Abstract
Toothed whales use powerful ultrasonic biosonar pulses (i.e. clicks) for echolocation. Underwater acoustic recordings have suggested that the majority of toothed whale species can be grouped acoustically as either producing broadband clicks or narrowband high-frequency (NBHF) clicks. Recently, it has been shown that Heaviside’s dolphins, Cephalorhynchus heavisidii, emit NBHF clicks for echolocation but also clicks of lower frequency and broader bandwidth for communication. Here, we use acoustic recorders and drone video footage to reinforce previous findings that Commerson’s dolphins (C. commersonii) produce signals similar to Heaviside’s dolphins. We reveal that they use clicks with a lower frequency and broader bandwidth in the form of click trains and burst-pulses. These sounds were not recorded in the presence of smaller groups of Commerson’s dolphins, indicating that they may fulfil a communication function in larger groups. Also, we utilised a novel combination of drone video footage paired with underwater acoustic recordings to estimate the source level of echolocation clicks produced by Commerson’s dolphins. In addition, we compare the acoustic signals produced by Commerson’s and Heaviside’s dolphins to identify interspecific similarities and differences. Spectral differences were found in NBHF click trains, buzzes and burst-pulses between species; however, bandwidth and duration parameters were not significantly different for broadband click trains. Our findings make it likely that all four species of the Cephalorhynchus genus have the ability to generate both signal types, and further challenges the evolutionary concept of NBHF signal production.
Significance statement
This study confirms the presence of a duel echolocation click (i.e. biosonar) strategy in Commerson’s dolphins, making them the second species of their genus known to produce two types of biosonar. We provide an in-depth quantitative analysis of Commerson’s dolphin acoustic signal types, and include a comparison of signal types between Commerson’s dolphins and the other species known to produce two types of biosonar, the Heaviside’s dolphin. In addition, this is the first study to combine drone footage with underwater acoustic recordings to measure the source level of toothed whale echolocation signals. We use this novel technique to provide source levels measured from Commerson’s dolphin echolocation clicks which are comparable to published values for this species calculated using an expensive and complicated array of hydrophones. Thus, we provide a simpler and more cost effective way to study sounds produced by marine mammals.
Similar content being viewed by others
Availability of data and material
All data generated or analysed during this study are included in this published article and its supplementary information files.
Code availability
The progam ‘Porpoise Tracker’ used for collecting measurements from the drone footage is freely available on github: https://github.com/henrikmidtiby/PorpoiseTracker
References
Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–266
Andersen S, Amundin M (1976) Possible predator-related adaption of sound production and hearing in the harbour porpoise (Phocoena phocoena). Aquat Mamm 4:56–57
Au WWL (1993) The sonar of dolphins. Springer-Verlag
Au WWL (1997) Echolocation in dolphins with a dolphin-bat comparison. Bioacoustics 8:137–162
Au WWL, Benoit-Bird KJ (2003) Automatic gain control in the echolocation system of dolphins. Nature 423:861–863
Au WWL, Kastelein RA, Rippe T, Schooneman NM (1999) Transmission beam pattern and echolocation signals of a harbor porpoise (Phocoena phocoena). J Acoust Soc Am 106:3699–3705
Blomqvist C, Amundin M. (2004) High-frequency burst-pulse sounds in agonistic/aggresive interactions in bottlenose dolphins, Tursiops truncatus in: Thomas J, Moss C, Vater M (eds) Echolocation in bats and dolphins. The University of Chicago Press, Chicago, pp. 425–431
Branstetter BK, Leger JS, Acton D, Stewart J, Houser D, Finneran JJ, Jenkins K (2017) Killer whale (Orcinus orca) behavioral audiograms. J Acoust Soc Am 141:2387–2398
Caillat M, Thomas L, Gillespie D (2013) The effects of acoustic misclassification on cetacean species abundance estimation. J Acoust Soc Am 134:2469–2476
Clark CW, Ellison WT, Southall BL, Hatch L, Van Parijs SM, Frankel A, Ponirakis D (2009) Acoustic masking in marine ecosystems: intuitions, analysis, and implication. Mar Ecol Prog Ser 395:201–222
Clausen KT, Wahlberg M, Beedholm K, Deruiter S, Madsen PT (2011) Click communication in harbour porpoises Phocoena phocoena. Bioacoustics 20:1–28
Coscarella MA, Bellazzi G, Gaffet ML, Berzano M, Degrati M (2015) Technique used by killer whales (Orcinus orca) when hunting for dolphins in Patagonia, Argentina. Aquat Mamm 41:192–197
Cremer MJ, Holz AC, Bordino P, Wells RS, Simões-Lopes PC (2017) Social sounds produced by franciscana dolphins, Pontoporia blainvillei (Cetartiodactyla, Pontoporiidae). J Acoust Soc Am 141:2047–2054
Dawson SM (1988) The high frequency sounds of free-ranging Hector’s dolphins, Cephalorhynchus hectori. Rep Int Whal Commn Special Issue 9:339–344
Dawson SM (1991) Clicks and communication: the behavioral and social contexts of Hector’s dolphin vocalizations. Ethology 88:265–276
Dawson SM, Thorpe CW (1990) A quantitative-analysis of the sounds of Hector’s dolphin. Ethology 86:131–145
DeRuiter SL, Bahr A, Blanchet M-A, Hansen SF, Kristensen JH, Madsen PT, Tyack PL, Wahlberg M (2009) Acoustic behaviour of echolocating porpoises during prey capture. J Exp Biol 212:3100–3107
DeRuiter SL, Hansen M, Koopman HN, Westgate AJ, Tyack PL, Madsen PT (2010) Propagation of narrow-band-high-frequency clicks: measured and modeled transmission loss of porpoise-like clicks in porpoise habitats. J Acoust Soc Am 127:560–567
Dziedzic A, De Buffrenil V (1989) Acoustic signals of the Commerson’s dolphin, Cephalorhynchus commersonii, in the Kerguelen Islands. J Mammal 70:449–452
Evans W, Awbrey F, Hackbarth H (1988) High frequency pulses produced by free-ranging Commerson’s dolphin (Cephalorhynchus commersonii) compared to those of phocoenids. In: Brownell RL, Donovan GP (eds) Reports of the International Whaling Commission (special issue 9). Biology of the genus Cephalorhynchus. International Whaling Commission, Cambridge, pp. 173–181
Falabella V, Campagna C, Croxall J (eds) (2009) Atlas of the Patagonian Sea: species and spaces. Wildlife Conservation Society and BirdLife International, Buenos Aires. http://www.atlas-marpatagonico.org. Accessed 10 July 2020
Fenton BM, Jensen FH, Kalko EK, Tyack PL (2014) Sonar signals of bats and toothed whales. In: Surlykke A, Nachtigall P, Fay R, Popper A (eds) Biosonar. Springer, New York, pp 11–59
Fletcher H, Munson WA (1937) Relation between loudness and masking. J Acoust Soc Am 9:1–10
Fox J, Weisberg S (2011) An R companion to applied regression. Sage, Thousand Oaks
Francois R, Garrison G (1982) Sound absorption based on ocean measurements: part I: pure water and magnesium sulfate contributions. J Acoust Soc Am 72:896–907
Frouin-Mouy H, Tenorio-Hallé L, Thode A, Swartz S, Urbán J (2020) Using two drones to simultaneously monitor visual and acoustic behaviour of gray whales (Eschrichtius robustus) in Baja California, Mexico. J Exp Mar Biol 525:151–321
Goodall RNP, Galeazzi AR, Leatherwood S, Miller KW, Cameron IS, Kastelein RK, Sobral AP (1988) Studies on Commerson’s dolphins, Cephalorhynchus commersonii, off Tierra del Fuego, 1976–1984, with a review of information on the species in the South Atlantic. Rep Int Whal Commn Special Issue 9:3–70
Götz T, Antunes R, Heinrich S (2010) Echolocation clicks of free-ranging Chilean dolphins (Cephalorhynchus eutropia). J Acoust Soc Am 128:563–566
Griffin DR, Webster FA, Michael CR (1960) The echolocation of flying insects by bats. Anim Behav 8:141–154
Hansen M, Wahlberg M, Madsen PT (2008) Low-frequency components in harbor porpoise (Phocoena phocoena) clicks: communication signal, by-products, or artifacts? J Acoust Soc Am 124:4059–4068
Hatakeyama Y, Ishii K, Soeda H, Shimamura T (1988) Acoustic surveys on Commerson’s dolphin. Document Submitted to the International North Pacific Fisheries Commission, Fisheries Agency of Japan, Tokyo, pp 1–21
Heiler J, Elwen SH, Kriesell H, Gridley T (2016) Changes in bottlenose dolphin whistle parameters related to vessel presence, surface behaviour and group composition. Anim Behav 117:167–177
Heinrich S, Elwen S, Bräger S (2010) Patterns of sympatry in Lagenorhynchus and Cephalorhynchus: dolphins in different habitats. In: Würsig B, Würsig M (eds) The dusky dolphin: master acrobat off different shores. Elsevier Academic Press, Amsterdam, pp 313–332
Henderson E, Hildebrand J, Smith M, Falcone E (2012) The behavioral context of common dolphin (Delphinus sp.) vocalizations. Mar Mammal Sci 28:439–460
Herman LM, Tavolga WN (1980) The communication systems of cetaceans. In: Herman LM (ed) Cetacean behavior: mechanisms and functions. Wiley & Sons Inc, New York, pp 149–209
Herzing DL (1996) Vocalizations and associated underwater behavior of free-ranging Atlantic spotted dolphins, Stenella frontalis and bottlenose dolphins, Tursiops truncatus. Aquat Mamm 22:61–80
Holy TE, Guo Z (2005) Ultrasonic songs of male mice. PLoS Biol 3:e386
Iñíguez MA, Tossenberger VP (2007) Commerson's dolphins (Cephalorhynchus commersonii) off Ria Deseado, Patagonia, Argentina. Aquat Mamm 33:276–285
Iñíguez MA, Tossenberger VP, Tomsin AL (2001) Biology and behaviour of Commerson’s dolphins (Cephalorhynchus commersonii) at Bahia san Julián, Patagonia, Argentina. Fourteenth Biennial Conference on the Biology of Marine Mammals, Vancouver, Canada, p 105 (abstract)
Janik VM (2009) Acoustic communication in delphinids. Adv Study Behav 40:123–157
Jensen FH, Rocco A, Mansur RM, Smith BD, Janik VM, Madsen PT (2013) Clicking in shallow rivers: short-range echolocation of Irrawaddy and Ganges river dolphins in a shallow, acoustically complex habitat. PLoS One 8:e59284
Kamminga C, Wiersma H (1981) Investigations on cetacean sonar II. Acoustical similarities and differences in odontocete sonar signals. Aquat Mamm 8:41–62
Kamminga C, Wiersma H (1982) Investigations on cetacean sonar V. The true nature of the sonar sound of Cephalorhynchus commersonii. Aquat Mamm 9:95–104
Koblitz JC, Wahlberg M, Stilz P, Madsen PT, Beedholm K, Schnitzler H-U (2012) Asymmetry and dynamics of a narrow sonar beam in an echolocating harbor porpoise. J Acoust Soc Am 131:2315–2324
Kyhn LA, Tougaard J, Jensen F, Wahlberg M, Stone G, Yoshinaga A, Beedholm K, Madsen PT (2009) Feeding at a high pitch: source parameters of narrow band, high-frequency clicks from echolocating off-shore hourglass dolphins and coastal Hector’s dolphins. J Acoust Soc Am 125:1783–1791
Kyhn LA, Jensen FH, Beedholm K, Tougaard J, Hansen M, Madsen PT (2010) Echolocation in sympatric Peale’s dolphins (Lagenorhynchus australis) and Commerson’s dolphins (Cephalorhynchus commersonii) producing narrow-band high-frequency clicks. J Exp Biol 213:1940–1949
Kyhn LA, Tougaard J, Beedholm K, Jensen FH, Ashe E, Williams R, Madsen PT (2013) Clicking in a killer whale habitat: narrow-band, high-frequency biosonar clicks of harbour porpoise (Phocoena phocoena) and Dall’s porpoise (Phocoenoides dalli). PLoS One 8:e63763
Lammers M, Au WWL, Aubauer R, Nachtigall PE (2004) A comparative analysis of the pulsed emissions of free-ranging Hawaiian spinner dolphins (Stenella longirostris). In: Thomas JA, Moss CF, Vater M (eds) Echolocation in bats and dolphins. The University of Chicago Press, Chicago, pp 414–419
Lesage V, Barrette C, Kingsley MC, Sjare B (1999) The effect of vessel noise on the vocal behavior of belugas in the St. Lawrence River estuary, Canada. Mar Mammal Sci 15:65–84
Madsen PT, Wahlberg M (2007) Recording and quantification of ultrasonic echolocation clicks from free-ranging toothed whales. Deep-Sea Res Pt I 54:1421–1444
Madsen PT, Kerr I, Payne R (2004) Source parameter estimates of echolocation clicks from wild pygmy killer whales (Feresa attenuata). J Acoust Soc Am 116:1909–1912
Madsen PT, Carder D, Bedholm K, Ridgway S (2005) Porpoise clicks from a sperm whale nose—convergent evolution of 130 kHz pulses in toothed whale sonars? Bioacoustics 15:195–206
Mann J (1999) Behavioral sampling methods for cetaceans: a review and critique. Mar Mammal Sci 15:102–122
Martin JP, Garese A, Sar A, Acuña FH (2015) Fouling community dominated by Metridium senile (Cnidaria: Anthozoa: Actiniaria) in Bahia San Julian (southern Patagonia, Argentina). Sci Mar 79:211–221
Martin MJ, Gridley T, Elwen SH, Jensen FH (2018a) Heaviside’s dolphins (Cephalorhynchus heavisidii) relax acoustic crypsis to increase communication range. Proc R Soc B 285:20181178
Martin MJ, Gridley T, Elwen SH, Jensen FH (2018b) Data from: Heaviside’s dolphins (Cephalorhynchus heavisidii) relax acoustic crypsis to increase communication range. Proc R Soc B Supplemental Material Appendix S1, https://royalsocietypublishing.org/action/downloadSupplement?doi=10.1098%2Frspb.2018.1178&file=rspb20181178supp2.pdf. Accessed 10 July 2020
Martin MJ, Elwen SH, Kassanjee R, Gridley T (2019) To buzz or burst-pulse? The functional role of Heaviside’s dolphin, Cephalorhynchus heavisidii, rapidly pulsed signals. Anim Behav 150:273–284
Merkens K, Keating-McCullugh J, Tregenza N, Urmy S, Oleson E (2019) Kogia conundrum: variability in the acoustic signals of dwarf and pygmy sperm whales in deep water. World Marine Mammal Conference, Barcelona (abstract)
Miller LA, Pristed J, Møhl B, Surlykke A (1995) The click-sounds of narwhals (Monodon monoceros) in Inglefield Bay, Northwest Greenland. Mar Mammal Sci 11:491–502
Morisaka T (2012) Evolution of communication sounds in odontocetes: a review. Int J Comp Psychol 25:1–20
Morisaka T, Connor R (2007) Predation by killer whales (Orcinus orca) and the evolution of whistle loss and narrow-band high frequency clicks in odontocetes. J Evol Biol 20:1439–1458
Morisaka T, Karczmarski L, Akamatsu T, Sakai M, Dawson S, Thornton M (2011) Echolocation signals of Heaviside’s dolphins (Cephalorhynchus heavisidii). J Acoust Soc Am 129:449–457
Nakano R, Takanashi T, Skals N, Surlykke A, Ishikawa Y (2010) To females of a noctuid moth, male courtship songs are nothing more than bat echolocation calls. Biol Lett 6:582–584
Ogle DH (2017) FSA: fisheries stock analysis. R package version 0.8 17:636. https://cran.r-project.org/web/packages/FSA/FSA.pdf. Accessed 12 Jan 2016
Parks SE, Clark CW, Tyack PL (2007) Short-and long-term changes in right whale calling behavior: the potential effects of noise on acoustic communication. J Acoust Soc Am 122:3725–3731
Payne RS (1971) Acoustic location of prey by barn owls (Tyto alba). J Exp Biol 54:535–573
Quick NJ, Janik VM (2008) Whistle rates of wild bottlenose dolphins (Tursiops truncatus): influences of group size and behavior. J Comp Psychol 122:305–311
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org. Accessed 12 Jan 2016
Reyes Reyes MV, Iñíguez MA, Hevia M, Hildebrand JA, Melcón ML (2015) Description and clustering of echolocation signals of Commerson’s dolphins (Cephalorhynchus commersonii) in Bahía San Julián, Argentina. J Acoust Soc Am 138:2046–2053
Reyes Reyes MV, Tossenberger VP, Iñiguez MA, Hildebrand JA, Melcón ML (2016) Communication sounds of Commerson’s dolphins (Cephalorhynchus commersonii) and contextual use of vocalizations. Mar Mammal Sci 32:1219–1233
Schreiber EA, Burger J (eds) (2001) Biology of marine birds. CRC Press, Boca Raton
Service of Naval Hydrography (SHN) (2009) Tidal charts of Puerto San Julián. http://www.hidro.gov.ar/oceanografia/Tmareas/Form_Tmareas.asp. Accessed 10 July 2020
Shochi Y, Zbinden K, Kraus C, Gihr M, Pilleri G (1982) Characteristics and directional properties of the sonar signals emitted by the captive Commerson’s dolphin, Cephalorhynchus commersonii (Gray, 1846). Investig Cetacea 13:137–202
Sørensen P, Wisniewska D, Jensen F, Johnson M, Teilmann J, Madsen P (2018) Click communication in wild harbour porpoises (Phocoena phocoena). Sci Rep 8:9702
Szymanski MD, Bain DE, Kiehl K, Pennington S, Wong S, Henry KR (1999) Killer whale (Orcinus orca) hearing: auditory brainstem response and behavioral audiograms. J Acoust Soc Am 106:1134–1141
Thode AM, Blackwell SB, Conrad AS, Kim KH, Marques T, Thomas L, Oedekoven CS, Harris D, Bröker K (2020) Roaring and repetition: how bowhead whales adjust their call density and source level (Lombard effect) in the presence of natural and seismic airgun survey noise. J Acoust Soc Am 147:2061–2080
Thorpe CW, Bates RH, Dawson SM (1991) Intrinsic echolocation capability of Hector’s dolphin, Cephalorhynchus hectori. J Acoust Soc Am 90:2931–2934
Tyack P (1998) Acoustic communication under the sea. In: Hopp SL, Owren MJ, Evans CS (eds) Animal acoustic communication. Sound analysis and research methods. Springer, Berlin, pp. 163–220
Urick RJ (1983) Principles of underwater sound. McGraw-Hill, New York
Wahlberg M, Beedholm K, Heerfordt A, Møhl B (2011) Characteristics of biosonar signals from the northern bottlenose whale, Hyperoodon ampullatus. J Acoust Soc Am 130:3077–3084
Watkins WA, Schevill WE (1980) Characteristic features of the underwater sounds of Cephalorhynchus commersonii. J Mammal 61:738–739
Wisniewska DM, Johnson M, Teilmann J, Rojano-Doñate L, Shearer J, Sveegaard S, Miller LA, Siebert U, Madsen PT (2016) Ultra-high foraging rates of harbor porpoises make them vulnerable to anthropogenic disturbance. Curr Biol 26:1441–1446
Yoshida YM, Morisaka T, Sakai M, Iwasaki M, Wakabayashi I, Seko A, Kasamatsu M, Akamatsu T, Kohshima S (2014) Sound variation and function in captive Commerson's dolphins (Cephalorhynchus commersonii). Behav Process 108:11–19
Acknowledgements
The authors gratefully acknowledge the Prefectura Naval Argentina (Argentinian Coast Guard) in Puerto San Julián, the Parque Interjurisdiccional Marino Makenke, Lic. Juan Jones, Guardaparque Nacional Matías Ventura, Guardaparque Nacional Paula Vazquez, the Dirección de Fauna – province of Santa Cruz, Amanda Manero (MSc), Captain Luis Koncevich and crew, Dr. Frants Jensen, Dr. Tess Gridley, Dr. Simon Elwen, Vanesa Tossenberger (BSc) and the anonymous reviewers for providing comments and helpful feedback to improve this manuscript. Also, we thank Henrik Dyrberg Egemose and Dr. Henrik Midtiby, University of Southern Denmark, for providing the program for analysing drone videos.
Funding
This study was funded by the University of Southern Denmark, the Whale and Dolphin Conservation and the Fundación Cethus.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Data collection was performed by MJM, STO, MVRR, AM and MIB. Material preparation and analysis were performed by MJM, STO and MW. The first draft of the manuscript was written by MJM and STO and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethics approval
This research was conducted by the Fundación Cethus in collaboration with the University of Southern Denmark with permission from the Dirección General de Recursos Naturales – Province of Santa Cruz (Provision 013/19) and following the ethics guidelines from the University of Southern Denmark, under a permit from the Danish Animal Experiments Inspectorate, based on EU Directive 2010/63/EU. This is an observational study based on focal animal sampling where dolphins were observed from a distance and not touched or harmed in any way during data collection. The engine and echo sounder of the motor boat was turned off around dolphin groups to promote a quieter, less polluting and less disturbing environment.
Consent to participate
All authors have provided their consent to participate in this research and related publication.
Consent for publication
All authors have provided their consent to publish the results of this study.
Conflict of interest
The authors have no conflicts of interest to declare that are relevant to the content of this article.
Additional information
Communicated by S. D Twiss
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Drone video footage paired with acoustic recordings from this study recorded during a large Commerson’s dolphin aggregation which contained broadband signals (MP4 78,397 kb)
Rights and permissions
About this article
Cite this article
Martin, M.J., Torres Ortiz, S., Reyes Reyes, M.V. et al. Commerson’s dolphins (Cephalorhynchus commersonii) can relax acoustic crypsis. Behav Ecol Sociobiol 75, 100 (2021). https://doi.org/10.1007/s00265-021-03035-y
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00265-021-03035-y