleuca). Bioacoustics, 23, 15-28. DOI URL
[3]	Blank DA, Yang W (2017) Mother-young recognition in goitered gazelle during hiding period. Behavioural Processes, 142, 21-28. DOI PMID
[4]	Bouchet H, Plat A, Levréro F, Reby D, Patural H, Mathevon N (2020) Baby cry recognition is independent of motherhood but improved by experience and exposure. Proceedings of the Royal Society B: Biological Sciences, 287, 20192499.
[5]	Brown AK, Pioon MO, Holekamp KE, Strauss ED (2021) Infanticide by females is a leading source of juvenile mortality in a large social carnivore. The American Naturalist, 198, 642-652. DOI PMID
[6]	Charlton BD, Huang Y, Swaisgood RR (2009a) Vocal discrimination of potential mates by female giant pandas (Ailuropoda melanoleuca). Biology Letters, 5, 597-599. DOI URL
[7]	Charlton BD, Owen MA, Keating JL, Martin-Wintle MS, Zhang HM, Swaisgood RR (2018) Sound transmission in a bamboo forest and its implications for information transfer in giant panda (Ailuropoda melanoleuca) bleats. Scientific Reports, 8, 12754. DOI PMID
[8]	Charlton BD, Reby D, Ellis WAH, Brumm J, Fitch WT (2012) Estimating the active space of male koala bellows: Propagation of cues to size and identity in a Eucalyptus forest. PLoS ONE, 7, e45420.
[9]	Charlton BD, Zhang ZH, Snyder RJ (2009b) The information content of giant panda, Ailuropoda melanoleuca, bleats: Acoustic cues to sex, age, and size. Animal Behaviour, 78, 893-898. DOI URL
[10]	Charrier I, Harcourt RG (2006) Individual vocal identity in mother and pup Australian sea lions (Neophoca cinerea). Journal of Mammalogy, 87, 929-938. DOI URL
[11]	Charrier I, Marchesseau S, Dendrinos P, Tounta E, Karamanlidis AA (2017) Individual signatures in the vocal repertoire of the endangered Mediterranean monk seal: New perspectives for population monitoring. Endangered Species Research, 32, 459-470. DOI URL
[12]	Charrier I, Pitcher BJ, Harcourt RG (2009) Vocal recognition of mothers by Australian sea lion pups: Individual signature and environmental constraints. Animal Behaviour, 78, 1127-1134. DOI URL
[13]	Clink DJ, Bernard H, Crofoot MC, Marshall AJ (2017) Investigating individual vocal signatures and small-scale patterns of geographic variation in female Bornean gibbon (Hylobates muelleri) great calls. International Journal of Primatology, 38, 656-671. DOI URL
[14]	Fan PL, Liu RS, Grueter CC, Li F, Wu F, Huang TP, Yao H, Liu DZ, Liu XC (2019) Individuality in coo calls of adult male golden snub-nosed monkeys (Rhinopithecus roxellana) living in a multilevel society. Animal Cognition, 22, 71-79. DOI PMID
[15]	Gittleman JL (1994) Are the pandas successful specialists or evolutionary failures? BioScience, 44, 456-464. DOI URL
[16]	Hull V, Roloff G, Zhang JD, Liu W, Zhou SQ, Huang JY, Xu WH, Ouyang ZY, Zhang HM, Liu JG (2014) A synthesis of giant panda habitat selection. Ursus, 25, 148-162. DOI URL
[17]	Lévy F, Keller M, Poindron P (2004) Olfactory regulation of maternal behavior in mammals. Hormones and Behavior, 46, 284-302. PMID
[18]	Lü Z, Pan WS, Harkness J (1994) Mother-cub relationships in giant pandas in the Qinling Mountains, China, with comment on rescuing abandoned cubs. Zoo Biology, 13, 567-568. DOI URL
[19]	Martin M, Gridley T, Fourie D, Elwen SH, Charrier I (2022) Mutual mother-pup vocal recognition in the highly colonial Cape fur seal: Evidence of discrimination of calls with a high acoustic similarity. Animal Cognition, 25, 1461-1472. DOI PMID
[20]	Masataka N (1985) Development of vocal recognition of mothers in infant Japanese macaques. Developmental Psychobiology, 18, 107-114. PMID
[21]	Nuñez CMV, Rubenstein DI (2020) Communication is key: Mother-offspring signaling can affect behavioral responses and offspring survival in feral horses (Equus caballus). PLoS ONE, 15, e0231343.
[22]	Phan ML, Pytte CL, Vicario DS (2006) Early auditory experience generates long-lasting memories that may subserve vocal learning in songbirds. Proceedings of the National Academy of Sciences, USA, 103, 1088-1093.
[23]	Pitcher BJ, Ahonen H, Harcourt RG, Charrier I (2009) Delayed onset of vocal recognition in Australian sea lion pups (Neophoca cinerea). Naturwissenschaften, 96, 901-909. DOI URL
[24]	Pitcher BJ, Harcourt RG, Charrier I (2010a) Rapid onset of maternal vocal recognition in a colonially breeding mammal, the Australian sea lion. PLoS ONE, 5, e12195.
[25]	Pitcher BJ, Harcourt RG, Charrier I (2010b) The memory remains: Long-term vocal recognition in Australian sea lions. Animal Cognition, 13, 771-776. DOI URL
[26]	Reby D, McComb K (2003) Anatomical constraints generate honesty: Acoustic cues to age and weight in the roars of red deer stags. Animal Behaviour, 65, 519-530. DOI URL
[27]	Robisson P, Aubin T, Bremond JC (1993) Individuality in the voice of the emperor penguin Aptenodytes forsteri: Adaptation to a noisy environment. Ethology, 94, 279-290. DOI URL
[28]	Schaller GB, Hu JC, Pan WS, Zhu J (1985) The Giant Pandas of Wolong. University of Chicago Press, Chicago.
[29]	Scheffers BR, Edwards DP, Diesmos A, Williams SE, Evans TA (2014) Microhabitats reduce animal’s exposure to climate extremes. Global Change Biology, 20, 495-503. DOI PMID
[30]	Sèbe F, Aubin T, Boué A, Poindron P (2008) Mother-young vocal communication and acoustic recognition promote preferential nursing in sheep. Journal of Experimental Biology, 211, 3554-3562. DOI PMID
[31]	Sibiryakova OV, Volodin IA, Volodina EV (2018) Advertising individual identity by mother and adolescent contact calls in Siberian wapiti Cervus elaphus sibiricus. Ethology, 124, 733-742. DOI URL
[32]	Stoeger AS, Charlton BD, Kratochvil H, Fitch WT (2011) Vocal cues indicate level of arousal in infant African elephant roars. The Journal of the Acoustical Society of America, 130, 1700-1710. DOI URL
[33]	Tebbe J, Humble E, Stoffel MA, Tewes LJ, Müller C, Forcada J, Caspers B, Hoffman JI (2020) Chemical patterns of colony membership and mother-offspring similarity in Antarctic fur seals are reproducible. PeerJ, 8, e10131.
[34]	Torriani MVG, Vannoni E, McElligott AG (2006) Mother-young recognition in an ungulate hider species: A unidirectional process. The American Naturalist, 168, 412-420. PMID
[35]	Volodin IA, Sibiryakova OV, Frey R, Efremova KO, Soldatova NV, Zuther S, Kisebaev TB, Salemgareev AR, Volodina EV (2017) Individuality of distress and discomfort calls in neonates with bass voices: Wild-living goitred gazelles (Gazella subgutturosa) and saiga antelopes (Saiga tatarica). Ethology, 123, 386-396. DOI URL
[36]	Wang HT (2014) Response Properties and Dynamical Behaviours of Single Neuron. PhD dissertation, Lanzhou University, Lanzhou. (in Chinese with English abstract)
	[王恒通 (2014) 神经元响应特性及其动力学行为. 博士学位论文, 兰州大学, 兰州.]
[37]	Wang JL, Tai FD, An SC (2009) Behavioral response of lactating Mandarin voles exposed to alien pups. Acta Theriologica Sinica, 29, 59-62. (in Chinese with English abstract)
	[王建礼, 邰发道, 安书成 (2009) 哺乳期棕色田鼠对非亲缘幼仔的行为反应. 兽类学报, 29, 59-62.]
[38]	Wei W, Swaisgood RR, Dai Q, Yang ZS, Yuan SB, Owen MA, Pilfold NW, Yang XY, Gu XD, Zhou H, Han H, Zhang JD, Hong MS, Zhang ZJ (2018) Giant panda distributional and habitat-use shifts in a changing landscape. Conservation Letters, 11, e12575.
[39]	Wei W, Swaisgood RR, Owen MA, Pilfold NW, Han H, Hong MS, Zhou H, Wei FW, Nie YG, Zhang ZJ (2019) The role of den quality in giant panda conservation. Biological Conservation, 231, 189-196. DOI
[40]	Wierucka K, Charrier I, Harcourt R, Pitcher BJ (2018) Visual cues do not enhance sea lion pups’ response to multimodal maternal cues. Scientific Reports, 8, 9845. DOI PMID
[41]	Wierucka K, Pitcher BJ, Harcourt R, Charrier I (2017) The role of visual cues in mother-pup reunions in a colonially breeding mammal. Biology Letters, 13, 20170444.
[42]	Zhang GQ, Zhang HM, Chen M, He TM, Wei RP, Mainka SA (1996) Growth and development of infant giant pandas (Ailuropoda melanoleuca) at the Wolong Reserve, China. Zoo Biology, 15, 13-19. DOI URL
[43]	Zhang ZJ, Swaisgood RR, Zhang SN, Nordstrom LA, Wang HJ, Gu XD, Hu JC, Wei FW (2011) Old-growth forest is what giant pandas really need. Biology Letters, 7, 403-406. DOI PMID
[44]	Zhu XJ, Lindburg DG, Pan WS, Forney KA, Wang DJ (2001) The reproductive strategy of giant pandas (Ailuropoda melanoleuca): Infant growth and development and mother-infant relationships. Journal of Zoology, 253, 141-155. DOI URL

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