Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71(S4): e57281, diciembre 2023 (Publicado Nov. 01, 2023)

First song description of the humpback whales, Megaptera novaeangliae

(Balaenopteridae: Artiodactyla), breeding off Nicaragua

Joelle De Weerdt1, 2*; https://orcid.org/0000-0003-4054-6609

Divna Djokic3, 4; https://orcid.org/0000-0002-6454-255X

Renata S. Sousa-Lima3, 4; https://orcid.org/0000-0002-2638-1695

Federica Pace5; https://orcid.org/0000-0001-8788-5427

1. Association ELI-S, Education, Liberté, Indépendance - Scientifique, Allée de Verdalle 39, 33470 Gujan-Mestras,

France; eliscientific@gmail.com (Correspondance*)

2. Marine Biology, Ecology and Biodiversity, Vrije Universiteit Brussel (VUB), Pleinlaan 2, 1050 Brussels, Belgium

3. Graduate Program of Psychobiology and Behavior, Biosciences Center, Universidade Federal do Rio Grande do Norte,

Natal, Rio Grande do Norte, Brazil, divna.divna@yahoo.com

4. Laboratory of Bioacoustics, Department of Physiology and Behavior, Biosciences Centre, Universidade Federal do Rio

Grande do Norte, Natal, Rio Grande do Norte, Brazil, sousalima.renata@gmail.com

5. JASCO Applied Sciences (Deutschland) GmbH., Schwentinental, Germany; federica.pace@jasco.com

Received 02-VIII-2022. Corrected 04-IV-2023. Accepted 07-VI-2023.

ABSTRACT

Introduction: Humpback whales belonging to the Central American (CA) Distinct Population Segment breed off

the Pacific coast of Nicaragua. Knowledge on this endangered population and its conservation status is limited.

Objective: The aim of this study is to provide the first description of the CA humpback whale song off Nicaragua,

which helps further understanding on the population’s dynamics.

Methods: Acoustic recordings of songs were obtained during dedicated boat-based surveys at two locations on

the Pacific coast of Nicaragua in 2018. Recordings were made from the boat using a portable system for a total

of 23 hours and 56 minutes over 32 days from January to April 2018. A total of nine recordings of high enough

quality for the song analysis were identified during this period from three different days at Padre Ramos (PR)

(northern site) and four different days at San Juan del Sur (southern site). Song structure was described using

standard humpback whale song elements, i.e. themes, phrases, and units.

Results: A total of seven themes, seven phrases, and 19 unit types were identified. Three of the themes were

common and frequently repeated in a song cycle while the others were less common in the repertoire and were

recorded only during the middle of the season. Song theme order was variable, both within and across song

sessions.

Conclusions: This study provides the first song description of humpback whales along the Pacific coast of

Nicaragua. Comparison of these songs with other datasets from the CA population and other breeding areas in

the Northern Hemisphere could help understand the migratory patterns of these animals and the level of con-

nectivity among populations since song can be socially learnt. Future data collection of humpback whale song

recordings in Nicaragua is necessary to gain further understanding on the song structure variation within this

population and the mechanisms of song transmission and dynamics across populations in the region.

Key words: Acoustics; Central America; Song structure; North Pacific; Reproduction.

https://doi.org/10.15517/rev.biol.trop..v71iS4.57281

SUPPLEMENT • WHALES

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71(S4): e57281, diciembre 2023 (Publicado Nov. 01, 2023)

INTRODUCTION

The humpback whale, Megaptera novaean-

gliae (Borowski, 1781) is known for its seasonal

migration between breeding and feeding areas.

There are 14 recognized Distinct Population

Segments (DPS), of which seven located in the

North Pacific, and amongst which the Central

America DPS (Bettridge et al., 2015), the focus

of this study. The Central America whales (here-

after CA whales) migrate to Central America

between January and April, from their feeding

areas on the West coast of the United States

(Calambokidis et al., 1997; Calambokidis et al.,

2000; De Weerdt et al., 2022). The waters off

Nicaragua are considered important breeding

habitats for CA whales with Padre Ramos being

used mainly by mother-calf pairs, and San Juan

del Sur mainly by adult whales (De Weerdt et

al., 2022). CA whales are listed as endangered

according to the National Marine Fisheries Ser-

vice (NMFS) and little information is available

on their ecology (Bettridge et al., 2015).

Humpback whale males produce structured

and complex songs (Payne & McVay, 1971), and

while singing activity occurs extensively during

the breeding season, it has also been described

along migration corridors and on feeding areas

(Kowarski et al., 2022; McSweeney et al., 1989;

Schall et al., 2022). Humpback whale songs are

used as a parameter to study individual move-

ments and population dynamics (Cerchio et

al., 2001; Cholewiak & Cerchio, 2022; Darling,

Goodwin, et al., 2019; Darling & Sousa-Lima,

2005). Males from the same population con-

form to similar songs, which evolve through the

season. This evolution partially happens by the

error accumulation of singers. Accumulation of

changes, the sharing of such changes and cul-

ture are determined by the social interactions

between singers (Garland et al., 2022).

Because only males are known to sing

(Cholewiak & Cerchio, 2022; Darling & Bérubé,

2001; Darling et al., 1983), their songs are

thought to be a male precopulatory display

RESUMEN

Primera descripción del canto de las ballenas jorobadas, Megaptera novaeangliae

(Balaenopteridae: Artiodactyla) que se reproducen en Nicaragua

Introducción: La ballena jorobada del segmento poblacional Centroamericano se reproduce en la costa Pacífica

de Nicaragua. El conocimiento sobre la biología y estado de conservación de esta población amenazada y su

estado de conservación es limitado.

Objetivo: El objetivo de este estudio es generar la primera descripción del canto de las ballenas jorobadas de la

población de Centroamérica observadas en aguas nicaragüenses.

Métodos: Se obtuvieron grabaciones acústicas durante salidas de investigación en dos localidades de la costa

Pacífica de Nicaragua en el 2018. Las grabaciones se realizaron desde el bote utilizando un sistema portátil

durante un total de 23 horas y 56 minutos en 32 días de enero hasta abril del 2018. Un total de nueve grabaciones

de suficiente calidad para el análisis de los cantos fueron identificados durante este periodo en tres días en Padre

Ramos (Norte) y cuatro días en San Juan del Sur (Sur). La estructura del canto se describió de acuerdo con los

elementos estándares de canciones de ballenas jorobadas: temas, frases y unidades.

Resultados: Se identificaron siete temas, siete frases y 19 unidades. Tres temas eran comunes y se repetían varias

veces dentro de una canción mientras que otras eran menos comunes en el repertorio de canto y se grabaron solo

en la mitad de la temporada. El orden de los temas en la canción fue variable a dentro de la canción y entre las

sesiones de canto.

Conclusiones: Este estudio representa la primera descripción del canto de las ballenas jorobadas en el Pacifico

nicaragüense. La comparación de estos cantos con los de otras localidades de la población de Centroamérica y con

otras áreas de reproducción de poblaciones en el hemisferio norte contribuirá a comprender mejor los patrones

migratorios de estos animales y el nivel de conectividad entre poblaciones desde que la canción fue aprendida. La

recolección futura de datos de cantos de ballenas jorobadas en Nicaragua es necesaria para mejorar la compren-

sión de la variación en la estructura del canto de esta población y el mecanismo de transmisión y dinámica de

canto entre poblaciones de la región.

Palabras clave: Acústica; Centroamérica; Estructura de canción; Pacifico Norte; Reproducción.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71(S4): e57281, diciembre 2023 (Publicado Nov. 01, 2023)

(Dines et al., 2015) used to attract females

and/or mediate male-male interactions (Her-

man, 2017; Smith et al., 2008; Tyack & Clark,

2000). Humpback whale songs are tradition-

ally classified into themes, phrases, and units,

allowing comparisons of song elements across

geographical regions (Darling & Sousa-Lima,

2005; Payne & Payne, 1985; Payne et al., 1983)

and between populations (Cholewiak & Cer-

chio, 2022; Garland et al., 2011; Schall et al.,

2022). Within a breeding season, the song can

vary, however, males eventually conform to

the same song for their population (Herman,

2017). Songs sung by humpback whales under-

go both an evolutionary and a revolutionary

process (Owen et al., 2019). The evolutionary

process consists of song modification over time

by accumulation of small changes resulting in a

progressive change (Cerchio et al., 2001; Gar-

land et al., 2011), while revolution, or cultural

diffusion, is a rapid change whereby a novel

song appears and is adopted by the popula-

tion (Noad et al., 2000). A song can therefore

change within and between seasons in any

given population.

Humpback whale song studies can provide

valuable insights on population connectivity

and function (Garland et al., 2011; Garland et

al., 2022; Garland, Gedamke, et al., 2013).

Understanding changes in humpback whale

songs within and between seasons can help

understand migratory routes, by comparing

songs between regions. Furthermore, studying

song composition within and between seasons

can provide insights on the cultural transmis-

sion that occurs in different humpback whale

populations (Darling, Acebes, et al., 2019; Gar-

land et al., 2015; Zandberg et al., 2021). Pres-

ently, there is only one study describing songs

of CA humpbacks at their breeding ground in

2016-2017 off Caño Island, Costa Rica (Chere-

skin et al., 2019). This present study provides

additional information on the song of CA

whales breeding in Central America; until now

no description of song is available for animals

breeding in Nicaraguan waters. Recent work

comparing phrase compositions of humpback

whale songs sung between 2011 and 2013 in

Mexico, Hawaii, the Philippines and Japan

showed that mixing of population throughout

the North Pacific occurs (Darling, Acebes, et

al., 2019).

Boat based surveys took place between

January and April 2018 on two study sites along

the Nicaraguan Pacific coast: Padre Ramos,

northern Nicaragua and San Juan del Sur,

southern Nicaragua. During the surveys, an

omni-directional hydrophone (H2a Aquarian)

connected to a recorder (Tascam DR-05V2)

was deployed to determine presence/absence

of singers every 30 minutes. Whenever a singer

was detected, and if their song was audible

above the background noise, a recording was

made at a sampling rate of 92 kHz and 24 bits

resolution for as long as the song was detectable.

A total of 108 recordings (San Juan del Sur,

n = 66; Padre Ramos, n = 42) were made in

32 days of boat survey effort during the 2018

breeding season. Any recordings with multiple

audible singers and/or with low signal-to-noise

ratio (SNR) were excluded from further analy-

ses. SNR was estimated by measuring NIST

Quick Signal-to-Noise ratio (Sostres Alonso &

Nuuttila, 2015) for each labeled unit in every

recording (RAVEN 1.5; (K. Lisa Yang Center

for Conservation Bioacoustics at the Cornell

Lab of Ornithology, 2022)). Recordings that

captured at least 10 minutes of a song were

selected for the analysis as humpback whale

songs are known to last on average 10-15

minutes (Cerchio et al., 2001). An additional

criterion was that the SNR of the recordings

had to be 14 dB or above. We considered a

humpback whale song as a continuous record-

ing containing at least one performance of

each theme in that moment of the season (as it

happens that themes are added or lost within

the season) (Cholewiak et al., 2013). Songs

recorded on different days were considered as

samples of distinct individuals (Warren et al.,

2020), while recordings from the same day

were assumed to be from the same individual.

Each analyzed recording contained either a

song or a song fragment (i.e., part of a song

composed of a stereotyped series of vocaliza-

tions, repeated at least once), as described in

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71(S4): e57281, diciembre 2023 (Publicado Nov. 01, 2023)

Kowarski et al. (2019). Whether songs were

incomplete because the animal moved away,

stopped singing or did not perform the full

song, could not be determined due to the logis-

tical constraints of the setup (e.g. boat drifting

substantially from original location). Only nine

recordings were above 10 minutes in length and

met our SNR criterion. The selected recordings

totaled 3 hours and 30 minutes for the analy-

sis. These recordings were collected on three

different days at PR and four different days at

SJDS; therefore, based on the assumption that

each day represents a new singer, an estimated

number of seven singers were recorded (Fig. 1).

Songs were manually analyzed in RAVEN

Pro by generating spectrograms, with a Fast

Fourier Transform (FTT) of 1 024 points reso-

lution, and a Hanning window (50 % overlap),

corresponding to frequency resolution of 43.1

Hz. Finer frequency resolution (2 Hz) was used

for the graphical representations presented in

this study. Following the method of Cholewiak

et al. (2013), songs were classified into themes,

phrases, and units. For the unit classification,

the following acoustic variables were consid-

ered: fundamental frequency contour, tonal

quality type (e.g. tonal or pulsed), duration

(delta time), peak, low, high, and delta fre-

quency (Malige et al., 2020). Each unit type was

assigned a unique letter (Green et al., 2011).

To test the consistency of the manual unit clas-

sification, a Random Forest Analysis (RFA) was

applied on the measured variables of the units:

low, high, Delta and peak frequencies and the

duration (Delta time). A Random Forest model

is a machine learning algorithm that combines

multiple decision trees using “bagging” to cre-

ate a final classification that averages all the

decisions. The Out Of Bag (OOB) score is a

way to validate a Random Forest model (Hastie

et al., 2009).

Phrases were assigned only after reviewing

multiple recordings to ensure consistency. The

guidelines described in Cholewiak et al. (2013)

were followed for the identification of phras-

es within the recordings. Transitional phrases

were also identified and marked as such. How-

ever, these are not included in the results to

clearly indicate the song sequence. Finally,

themes were identified and assigned a unique

color (Cholewiak et al., 2013), based on the

phrase delimitations and sequence. A total of 19

unit types were identified based on the manual

classification. The RFA of 1500 trees tested the

manual classification of units and gave an OOB

error rate of 31 %, showing duration and peak

frequency as the most important measurable

variables for unit classification. This OOB value

indicates that manual classification was robust

and reliable throughout the dataset. All unit

types were shared on both Nicaraguan sites.

The CA male whales in Nicaragua sang

songs made of seven themes represented by

different colors in Fig. 1. The themes repre-

sented by the colors light and dark green are

constituted of the repetition of phrases 4 or 3,

respectively. These phrases differed by just one

unit (j vs. n). However, since they were sung

consistently separately, they were considered

as unique themes (Fig. 1). The red and purple

themes are made up of the repetition of phrases

1 and 2 respectively. These phrases share a com-

mon subphrase made of units a and b at the

beginning of the phrase. At the start of the sea-

son, almost all themes were recorded on both

sites. However, the sequence of themes varied

between study sites (and within the season). In

January, all themes were present in San Juan del

Sur, except for the light green theme. However,

the sample size at this location is limited to a

single day of recording for January. The same

themes observed in January in San Juan del

Sur were present in Padre Ramos in February,

except for the light green theme that appeared

in Padre Ramos. Finally, the yellow and orange

themes were not encountered in March at

both sites and in April in San Juan del Sur

only. There was only one common month of

recording between sites (March), but both sites

presented the same overall number of themes.

Due to the lack of common recordings in the

same months, it is challenging to compare the

two sites.

The results of this study show a lot of

variability in theme sequences. This indicates

the 2018 Nicaragua CA song did not follow a

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71(S4): e57281, diciembre 2023 (Publicado Nov. 01, 2023)

strict theme order, as described for some other

Southern hemisphere populations (Garland,

Noad, et al., 2013). The presence of common

themes at both sites suggests that a certain

level of movement of males takes place; this is

in contrast with the low level of photographic

recapture observed between sites (De Weerdt

et al., 2022). This inconsistency highlights the

need for further research to understand whale

movements in this area. To confirm if the same

song is sung on both sites at the same time,

synchronous recordings during the entire sea-

son would be needed. Gradual change of song

along the season was observed in studies on

other breeding grounds, such as Mexico and

Hawaii (Cerchio et al., 2001; Darling, Acebes, et

al., 2019). Compared to other Northern hemi-

sphere songs, this study showed a more ‘elabo-

rate’ and less organized song structure than

previously reported for the 2016-2017 breeding

season in Caño Island, Costa Rica (Chereskin

et al., 2019). No further comparison with the

song from Costa Rica could be achieved due

to the limited information presented about

individual unit characteristics and the resolu-

tion of the spectrograms. Within season com-

parison between breeding grounds would allow

to gain a better insight on the dynamics and

potential exchanges between animals in these

breeding grounds.

Fig. 1. Spectrograms of phrases identified in CA humpback whales singing off Nicaragua (hamming window, frequency

resolution: 2 Hz, frame length: 0.128 s, time step: 0.032 s); the repetition of such phrases results in the theme identified at the

top of each spectrogram. Distinct themes are represented by the colors red, yellow, orange, dark green, light green, purple and

blue. The sequence of themes per recording are presented per site at Padre Ramos: PR (north) and at San Juan del Sur: SJDS

(south) at the bottom of the figure (table) (P = Pause in whale singing; E = End of recording). A new line was started when

there was a pause in the singing in the recording that was longer than the silence between phrases. The theme sequence was

aligned (thick vertical black lines) arbitrarily to try to identify matching sequences across recordings.

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71(S4): e57281, diciembre 2023 (Publicado Nov. 01, 2023)

Although our dataset was rather small, a

poorly structured theme sequence could be

observed in the second half of the season; this

could be due to the mixing with other popula-

tions such as the Mexican DPS; furthermore,

error accumulation over the entire season could

be an alternative or concurrent explanation for

the observed lack of structured sequence in the

song (Mcloughlin et al., 2018; Mercado III et

al., 2005) and/or the evolution of the song as

the season progresses. In other words, whales

may be rearranging themes and introducing or

removing elements until the end of the season.

A broader dataset would be required to deter-

mine if the pattern observed in this study is rep-

resentative of the CA population in Nicaragua

or if these are idiosyncrasies from individual

singers. Interestingly, an extensive variability

in the order in which themes are sung was also

observed in some recordings from Socorro,

Mexico, in unpublished work from Smith-

Aguilar, as reported in Cholewiak et al. (2013).

The gradual replacement of the yellow and

orange themes by the more common blue

theme as the season progressed, suggests that

gradual song changes took place in the songs of

Nicaraguan whales. This process is described as

song evolution and it has been widely reported

for other humpback whale populations in both

hemispheres (Fournet et al., 2018; Garland et

al., 2011; Mercado, 2021; Payne & Payne, 1985).

The findings of this paper can be used for

future regional song comparisons with whales

from the North Pacific to assess population

connectivity. Future work should explore song

evolution and the seasonal dynamics within the

Central America population.

Ethical statement: the authors declare that

they all agree with this publication and made

significant contributions; that there is no con-

flict of interest of any kind; and that we fol-

lowed all pertinent ethical and legal procedures

and requirements. All financial sources are fully

and clearly stated in the acknowledgments sec-

tion. A signed document has been filed in the

journal archives.

Author Contributions: JDW, conceptual-

ized the study, acquired the data, and contrib-

uted to analysis interpretation, and drafted the

initial and revised versions of this manuscript.

DD, RSL, and FP contributed to data analysis

and interpretation of results, and contributed

to the drafting of the manuscript at all stages.

ACKNOWLEDGMENTS

We wish to acknowledge all research assis-

tants that participated in data collection with

Association ELI-S. To Professor Marcelo Rivad-

eneira that assisted with the Random For-

est analysis. Financial support was received

from the Rufford Foundation, Cetacean Society

International, Fondation Yves-Rocher, and pri-

vate donors from Association ELI-S. This study

was financed in part by the Coordenação de

Aperfeiçoamento de Pessoal de Nível Superior -

Brasil (CAPES) - Finance Code 001. RSL is sup-

ported by the Brazilian research agency CNPq

through a fellowship (process 312763/2019-0)

and a grant (number 443308/2019-5). Unit clas-

sification was based on DDj PhD work financed

by CAPES (process 88882.344 054/2019-01).

This research was done under research permit

No DGPNB – IC – 011 – 2018 from MARENA.

Special thanks to Aldo Pacheco for Spanish cor-

rections in the summary.

REFERENCES

Bettridge, S., Baker, C. S., Barlow, J. P., Clapham, P. J.,

Ford, M., Gouveia, D., Mattila, D. K., Pace, R. M.,

III, Rosel, P. E., Silber, G. K., & Wade, P. R. (2015).

Status review of the humpback whale (Megaptera

novaeangliae) under the Endangered Species Act (No.

NOAA-TM-NMFS-SWFSC-540). National Oceanic

and Atmospheric Administration. https://repository.

library.noaa.gov/view/noaa/4883

Calambokidis, J., T. Chandler, K. Rasmussen, G.H. Steiger,

and L. Schlender. (2000). Humpback and blue whale

photographic identification research off California,

Oregon, and Washington in 1999 [Final report]. Cas-

cadia Research. https://cascadiaresearch.org/publi-

cations/ .

Calambokidis, J., Steiger, G. H., Straley, J. M., Quinn, T. J.,

III, Herman, L. M., Cerchio, S., Salden, D. R., Yama-

guchi, M., Sato, F., Urbán, J., Jacobsen, J., von Ziegesar,

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71(S4): e57281, diciembre 2023 (Publicado Nov. 01, 2023)

O., Balcomb, K. C., III, Gabriele, C. M., Dahlheim, M.

E., Higashi, N., Uchida, S., Ford, J. K. B., Miyamura,

Y., … Rasmussen, K. (1997). Abundance and popula-

tion structure of humpback whales in the North Pacific

basin [Final Report] Cascadia Research. https://casca-

diaresearch.org/publications/

Cerchio, S., Jacobsen, J. K., & Norris, T. F. (2001). Temporal

and geographical variation in songs of humpback

whales, Megaptera novaeangliae: Synchronous change

in Hawaiian and Mexican breeding assemblages. Ani-

mal Behaviour, 62, 313–329. https://doi.org/10.1006/

anbe.2001.1747

Chereskin, E., Beck, L., Gamboa-Poveda, M. P., Palacios-

Alfaro, J. D., Monge-Arias, R., Chase, A. R., Coven, B.

M., Gloria Guzmán, A., McManus, N. W., Neuhaus,

A. P., O’Halloran, R. A., Rosen, S. G., & May-Collado,

L. J. (2019). Song structure and singing activity of two

separate humpback whales populations wintering off

the coast of Caño Island in Costa Rica. Journal of the

Acoustical Society of America, 146, El509. https://doi.

org/10.1121/1.5139205

Cholewiak, D. M., & Cerchio, S. (2022). Humpback Whales:

Exploring Global Diversity and Behavioral Plasti-

city in an Undersea Virtuoso. In C. W. Clark & E.

C. Garland (Eds.), Ethology and Behavioral Ecology

of Mysticetes (pp. 247–276). Springer. https://doi.

org/10.1007/978-3-030-98449-6_11

Cholewiak, D. M., Sousa-Lima, R. S., & Cerchio, S. (2013).

Humpback whale song hierarchical structure: His-

torical context and discussion of current classifica-

tion issues. Marine Mammal Science, 29, E312–E332.

https://doi.org/10.1111/mms.12005

Darling, J. D., Acebes, J. M. V., Frey, O., Jorge Urbán, R., &

Yamaguchi, M. (2019). Convergence and divergence

of songs suggests ongoing, but annually variable,

mixing of humpback whale populations throughout

the North Pacific. Scientific Reports, 9, 7002. https://

doi.org/10.1038/s41598-019-42233-7

Darling, J. D., & Bérubé, M. (2001). Interactions of sin-

ging humpback whales with other males. Mari-

ne Mammal Science, 17, 570–584. https://doi.

org/10.1111/j.1748-7692.2001.tb01005.x

Darling, J. D., Gibson, K. M., & Silber, G. K. (1983).

Observations on the abundance and behavior of hum-

pback whales (Megaptera novaeangliae) of West Maui,

Hawaii 1977-79. In R. Payne (Ed.), Communication

and behavior of whales (pp. 201–222). Westview Press.

Darling, J. D., Goodwin, B., Goodoni, M. K., Taufmann,

A. J., & Taylor, M. G. (2019). Humpback whale calls

detected in tropical ocean basin between known

Mexico and Hawaii breeding assemblies. Journal of

the Acoustical Society of America, 145, EL534–EL540.

https://doi.org/10.1121/1.5111970

Darling, J. D., & Sousa-Lima, R. S. (2005). Songs indicate

interaction between humpback whale (Megaptera

novaeangliae) populations in the western and eastern

South Atlantic Ocean. Marine Mammal Science, 21,

557–566. https://doi.org/10.1111/j.1748-7692.2005.

tb01249.x

De Weerdt, J., Calambokidis, J., Pouplard, E., Pouey-San-

talou, V., Patulny, C., Vanschoenwinkel, B., Kochzius,

M., & Clapham, P. (2022). Abundance, distribu-

tion and behaviour of humpback whales (Megaptera

novaeangliae) along the Pacific coast of Nicaragua,

Central America. Marine and Freshwater Research, 73,

1041–1055. https://doi.org/https://doi.org/10.1071/

MF21326

Dines, J. P., Mesnick, S. L., Ralls, K., May-Collado, L.,

Agnarsson, I., & Dean, M. D. (2015). A trade-off bet-

ween precopulatory and postcopulatory trait inves-

tment in male cetaceans. Evolution, 69, 1560–1572.

https://doi.org/https://doi.org/10.1111/evo.12676

Fournet, M. E. H., Jacobsen, L., Gabriele, C. M., Mellinger,

D. K., & Klinck, H. (2018). More of the same: Allo-

patric humpback whale populations share acoustic

repertoire. PeerJ, 6, e5365. https://doi.org/10.7717/

peerj.5365

Garland, E. C., Garrigue, C., & Noad, M. J. (2022). When

does cultural evolution become cumulative culture?

A case study of humpback whale song. Philosophi-

cal Transactions of the Royal Society B: Biological

Sciences, 377, 20200313. https://doi.org/doi:10.1098/

rstb.2020.0313

Garland, E. C., Gedamke, J., Rekdahl, M. L., Noad, M.

J., Garrigue, C., & Gales, N. (2013). Humpback

Whale Song on the Southern Ocean Feeding

Grounds: Implications for Cultural Transmission.

PLOS ONE, 8, e79422. https://doi.org/10.1371/jour-

nal.pone.0079422

Garland, E. C., Goldizen, A. W., Lilley, M. S., Rekdahl, M.

L., Garrigue, C., Constantine, R., Hauser, N. D., Poole,

M. M., Robbins, J., & Noad, M. J. (2015). Population

structure of humpback whales in the western and

central South Pacific Ocean as determined by vocal

exchange among populations. Conservation Biology,

29, 1198–1207. https://doi.org/10.1111/cobi.12492

Garland, E. C., Goldizen, A. W., Rekdahl, M. L., Cons-

tantine, R., Garrigue, C., Hauser, N., Poole, M. M.,

Robbins, J., & Noad, M.J. (2011). Dynamic horizontal

cultural transmission of humpback whale song at

the ocean basin scale. Current Biology, 21, 687–691.

https://doi.org/10.1016/j.cub.2011.03.019

Garland, E. C., Noad, M. J., Goldizen, A. W., Lilley,

M. S., Rekdahl, M. L., Garrigue, C., Constantine,

R., Daeschler Hauser, N., Poole, M. M., & Robb-

ins, J. (2013). Quantifying humpback whale song

sequences to understand the dynamics of song

exchange at the ocean basin scale. Journal of the

Acoustical Society of America, 133, 560–569. https://

doi.org/10.1121/1.4770232

8Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71(S4): e57281, diciembre 2023 (Publicado Nov. 01, 2023)

Green, S. R., Mercado III, E., Pack, A. A., & Herman, L.

M. (2011). Recurring patterns in the songs of hum-

pback whales (Megaptera novaeangliae). Behaviou-

ral Processes, 86, 284–294. https://doi.org/10.1016/j.

beproc.2010.12.014

Hastie, T., Tibshirani, R., & Friedman, J. (2009). Random

Forests. In T. Hastie, R. Tibshirani, & J. Friedman

(Eds.), The Elements of Statistical Learning: Data

Mining, Inference, and Prediction (pp. 587–604). Sprin-

ger. https://doi.org/10.1007/978-0-387-84858-7_15

Herman, L. M. (2017). The multiple functions of male song

within the humpback whale (Megaptera novaean-

gliae) mating system: Review, evaluation, and synthe-

sis. Biological Reviews, 92, 1795–1818. https://doi.

org/10.1111/brv.12309

K. Lisa Yang Center for Conservation Bioacoustics at the

Cornell Lab of Ornithology. (2022). Raven Pro: Inte-

ractive Sound Analysis Software [Computer software].

The Cornell Lab of Ornithology. https://ravensound-

software.com/

Kowarski, K. A., Cerchio, S., Whitehead, H., Cholewiak,

D. M., & Moors-Murphy, H. B. (2022). Seasonal song

ontogeny in western North Atlantic humpback wha-

les: Drawing parallels with songbirds. Bioacoustics,

32, 325–347. https://doi.org/10.1080/09524622.2022

.2122561

Kowarski, K. A., Moors-Murphy, H. B., Maxner, E. E., &

Cerchio, S. (2019). Western North Atlantic humpback

whale fall and spring acoustic repertoire: Insight into

onset and cessation of singing behavior. Journal of the

Acoustical Society of America, 145, 2305–2316. https://

doi.org/10.1121/1.5095404

Malige, F., Djokic, D., Patris, J., Sousa-Lima, R., & Glotin,

H. (2020). Use of recurrence plots for identification

and extraction of patterns in humpback whale song

recordings. Bioacoustics, 30, 680–695. https://doi.org

/10.1080/09524622.2020.1845240

Mcloughlin, M., Lamoni, L., Garland, E. C., Ingram, S.,

Kirke, A., Noad, M. J., Rendell, L., & Miranda,

E. (2018). Using agent-based models to unders-

tand the role of individuals in the song evolution

of humpback whales (Megaptera novaeangliae).

Music & Science, 1, 2059204318757021. https://doi.

org/10.1177%2F2059204318757021

McSweeney, D. J., Chu, K. C., Dolphin, W. F., & Gui-

nee, L. N. (1989). North Pacific humpback whale

songs: A comparison of southeast Alaskan feeding

ground songs with Hawaiian wintering ground songs.

Marine Mammal Science, 5, 139–148. https://doi.

org/10.1111/j.1748-7692.1989.tb00328.x

Mercado, E. (2021). Song Morphing by Humpback

Whales: Cultural or Epiphenomenal? Frontiers in

Psychology, 11, 574403. https://doi.org/10.3389/

fpsyg.2020.574403

Mercado III, E., Herman, L. M., & Pack, A. A. (2005). Song

copying by humpback whales: Themes and variations.

Animal Cognition, 8, 93–102. https://doi.org/10.1007/

s10071-004-0238-7

Noad, M. J., Cato, D. H., Bryden, M. M., Jenner, M.

N., & Jenner, K. C. S. (2000). Cultural revolution

in whale songs. Nature, 408, 537–537. https://doi.

org/10.1038/35046199

Owen, C., Rendell, L., Constantine, R., Noad, M. J., Allen,

J. A., Andrews, O., Garrigue, C., Poole, M. M., Don-

nelly, D., Hauser, N., & Garland, E. C. (2019). Migra-

tory convergence facilitates cultural transmission of

humpback whale song. Royal Society Open Science, 6,

190337. https://doi.org/10.1098/rsos.190337

Payne, K. B., & Payne, R. S. (1985). Large scale changes over

19 years in songs of humpback whales in Bermuda.

Zeitschrift für Tierpsychologie, 68, 89114. https://doi.

org/10.1111/j.1439-0310.1985.tb00118.x

Payne, K. B., Tyack, P. L., & Payne, R. S. (1983). Progressive

changes in the songs of humpback whales (Megaptera

novaeangliae): A detailed analysis of two seasons in

Hawaii. In R. S. Payne (Ed.), Communication and

behavior of whales (pp. 9–57). Westview Press.

Payne, R. S., & McVay, S. (1971). Songs of humpback wha-

les. Science, 173, 585–597. https://doi.org/10.1126/

science.173.3997.585

Schall, E., Djokic, D., Ross-Marsh, E. C., Oña, J., Denkinger,

J., Ernesto Baumgarten, J., Rodrigues Padovese, L.,

Rossi-Santos, M. R., Carvalho Gonçalves, M. I., Sou-

sa-Lima, R., Hucke-Gaete, R., Elwen, S., Buchan, S.,

Gridley, T., & Van Opzeeland, I. (2022). Song recor-

dings suggest feeding ground sharing in Southern

Hemisphere humpback whales. Scientific Reports, 12,

13924. https://doi.org/10.1038/s41598-022-17999-y

Smith, J. N., Goldizen, A. W., Dunlop, R. A., & Noad, M. J.

(2008). Songs of male humpback whales, Megaptera

novaeangliae, are involved in intersexual interac-

tions. Animal Behaviour, 76, 467–477. https://doi.

org/10.1016/j.anbehav.2008.02.013

Sostres Alonso, M., & Nuuttila, H. K. (2015). Detection

rates of wild harbour porpoises and bottlenose dolph-

ins using static acoustic click loggers vary with depth.

Bioacoustics, 24, 101–110. https://doi.org/10.1080/095

24622.2014.980319

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71(S4): e57281, diciembre 2023 (Publicado Nov. 01, 2023)

Tyack, P. L., & Clark, C. W. (2000). Communication and

Acoustic Behavior of Dolphins and Whales. In W. W.

L. Au, R. R. Fay, & A. N. Popper (Eds.), Hearing by

Whales and Dolphins (pp. 156–224). Springer. https://

doi.org/10.1007/978-1-4612-1150-1_4

Warren, V. E., Constantine, R., Noad, M. J., Garrigue, C.,

& Garland, E. C. (2020). Migratory insights from

singing humpback whales recorded around central

New Zealand. Royal Society Open Science, 7, 201084.

https://doi.org/10.1098/rsos.201084

Zandberg, L., Lachlan, R. F., Lamoni, L., & Garland, E. C.

(2021). Global cultural evolutionary model of hum-

pback whale song. Philosophical Transactions of the

Royal Society B: Biological Sciences, 376, 20200242.

https://doi.org/doi:10.1098/rstb.2020.0242