Advertisement

Animal Cognition

, Volume 22, Issue 6, pp 1115–1128 | Cite as

Acoustic structure of forest elephant rumbles: a test of the ambiguity reduction hypothesis

  • Daniela HedwigEmail author
  • Anahita K. Verahrami
  • Peter H. Wrege
Original Paper

Abstract

Quantitative assessments of the structure of vocalizations are a fundamental prerequisite to understand a species’ vocal communication system and, more broadly, the selective pressures shaping vocal repertoires. For example, to reduce ambiguity in signal interpretation in the absence of auxiliary visual cues, species in densely vegetated habitats should exhibit more discrete vocal signals than species in open habitats. To test this “ambiguity reduction hypothesis”, we conducted the first quantitative assessment of the rumble vocalizations of the forest elephant. Based on 686 forest elephant rumbles recorded with autonomous acoustic recording units at four sites across Central Africa, we used model-based cluster analyses paired with subsequent evaluation of cluster-discreteness and discriminant function analyses to quantify the structure of rumbles based on 23 source- and filter-related acoustic parameters. Model-based cluster analyses suggest that rumbles can be classified into five to eight types. Similar to previous findings in savannah elephants and contrary to the ambiguity reduction hypothesis, average silhouette coefficients below 0.34 indicated that these rumble types were highly intergraded. However, discriminant function analyses predicted rumble types with at least 75% accuracy whereby the location of the minimum fundamental frequency, middle slope and peak frequency contributed most to separation between types. In line with an increasing number of studies highlighting that a distinction between discrete and graded repertoires may have little biological significance, we propose that ambiguity reduction may take place through the evolution of perceptual and cognitive mechanisms, rather than acting on vocal production.

Keywords

Discreteness Vocal repertoires Habitat differences Acoustic adaptation Categorical perception Loxodonta cyclotis 

Notes

Acknowledgements

This study was supported by a grant to PHW from the US Fish and Wildlife Service, the Robert G. and Jane V. Engle Foundation, and through a generous gift from Lisa Yang to the Cornell Lab of Ornithology. Research clearance was approved by the Gabon government’s National Center for Scientific Research and Technology, by the Republic of Congo’s Ministry of Forestry, and by the Central African Republic’s Ministry of Education and Water and Forests. Special thanks go to Elizabeth D. Rowland, Andrea Turkalo, Frelcia Bambi, Phael Malonga, Terry Brncic and Herve Londo for superb assistance with data collection and Precious Woods Gabon for critical logistics support.

Supplementary material

10071_2019_1304_MOESM1_ESM.docx (723 kb)
Supplementary material 1 (DOCX 723 kb)
10071_2019_1304_MOESM2_ESM.docx (491 kb)
Supplementary material 2 (DOCX 491 kb)
10071_2019_1304_MOESM3_ESM.docx (843 kb)
Supplementary material 3 (DOCX 843 kb)
10071_2019_1304_MOESM4_ESM.docx (18 kb)
Supplementary material 4 (DOCX 18 kb)

References

  1. August PV, Anderson JG (1987) Mammal sounds and motivation-structural rules: a test of the hypothesis. J Mammal 68:1–9CrossRefGoogle Scholar
  2. Bagley KR, Goodwin TE, Rasmussen LEL, Schulte BA (2006) Male African elephants, Loxodonta africana, can distinguish oestrous status via urinary signals. Anim Behav 71:1439–1445.  https://doi.org/10.1016/j.anbehav.2006.01.003 CrossRefGoogle Scholar
  3. Baotic A, Stoeger AS (2017) Sexual dimorphism in African elephant social rumbles. PLoS One 12:e0177411CrossRefPubMedPubMedCentralGoogle Scholar
  4. Barreda S (2015) phonTools: functions for phonetics in R. R Package Version 02-21Google Scholar
  5. Bates LA, Sayialel KN, Njiraini NW et al (2007) Elephants classify human ethnic groups by odor and garment color. Curr Biol 17:1938–1942.  https://doi.org/10.1016/j.cub.2007.09.060 CrossRefGoogle Scholar
  6. Bates LA, Sayialel KN, Njiraini NW et al (2008) African elephants have expectations about the locations of out-of-sight family members. Biol Lett 4:34–36.  https://doi.org/10.1098/rsbl.2007.0529 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Baugh AT, Akre KL, Ryan MJ (2008) Categorical perception of a natural, multivariate signal: mating call recognition in túngara frogs. Proc Natl Acad Sci 105:8985–8988CrossRefPubMedPubMedCentralGoogle Scholar
  8. Blumstein DT, Armitage KB (1997) Does sociality drive the evolution of communicative complexity? A comparative test with ground-dwelling sciurid alarm calls. Am Nat 150:179–200.  https://doi.org/10.1086/286062 CrossRefPubMedGoogle Scholar
  9. Boncoraglio G, Saino N (2006) Habitat structure and the evolution of bird song: a meta-analysis of the evidence for the acoustic adaptation hypothesis. Funct Ecol 21:134–142.  https://doi.org/10.1111/j.1365-2435.2006.01207.x CrossRefGoogle Scholar
  10. Bouchet H, Blois-Heulin C, Pellier A-S et al (2012) Acoustic variability and individual distinctiveness in the vocal repertoire of red-capped mangabeys (Cercocebus torquatus). J Comp Psychol 126:45CrossRefGoogle Scholar
  11. Bouchet H, Blois-Heulin C, Lemasson A (2013) Social complexity parallels vocal complexity: a comparison of three non-human primate species. Frontiers in Psychology 4:390.  https://doi.org/10.3389/fpsyg.2013.00390
  12. Caves EM, Brandley NC, Johnsen S (2018) Visual acuity and the evolution of signals. Trends Ecol Evol 33:358–372.  https://doi.org/10.1016/j.tree.2018.03.001 CrossRefPubMedGoogle Scholar
  13. Cheney DL, Seyfarth RM (1982) How vervet monkeys perceive their grunts: field playback experiments. Anim Behav 30:739–751.  https://doi.org/10.1016/S0003-3472(82)80146-2 CrossRefGoogle Scholar
  14. Dobson AJ, Barnett A (2008) An introduction to generalized linear models. CRC Press, Boca RatonGoogle Scholar
  15. Elowson AM, Snowdon CT (1994) Pygmy marmosets, Cebuella pygmaea, modify vocal structure in response to changed social environment. Anim Behav 47:1267–1277.  https://doi.org/10.1006/anbe.1994.1175 CrossRefGoogle Scholar
  16. Ey E, Fischer J (2009) The “acoustic adaptation hypothesis”—a review of the evidence from birds, anurans and mammals. Bioacoustics 19:21–48.  https://doi.org/10.1080/09524622.2009.9753613 CrossRefGoogle Scholar
  17. Ey E, Rahn C, Hammerschmidt K, Fischer J (2009) Wild female olive baboons adapt their grunt vocalizations to environmental conditions. Ethology 115:493–503.  https://doi.org/10.1111/j.1439-0310.2009.01638.x CrossRefGoogle Scholar
  18. Fant G (1981) The source filter concept in voice production. STL QPSR 1:21–37Google Scholar
  19. Field A (2009) Discovering statistics using SPSS. Sage publicationsGoogle Scholar
  20. Fischer J (1998) Barbary macaques categorize shrill barks into two call types. Anim Behav 55:799–807CrossRefGoogle Scholar
  21. Fischer J, Hammerschmidt K, Cheney DL, Seyfarth RM (2001) Acoustic features of female chacma baboon barks. Ethology 107:33–54.  https://doi.org/10.1111/j.1439-0310.2001.00630.x CrossRefGoogle Scholar
  22. Fishlock V, Lee PC (2013) Forest elephants: fission–fusion and social arenas. Anim Behav 85:357–363CrossRefGoogle Scholar
  23. Fitch W (2006) Production of vocalizations in mammals. Vis Commun 3:145Google Scholar
  24. Fraley C, Raftery AE (2006) MCLUST version 3: an R package for normal mixture modeling and model-based clusteringGoogle Scholar
  25. Freeberg TM (2016) Social complexity can drive vocal complexity. Psychol Sci 17(7):557–561Google Scholar
  26. Hedwig D, Hammerschmidt K, Mundry R et al (2014) Acoustic structure and variation in mountain and western gorilla close calls: a syntactic approach. Behaviour 151:1091–1120CrossRefGoogle Scholar
  27. Hedwig D, Mundry R, Robbins MM, Boesch C (2015) Audience effects, but not environmental influences, explain variation in gorilla close distance vocalizations—a test of the acoustic adaptation hypothesis. Am J Primatol 77:1239–1252CrossRefGoogle Scholar
  28. Hedwig D, DeBellis M, Wrege PH (2018) Not so far: attenuation of low-frequency vocalizations in a rainforest environment suggests limited acoustic mediation of social interaction in African forest elephants. Behav Ecol Sociobiol 72:33.  https://doi.org/10.1007/s00265-018-2451-4 CrossRefGoogle Scholar
  29. Horn JL (1965) A rationale and test for the number of factors in factor analysis. Psychometrika 30:179–185CrossRefGoogle Scholar
  30. Keen SC, Shiu Y, Wrege PH, Rowland ED (2017) Automated detection of low-frequency rumbles of forest elephants: a critical tool for their conservation. J Acoust Soc Am 141:2715–2726.  https://doi.org/10.1121/1.4979476 CrossRefPubMedGoogle Scholar
  31. Keenan S, Lemasson A, Zuberbühler K (2013) Graded or discrete? A quantitative analysis of Campbell’s monkey alarm calls. Anim Behav 85:109–118.  https://doi.org/10.1016/j.anbehav.2012.10.014 CrossRefGoogle Scholar
  32. King LE, Soltis J, Douglas-Hamilton I et al (2010) Bee threat elicits alarm call in African elephants. PLoS One 5:e10346.  https://doi.org/10.1371/journal.pone.0010346 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Lachenbruch PA, Mickey MR (1968) Estimation of error rates in discriminant analysis. Technometrics 10:1–11CrossRefGoogle Scholar
  34. Langbauer WR (2000) Elephant communication. Zoo Biol 19:425–445.  https://doi.org/10.1002/1098-2361(2000) CrossRefGoogle Scholar
  35. Langbauer WR, Payne KB, Charif RA et al (1991) African elephants respond to distant playbacks of low-frequency conspecific calls. J Exp Biol 157:35–46Google Scholar
  36. Le Prell CG, Hauser MD, Moody DB (2002) Discrete or graded variation within rhesus monkey screams? Psychophysical experiments on classification. Anim Behav 63:47–62.  https://doi.org/10.1006/anbe.2001.1888 CrossRefGoogle Scholar
  37. Lemasson A, Hausberger M (2011) Acoustic variability and social significance of calls in female Campbell’s monkeys (Cercopithecus campbelli campbelli). J Acoust Soc Am 129:3341–3352CrossRefGoogle Scholar
  38. Leong K, Ortolani A, Graham L, Savage A (2003a) The use of low-frequency vocalizations in African elephant (Loxodonta africana) reproductive strategies. Horm Behav 43:433–443.  https://doi.org/10.1016/S0018-506X(03)00025-4 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Leong KM, Ortolani A, Burks KD et al (2003b) Quantifying acoustic and temporal characteristics of vocalizations for a group of captive African elephants Loxodonta africana. Bioacoustics 13:213–231CrossRefGoogle Scholar
  40. Lieberman P, Blumstein SE (1988) Speech physiology, speech perception, and acoustic phonetics. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  41. Markel J, Gray A (1976) Linear prediction of speech. Springer, New YorkCrossRefGoogle Scholar
  42. Marler P (1967) Animal communication signals: we are beginning to understand how the structure of animal signals relates to the function they serve. Science 157:769–774.  https://doi.org/10.1126/science.157.3790.769 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Marler P (1976) Social organization, communication and graded signals: the chimpanzee and the gorilla. Growing points in ethology. Cambridge University Press, OxfordGoogle Scholar
  44. Marler P (1977) The structure of animal communication sounds. Recognition of complex acoustic signals. Dahlem Konferenzen, Berlin, pp 17–35Google Scholar
  45. Marler P, Kavanaugh JF, Cutting JE (1975) On the origin of speech from animal sounds. Role Speech Lang 1975:11–37Google Scholar
  46. McComb K, Moss C, Sayialel S, Baker L (2000) Unusually extensive networks of vocal recognition in African elephants. Anim Behav 59:1103–1109.  https://doi.org/10.1006/anbe.2000.1406
  47. McComb K, Reby D, Baker L et al (2003) Long-distance communication of acoustic cues to social identity in African elephants. Anim Behav 65:317–329.  https://doi.org/10.1006/anbe.2003.2047 CrossRefGoogle Scholar
  48. McComb K, Semple S (2005) Coevolution of vocal communication and sociality in primates. Biol Lett 1(4):381–385Google Scholar
  49. McCowan B, Reiss D (1995) Whistle contour development in captive-born infant bottlenose dolphins (Tursiops truncatus): role of learning. J Comp Psychol 109:242CrossRefGoogle Scholar
  50. Mitani JC, Brandt KL (1994) Social factors influence the acoustic variability in the long-distance calls of male chimpanzees. Ethology 96:233–252CrossRefGoogle Scholar
  51. Mitani JC, Hunley KL, Murdoch ME (1999) Geographic variation in the calls of wild chimpanzees: a reassessment. Am J Primatol 47(2):133–151CrossRefPubMedPubMedCentralGoogle Scholar
  52. Morris-Drake A, Mumby HS (2018) Social associations and vocal communication in wild and captive male savannah elephants Loxodonta africana. Mammal Rev 48:24–36.  https://doi.org/10.1111/mam.12106 CrossRefGoogle Scholar
  53. Morton ES (1975) Ecological sources of selection on avian sounds. Am Nat 109:17–34CrossRefGoogle Scholar
  54. Morton ES (1977) On the occurrence and significance of motivation-structural rules in some bird and mammal sounds. Am Nat 111:855–869CrossRefGoogle Scholar
  55. Morton ES (1982) Grading, discreteness, redundancy, and motivation-structural rules. Acoust Commun Birds 1:183–212CrossRefGoogle Scholar
  56. Moss CJ, Croze H, Lee PC (2012) The amboseli elephants: a long-term perspective on a long-lived mammal. University of Chicago Press, ChicagoGoogle Scholar
  57. Nelson DA, Marler P (1989) Categorical perception of a natural stimulus continuum: birdsong. Science 244:976–978CrossRefGoogle Scholar
  58. Payne KB, Thompson M, Kramer L (2003) Elephant calling patterns as indicators of group size and composition: the basis for an acoustic monitoring system. Afr J Ecol 41:99–107.  https://doi.org/10.1046/j.1365-2028.2003.00421.x CrossRefGoogle Scholar
  59. Pettigrew JD, Manger PR (2008) Retinal ganglion cell density of the black rhinoceros (Diceros bicornis): calculating visual resolution. Vis Neurosci 25:215–220.  https://doi.org/10.1017/S0952523808080498 CrossRefPubMedGoogle Scholar
  60. Pettigrew JD, Bhagwandin A, Haagensen M, Manger PR (2010) Visual acuity and heterogeneities of retinal ganglion cell densities and the tapetum lucidum of the African Elephant (Loxodonta africana). Brain Behav Evol 75:251–261.  https://doi.org/10.1159/000314898 CrossRefPubMedGoogle Scholar
  61. Plotnik JM, Shaw RC, Brubaker DL et al (2014) Thinking with their trunks: elephants use smell but not sound to locate food and exclude nonrewarding alternatives. Anim Behav 88:91–98.  https://doi.org/10.1016/j.anbehav.2013.11.011 CrossRefGoogle Scholar
  62. Plotnik JM, Brubaker DL, Dale R et al (2019) Elephants have a nose for quantity. Proc Natl Acad Sci 116:12566.  https://doi.org/10.1073/pnas.1818284116 CrossRefPubMedGoogle Scholar
  63. Pollard KA, Blumstein DT (2012) Evolving communicative complexity: insights from rodents and beyond. Philos Trans R Soc Biol 367:1869–1878CrossRefGoogle Scholar
  64. Poole JH (1999) Signals and assessment in African elephants: evidence from playback experiments. Anim Behav 58:185–193CrossRefPubMedPubMedCentralGoogle Scholar
  65. Poole JH, Payne K, Langbauer WR, Moss CJ (1988) The social contexts of some very low frequency calls of African elephants. Behav Ecol Sociobiol 22:385–392Google Scholar
  66. Poole JH, Tyack PL, Stoeger-Horwath AS, Watwood S (2005) Animal behaviour: elephants are capable of vocal learning. Nature 434:455–456.  https://doi.org/10.1038/434455a CrossRefPubMedPubMedCentralGoogle Scholar
  67. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  68. Rendall D, Seyfarth RM, Cheney DL, Owren MJ (1999) The meaning and function of grunt variants in baboons. Anim Behav 57:583–592CrossRefPubMedPubMedCentralGoogle Scholar
  69. Revelle W (2018) psych: procedures for psychological, psychometric, and personality research. Northwestern University, EvanstonGoogle Scholar
  70. Rousseeuw PJ (1987) Silhouettes: a graphical aid to the interpretation and validation of cluster analysis. J Comput Appl Math 20:53–65.  https://doi.org/10.1016/0377-0427(87)90125-7 CrossRefGoogle Scholar
  71. Schwarz G (1978) Estimating the dimension of a model. Ann Stat 6:461–464.  https://doi.org/10.1214/aos/1176344136 CrossRefGoogle Scholar
  72. Shyan-Norwalt MR, Peterson J, Milankow King B et al (2010) Initial findings on visual acuity thresholds in an African elephant (Loxodonta africana). Zoo Biol 29:30–35.  https://doi.org/10.1002/zoo.20259 CrossRefPubMedGoogle Scholar
  73. Soltis JM, Savage A, Leong KM (2004) How many rumbles are there? Acoustic variation and individual identity in the rumble vocalizations of African elephants (Loxodonta africana). J Acoust Soc Am 115:2555.  https://doi.org/10.1121/1.4783864 CrossRefGoogle Scholar
  74. Soltis J, Leong K, Savage A (2005a) African elephant vocal communication II: rumble variation reflects the individual identity and emotional state of callers. Anim Behav 70:589–599.  https://doi.org/10.1016/j.anbehav.2004.11.016 CrossRefGoogle Scholar
  75. Soltis J, Leong K, Savage A (2005b) African elephant vocal communication I: antiphonal calling behaviour among affiliated females. Anim Behav 70:579–587.  https://doi.org/10.1016/j.anbehav.2004.11.015 CrossRefGoogle Scholar
  76. Soltis J, Leighty KA, Wesolek CM, Savage A (2009) The expression of affect in african elephant (Loxodonta Africana) rumble vocalizations. J Comp Psychol 123:222–225CrossRefGoogle Scholar
  77. Soltis J, Blowers Tracy E, Savage A (2011) Measuring positive and negative affect in the voiced sounds of African elephants (Loxodonta africana). J Acoust Soc Am 129:1059–1066.  https://doi.org/10.1121/1.3531798 CrossRefPubMedPubMedCentralGoogle Scholar
  78. Soltis J, King LE, Douglas-Hamilton I et al (2014) African elephant alarm calls distinguish between threats from humans and bees. PLoS One 9:e89403.  https://doi.org/10.1371/journal.pone.0089403 CrossRefPubMedPubMedCentralGoogle Scholar
  79. Stoeger AS, Baotic A (2016) Information content and acoustic structure of male African elephant social rumbles. Sci Rep 6:27585.  https://doi.org/10.1038/srep27585 CrossRefPubMedPubMedCentralGoogle Scholar
  80. Stoeger AS, Heilmann G, Zeppelzauer M et al (2012) Visualizing sound emission of elephant vocalizations: evidence for two rumble production types. PLoS One 7:e48907CrossRefPubMedPubMedCentralGoogle Scholar
  81. Stoeger AS, Zeppelzauer M, Baotic A (2014) Age-group estimation in free-ranging African elephants based on acoustic cues of low-frequency rumbles. Bioacoustics 23:231–246.  https://doi.org/10.1080/09524622.2014.888375 CrossRefPubMedPubMedCentralGoogle Scholar
  82. Stoeger-Horwath AS, Stoeger S, Schwammer HM, Kratochvil H (2007) Call repertoire of infant African elephants: first insights into the early vocal ontogeny. J Acoust Soc Am 121:3922–3931.  https://doi.org/10.1121/1.2722216 CrossRefPubMedPubMedCentralGoogle Scholar
  83. Sugiura H (1993) Effects of proximity and behavioral context on acoustic variation in the coo calls of Japanese macaques. Am J Primatol 69:1412–1424.  https://doi.org/10.1002/ajp.20447 CrossRefGoogle Scholar
  84. Taylor AM, Reby D (2009) The contribution of source-filter theory to mammal vocal communication research. J Zool 280:221–236.  https://doi.org/10.1111/j.1469-7998.2009.00661.x CrossRefGoogle Scholar
  85. Taylor AM, Charlton BD, Reby D (2016) Vocal production by terrestrial mammals: source, filter, and function. Vertebrate sound production and acoustic communication. Springer, Cham, pp 229–259CrossRefGoogle Scholar
  86. Thompson M (2009) African forest elephant (Loxodonta africana cyclotis) vocal behavior and its use in conservation. Cornell University, CornellGoogle Scholar
  87. Thompson ME, Schwager SJ, Payne KB (2010) Heard but not seen: an acoustic survey of the African forest elephant population at Kakum Conservation Area, Ghana. Afr J Ecol 48:224–231.  https://doi.org/10.1111/j.1365-2028.2009.01106.x CrossRefGoogle Scholar
  88. Turkalo A, Fay J (1995) Studying forest elephants by direct observation. Pachyderm 1995:45–54Google Scholar
  89. Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, New YorkCrossRefGoogle Scholar
  90. Wadewitz P, Hammerschmidt K, Battaglia D et al (2015) Characterizing vocal repertoires—hard vs. soft classification approaches. PLoS One 10:e0125785.  https://doi.org/10.1371/journal.pone.0125785 CrossRefPubMedPubMedCentralGoogle Scholar
  91. Waser PM, Brown CH (1986) Habitat acoustics and primate communication. Am J Primatol 10:135–154.  https://doi.org/10.1002/ajp.1350100205 CrossRefGoogle Scholar
  92. Wesolek CM, Soltis J, Leighty KA, Savage A (2009) Infant African elephant rumble vocalizations vary according to social interactions with adult females. Bioacoustics 18:227–239.  https://doi.org/10.1080/09524622.2009.9753603 CrossRefGoogle Scholar
  93. White JW, Ruttenberg BI (2007) Discriminant function analysis in marine ecology: some oversights and their solutions. Mar Ecol Prog Ser 329:301–305CrossRefGoogle Scholar
  94. Wiley RH, Richards DG (1978) Physical constraints on acoustic communication in the atmosphere: implications for the evolution of animal vocalizations. Behav Ecol Sociobiol 3:69–94.  https://doi.org/10.1007/BF00300047 CrossRefGoogle Scholar
  95. Wood JD, McCowan B, Langbauer WR et al (2005) Classification of African elephant Loxodonta africana rumbles using acoustic parameters and cluster analysis. Bioacoustics 15:143–161CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Elephant Listening Project, Center for Conservation Bioacoustics, Cornell Lab of OrnithologyCornell UniversityIthacaUSA

Personalised recommendations