You are on page 1of 4

Downloaded from http://rsbl.royalsocietypublishing.

org/ on April 8, 2018

Animal behaviour

Extreme diversity in the songs


rsbl.royalsocietypublishing.org of Spitsbergen’s bowhead whales
K. M. Stafford1, C. Lydersen2, Ø. Wiig3 and K. M. Kovacs2
1
Applied Physics Laboratory, University of Washington, Seattle, WA 98105, USA
Research 2
3
Norwegian Polar Institute, NO-9296 Tromsø, Norway
Natural History Museum, University of Oslo, N-0318 Oslo, Norway
Cite this article: Stafford KM, Lydersen C,
KMS, 0000-0003-0039-5025
Wiig Ø, Kovacs KM. 2018 Extreme diversity in
the songs of Spitsbergen’s bowhead whales. Almost all mammals communicate using sound, but few species produce
Biol. Lett. 14: 20180056. complex songs. Two baleen whales sing complex songs that change
http://dx.doi.org/10.1098/rsbl.2018.0056 annually, though only the humpback whale (Megaptera novaeangliae) has
received much research attention. This study focuses on the other baleen
whale singer, the bowhead whale (Balaena mysticetus). Members of the Spits-
bergen bowhead whale population produced 184 different song types over a
Received: 23 January 2018 3-year period, based on duty-cycled recordings from a site in Fram Strait in
the northeast Atlantic. Distinct song types were recorded over short periods,
Accepted: 12 March 2018
lasting at most some months. This song diversity could be the result of
population expansion, or immigration of animals from other populations
that are no longer isolated from each other by heavy sea ice. However,
this explanation does not account for the within season and annual shifting
Subject Areas: of song types. Other possible explanations for the extraordinary diversity in
behaviour songs could be that it results either from weak selection pressure for inter-
specific identification or for maintenance of song characteristics or,
alternatively, from strong pressure for novelty in a small population.
Keywords:
bowhead whale, Arctic, Balaena mysticetus,
song

1. Background
Complex ‘song’ in mammals is rare. While many mammalian taxa produce
Author for correspondence:
repetitive ‘calls’, sometimes called advertisement songs [1–3], few mammals
K. M. Stafford produce vocal displays akin to bird song, which is defined by multiple frequen-
e-mail: kate2@uw.edu cies and amplitude-modulated elements combined into phrases and organized
in long bouts [4]. Such songs have been documented in only a few mammalian
species, including some bats (Chiroptera), gibbons (Hylobatidae), mice (Scoti-
nomys spp.), rock hyraxes (Procavia capensis), and two great whales, humpback
(Megaptera novaeangliae) and bowhead (Balaena mysticetus) whales [3,5–8].
With the exception of gibbons, in which males and females duet [5], complex
songs in mammals are thought to be produced only by males [6,9–11]. Male
mammals are thought to sing to defend territories, advertise their quality, attract
mates or some combination of these functions [5,11].
The song in baleen whales has been studied extensively only in humpback
whales, which sing similar songs within a season across a whole population.
The structure of that song gradually evolves over the season in unison [12]
and transfer of song types has been documented to occur directionally from
one population to another over a period of years [13]. Humpback whale
songs are composed of a hierarchy from units to sub-phrases to phrases to
themes [12].
Less is known about the songs of bowhead whales compared with hump-
Electronic supplementary material is available back whales, but bowhead whale songs generally consist of a single phrase
that includes amplitude- and frequency-modulated elements repeated in
online at https://dx.doi.org/10.6084/m9.
figshare.c.4035239.
& 2018 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution
License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original
author and source are credited.
Downloaded from http://rsbl.royalsocietypublishing.org/ on April 8, 2018

50 80 2
2013–2014
2012–2013

rsbl.royalsocietypublishing.org
cumulative number of songs
40 2010–2011

no. new songs by month


60

30
40
20

20
10

Biol. Lett. 14: 20180056


0 0
Oct Nov Dec Jan Feb Mar Apr
month
Figure 1. Total numbers of bowhead whale song types recorded in each month (bars) and cumulative number of song types (dashed lines) by year. The greatest
number of different song types occurs in December and January, presumed to be the peak of mating season for bowhead whales.

bouts, with two different sounds often produced simul- study period. Each song type was recorded in only one
taneously [14]. A pilot study from the Fram Strait in 2008 – deployment period.
2009 provided the first indication that tens of song types There was interannual variation in the number and
were produced by bowhead whales in this region within a timing of songs. The fewest songs were recorded in 2010–
single overwinter period [8]. No year-round studies of song 2011 (39 song types total, 895 recordings). Both 2012– 2013
diversity exist for other bowhead whale populations (69 song types total, 1338 recordings) and 2013 –2014 (76
although multiple song types in a single year have been song types total, 998 recordings) had approximately twice
documented for two other populations [15,16]. Herein, we as many different songs (figure 1).
document extremely high inter- and intra-annual diversity While most song types were short-lived—from hours to
in the mammalian song from the Spitsbergen bowhead days—and seldom lasted longer than a month (figure 2),
whale population. every year a few song types persisted throughout the winter.
The overall trend for all years was a progression of song
types appearing and then disappearing over time, with the
2. Material and methods greatest within-year diversity occurring in January for all
Omni-directional hydrophone recorders were deployed and 3 years examined.
redeployed annually from 2010 to 2014 in September on a Of the 3231 recordings containing songs over the 3 years,
long-term oceanographic mooring in western Fram Strait, at slightly over half (53%) contained only a single song type,
about 78849 N, 58 W (electronic supplementary material, figure while two different songs occurred in 37% of the recording
S1). The mooring deployed in 2011 was not recovered. Instru-
periods. Less than 10% of all recordings contained more
ments recorded acoustic data for the first 14 – 17 min h21
than two different song types.
throughout the year. Upon recovery, the data were downloaded
and spectrograms (10– 4000 Hz, 2048 point FFT, 50% overlap,
Hann window) were created for each data file. Spectrograms
were then reviewed visually for the presence of bowhead
whale songs that were classified by eye based on time-frequency 4. Discussion
characteristics of each song type [17]. Files with ‘loud’ songs The diversity and interannual variability in songs of bow-
( possessing distinct units, song bandwidth exceeding 500 Hz) head whales in this 3-year study are rivalled only by a few
were analysed further to determine the unit structure and song species of songbirds [4]. Among other mammalian singers,
composition. Individual songs were assigned a unique number mice and gibbons tend to produce highly stereotyped and
if more than one iteration occurred (e.g. Fram2012-11 was the repetitive songs with few elements (e.g. [3,5]). Variation in
11th song recorded in the 2012 – 2013 season while Fram2012-
rock hyrax and bat songs is primarily through changes in
54 was the 54th; electronic supplementary material, S1 – S4).
the arrangement of units [6,11]. Humpback whales produce
Each song type was characterized by frequency, duration and
amplitude and/or frequency modulation, number of units complex songs that are similar within a year [7,12,13].
and phrases and compared to all other song types within and Although the repertoire of any one individual bowhead
between years to determine the minimum number of different whale in this study cannot be determined, the catalogue of
song types detected and to describe the diversity of songs in song types (184) is remarkably varied.
this species at this location. It is not known whether individual bowhead whales sing
multiple song types in a season, but some are known to
share the same song type in the same period in the Bering–
3. Results Chukchi–Beaufort (BCB) population [14,16]. Nor is it known
Bowhead whale songs were detected 24 h per day through- if individual bowhead whales maintain the same song
out most of the winter every year (electronic supplementary throughout their lifetime or if they switch within and/or
material, figure S2). The greatest number of different song between years.
types was recorded in December and January (figure 1). A One explanation for the very high song diversity in the
total of 184 different song types were recorded in the 3-year Spitsbergen bowhead whale population could be that the
Downloaded from http://rsbl.royalsocietypublishing.org/ on April 8, 2018

(a) (b) (c) 3


2013.76
2012.75
2013.74

rsbl.royalsocietypublishing.org
2013.73
2013.72
2012.69 2013.71
2012.68 2013.70
Apr 2012.67
2012.66
2013.69
2013.68
2012.65 2013.67
Mar 2012.64 2013.66
2012.63 2012.65
2012.62 2013.64
Feb 2012.61 2013.63
2012.60 2013.62
Jan 2012.59
2012.58
2013.61
2013.60
2012.57 2013.59
Dec 2012.56 2013.58
2012.55 2013.57
2012.54 2013.56
Nov 2012.53 2013.55
2012.52 2013.54
Oct 2012.51 2013.53
2013.52
2012.50
2012.49 2013.51
2012.48 2013.50
2012.47 2013.49
2012.46 2013.48
2013.47
2012.45 2013.46
2012.44 2013.45

song type number


2012.43

Biol. Lett. 14: 20180056


2013.44
2012.42 2013.43
2012.41 2013.42
song type number

song type number


2012.40 2013.41
2010.39 2012.39 2013.40
2010.38 2012.38 2013.39
2010.37 2012.37 2013.38
2010.36 2012.36 2013.37
2010.35 2012.35 2013.36
2010.34 2012.34 2013.35
2010.33 2012.33 2013.34
2010.32 2012.32 2013.33
2010.31 2012.31 2013.32
2010.30 2012.30 2013.31
2010.29 2012.29 2013.30
2010.28 2012.28 2013.29
2010.27 2012.27 2013.28
2010.26 2012.26 2013.27
2010.25 2012.25 2013.26
2010.24 2012.24 2013.25
2010.23 2012.23 2013.24
2010.22 2012.22 2013.23
2010.21 2012.21 2013.22
2013.21
2010.20 2012.20 2013.20
2010.19 2012.19 2013.19
2010.18 2012.18 2013.18
2010.17 2012.17 2013.17
2010.16 2012.16 2013.16
2010.15 2012.15 2013.15
2010.14 2012.14 2013.14
2010.13 2012.13 2013.13
2010.12 2012.12 2013.12
2010.11 2012.11 2013.11
2010.10 2012.10 2013.10
2010.9 2012.9 2013.9
2010.8 2012.8 2013.8
2010.7 2012.7 2013.7
2010.6 2012.6 2013.6
2010.5 2012.5 2013.5
2010.4 2012.4 2013.4
2010.3 2012.3 2013.3
2010.2 2012.2 2013.2
2010.1 2012.1 2013.1
0 100 200 300 400 500 600 700 800 0 50 100 150 200 250 300 350 400 0 20 40 60 80 100 120
no. hours with each song by month no. hours with each song by month no. hours with each song by month

Figure 2. Total number of hours and months during which each song type was recorded by year. In most cases, a song type was only recorded in one month,
though in some instances the same song type was recorded in two to four different months. (a) 2010 – 2011: 38 song types were recorded; (b) 2012 – 2013: 69 song
types were recorded; (c) 2013– 2014: 76 song types were recorded.

animals occupying this area in modern times include immi- population over the other. For example, humpback whales
grants from both the BCB and the eastern Canada–western have relatively small testes, and engage in physical compe-
Greenland bowhead populations. Until recently, these popu- tition as well as producing complex song displays, while
lations have been assumed to be isolated from each other due right whales (Eubalaena spp.) have enormous testes, are
to extensive, impenetrable sea ice cover in the High Arctic. drawn to ‘surface active groups’ by a vocalizing female,
However, in the past few decades, extreme declines in sea and lack any apparent male acoustic display [27–29].
ice extent and thickness may have facilitated contact between However, bowhead whales have both large testes and large
these populations [18]. However, even if this region contains vocal repertoires [30].
bowhead whales from multiple populations, this does not Bowhead whales are the only High Arctic resident baleen
fully explain the high numbers of different song types whale. Thus, interspecific identification via song may not
recorded in this study or the lack of recurrence of song confer the same selective advantage for bowheads that it
types from year to year. might for other cetacean species. This could reduce selection
It is plausible that the bowhead whales in the Fram Strait pressure on song stereotypy, allowing for greater variation in
are simply a remnant of the original Spitsbergen population song types as a result of a long-term cultural mutation in
that survived the extreme historical levels of exploitation songs, or song novelty itself might confer an advantage
[19]. The influence of small population size on song diversity [4,20,22,23].
is conflicted; some studies suggest song diversity increases Because bowhead whales sing underwater, in heavy ice
in smaller populations, although others have found that during the polar night, a nuanced understanding of the vari-
reduced or isolated populations exhibit a reduction in song able syntax of this species will be difficult to obtain.
diversity and produce simpler songs [20,21]. Nevertheless, the singing behaviour of Spitsbergen bowhead
In some species, females appear to prefer a diverse song whales, in which tens of distinct song types are produced
repertoire [22 –25], suggesting that increased complexity of annually, makes them remarkable among mammals.
singing might confer reproductive advantages. A recent
study of howler monkeys (Alouatta spp.) documented trade- Data accessibility. Exemplar song files are deposited in Dryad Digital
offs in male reproductive characteristics based on (temporary) Repository (doi:10.5061/dryad.1ck400f ) [31].
social structure: in groups with fewer males, or smaller social Authors’ contributions. All authors collected the data and conceived the
idea for analysis. K.M.S. analysed the data. All authors contributed
groups, males invested more in vocal displays as a reproduc- to interpreting the results, writing the manuscript and agree to its
tive tactic [26]. Normally, testes size and vocal repertoire (or publication. All authors are accountable for all aspects of the work.
other reproductive displays) are considered evolutionary Competing interests. We have no competing interests.
trade-offs: depending upon social context, one of these may Funding. This work was funded by NPI, The Svalbard Environmental
provide a selective advantage for individuals within a Protection Fund, Svalbard Science Forum, the Fram Centre
Downloaded from http://rsbl.royalsocietypublishing.org/ on April 8, 2018

Incentive Fund and the Norwegian Research Council (grant no. Acknowledgements. Kristen Fossan serviced the Fram Strait hydrophone 4
244488/E10). annually.

rsbl.royalsocietypublishing.org
References
1. Clutton-Brock TH, Albon SD. 1979 The roaring of red classification issues. Mar. Mamm. Sci. 29, populations. PLoS ONE 3, e1822. (doi:10.1371/
deer and the evolution of honest advertisement. E312 –E332. (doi:10.1111/mms.12005) journal.pone.0001822)
Behaviour 69, 145–170. (doi:10.1163/ 13. Garland EC, Goldizen AW, Rekdahl ML, Constantine 22. Byers BE, Kroodsma DE. 2009 Female mate choice
156853979X00449) R, Garrigue C, Hauser ND, Poole MM, Robbins J, and songbird song repertoires. Anim. Behav. 77,
2. Watkins W. 1981 Activities and underwater sounds of Noad MJ. 2011 Dynamic horizontal cultural 13– 22. (doi:10.1016/j.anbehav.2008.10.003)

Biol. Lett. 14: 20180056


fin whales. Sci. Rep. Whales Res. Inst. 33, 83 –117. transmission of humpback whale song at the ocean 23. Chabout J, Sarkar A, Dunson DB, Jarvis ED. 2015
3. Miller JR, Engstrom MD. 2007 Vocal stereotypy and basin scale. Curr. Biol. 21, 687– 691. (doi:10.1016/ Male mice song syntax depends on social contexts
singing behavior in Baiomyine mice. J. Mammal. j.cub.2011.03.019) and influences female preferences. Front. Behav.
88, 1447 –1465. (doi:10.1644/06-MAMM-A-386R.1) 14. Würsig B, Clark CW. 1993 Behavior. In The bowhead Neurosci. 9, 1 –16. (doi:10.3389/fnbeh.2015.00076)
4. Kroodsma DE. 2004 The diversity and plasticity of whale (eds JJ Burns, JJ Montague, CJ Cowles), 24. Sullivan B, Hinshaw S. 1992 Female choice and
birdsong. In Nature’s music: the science of birdsong pp. 157–199. Special Publication Number 2, selection on male calling behaviour in the grey
(eds P Marler, H Slabbekoorn), pp. 108–131. The Society for Marine Mammalogy. Lawrence, KS: treefrog Hyla versicolor. Anim. Behav. 44, 733 –744.
Amsterdam, The Netherlands: Elsevier. Allen Press. (doi:10.1016/S0003-3472(05)80299-4)
5. Cowlishaw G. 1992 Song function in gibbons. 15. Stafford KM, Moore SE, Laidre KL, Heide-Jørgensen 25. Pasteau M, Nagle L, Kreutzer M. 2004 Preferences
Behaviour 121, 131– 153. (doi:10.1163/ MP. 2008 Bowhead whale springtime song off West and predispositions for intra-syllabic diversity in
156853992X00471) Greenland. J. Acoust. Soc. Am. 124, 3315–3323. female canaries (Serinus canaria). Behaviour 141,
6. Kershenbaum A, Ilany A, Blaustein L, Geffen E. 2012 (doi:10.1121/1.2980443) 571–583. (doi:10.1163/1568539041166735)
Syntactic structure and geographical dialects in the 16. Johnson HD, Stafford KM, George JC, Ambrose Jr 26. Dunn JC, Halenar LB, Davies TG, Cristobal-Azkarate
songs of male rock hyraxes. Proc. R. Soc. B 279, WG, Clark CW. 2014 Song sharing and diversity in J, Reby D, Sykes D, Dengg S, Fitch WT, Knapp LA.
2974–2981. (doi:10.1098/rspb.2012.0322) the Bering-Chukchi-Beaufort population of bowhead 2015 Evolutionary trade-off between vocal tract and
7. Payne RS, McVay S. 1971 Songs of humpback whales (Balaena mysticetus), spring 2011. Mar. testes dimensions in howler monkeys. Curr. Biol. 25,
whales. Sci. New Ser. 173, 585– 597. (doi:10.1126/ Mamm. Sci. 31, 902– 922. (doi:10.1111/mms. 1–7. (doi:10.1016/j.cub.2014.10.064)
science.173.3997.585) 12196) 27. Brownell Jr RL, Ralls K. 1986 Potential for sperm
8. Stafford KM, Moore SE, Berchok CL, Wiig Ø, 17. Kershenbaum A et al. 2014 Acoustic sequences competition in baleen whales. Rep. Int. Whal.
Lydersen C, Hansen E, Kalmbach D, Kovacs KM. in non-human animals: a tutorial review and Commn. Spec. Iss. 8, 97 –112.
2012 Spitsbergen’s endangered bowhead whales prospectus. Biol. Rev. 91, 13– 52. (doi:10.1111/ 28. Tyack P, Whitehead H. 1982 Male competition
sing through the polar night. Endang. Species Res. brv.12160) in large groups of wintering humpback whales.
18, 95 –103. (doi:10.3354/esr00444) 18. Heide-Jørgensen MP, Laidre KL, Quakenbush LT, Behaviour 83, 132–154. (doi:10.1163/
9. Winn HE, Winn LK. 1978 The song of the humpback Citta JJ. 2012 The Northwest Passage opens for 156853982X00067)
whale Megaptera novaeangliae in the West bowhead whales. Biol. Lett. 8, 270–273. (doi:10. 29. Parks SE. 2003 Response of North Atlantic right
Indies. Mar. Biol. 47, 97 –114. (doi:10.1007/ 1098/rsbl.2011.0731) whales (Eubalaena glacialis) to playback of calls
BF00395631) 19. Vacquié-Garcia J, Lydersen C, Marques TA, Aars J, recorded from surface active groups in both the
10. Davidson SM, Wilkinson GS. 2004 Function of male Ahonen H, Skern-Mauritzen M, Øien N, Kovacs KM. North and South Atlantic. Mar. Mamm. Sci. 19,
song in the greater white-lined bat, Saccopteryx 2017 Late summer distribution and abundance of 563–580. (doi:10.1111/j.1748-7692.2003.
bilineata. Anim. Behav. 67, 883–891. (doi:10.1016/ ice-associated whales in the Norwegian High Arctic. tb01321.x)
j.anbehav.2003.06.016) Endang. Species Res. 32, 59 –70. (doi:10.3354/ 30. Haldiman JT, Tarpley RJ. 1993 Anatomy and
11. Bohn KM, Schmidt-French B, Schwartz C, esr00791) physiology. In The bowhead whale (eds JJ Burns,
Smotherman M, Pollak GD. 2009 Versatility and 20. Hamao S, Ueda K. 2000 Simplified song in an island JJ Montague, CJ Cowles), pp. 71 –156. The Society
stereotypy of free-tailed bat songs. PLoS ONE 4, population of the bush warbler Cettia diphone. for Marine Mammalogy. Lawrence, KS: Allen Press.
e6746. (doi:10.1371/journal.pone.0006746) J. Ethology 18, 53 –57. (doi:10.1007/ 31. Stafford KM, Lydersen C, Wiig Ø, Kovacs KM. 2018
12. Cholewiak DM, Sousa-Lima RS, Cerchio S. 2012 s101640070025) Data from: Extreme diversity in the songs of
Humpback whale song hierarchical structure: 21. Laiolo P, Vögeli M, Serrano D, Tella JL. 2008 Song Spitsbergen’s bowhead whales. Dryad Digital
historical context and discussion of current diversity predicts the viability of fragmented bird Repository. (doi:10.5061/dryad.1ck400f )

You might also like