Abstract
In all colonial pinnipeds studied, mother–young vocal recognition exists and allows rapid and reliable meetings in spite of the confusing environment of the breeding colony. The efficiency of this recognition process guarantees pup survival, especially in species where females alternate foraging sea trips and lactation periods on land. The Atlantic Walrus (Odobenus rosmarus rosmarus) is a highly gregarious pinniped with females attending their calves for an extended period of time (2–3 years). Although we expect mother–calf vocal recognition to occur in this species due to the high density of individuals packed in herds, it has never been experimentally demonstrated. Here, we assessed the individual stereotypy of both mother and calf barks recorded in the wild by measuring frequency and temporal acoustic parameters. Both discriminant function and artificial neural network analyses resulted in high correct classification rates, underlying a well-defined individual stereotypy in parameters related to frequency modulation and frequency values. Playback experiments showed that mothers were more responsive to the barks of their own calf than to those of unrelated young. Finally, propagation experiments revealed that barks propagate at greater distances over water surface than over ice, acoustic features such as frequency modulation and frequency spectrum being highly resistant to degradation during propagation. Thus, acoustic analysis and propagation experiments suggest that these frequency parameters might be the key acoustic features involved in the individual identification process. This experimental study clearly demonstrates that Atlantic walrus has developed a highly reliable mother–calf vocal communication allowing such strong social bond.
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References
Aubin T, Jouventin P (2002) How to identify vocally a kin in a crowd? The penguin model. Adv Stud Behav 31:243–277
Bonner WN (1968) The fur seal of South Georgia. Br Antarct Surv Sci Rep 56:1–81
Charrier I, Harcourt RG (2006) Individual vocal identity in mother and pup Australian sea lion Neophoca cinerea. J Mammal 87:929–938
Charrier I, Mathevon N, Jouventin P, Aubin T (2001) Acoustic communication in a black-headed gull colony: how chicks identify their parents? Ethology 107:964–974
Charrier I, Mathevon N, Jouventin P (2002) How does a fur seal mother recognize the voice of her pup? An experimental study of Arctocephalus tropicalis. J Exp Biol 205:603–612
Charrier I, Mathevon N, Jouventin P (2003) Vocal signature recognition of mothers by fur seal pups. Anim Behav 65:543–550
Clark CW, Marler P, Beeman K (1987) Quantitative analysis of animal vocal phonology: an application to Swamp Sparrow song. Ethology 76:101–115
COSEWIC (2006) COSEWIC assessment and update status report on the Atlantic walrus Odobenus rosmarus rosmarus in Canada. Committee on the Status of Endangered Wildlife in Canada
Deecke VB, Janik VM (2006) Automated categorization of bioacoustic signals: avoiding perceptual pitfalls. J Acoust Soc Am 119:645–653
DFO (2000) Atlantic walrus. DFO science stock status report E5-21, pp 1–19
Fay FH (1982) Ecology and biology of the Pacific walrus Odobenus rosmarus divergens. N Am Fauna 74:1–279
Fisher KI, Stewart REA (1997) Summer foods of Atlantic walrus Odobenus rosmarus rosmarus in Foxe Basin, Northwest Territories. Can J Zool 75:1166–1175
Georges JY, Sevot X, Guinet C (1999) Fostering in a subantarctic fur seal. Mammalia 63:384–388
Halliday T (1983) Information and communication. In: Halliday TR, Slater PJB (eds) Animal behaviour communication, vol 2. Blackwell, Oxford, pp 43–81
Harcourt RG (1991) Maternal aggression in the South American fur seal in Peru. Can J Zool 70:320–325
Harcourt RG (1992) Factors affecting early mortality in the South American fur seal (Arctocephalus australis) in Peru: density-related effects and predation. J Zool Lond 226:259–270
Illmann G, Schrader L, Spinka M, Sustr P (2002) Acoustical mother recognition in pigs (Sus scrofa domestica). Behaviour 139:487–505
Insley SJ (1992) Mother-offspring separation and acoustic stereotypy: a comparison of call morphology in two species of pinnipeds. Behaviour 120:103–121
Insley SJ, Phillips AV, Charrier I (2003) A review of social recognition in pinnipeds. Aquat Mamm 29:181–201
Janik VM, Sayigh LS, Wells RS (2006) Signature whistle shape conveys identity information to bottlenose dolphins. Proc Natl Acad Sci USA 103:8293–8297
Kastelein RA, van Ligtenberg CL, Gjertz I, Verboom WC (1993) Free field hearing tests on wild Atlantic walruses (Odobenus rosmarus rosmarus) in air. Aquat Mamm 19:143–148
Kastelein RA, Postma J, Verboom WC (1995) Airborne vocalizations of Pacific walrus pups (Odobenus rosmarus divergens). In: Nachtigall PE (ed) Sensory systems of aquatic mammals. De Spil, Woerden, pp 265–285
Kastelein RA, Mosterd P, van Ligtenberg CL, Verboom WC (1996) Aerial hearing sensitivity tests with a male Pacific walrus (Odobenus rosmarus divergens), in the free field and with headphones. Aquat Mamm 22:81–93
Kelemen G (1963) Comparative anatomy and performance of the vocal organ in vertebrates. In: Busnel RG (ed) Acoustic behaviour of animals. Elsevier, Amsterdam, pp 489–521
Keppel G (1991) Design and analysis, a researcher’s handbook. Prentice-Hall, Englewood Cliffs
Khanna H, Gaunt LL, McCallum DA (1997) Digital spectrographic cross-correlation: tests of sensitivity. Bioacoustics 7:209–234
Kibal’chich AA, Lisitsina TY (1979) Some acoustical signals of calves of the Pacific walrus. Zoologicheskii zhurnal 58:1247–1249
Knornschild M, Von Helversen O (2008) Nonmutual vocal mother-pup recognition in the greater sac-winged bat. Anim Behav 76:1001–1009
Knudtson P (1998) The world of the walrus. Sierra Club Books, San Francisco
Kovacs KM, Lavigne DM (1992) Maternal investment in otariid seals and walruses. Can J Zool 70:1953–1964
Lingle S, Rendall D, Pellis SM (2007) Altruism and recognition in the antipredator defence of deer: 1. Species and individual variation in fawn distress calls. Anim Behav 73:897–905
McArthur P (1982) Mechanisms and development of parent-young vocal recognition in the pinon jay. Anim Behav 30:62–74
Miller EH (1985) Airborne acoustic communication in the walrus Odobenus rosmarus. Nat Geo Res 1:124–145
Miller EH, Boness DB (1983) Summer behaviour of Atlantic walruses Odobenus rosmarus rosmarus at Coats Island, N. W. T. (Canada). Zeitschrift fur Saugetierkunde 48:298–313
Moser BK, Stevens GR (1992) Homogeneity of variance in the two-sample means test. J Am Stat Assoc 46:19–20
Moser BK, Stevens GR, Watts CL (1989) The two sample t-test versus Satterthwaite’s approximate F test. Comm Stat Theory Methods 18:3963–3975
NAMMCO (1995) Report of the third meeting of the Scientific Committee. In: NAMMCO annual report 1995. North Atlantic Marine Mammal Commission, Tromsø, pp 71–127
Nowak RM (2003) Walker’s marine mammals of the world. The Johns Hopkins University Press, Baltimore
Page B, Goldsworthy SD, Hindell MA (2002) Individual vocal traits of mother and pup fur seals. Bioacoustics 13:121–143
Parsons S, Jones G (2000) Acoustic identification of twelve species of echolocation bat by discrimination function analysis and artificial neural network. J Exp Biol 03:2641–2656
Phillips AV, Stirling I (2000) Vocal individuality in mother and pup South American fur seals, Arctocephalus australis. Mar Mamm Sci 16:592–616
Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge
Reby D, Lek S, Dimopoulos I, Joachim J, Lauga J, Aulagnier S (1997) Artificial neural networks as a classification method in the behavioural sciences. Behav Proc 40:35–43
Reby D, Cargnelutti B, Joachim J, Aulagnier S (1999) Spectral acoustic structure of barking in roe deer (Capreolus capreolus). Sex-, age and individual-related variations. C R Acad Sci 322:271–279
Renouf D (1991) Behaviour of pinnipeds. Chapman and Hall, London
Riedman M (1990) The pinnipeds: seals, sea lions and walruses. University of California Press, Berkeley
Robisson P, Aubin T, Brémond J (1993) Individuality in the voice of emperor penguin Aptenodytes forsteri: adaptation to a noisy environment. Ethology 94:279–290
Rumelhart DEG, Hinton GE, Williams RJ (1986) Learning internal representations by back-propagation errors. Nature 323:533–536
Scherrer JA, Wilkinson GS (1993) Evening bat isolation calls provide evidence for heritable signatures. Anim Behav 46:847–860
Schusterman RJ, Reichmuth C (2008) Novel sound production via contingency learning in the Pacific walrus (Odobenus rosmarus divergens). Anim Cogn 11:319–327
Sjare B, Stirling I (1996) The breeding behavior of Atlantic walruses, Odobenus rosmarus rosmarus, in the Canadian High Arctic. Can J Zool 74:897–911
Stewart REA, Fay FH (2001) Walrus. In: Macdonald D (ed) The new encyclopedia of mammals. Oxford University Press, Oxford, pp 174–179
Stirling I (1971) Studies on the behaviour of the south Australian fur seal, Arctocephalus forsteri. 2-adult females and pups. Aust J Zool 19:267–273
Tang Halpin Z (1991) Kin recognition cues of vertebrates. In: Hepper PG (ed) Kin recognition. Cambridge University Press, Cambridge, pp 220–258
Terrazas A, Ferreira G, Lévy F, Nowak R, Serafin N, Orgeur P, Soto R, Poindron P (1999) Do ewes recognize their lambs within the first day postpartum without the help of olfactory cues? Behav Proc 47:19–29
Torriani MVG, Vannoni E, McElligott AG (2006) Mother-young recognition in an ungulate hider species: a unidirectional process. Am Nat 168:412–420
Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and descent of man. Aldine, Chicago, pp 136–179
Wartzok D, Ketten DR (1999) Marine mammals sensory systems. In: Reynolds JR III, Rommel SA (eds) Biology of marine mammals. Smithsonian Institution Press, Washington, pp 117–175
Welch BL (1938) The significance of the differences between two means when the population variances are unequal. Biometrika 29:350–362
Acknowledgments
This research has been funded by the French Polar Institute (IPEV, France—IC: program Arctic 450) and by the CNRS (French Institute for Scientific Research). NM is funded by the Institut Universitaire de France. The study was approved by the Ethical Committee of the French Polar Institute in France and by the Freshwater Institute Animal Care Committee (Animal Care Protocol: FWI-ACC-2005-2006-003; DFO Research License: S-08-09-1001-NU) in Canada. We would like to thank Tamaressee Akittirq and Brad Parker for providing us a great help in organising this fieldwork, and all the logistics in Igloolik. We also warmly thank Pakak Qamaniq, Laimikie Iqqaqsaq, Sam Iqqaqsaq our local guides for their wonderful help to find walruses. Special thanks to HTA Igloolik members and Qikiqtaaluk Wildlife Board Members for approving our research program. We also thank Vincent Rouvreau for his invaluable assistance with ANN methods; Ian Stirling, Becky Sjare and Robert Stewart for their assistance and their helpful advice in developing this project in the Canadian Arctic; Andrew Iwaniuk and Ben Pitcher for their useful comments on an earlier draft of the manuscript; and reviewers for their constructive comments. Special thanks to Antonio Fischetti for his great audio and video documentaries, and his gigantic patience during the 2008 fieldtrip.
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Charrier, I., Aubin, T. & Mathevon, N. Mother–Calf vocal communication in Atlantic walrus: a first field experimental study. Anim Cogn 13, 471–482 (2010). https://doi.org/10.1007/s10071-009-0298-9
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DOI: https://doi.org/10.1007/s10071-009-0298-9