Fin whale song evolution in the North Atlantic

  1. Miriam Romagosa
  2. Sharon Nieukirk
  3. Irma Cascão
  4. Tiago A Marques
  5. Robert Dziak
  6. Jean-Yves Royer
  7. Joanne O'Brien
  8. David K Mellinger
  9. Andreia Pereira
  10. Arantza Ugalde
  11. Elena Papale
  12. Sofia Aniceto
  13. Giuseppa Buscaino
  14. Marianne Rasmussen
  15. Luis Matias
  16. Rui Prieto
  17. Mónica A Silva

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    This study is a valuable contribution to our understanding of vocal variation in acoustic displays of male baleen whales, part of a developing story about cultural change in songs in species other than the relatively well studied humpback whales. The authors present solid evidence of changes at various timescales in 20-Hz song note intervals and call center frequency over decadal time scales and large spatial scales.

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Abstract

Animal songs can change within and between populations as the result of different evolutionary processes. When these processes include cultural transmission, the social learning of information or behaviours from conspecifics, songs can undergo rapid evolutions because cultural novelties can emerge more frequently than genetic mutations. Understanding these song variations over large temporal and spatial scales can provide insights into the patterns, drivers and limits of song evolution that can ultimately inform on the species’ capacity to adapt to rapidly changing acoustic environments. Here, we analysed changes in fin whale ( Balaenoptera physalus ) songs recorded over two decades across the central and eastern North Atlantic Ocean. We document a rapid replacement of song INIs (inter-note intervals) over just four singing seasons, that co-occurred with hybrid songs (with both INIs), and a clear geographic gradient in the occurrence of different song INIs during the transition period. We also found gradual changes in INIs and note frequencies over more than a decade with fin whales adopting song changes. These results provide evidence of vocal learning in fin whales and reveal patterns of song evolution that raise questions on the limits of song variation in this species.

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  1. Version published to 10.7554/elife.83750 on eLife
  2. eLife

    eLife assessment

    This study is a valuable contribution to our understanding of vocal variation in acoustic displays of male baleen whales, part of a developing story about cultural change in songs in species other than the relatively well studied humpback whales. The authors present solid evidence of changes at various timescales in 20-Hz song note intervals and call center frequency over decadal time scales and large spatial scales.

  3. eLife

    Reviewer #1 (Public Review):

    Romagosa, Nieukirk et al. present an interesting approach and interpretation to what is assumed to be a learned animal behavior. In this case, the observed behavior is fin whale (Balaenoptera physalus) singing and the analyses provide results indicating spatio-temporal variation in three fin whale song features at distinct locations within the Central and Northeast North Atlantic Ocean (ONA) region within a two-decade time period. The data set is a non-standardized collection of acoustic recordings obtained from multiple research scientists. Most of the acoustic recording samples are very sparse, with the majority of data coming from an area around the Azores and collected by Okeanos scientists. The senior author undertook the enormously demanding task of analyzing the acoustic data using non-automatic, standardized techniques and protocols. Songs from individual periods of singing on any given day were selected for analysis based on song quality. Song measurements included interval of time between successive 20-Hz song notes (INI), peak frequencies of those 20-Hz notes and peak frequencies of higher frequency notes (HF note). The resultant units of analysis are daily measures of INI (average and s.d.), 20-Hz note peak frequencies (average and s.d.), and HF note peak frequencies (average and s.d.). Several of the figures are confused by not representing the time axis in a typical, uniformly linear way (Fig. 2A and Fig. 3). This form of dynamic time warping smooths and distorts the time-varying features of the results and obscures the inherent sparseness of and high variability in the durations and locations of recordings in available data set. This fundamental characteristic of the available data (see Fig. S1), represents a form of sample aliasing, is not adequately addressed in the paper in terms of how it influences or restricts interpretation of the results. Another possible over-interpretation of results involves misrepresentation of the actual areas sampled. For example, data were collected on Dec 2007-Feb 2008 and Oct 2015 March from a recorder location off the southwest of the Iberian Peninsula. The acoustic sampling detection space is restricted to the ocean within some tens of kilometers of a single sensor, a very small dot on the maps in the manuscript, yet the data from this recorder are assigned to the relatively very large region referred to as the "Bay of Biscay & Iberian Coast". Within the two-decade period of the study (ca. 120 months), recordings were collected at this site (E in Figure 1) for 9 months (7.5%), and the two sampling periods occurred within the December 2007 through March 2018 time span (see Fig S1). It is scientifically inappropriate to translate this as data representing the Bay of Biscay & Iberian Coast as this kind of misrepresentation can lead to misinterpretation of the results.

    Despite these spatial and temporal sampling issues, the analyses reveal several important features (Fig. 2 and Fig. 3) about fin whale song in the ONA. The import of the analytical results is that the time span and spatial scale over which recordings were collected provide a unique opportunity to observe whether or not there were variations in fin whale song features within a large ocean region, across a span of two decades. One can consider these spatial and temporal scales appropriately matched to the known scales of fin whale natural history and ecology. Thus, the study results, although confronted by some sampling issues, are not biased by inappropriately sized spatial and temporal scales.

    This MS joins a small but growing list of papers documenting variability in baleen whale acoustic behaviors over ecologically appropriate spatial and temporal scales. These papers are primarily focused on singing, an acoustically obvious male reproductive display. As with several recent papers, the author takes advantage of a growing body of data collected during previous studies. The actual measurements utilized several established acoustic analysis software tools. The interpretation of the results focuses on evidence of vocal learning in fin whale singers (i.e. males performing reproductive displays) and wisely remains tangential to interpreting fin whale song through a cultural lens.

  4. eLife

    Reviewer #2 (Public Review):

    This research brings togethor an impressively long timescale dataset of fin whale song vocalisations in the North Atlantic, measuring the note frequency content and inter-note intervals and thereby tracking shifts in both over time. Different time periods are covered in different regions of the north Atlantic during the course of the study. There are two principal results - the study documents a shift in the inter-note interval (INI) in an ICES eco-region termed 'Oceanic Northeast Atlantic' (although the relevance of this to fin whale populations is unclear) occuring relatively rapidly in the years 2000-2001. This shift is discontuous and appears to show an abrupt change in note intervals in most (though not all) of the songs recorded. The second key result is that this INI measure and also the peak frequency of song element termed the 'HF note' both show consistent directional change over timescales of 12 years. The INI measure begins to change back toward the value it held prior to the 2000/2001 shift, suggestive of a cyclical process of change coupled with resets. The average HF note peak frequency descended by about 5Hz during the study period but there was no evidence of abrupt shifts.

    The research significance is largely in the description of these processes in a new area, similar changes in rorqual song have been examined in the Southern Ocean and Mediterranean, and the argued interpretation of these changes as evidence for cultural learning processes in song change - the debate over whether these changes have environmental causation or are due to learning processes similar to song change in humpbacks is ongoing and this study therefore contributes interesting evidence from a newly covered population.

    I think the methods and analyses broadly support the claims but also that there are weaknesses in interpretation and presentation that should be addressed. I think perhaps the degree to which this is evidence of vocal learning may be a bit overplayed. Definitely there is change, but it is tricky to compare this to e.g. experimental demonstrations. For example, age-related changes in a changing post-whaling demographic scenario should at least be considered? Is there also any possibility for large-scale oceanographic variations to be included in some way - temperature shifts, for example? This could help understand the different roles of environment and learning in these processes. I think it is also important that these results be placed in a more detailed context of current knowledge of fin whale population structure in the north Atlantic - could population range shifts be a factor? The INI data show an interesting variation in the recordings from the Barents Sea and this could be discussed in the light of population structure knowledge also. It is unclear from the presentation whether the INI shift in 2000/2001 was coupled with any frequency shifts - if not, it suggests different trajectories and processes affecting these two aspects of the acoustic display.

    I am not convinced the main story here is about conformity, and I think it would be a mistake to too easily reach for the humpback comparison but there are certainly questions to be asked about the 2000/2001 shift in terms of the processes that led to it.

  5. eLife

    Reviewer #3 (Public Review):

    The authors used passive acoustic monitoring over a vast range of the North Atlantic to study the call rates of fin whales. They found a 'take over' of a new rythm (inter call intervals) during their study period. This was interpreted as a change in song production.

    I am not completely convinced the authors are correct in describing this change in rate as a change in the song. Even though fin whale calls are evidently a male mating ground display, little is known about its function. Compared to humpback whales with their impressive repertoire of vocalizations, repeating themselves on the breeding grounds after some tens of minutes and therefore qualifying as a very slow 'song' similar to bird song, fin whale only emit a single type of call, which is remaining the same throughout the study period. It can be contested, I would assume, that a ,erely change the repetition rate of calls, even though seemingly done here in an 'overtake' fasion, can qualify as a change and learning of song,

  6. Version published to 10.1101/2022.10.05.510968v1 on bioRxiv
  7. Version published to 10.1101/2022.10.05.510968v2 on bioRxiv