Abstract
Vocal and gestural sequences of several primates have been found to conform to two general principles of information compression: the compensation between the duration of a construct and that of its components (Menzerath–Altmann law) and an inverse relationship between signal duration and its occurrence (Zipf’s law of abbreviation). Even though Zipf’s law of brevity has been proposed as a universal in animal communication, evidence on non-human primate vocal behavior conformity to linguistic laws is still debated, and information on strepsirrhine primates is lacking. We analyzed the vocal behavior of the unique singing lemur species (Indri indri) to assess whether the song of the species shows evidence for compression. As roars have a chaotic structure that impedes the recognition of each individual utterance, and long notes are usually given by males, we focused on the core part of the song (i.e., the descending phrases, composed of two–six units). Our results indicate that indris’ songs conform to Zipf’s and Menzerath–Altmann linguistic laws. Indeed, shorter phrases are more likely to be included in the song, and units’ duration decrease at the increase of the size of the phrases. We also found that, despite a sexual dimorphism in the duration of both units and phrases, these laws characterize sequences of both males and females. Overall, we provide the first evidence for a trade-off between signal duration and occurrence in the vocal behavior of a strepsirrhine species, suggesting that selective pressures for vocal compression are more ancestral than previously assumed within primates.
Similar content being viewed by others
Data availability
Data used in this study can be found at https://github.com/sciabola/ANCO2021_DATA
References
Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267. https://doi.org/10.1163/156853974X00534
Altmann G (1980) Prolegomena to Menzerath’s law. Glottometrika 2:1–10
Barr DJ, Levy R, Scheepers C, Tily HJ (2013) Random effects structure for confirmatory hypothesis testing: keep it maximal. J Mem Lang 68:255–278. https://doi.org/10.1016/j.jml.2012.11.001
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed- effects models using lme4. J Stat Softw 67:1–48
Bezerra BM, Souto AS, Radford AN, Jones G (2011) Brevity is not always a virtue in primate communication. Biol Lett 7:23–25
Boersma P, Weenink D (2017) Praat: Doing phonetics by computer [Computer Program]. Version 6.0.28. http://www.praat.org. Accessed 23 Mar 2017
Bonadonna G, Torti V, Randrianarison RM, Martinet N, Gamba M, Giacoma C (2014) Behavioral correlates of extra-pair copulation in Indri indri. Primates 55(1):119–123. https://doi.org/10.1007/s10329-013-0376-0
Bonadonna G, Torti V, Sorrentino V, Randrianarison RM, Zaccagno M, Gamba M, Giacoma C (2017) Territory exclusivity and intergroup encounters in the indris (Mammalia: Primates: Indridae: Indri indri) upon methodological tuning. Eur Zool J 84:238–251. https://doi.org/10.1080/24750263.2017.1318184
Bonadonna G, Torti V, De Gregorio C, Valente D, Randrianarison RM, Pozzi L, Gamba M, Giacoma C (2019) Evidence of genetic monogamy in the lemur Indri (Indri indri). Am J Primatol 81(6):e22993. https://doi.org/10.1002/ajp.22993
Bonadonna G, Zaccagno M, Torti V, Valente D, De Gregorio C, Randrianarison RM, Tan C, Gamba M, Giacoma C (2020) Intra-and intergroup spatial dynamics of a pair-living singing primate, Indri indri: a multiannual study of three Indri groups in Maromizaha Forest, Madagascar. Int J Primatol 41:1–22. https://doi.org/10.1007/s10764-019-00127-5
Bretz F, Hothorn T, Westfall P (2010) Multiple comparisons using R. Chapman & Hall/CRC Press, Boca Raton
Briseño-Jaramillo M, Ramos-Fernandez G, Palacios-Romo TM, Sosa-López JR, Lemasson A (2018) Age and social affinity effects on contact call interactions in free-ranging spider monkeys. Behav Ecol Sociobiol 72:192. https://doi.org/10.1007/s00265-018-2615-2
Cäsar C, Zuberbühler K (2012) Referential alarm calling behaviour in New World primates. Curr Zool 58(5):680–697. https://doi.org/10.1093/czoolo/58.5.680
Clay Z, Zuberbühler K (2009) Food-associated calling sequences in bonobos. Anim Behav 77:1387–1396. https://doi.org/10.1016/j.anbehav.2009.02.016
Clink DJ, Tasirin JS, Klinck H (2020a) Vocal individuality and rhythm in male and female duet contributions of a nonhuman primate. Curr Zool 66(2):173–186. https://doi.org/10.1093/cz/zoz035
Clink DJ, Ahmad AH, Klinck H (2020b) Brevity is not a universal in animal communication: evidence for compression depends on the unit of analysis in small ape vocalizations. R Soc Open Sci 7:200151. https://doi.org/10.1098/rsos.200151
De Gregorio C, Zanoli A, Valente D, Torti V, Bonadonna G, Randrianarison RM, Giacoma C, Gamba M (2019) Female indris determine the rhythmic structure of the song and sustain a higher cost when the chorus size increases. Curr Zool 65(1):89–97. https://doi.org/10.1093/cz/zoy058
Demartsev V, Gordon N, Barocas A, Bar-Ziv E, Ilany T, Goll Y, Ilany A, Geffen E (2019) The ‘Law of Brevity’ in animal communication: sex-specific signaling optimization is determined by call amplitude rather than duration. Evol Lett 3:623–634. https://doi.org/10.1002/evl3.147
Dobson AJ (2002) An introduction to generalized linear models. CRC Press, Boca Raton
Egnor SER, Hauser MD (2006) Noise-induced vocal modulation in cotton-top tamarins (Saguinus oedipus). Am J Primatol 68(12):1183–1190. https://doi.org/10.1002/ajp.20317
Endler A (1992) Signals, signal conditions, and the direction of evolution. Am Nat 139(1):125–153. https://doi.org/10.1086/285308
Favaro L, Gamba M, Cresta E, Fumagalli E, Bandoli F, Pilenga C, Isaja V, Mathevon N, Reby D (2020) Do penguins’ vocal sequences conform to linguistic laws? Biol Lett 16:20190589. https://doi.org/10.1098/rsbl.2019.0589
Fedurek P, Slocombe KE (2011) Primate vocal communication: a useful tool for understanding human speech and language evolution? Hum Biol 83(2):153–173. https://doi.org/10.3378/027.083.0202
Fedurek P, Zuberbühler K, Semple S (2017) Trade-offs in the production of animal vocal sequences: insights from the structure of wild chimpanzee pant hoots. Front Zool 14:50. https://doi.org/10.1186/s12983-017-0235-8
Ferrer-i-Cancho R, Hernández-Fernández A (2013) The failure of the law of brevity in two New World primates. Statistical caveats. Glottotheory Int J Theor Linguist 4:45–55. https://doi.org/10.1524/glot.2013.0004
Ferrer-i-Cancho R, Lusseau D (2009) Efficient coding in dolphin surface behavioral patterns. Complexity 14(5):23–25. https://doi.org/10.1002/cplx.20266
Ferrer-i-Cancho R, McCowan B (2012) The span of correlations in dolphin whistle sequences. J Stat Mech Theory Exp. https://doi.org/10.1088/1742-5468/2012/06/p06002
Ferrer-i-Cancho R, Hernández-Fernández A, Lusseau D, Agoramoorthy G, Hsu MJ, Semple S (2013) Compression as a universal principle of Animal behavior. Cogn Sci 37:1565–1578. https://doi.org/10.1111/cogs.12061
Ferrer-i-Cancho R, Bentz C, Seguin C (2020) Optimal Coding and the Origins of Zipfian Laws. J Quant Linguist. https://doi.org/10.1080/09296174.2020.1778387
Fox J, Weisberg S (2011) An R companion to applied regression, 2nd edn. SAGE Publications Inc, Thousand Oaks
Freeberg TM, Lucas JR (2012) Information theoretical approaches to chick-a-dee calls of Carolina chickadees (Poecile carolinensis). J Comp Psychol 126:68. https://doi.org/10.1037/a0024906
Gamba M, Favaro L, Torti V, Sorrentino V, Giacoma C (2011) Vocal tract flexibility and variation in the vocal output in wild indris. Bioacoustics 20:251–265. https://doi.org/10.1080/09524622.2011.9753649
Gamba M, Torti V, Estienne V, Randrianarison RM, Valente D, Rovara P, Bonadonna G, Friard O, Giacoma C (2016) The indris have got rhythm! Timing and pitch variation of a primate song examined between sexes and age classes. Front Neurosci 10:249. https://doi.org/10.3389/fnins.2016.00249
Geissmann T (2000) Gibbon songs and human music from an evolutionary perspective. In: Wallin NL, Merker B, Brown S (eds) The origins of music. MIT Press, Cambridge, pp 103–123
Genty E, Byrne RW (2010) Why do gorillas make sequences of gestures? Anim Cogn 13:287–301. https://doi.org/10.1007/s10071-009-0266-4
Ghazanfar AA, Liao DA, Takahasi DY (2019) Volition and learning in primate vocal behaviour. Anim Behav 151:239–247. https://doi.org/10.1016/j.anbehav.2019.01.021
Giacoma C, Sorrentino V, Rabarivola C, Gamba M (2010) Sex differences in the song of Indri indri. Int J Primatol 31:539–551. https://doi.org/10.1007/s10764-010-9412-8
Glazko GV, Nei M (2003) Estimation of divergence times for major lineages of primate species. Mol Biol Evol 20(3):424–434. https://doi.org/10.1093/molbev/msg050
Gustison ML, Semple S, Ferrer-i-Cancho R, Bergman TJ (2016) Gelada vocal sequences follow Menzerath’s linguistic law. Proc Natl Acad Sci USA 113(19):2750–2758. https://doi.org/10.1073/pnas.1522072113
Haimoff EH (1986) Convergence in the duetting of monogamous Old World primates. J Hum Evol 15:51–59. https://doi.org/10.1016/S0047-2484(86)80065-3
Heesen R, Hobaiter C, Ferrer-i-Cancho R, Semple S (2019) Linguistic laws in chimpanzee gestural communication. Proc R Soc B 286:20182900. https://doi.org/10.1098/rspb.2018.2900
Herrera JP, Dávalos LM (2016) Phylogeny and divergence times of lemurs inferred with recent and ancient fossils in the tree. Syst Biol 65(5):772–791. https://doi.org/10.1093/sysbio/syw035
Hewitt G, MacLarnon A, Jones KE (2002) The functions of laryngeal air sacs in primates: a new hypothesis. Folia Primatol 73:70–94. https://doi.org/10.1159/000064786
Huang M, Ma H, Ma C, Garber PA, Fan P (2020) Male gibbon loud morning calls conform to Zipf’s law of brevity and Menzerath’s law: insights into the origin of human language. Anim Behav 160:145–155. https://doi.org/10.1016/j.anbehav.2019.11.017
Katsu N, Yamada K, Okanoya K, Nakamichi M (2019) Temporal adjustment of short calls according to a partner during vocal turn-taking in Japanese macaques. Curr Zool 65(1):99–105. https://doi.org/10.1093/cz/zoy077
Kershenbaum A, Blumstein DT, Roch MA et al (2016) Acoustic sequences in non-human animals: a tutorial review and prospectus. Biol Rev 91:13–52. https://doi.org/10.1111/brv.12160
Leroux M, Townsend S (2020) Call Combinations in great apes and the evolution of syntax. Anim Behav Cogn 7(2):131–139
Lindblom B, Sundberg J (2007) The human voice in speech and singing. In: Rossing TD (ed) Springer handbook of acoustics. Springer-Verlag, New York, pp 669–712
Luo B, Jiang T, Liu Y, Wang J, Lin A, Wei X, Feng J (2013) Brevity is prevalent in bat short-range communication. J Comp Physiol A 199:325–333. https://doi.org/10.1007/s00359-013-0793-y
MacLarnon AM, Hewitt GP (1999) The evolution of human speech: the role of enhanced breathing control. Am J Phys Anthropol 109:341–363. https://doi.org/10.1002/(SICI)1096-8644(199907)109:3%3c341::AID-AJPA5%3e3.0.CO;2-2
Marler P (1967) Animal communication signals. Science 157:769–774. https://doi.org/10.1126/science.157.3790.769
Ouattara K, Lemasson A, Zuberbühler K (2009) Campbell’s monkeys concatenate vocalizations into context-specific call sequences. Proc Natl Acad Sci USA 106(51):22026–22031. https://doi.org/10.1073/pnas.0908118106
Piantadosi ST, Tily H, Gibson E (2011) Word lengths are optimized for efficient communication. Proc Natl Acad Sci USA 108(9):3526–3529. https://doi.org/10.1073/pnas.1012551108
Plotkin JB, Nowak MA (2000) Language evolution and information theory. J Theor Biol 205(1):147–159. https://doi.org/10.1006/jtbi.2000.2053
Pollock JI (1986) The song of the Indris (Indri indri; Primates: Lemuroidea): natural history, form and function. Int J Primatol 7:225–267. https://doi.org/10.1007/BF02736391
R Core Team (2019). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Roy S, Miller C, Gottsch D, Wang X (2011) Vocal control by the common marmoset in the presence of interfering noise. J Exp Biol 214:3619–3629. https://doi.org/10.1242/jeb.056101
Savage P, Brown S, Sakai E, Currie T (2015) Statistical universals reveal the structures and functions of human music. Proc Natl Acad Sci USA 112(29):8987
Semple S, Hsu MJ, Agoramoorthy G (2010) Efficiency of coding in macaque vocal communication. Biol Lett 6:469–471. https://doi.org/10.1098/rsbl.2009.1062
Semple S, Hsu MJ, Agoramoorthy G, Ferrer-i-Cancho R (2013) The law of brevity in macaque vocal communication is not an artefact of analysing mean call durations. J Quant Linguist 20(3):209–217. https://doi.org/10.1080/09296174.2013.799917
Slocombe KE, Zuberbühler K (2005) Functionally referential communication in a chimpanzee. Curr Biol 15(19):1779–1784. https://doi.org/10.1016/j.cub.2005.08.068
Sorrentino V, Gamba M, Giacoma C (2013) A quantitative description of the vocal types emitted in the Indri’s song. In: Masters J, Gamba M, Génin F (eds) Leaping ahead: advances in Prosimian biology. Springer Science + Business Media, New York, pp 315–322
Strauss U, Grzybek P, Altmann G (2007) Word length and word frequency. In: Grzybek P (ed) Contributions to the science of text and language. Springer, Dordrecht, The Netherlands, pp 277–294
Sueur J, Aubin SC (2008) Seewave: a free modular tool for sound analysis and synthesis. Bioacoustics 18:213–226. https://doi.org/10.1080/09524622.2008.9753600
Thalmann U, Geissmann T, Simona A, Mutschler T (1993) The indris of Anjanaharibe-Sud, northeastern Madagascar. Int J Primatol 14:357–381. https://doi.org/10.1007/BF02192772
Torti V, Gamba M, Rabemananjara ZH, Giacoma C (2013) The songs of the indris (Mammalia: Primates: Indridae): contextual variation in the long-distance calls of a lemur. Ital J Zool 80:596–607. https://doi.org/10.1080/11250003.2013.845261
Torti V, Bonadonna G, De Gregorio C, Valente D, Randrianarison RM, Friard O, Giacoma C (2017) An intra-population analysis of the indris’ song dissimilarity in the light of genetic distance. Sci Rep 7:10140. https://doi.org/10.1038/s41598-017-10656-9
Torti V, Valente D, De Gregorio C, Comazzi C, Miaretsoa L, Ratsimbazafy J, Giacoma C, Gamba M (2018) Call and be counted! Can we reliably estimate the number of callers in the indri’s (Indri indri) song? PLoS ONE 13(8):e0201664. https://doi.org/10.1371/journal.pone.0201664
Waser PM, Brown CH (1986) Habitat acoustics and primate communication. Am J Primatol 10(2):135–154. https://doi.org/10.1002/ajp.1350100205
Watson SK, Heesen R, Hedwig D, Robbins MM, Townsend SW (2020) An exploration of Menzerath’s law in wild mountain gorilla vocal sequences. Biol Lett 16:20200380. https://doi.org/10.1098/rsbl.2020.0380
Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York
Zanoli A, De Gregorio C, Valente D, Torti V, Bonadonna G, Randrianarison RM, Giacoma C, Gamba M (2020) Sexually dimorphic phrase organization in the song of the indris (Indri indri). Am J Primatol 82:e23132. https://doi.org/10.1002/ajp.23132
Zipf GK (1936) The Psycho-biology of language: an introduction to dynamic philology. George Routledge and Sons Ltd, London
Zipf GK (1945) The meaning-frequency relationship of words. J Gen Psychol 33:251–256
Zipf GK (1949) Human behavior and the principle of least effort. An introduction to human ecology. Hafner Publishing Company, New York and London
Acknowledgments
This research was supported by Università degli Studi di Torino and by grants from the Parco Natura Viva—Garda Zoological Park. We are grateful to Cesare Avesani Zaborra and Caterina Spiezio for their support. We also thank the GERP (Groupe d’Étude et de Recherche sur les Primates de Madagascar) for the field logistics organization and to both field guides and assistants helping during the data collection.
Author information
Authors and Affiliations
Contributions
DV, MG, and LF conceived the study design and the methodology; VT, DV, CDG, AZ, and TR collected the data; DV and MG conducted the formal analysis and investigation; DV wrote the manuscript, all authors edited the manuscript and approved its final version.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Ethical approval
Research permits for this research have been granted from Direction des Eaux et Forêts and ‘Madagascar National Parks’ (formerly ANGAP). 2004: N190/MINENV.EF/SG/DGEF/ DPB/SCBLF/RECH; 2005: N197/MINENV.EF/SG/DGEF/DPB/SCBLF/RECH; 2006: N172/06/ MINENV.EF/SG/DGEF/DPB/SCBLF; 2007: N0220/07/MINENV.EF/SG/DGEF/DPSAP/SSE; 2008: N258/08/MEFT/SG/ DGEF/DSAP/SSE; 2009: N243/09/MEF/SG/DGF/DCB.SAP/SLRSE; 2010: N118/10/MEF/SG/DGF/DCB.SAP/SCBSE and 293/10/MEF/SG/DGF/DCB.SAP/SCB; 2011: N274/11/MEF/SG/DGF/DCB.SAP/SCB; 2012: N245/12/MEF/ SG/DGF/DCB.SAP/SCB; 2013: permit not required as data collection was performed by Malagasy citizens only. 2014: N066/14/MEF/SG/DGF/DCB.SAP/SCB; 2015: N180/15/MEEMF/SG/DGF/DAPT/SCBT; 2016: N98/16/MEEMF/SG/DGF/DAPT/SCB.Re and N217/16/MEEMF/SG/DGF/DSAP/SCB.Re; 2017: 73/17/MEEF/SG/DGF/DSAP/SCB.RE; 2018: 91/18/MEEF/SG/DGF/DSAP/SCB.Re; 2019: 118/19/MEDD/SG/DGEF/DSAP/DGRNE and 284/19/MEDD/SG/DGEF/DSAP/DGRNE; 2019/2020: 338/19/MEDD/SG/DGEF/DSAP/DGRNE. Approval for observational researches and for studies that do not involve animal handling are not required by our institutional committees.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Valente, D., De Gregorio, C., Favaro, L. et al. Linguistic laws of brevity: conformity in Indri indri. Anim Cogn 24, 897–906 (2021). https://doi.org/10.1007/s10071-021-01495-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10071-021-01495-3