Characterising the harmonic vocal repertoire of the Indian wolf (Canis lupus pallipes)


Autoři: Sougata Sadhukhan aff001;  Lauren Hennelly aff002;  Bilal Habib aff001
Působiště autorů: Department of Animal Ecology and Conservation Biology, Wildlife Institute of India, Dehradun, India; aff001;  Mammalian Ecology and Conservation Unit, Veterinary Genetics Laboratory, University of California Davis, Davis, California, United States of America aff002
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0216186

Souhrn

Vocal communication in social animals plays a crucial role in mate choice, maintaining social structure, and foraging strategy. The Indian grey wolf, among the least studied subspecies, is a social carnivore that lives in groups called packs and has many types of vocal communication. In this study, we characterise harmonic vocalisation types of the Indian wolf using howl survey responses and opportunistic recordings from captive and nine packs (each pack contains 2–9 individuals) of free-ranging Indian wolves. Using principal component analysis, hierarchical clustering, and discriminant function analysis, we found four distinct vocalisations using 270 recorded vocalisations (Average Silhouette width Si = 0.598) which include howls and howl-barks (N = 238), whimper (N = 2), social squeak (N = 28), and whine (N = 2). Although having a smaller body size compared to other wolf subspecies, Indian wolf howls have an average mean fundamental frequency of 422 Hz (±126), which is similar to other wolf subspecies. The whimper showed the highest frequency modulation (37.296±4.601) and the highest mean fundamental frequency (1708±524 Hz) compared to other call types. Less information is available on the third vocalisation type, i.e. ‘Social squeak’ or ‘talking’ (Mean fundamental frequency = 461±83 Hz), which is highly variable (coefficient of frequency variation = 18.778±3.587). Lastly, we identified the whine, which had a mean fundamental frequency of 906Hz (±242) and is similar to the Italian wolf (979±109 Hz). Our study’s characterisation of the Indian wolf’s harmonic vocal repertoire provides a first step in understanding the function and contextual use of vocalisations in this social mammal.

Klíčová slova:

Acoustics – Geological surveys – Hierarchical clustering – Physiological parameters – Principal component analysis – Social communication – Vocalization – Wolves


Zdroje

1. Theberge JB, Falls JB. Howling as a means of communication in timber wolves. Am Zool. 1967;7: 331–338. doi: 10.1093/icb/7.2.331

2. Kingston T, Lara MC, Jones G, Akbar Z, Kunz TH, Schneider CJ. Acoustic divergence in two cryptic Hipposideros species: a role for social selection? Proc R Soc Biol Sci. The Royal Society; 2001;268: 1381–6. doi: 10.1098/rspb.2001.1630 11429138

3. Harrington FH, Mech DL. An analysis of howling response parameters useful for wolf pack censusing. J Wildl Manage. 1982;46: 686–693. doi: 10.2307/3808560

4. Scott JP. The Evolution of Social Behavior in Dogs and Wolves. Am Zool. 1967;7: 373–381.

5. Garber P a., Estrada A, Bicca-Marques JC, Heymann EW, Strier KB. South American Primates: Comparative Perspectives in the Study of Behavior, Ecology, and Conservation. 2009. doi: 10.1007/978-0-387-78705-3

6. Nawroth C, Brett JM, McElligott AG. Goats display audience-dependent human-directed gazing behaviour in a problem-solving task. Biol Lett. 2016;12: 2016–2019. doi: 10.1098/rsbl.2016.0283 27381884

7. Gazzola A, Avanzinelli E, Mauri L, Scandura M, Apollonio M. Temporal changes of howling in south European wolf packs. Ital J Zool. Taylor & Francis; 2002;69: 157–161. doi: 10.1080/11250000209356454

8. Kershenbaum A, Root-Gutteridge H, Habib B, Koler-Matznick J, Mitchell B, Palacios V, et al. Disentangling canid howls across multiple species and subspecies: Structure in a complex communication channel. Behav Processes. Elsevier B.V.; 2016;124: 149–157. doi: 10.1016/j.beproc.2016.01.006 26809021

9. Tembrock G. Acoustic behaviour of mammals. In Acoustic Behavior of Animals (René Guy Busnel). Elsevier; 1963. pp. 751–786. Available: https://www.researchgate.net/publication/260796117

10. Wilkins MR, Seddon N, Safran RJ. Evolutionary divergence in acoustic signals: causes and consequences. Trends Ecol Evol. Elsevier Current Trends; 2013;28: 156–166. doi: 10.1016/j.tree.2012.10.002 23141110

11. Mech DL, Boitani L, (IUCN SSC Wolf Specialist Group). The IUCN Red List of Threatened Species 2010. 2010. http://dx.doi.org/10.2305/IUCN.UK.2010-4.RLTS.T3746A10049204.en Copyright:

12. Sharma DK, Maldonado JE, Jhala Y V, Fleischer RC. Ancient wolf lineages in India. Proc R Soc London B Biol Sci. The Royal Society; 2004;271: S1—S4. doi: 10.1098/rsbl.2003.0071 15101402

13. Werhahn G, Senn H, Kaden J, Joshi J, Bhattarai S, Kusi N, et al. Phylogenetic evidence for the ancient Himalayan wolf: towards a clarification of its taxonomic status based on genetic sampling from western Nepal. R Soc Open Sci. The Royal Society Publishing; 2017;4: 170186. doi: 10.1098/rsos.170186 28680672

14. Ersmark E, Klütsch CFC, Chan YL, Sinding M-HS, Fain SR, Illarionova NA, et al. From the Past to the Present: Wolf Phylogeography and Demographic History Based on the Mitochondrial Control Region. Front Ecol Evol. Frontiers; 2016;4: 134. doi: 10.3389/fevo.2016.00134

15. Aggarwal RK, Kivisild T, Ramadevi J, Singh L. Mitochondrial DNA coding region sequences support the phylogenetic distinction of two Indian wolf species. J Zool Syst Evol Res. 2007;45: 163–172. doi: 10.1111/j.1439-0469.2006.00400.x

16. Shrotriya S, Lyngdoh S, Habib B. Wolves in Trans-Himalayas: 165 years of taxonomic confusion. Curr Sci. JSTOR; 2012;103: 885–887.

17. Harrington FH, Mech DL. Wolf Howling and Its Role in Territory Maintenance. Behaviour. 1978;68: 207–249. Available: http://www.jstor.org/stable/4533952

18. Harrington FH. Aggressive howling in wolves. Anim Behav. Academic Press; 1987;35: 7–12. doi: 10.1016/S0003-3472(87)80204-X

19. Schassburger RM. Vocal communication in the timber wolf, Canis lupus, Linnaeus: structure, motivation, and ontogeny; with 6 tables. Parey Scientific Publ.; 1993.

20. Tooze ZJ, Harrington FH, Fentress JC. Individually distinct vocalizations in timber wolves, Canis lupus. Anim Behav. 1990;40: 723–730. doi: 10.1016/S0003-3472(05)80701-8

21. Palacios V, Font E, Márquez R. Iberian wolf howls: acoustic structure, individual variation, and a comparison with north american populations. J Mammal. 2007;88: 606–613. doi: 10.1644/06-MAMM-A-151R1.1

22. Root-Gutteridge H, Bencsik M, Chebli M, Gentle LK, Terrell-Nield C, Bourit A, et al. Improving individual identification in captive Eastern grey wolves (Canis lupus lycaon) using the time course of howl amplitudes. Bioacoustics-the Int J Anim Sound Its Rec. 2014;23: 39–53. doi: 10.1080/09524622.2013.817318

23. Root-Gutteridge H, Bencsik M, Chebli M, Gentle LK, Terrell-Nield C, Bourit A, et al. Identifying individual wild Eastern grey wolves (Canis lupus lycaon) using fundamental frequency and amplitude of howls. Bioacoustics Int J Anim Sound Its Rec. 2014;23: 55–66. doi: 10.1080/09524622.2013.817317

24. Watson SK, Townsend SW, Range F. Wolf howls encode both sender- and context-speci fi c information. Anim Behav. Elsevier Ltd; 2018;145: 59–66. doi: 10.1016/j.anbehav.2018.09.005

25. Zaccaroni M, Passilongo D, Buccianti A, Dessi-Fulgheri F, Facchini C, Gazzola A, et al. Group specific vocal signature in free-ranging wolf packs. Ethol Ecol Evol. Taylor & Francis; 2012;24: 322–331.

26. Hennelly LH, Habib B, Root-Gutteridge H, Palacios V, Passilongo D. Howl variation across Himalayan, North African, Indian, and Holarctic wolf clades: tracing divergence in the world ‘ s oldest wolf lineages using acoustics. Curr Zool. 2017; 1–8. doi: 10.1093/cz/zox001 29491993

27. Coscia EM, Phillips DP, Fentress JC. Spectral analysis of neonatal wolf canis lupus vocalizations. Bioacoustics. 1991;3: 275–293. doi: 10.1080/09524622.1991.9753190

28. McCarley H. Vocalizations of Red Wolves (Canis rufus). J Mammal. Oxford University Press; 1978;59: 27–35. doi: 10.1644/859.1.Key

29. Cohen JA, Fox MW. Vocalizations in wild canids and possible effects of domestication. Behav Processes. 1976;1: 77–92. doi: 10.1016/0376-6357(76)90008-5 24923546

30. Faragó T, Townsend S, Range F. The Information Content of Wolf (and Dog) Social Communication. In: Witzany G, editor. Biocommunication of Animals. Dordrecht: Springer Netherlands; 2014. pp. 41–62. doi: 10.1007/978-94-007-7414-8_4

31. Mech DL. The wolf: the ecology and behavior of endangered species. New York: University of Minnesota Press; 1981.

32. Mech DL, Boitani L. Wolves: behavior, ecology, and conservation. Chicago: University of Chicago Press; 2010.

33. Feddersen-Petersen DU. Vocalization of European wolves (Canis lupus lupus L.) and various dog breeds (Canis lupus f. fam.). Arch für Tierzucht. 2000;43: 387–397. doi: 10.5194/aab-43-387-2000

34. Mech DL, Boitani L. Wolves: behavior, ecology and conservation. University of Chicago Press, Chicago; 2003.

35. Joslin P. Summer activities of two timber wolf (Canis lupus) packs in Algonquin Park. University of Toronto. 1966.

36. Fentress JC. Observations on the Behavioral Development of a Hand-Reared Male Timber Wolf. 1967;351: 339–351.

37. Nikolʹskij AA, Frommolʹt K-C. Zvukovaja aktivnostʹ volka: Lautaktivität des Wolfes. Izdatelʹstvo Moskovskogo universiteta; 1989.

38. Mech LD. wolves of Isle Royale. 1966;

39. Passilongo D, Marchetto M, Apollonio M. Singing in a wolf chorus: Structure and complexity of a multicomponent acoustic behaviour. Hystrix, Ital J Mammal Online. 2017;28: 180–185. doi: 10.4404/hystrix-28.2–12019

40. Habib B. Ecology of Indian wolf [canis lupus pallipes sykes. 1831), and modeling its potential habitat in the great Indian bustard sanctuary, Maharashtra, India. Aligarh Muslim University, Aligarh (India). 2007.

41. Singh M, Kumara HN. Distribution, status and conservation of Indian gray wolf (Canis lupus pallipes) in Karnataka, India. J Zool. 2006;270: 164–169. doi: 10.1111/j.1469-7998.2006.00103.x

42. Jethva BD, Jhala Y V. Foraging ecology, economics and conservation of Indian wolves in the Bhal region of Gujarat, Western India. Biol Conserv. 2004;116: 351–357. doi: 10.1016/S0006-3207(03)00218-0

43. Habib B, Kumar S. Den shifting by wolves in semi-wild landscapes in the Deccan Plateau, Maharashtra, India. J Zool. 2007;272: 259–265. doi: 10.1111/j.1469-7998.2006.00265.x

44. Kumar S, Rahmani AR. Predation by wolves (Canis lupus pallipes) on blackbuck (Antilope cervicapra) in the Great Indian Bustard Sanctuary, Nannaj, Maharashtra, India. Int J Ecol Environ Sci. 2008;34: 99–112.

45. Rodgers WA, Panwar SH. Biogeographical classification of India. New For Dehra Dun, India. 1988;

46. Reddy CS, Jha CS, Diwakar PG, Dadhwal VK. Nationwide classification of forest types of India using remote sensing and GIS. Environ Monit Assess. Springer International Publishing; 2015;187: 777. doi: 10.1007/s10661-015-4990-8 26615560

47. Bioacoustics Research Program. Raven Pro: interactive sound analysis software [Internet]. The Cornell Lab of Ornithology. Ithaca, NY: The Cornell Lab of Ornithology.; 2014. Available: http://www.birds.cornell.edu/raven

48. Rader CM. Discrete Fourier transforms when the number of data samples is prime. Proc IEEE. 1968;56: 1107–1108. doi: 10.1109/PROC.1968.6477

49. Rohatgi A. WebPlotDigitizer. Austin, Texas, USA; 2017.

50. Smith LI. A tutorial on Principal Components Analysis Introduction. Statistics (Ber). 2002;51: 52. doi: 10.1080/03610928808829796

51. Kaiser HF. Computer Program for Varimax Rotation in Factor Analysis. Educ Psychol Meas. 1959;19: 413–420. doi: 10.1177/001316445901900314

52. Maechler M, Rousseeuw P, Struyf A, Hubert M, Hornik K. cluster: Cluster Analysis Basics and Extensions. 2019.

53. Kaufman L, Rousseeuw PJ. Agglomerative Nesting (Program AGNES). Finding Groups in Data. Wiley; 2009. pp. 199–252.

54. Rousseeuw PJ. Silhouettes: A graphical aid to the interpretation and validation of cluster analysis. J Comput Appl Math. 1987;20: 53–65. doi: 10.1016/0377-0427(87)90125-7

55. Galili T. dendextend: an R package for visualizing, adjusting, and comparing trees of hierarchical clustering. Bioinformatics. 2015; doi: 10.1093/bioinformatics/btv428 26209431

56. Kaiser HF. Coefficient Alpha for a Principal Component and the Kaiser-Guttman Rule. Psychol Rep. SAGE PublicationsSage CA: Los Angeles, CA; 1991;68: 855–858. doi: 10.2466/pr0.1991.68.3.855

57. Crisler L. Arctic Wild. London: Secker & Warburg; 1959.

58. Weir JN. The contexts and sound of the squeaking vocalization of wolves (Canis lupus) [Internet]. Memorial University of Newfoundland. 1999. Available: https://research.library.mun.ca/9649/

59. Goldman JA, Phillips DP, Fentress JC. An acoustic basis for maternal (Canis lupus)? recognition in timber wolves. 1995;97: 1970–1973. doi: 10.1121/1.412070 7699177

60. Buxton R, Lendrum P, Crooks KR, Wittemyer G. Pairing camera traps and acoustic recorders to monitor the ecological impact of human disturbance. Glob Ecol Conserv. Elsevier; 2018; e00493.

61. Stevenson BC, Borchers DL, Altwegg R, Swift RJ, Gillespie DM, Measey GJ. A general framework for animal density estimation from acoustic detections across a fixed microphone array. Methods Ecol Evol. Wiley Online Library; 2015;6: 38–48.

62. Fuller TK, Sampson BA. Evaluation of a simulated howling survey for wolves. J Wildl Manage. JSTOR; 1988; 60–63.

63. Papin M, Aznar M, Germain E, Guérold F, Pichenot J. Using acoustic indices to estimate wolf pack size. Ecol Indic. Elsevier; 2019;103: 202–211. doi: 10.1016/j.ecolind.2019.03.010

64. Palacios V, López-bao JV, Llaneza L, Fernández C. Decoding Group Vocalizations: The Acoustic Energy Distribution of Chorus Howls Is Useful to Determine Wolf Reproduction. 2016; 1–12. doi: 10.1371/journal.pone.0153858 27144887

65. Passilongo D, Mattioli L, Bassi E, Szabó L, Apollonio M. Visualizing sound: counting wolves by using a spectral view of the chorus howling. Front Zool. Frontiers in Zoology; 2015;12: 12–22. doi: 10.1186/s12983-015-0101-5

66. Harrington FH, Mech DL. Wolf Vocalization. Wolf and Man. Elsevier; 1978. pp. 109–132. doi: 10.1016/B978-0-12-319250-9.50014–1

67. Macdonald D., & Sillero-Zubiri C. The Biology and Conservation of Wild Canids [Internet]. Oxford: Oxford University Press; 2004. doi: 10.1093/acprof:oso/9780198515562.001.0001

68. Manser MB, Jansen DA, Graw B, Hollén LI, Bousquet CAH, Furrer RD, et al. Vocal complexity in meerkats and other mongoose species. Advances in the Study of Behavior. Elsevier; 2014. pp. 281–310.

69. Holekamp KE, Boydston EE, Szykman M, Graham I, Nutt KJ, Birch S, et al. Vocal recognition in the spotted hyaena and its possible implications regarding the evolution of intelligence. Anim Behav. Elsevier; 1999;58: 383–395.

70. Pollard KA, Blumstein DT. Evolving communicative complexity: insights from rodents and beyond. Philos Trans R Soc B Biol Sci. The Royal Society; 2012;367: 1869–1878.


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2019 Číslo 10