Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71(S4): e57280, diciembre 2023 (Publicado Nov. 01, 2023)

Southern Hemisphere humpback whales (Megaptera novaeangliae)

(Artiodactyla: Balaenopteridae) singing activity at Caño Island Biological

Reserve, Costa Rica before, during, and after COVID-19 lockdowns

Laura J. May-Collado1, 2*; https://orcid.org/0000-0002-4790-9524

Sawyer Bottoms1; https://orcid.org/0000-0002-8821-7348

Grace Durant1; https://orcid.org/0000-0002-1896-3900

Jose David Palacios-Alfaro3; https://orcid.org/0000-0002-0315-094X

Juan Jose Alvarado4, 5, 6; https://orcid.org/0000-0002-2620-9115

1. Department of Biology, University of Vermont, Burlington, VT 05405, USA; sawyer.miller-bottoms@uvm.edu,

grace.durant@uvm.edu

2. Smithsonian Tropical Research Institute, Panama, Panama; lmaycoll@uvm.edu (*corresponding author)

3. Fundación Panacetacea, St Paul Minnesota, 55118, USA; pala1611@gmail.com

4. Escuela de Biología, Universidad de Costa Rica, San José, Costa Rica, juan.alvarado@ucr.ac.cr

5. Centro de Investigación en Ciencias del Mar y Limología (CIMAR), Universidad de Costa Rica, San José, Costa Rica.

6. Ecología Tropical (CIBET), Universidad de Costa Rica, San José, Costa Rica.

Received 21-IX-2022. Corrected 13-II-2023. Accepted 11-IV-2023.

ABSTRACT

Introduction: Boat traffic is recognized as a major contributor of underwater noise. Increasing presence of boats

in coastal habitats is predicted to have important repercussions on the communication of marine mammals. In

Costa Rica, the waters of the Caño Island Biological Reserve are an important breeding area for humpback whales

from the Breeding-Stock G (BSG). Their predicted and abundant presence has fueled the development of whale

watching activities as an important component of the local economy, and while the country has norms of conduct

for this activity, whales often interact with multiple boats at the same time. The lockdowns associated with the

COVID-19 pandemic provided a unique opportunity to study the potential impacts of noise associated with boat

traffic on the singing activity of humpback whales.

Objective: Determine whether noise levels and boat acoustic presence around Caño Island Biological Reserve

changed during the COVID-19 lockdowns, and if it did, what is the impact on song detection of BSG humpback

whales.

Methods: Acoustic recordings were made using a bottom-mounted autonomous underwater recorder for 30 days

in September 2019, 2020, and 2021, resulting in a total recording effort of 480 hours.

Results: Our results show that broadband underwater noise levels (dBRMS) during pre-lockdown were signifi-

cantly higher, particularly at frequencies below 1kHz, than during and post-lockdown. This is likely due to a

decrease in the proportion of boat acoustic presence during the lockdown. Although the proportion of whale

songs detected did not vary among years, whale songs were detected similarly throughout the day during the

lockdown, compared to pre-and-post lockdown where the proportion of whale song presence decreased during

hours when more boats were present.

Conclusions: This study shows a clear change in underwater noise levels during the COVID-19 lockdown, likely

due to a decrease in boat presence. The study also highlights the potential impact of noise associated with boat

traffic on humpback whale singing activity. The results of this study can inform the Conservation Areas of Osa

https://doi.org/10.15517/rev.biol.trop..v71iS4.57280

SUPPLEMENT • WHALES

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71(S4): e57280, diciembre 2023 (Publicado Nov. 01, 2023)

INTRODUCTION

Boat traffic (i.e., ecotourism, personal use,

fishing, water-taxis) is increasing rapidly in

many coastal environments contributing to an

increasingly noisier ocean (Erbe et al., 2019).

Concerns about the potential repercussions

of underwater noise impacts on whale com-

munication are increasing among scientists

worldwide (e.g., Cholewiak et al., 2018, Erbe et

al., 2019). High noise levels can reduce the dis-

tance at which these animals can communicate

(e.g., Cholewiak et al., 2018, Rey-Barquero et

al., Laude et al., 2022) and can interrupt bio-

logically important behaviors (e.g., Amrein et

al., 2020; Sprogis et al., 2020). For example,

Rey-Barquero et al., (2021) developed a model

based on empirical data that showed that even

in the presence of a single whale-watching

boat, humpback whale, Megaptera novaean-

gliae (Borowski, 1781) song communication

could be reduced by as much as 63 %. Another

study found whale-watching activities to be

one of the factors contributing to a decrease in

communication space, with humpback whales

experiencing masking levels of 80% or more

(ACOSA) in charge of managing Caño Island Biological Reserve, to develop and implement mitigation measures

to regulate underwater anthropogenic noise associated with tour boats.

Key words: ambient noise levels; boat traffic; whale-watching; tourism; bioacoustics.

RESUMEN

Actividad de canto de las ballenas jorobadas (Megaptera novaeangliae) (Artiodactyla: Balaenopteridae) del

hemisferio sur en la Reserva Biológica de la Isla del Caño, Costa Rica, antes, durante

y después de los cierres asociados a la pandemia de COVID-19

Introducción: Se reconoce que el tráfico de embarcaciones es uno de los principales contribuyentes al ruido

marino. Se predice que la creciente presencia de barcos en los hábitats costeros tendrá importantes repercusiones

en la comunicación de los mamíferos marinos. En Costa Rica, las aguas de la Reserva Biológica Isla del Caño son

un hábitat reproductivo importante para las ballenas jorobadas de la población reproductiva G (BSG). Su presen-

cia ha impulsado el desarrollo de las actividades de observación comercial de ballenas, el cual es un componente

importante de la economía local. Aunque el país tiene normas de conducta para esta actividad, las ballenas a

menudo interactúan con múltiples barcos turísticos al mismo tiempo. Los cierres y limitaciones de movilización

de botes asociados a la pandemia de COVID-19 brindan una oportunidad para estudiar el impacto potencial del

ruido asociado al tráfico de embarcaciones en la actividad de canto de las ballenas jorobadas.

Objetivo: Determinar si los niveles de ruido ambiental bajo el agua y la presencia de botes cambiaron antes,

durante y después de los cierres y cuarentena por COVID-19, y si estos cambios influyen en la detección de cantos

de machos de ballenas jorobadas.

Métodos: las grabaciones acústicas se realizaron con una grabadora autónoma montada en el fondo marino

durante 30 días en septiembre de 2019, 2020 y 2021, resultando en un esfuerzo de grabación de 480 horas.

Resultados: Nuestros resultados muestran que los niveles de ruido ambiental (dBRMS) antes del cierre (2019)

fueron significativamente más altos, particularmente a frecuencias bajas (<1kHz), que durante y después de los

cierres asociados a la pandemia de COVID-19. Es probable que esto se deba a una reducción en la presencia de

embarcaciones durante el cierre. Aunque la detección de cantos de ballenas jorobadas no varió entre años, durante

la cuarentena se detectaron los cantos de ballenas de forma uniforme durante el día, mientras que antes y después

de la cuarentena se notó un decrecimiento en la proporción de cantos a horas donde hay más detección de botes

presentes.

Conclusiones: Este estudio muestra un cambio claro en los niveles de ruido ambiental durante el cierre de

COVID-19, probablemente debido a una disminución en la presencia de embarcaciones. El estudio también

muestra el potencial impacto del ruido asociado al tráfico de embarcaciones en la actividad del canto de las

ballenas jorobadas. Los resultados de este estudio pueden informar al Área de Conservación de Osa (ACOSA), la

cual está a cargo de la Reserva Biológica Isla del Caño, a desarrollar e implementar medidas que regulen el ruido

antropogénico bajo el agua asociado a tráfico de botes turísticos.

Palabras clave: ruido ambiental; tráfico de botes; observación de ballenas; turismo; bioacoustica.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71(S4): e57280, diciembre 2023 (Publicado Nov. 01, 2023)

(Cholewiak et al., 2018). These studies show the

potential negative impact of noise associated

with boat traffic, particularly that of activities

that directly target these animals, such as whale

watching activities.

Whale-watching is a major catalyst of the

local economy in Latin America (Tambutti

& Gómez, 2020). The most recent review of

the state of whale watching in Latin America

is by Hoyt and Iñiguez (2008). The authors

find that between 1996 and 2006, boat-based

whale watching activities in the region grew

at a rate three times higher than the rate of

world tourism and five times higher than the

rate of all Latin American tourism over the

same period. Although many countries have

adopted whale watching guidelines, compliance

and enforcement remains limited (Gagne et al.,

2022). As a result, whales might be exposed to

noisy soundscapes.

In March 2020, the COVID-19 pandemic

led to a global and national lockdown in Costa

Rica to limit the spread of the virus. Widespread

mandatory lockdowns and stay-at-home orders

severely limited human mobility and activities

in land and in the ocean. Costa Rica’s economy

shrank by 4.1% in 2020 as a consequence of

these measures, and among the factors driving

this trend was the sharp drop in tourism (Eco-

nomic Survey of Latin America and the Carib-

bean, ECLAC, 2021). According to the CEIC

Global Economy Database (2022), the number

of air transported passengers dropped from

2,033,146 to 455,830 passengers. Worldwide,

this drop in human mobility resulted in an

increase in animal communication ranges; for

urban songbirds, their communication range

doubled in some places (Derryberry et al.,

2020) and for dolphin and fish it increased to

up to 65 % (Pine et al., 2021).

Male humpback whales are highly vocal

animals that perform acoustic displays pri-

marily during the breeding season (Herman

et.al., 2013). The South Pacific waters off the

coast of Costa Rica, and particularly the north

and east side of Caño Island, are an important

breeding area for Southeastern Pacific hump-

back whales, also known as the International

Whaling Commission, designated Breeding

Stock G (BSG) (Palacios-Alfaro et al., 2012;

Rasmussen et al., 2007) as well as for whales

from the “Central America” distinct population

segment (DPS) (Bettridge et al., 2015). The

BSG whales observed in Costa Rica migrate

from feeding areas off the Antarctic Penin-

sula and the Fuegian Archipelago in Chile

(Acevedo et al., 2017; Rasmussen et al., 2007).

Multiyear boat surveys in this area indicate

that BSG whales are particularly abundant in

September (Palacios-Alfaro et al., 2012), and

for this reason coastal communities in the area

celebrate a whale festival during this month

(Palacios-Alfaro, personal communication, 1

september 2022).

A previous study using passive acoustic

monitoring data near Caño island found that

male song activity occurred throughout the day,

with a drop in singing activity during the morn-

ing hours, suggesting a potential response to

whale watching tour boats presence (Chereskin

et al., 2019). In other breeding areas in Brazil,

increased boat traffic was shown to have a neg-

ative effect on humpback whale singing activity,

with whales singing less when the number of

boats increased (Sousa-Lima & Clark, 2008). In

a recent study, Laute et al. (2022) found that on

Icelandic foraging areas during the COVID-19

pandemic, whale watching trips were reduced

by 68.6 %, and humpback whale call detection

increased by nearly twofold. In this study we

examine whether noise levels and boat acous-

tic presence around Caño Island Biological

Reserve changed during the COVID-19 lock-

downs, and if it did, how the detection of BSG

humpback whale song was impacted.

MATERIALS AND METHODS

Study Area: This study took place at Caño

Island Biological Reserve, 16 km northeast off

the Osa Peninsula in the south Pacific coast of

Costa Rica. This reserve protects approximately

58 km2 of marine habitat around the island

(Executive Decree 20790-MIRENEM, 1991).

An autonomous underwater recorder was

deployed in a location at the northeast side of

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71(S4): e57280, diciembre 2023 (Publicado Nov. 01, 2023)

the island called El Jardin (8.719 N/-83.863W,

Fig. 1) at a depth of 25 m. This location is

approximately 0.8 km from the island and is

characterized by a sandy bottom (Chereskin

et al., 2019). This area of the island has been

highlighted by previous studies as an important

reproductive habitat for BSG humpback whales

(e.g., Rasmussen et al., 2007; Palacios-Alfaro et

al., 2012). The island is also a tourist attraction

with tour boats arriving to the island through-

out the day to observe whales and dolphins,

snorkel, and scuba dive.

Data Collection: An autonomous under-

water recorder, a Soundtrap model 300 SD

(Ocean Instruments; frequency range 20 Hz-150

kHz ±3dB; self-noise of less than sea-state in

the bandwidth 100 Hz-2 kHz, and sensitivity of

-203 dB re V/µPa) was deployed in El Jardin for

the entire month of September 2019, 2020, and

2021. The recorder was programmed to record

the soundscape at a sampling rate of 48 kHz

for five minutes every 30 minutes in 2019, and

for 15 minutes every 60 minutes in 2020 and

2021, resulting in a total of 480 hours record-

ing effort. For this study, we only analyzed the

first five minutes of every hour for each year,

resulting in a total of 180 hours analyzed. These

5-min files were uploaded to RFCx ARBIMON

(Rainforest Connection, 2020) for cataloguing

and spectral inspection for presence/absence

of whale songs and boats. The proportion of

acoustic files with song and boat presence was

calculated by dividing the number of 5-min

files with whale songs and boats by the total

number of 5-min files per year and time of day.

Fig. 1. Location of Caño Island Biological Reserve off the Osa Peninsula in the South Pacific of Costa Rica. The figure also

shows a cartoon of a straight-line from Costa Rica towards the feeding areas off the Antarctica Peninsula and the Fuegian

Archipelago in Chile to Caño Island, Costa Rica. The black star represents the deployment site of the autonomous underwater

recorder.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71(S4): e57280, diciembre 2023 (Publicado Nov. 01, 2023)

Ambient Noise Levels: To measure broad-

band ambient noise levels we used the software

dBWav from Marshall-Day Acoustics (https://

www.marshallday.com) which is tailored for

Ocean Instrument Soundtrap hydrophones.

Upon calibration following Ocean Instruments

instructions, the first five minutes of every hour

were selected manually. Manual selection was

done because dBWav does not automatically

select the region of interest. We selected a sub-

sample of days for this part of the data analysis

including the following days for each year: 4,

7, 10, 13, 16, 19, 22, 25, and 28. The average

root-mean-square (RMSdB) was then generated

for each 1/3 octave bands ranging from 12.5 Hz

to 10 kHz.

Statistical analysis: The statistical software

SPSS 25 (IBM, 2017) was used for summary

statistics and statistical analyses. An ANOVA

test for multiple independent variables (n-way)

was used to study the effect of year (pre, during,

and post lockdown), time of day (hour), and 1/3

octave frequency bands on noise levels (RMSdB).

Broadband noise levels were compared among

years using a non-parametric Kruskal-Wallis’

test. The 1/3 octave bands were grouped into

two categories: below and above 1kHz frequen-

cy categories. Below 1 kHz included bands from

12.5 to 800 Hz and above 1 kHz bands from 1

to 10 kHz. A Kruskal-Wallis test was also used

to assess if there are differences in these two fre-

quency categories among years. A Chi-Square

one sample test for goodness of fit was used

to compare the proportion of recordings with

whale song and boat presence per year. Finally,

the proportion of noise levels, whale song, and

boat presence were plotted against time of day

using a smoothing spline with a bootstrap con-

fidence of fit using a lambda of 0.05 to look for

diel patterns in ambient noise levels and whale

song and boat presence within each year.

RESULTS

Ambient Noise Levels: The results from

the ANOVA analysis suggest that year (F

=1610.5, df=2, p<0.001), time of day (hour)

(F=4.8, df=23, p<0.001), 1/3 octave frequency

bands (F=369.8, df=27, p <0.001), and the

interactions between year*time of day (F=9.6,

df=46, p <0.001) and year*1/3 octave frequency

bands (F=176.7, df=52, p <0.001) influenced

the variation in ambient noise levels. Broad-

band ambient noise levels varied significantly

among years (Kruskal-Wallis=876.06; df=2, p

<0.001, Table 1, Fig. 2A, Fig. 2B). In general,

ambient noise levels were higher in pre-lock-

down than during and post-lockdown (Table

1, Fig. 2A) and these differences among years

were maintained throughout the day (Fig. 2B).

When accounting for frequency categories

Tabl e 1

Summary statistics of ambient noise levels (in dB) and the proportion of whale song and boat presence in pre-lockdown,

during lockdown, and post-lockdown at Caño Island Biological Reserve.

Pre-lockdown (2019) During lockdown (2020) Post-lockdown (2021)

Ambient noise levels (dB)

Mean±SD 99.8 ± 15.3 93.0 ± 11.6 92.0 ± 11.0

Coefficient of Variation (CV) 15.3 12.5 11.8

Range (minimum-maximum) 63.9 –- 134 63.7 –- 127.4 62.1 –- 126.8

Acoustic boat presence

Mean±SD 0.08 ± 0.13 0.03 ± 0.06 0.04 ± 0.09

Coefficient of Variation (CV) 152.8 169.6 193.9

Range (minimum-maximum) 0 – 0.44 0 – 0.22 0 – 0.30

Acoustic whale song presence

Mean±SD 0.98 ± 0.02 0.99 ± 0.01 0.97 ± 0.04

Coefficient of Variation (CV) 2.0 0.8 4.2

Range (minimum-maximum) 0.93 – 1 0.96 – 1 0.86 – 1

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71(S4): e57280, diciembre 2023 (Publicado Nov. 01, 2023)

Fig. 2. A. Broadband ambient noise (RMSdB) levels by year. B. Broadband ambient noise levels (RMSdB) by time of day. C.

Broadband ambient noise levels (RMSdB) by year and frequency category. Broadband noise levels measured as the average

root-mean-square (RMSdB) (a) by year and (b) time of day, in blue pre-lockdown (2019), in red during lockdown (2020) and

in green post-lockdown (2021), and by (c) 1/3 octave frequency bands grouped into two categories below 1 kHz in red (12.5

to 800 Hz) and above 1 kHz in blue (1-10 kHz) and year, at Caño Island Biological Reserve, Costa Rica. The box plots display

median, first and third quartiles, and maximum and lower values (excluding outliers) and the line plot uses a smoothing

spline and bootstrap confidences of fit with a lambda of 0.05.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71(S4): e57280, diciembre 2023 (Publicado Nov. 01, 2023)

above and below 1 kHz we find significant

differences among years. Ambient noise lev-

els below 1 kHz were significantly higher in

pre-lockdown (Kruskal-Wallis=1138.5; df=2,

p <0.001, Fig. 2C) while ambient noise levels

above 1 kHz were significantly higher during

and in post-lockdown (Kruskal-Wallis=465.5;

df=2, p <0.001, Fig. 2C).

Acoustic presence of whale songs and

boats: A total of 2 058 5-min per hour files

were used for this analysis (2019 = 695 files,

2020 = 643 files, 2021 = 720 files). Of these, a

total of 2 028 5-min files had an acoustic pres-

ence of whale song (2019 = 686 files, 2020 =

642 files, 2021 = 700 files) and 117 5-min files

contained sounds of passing boats (2019 =

60 files, 2020 = 22 files, 2021 = 35 files). The

proportion of 5-min files with boats passing by

was significantly lower during lockdown than

in pre-lockdown and post-lockdown (χ2=61,

df=2, p =0.003, Table 1). Interestingly, the diel

acoustic presence of boats across years fol-

lowed a similar pattern, with a peak in presence

between 9 a.m. and noon for all years (Fig. 3A).

No significant differences (p >0.05) were found

in the proportion of 5-min files with whale

songs across years, but pre-lockdown and post-

lockdown years showed the greatest reduction

in the proportion of files with whale songs com-

pared to during the lockdown (Table 1, Fig. 3B).

In addition, we found differences in diel pat-

terns of the proportion of whale song presence

among years. During pre-lockdown, the high-

est proportion of recordings with whale songs

occurred at midnight and around 2 p.m. Dur-

ing the lockdown, the presence of whale songs

was almost constant throughout the day, with a

slight decrease between 9 a.m. and 2 p.m., and

in post-lockdown a sharper decrease in whale

song presence occurs approximately between 5

a.m. and 6 p.m., with the lowest proportion of

whale song presence occurring between 10 a.m.

and noon (Fig. 3B).

DISCUSSION

This study shows that underwater ambient

noise levels and boat presence changed between

pre-lockdown, during lockdown, and post-

lockdown periods around Caño Island Bio-

logical Reserve. The year before the COVID-19

pandemic had the highest mean underwa-

ter noise levels, particularly at low frequency

below 1 kHz, and a higher proportion of boat

presence. Although the proportion of whale

song presence did not vary significantly among

years, but we did observe a decrease in the

proportion of acoustic files with whale songs

during pre-and-post-lockdown. We also found

differences in the diel pattern of song presence

by time of day among years, suggesting a poten-

tial impact of tour-boat traffic in the area.

Boat traffic and shipping activities are the

most dominant sources of underwater noise

at low frequency (Southall et al., 2017). Dur-

ing the COVID-19 pandemic these activities

were significantly reduced due to a slowdown

of the global trade activity in order to mitigate

and minimize the spread of the virus (Ryan

et al., 2021; Thompson & Barclay 2020). This

decrease in low-frequency underwater noise

levels resulted in a potential increase in animal

communication ranges during the COVID-

19 lockdowns. For example, in New Zealand,

underwater ambient noise levels dropped

nearly threefold, resulting in an increased in

dolphin and fish communication ranges to up

to 65 % (Pine et al., 2021), while in Iceland a

reduction of whale watching trips resulted in a

twofold increase in humpback whale call (Laute

et al., 2022), and a similar increase in dolphin

whistle detection rates were found in Panama

(Gagne et al., 2022).

Caño Island Biological Reserve is an

important breeding area for humpback whales

(Rasmussen et al., 2007). Therefore, it is not

surprising that their overall presence did not

change between periods. However, Caño Island