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Applications of bioacoustics in animal ecology

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DOI: 10.1016/j.ecocom.2020.100847

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 Ecological Complexity 43 (2020) 100847

Contents lists available at ScienceDirect

Ecological Complexity
journal homepage: www.elsevier.com/locate/ecocom

Review

Applications of bioacoustics in animal ecology T

⁎
Weronika Penar , Angelika Magiera, Czesław Klocek
Faculty of Animal Sciences, Department of Animal Genetics, Husbandry and Ethology, University of Agriculture in Krakow, Al. Adama Mickiewicza 24/28, 30-059
Kraków, Poland

A R T I C LE I N FO A B S T R A C T

Keywords: In communication animals use a full range of signals: acoustic, visual, chemical, electrical and tactile. The
Vocal communications processes involved in how and why animals communicate have long held veritable fascination for scientists. A
Climate change branch of science concerned with the production of sound and its effects on living organisms is bioacoustics.
Biodiversity The main purpose of the present study is to raise and discuss some issues related to the relationship between
Ocean acidification
animals, their sounds and ecology, including presentation of methods of analysis of sound recordings. A better
Nature conservation
understanding of the relationship between the studied animals will allow for development of a better framework
Ornithology
for future research, as well as a better grasp of interactions between different organisms, including humans. The
paper discusses the significance of acoustic research in animal ecology and its possible applications in the future.
The author also summarizes previous research in the field of sound communication of various animal species.
The paper proves that vocalizations of every acoustically communicating animal are threatened by climate
change. For marine animals, the source of changes in vocalization abilities is ocean acidification and increased
ambient noise, which can affect communication and foraging behavior. For terrestrial animals, changes in
precipitation and temperature may result in modifications of the sounds emitted, as well as certain modifications
to the auditory system. Together with changes in species distribution due to environmental parameters, cu-
mulatively these factors can cause changes in the entire landscape of acoustics ecosystems. Thanks to acoustic
biomonitoring, we can understand how the sounds of entire habitats and acoustic ecosystems will change in
response to the changing climate and how it will affect bioacoustics on a global scale.

1. Introduction
Animal communications means transmission of specific signals (in-
formation) between individuals of one or different species to elicit
specific, usually expected behavior. More precisely, we define animal
communications as the process of transmitting information by the
sender to the receiver in order to increase the likelihood of a beneficial
(for the sender) response on behalf of the receiver; assuming at the
same time that the recipient benefits (on average) from the information
obtained (Bradbury and Vehrencamp, 1998). The nature of a given
communication is determined by a wide range of factors such as: animal
species, its social system, behavioral context, function of a given signal,
interests of senders and receivers as well as sensory methods (ability to
produce, receive and process a given message) (Naguib, 2006).
In communication animals use a full range of signals: acoustic, vi-
sual, chemical, electrical and tactile. Each sensory method has its pros
and cons. The communication method selected by the animal at a given
time depends on the type of information, its biological significance,
abilities of the species and restrictions imposed by the environment the
signal must pass through (Maynard Smith and Harper, 2003; Barrows,
2011). The study of animal communication is a specialty field that
covers a wide and diverse range of biological disciplines, from neu-
roscience and biomechanics to evolution and psychology (Naguib and
Priece, 2013). The challenge in this field is that communication itself is
a phenomenon that is intuitively easy to understand, but difficult to
clearly define.
Voice is a very complex acoustic and mechanical phenomenon. To
emit it, it is necessary to be able to produce its basic component, which
is sound. In physical terms, sound is constituted by mechanical
(acoustic) vibrations, consisting in the movement of the elastic medium
particles relative to the equilibrium position. The environment in which
vibrations occur can be any liquid, gas or solid medium, in particular -
air. Manifestation of vibrations in the air medium are local compres-
sions and rarefactions of air, resulting in localized pressure variations
relative to atmospheric pressure (known as acoustic pressure), propa-
gating in the form of waves to which animal ear is sensitive (Heffner,
1999).
Sound can be defined as wave motion in the air or in another elastic

⁎
Corresponding author.
E-mail address: weronika.penar@gmail.com (W. Penar).

https://doi.org/10.1016/j.ecocom.2020.100847
Received 26 November 2019; Received in revised form 16 April 2020; Accepted 31 May 2020
1476-945X/ © 2020 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/BY-NC-ND/4.0/).
W. Penar, et al.
medium (stimulus), or as stimulation of the hearing organ as a result of
reception of this wave (auditory impression). Under normal tempera-
ture and pressure, the speed of sound in the air is 344 m/s (about 1240
km/h); it increases though with growing temperature and humidity
(Everest and Pohlmann, 2009).
The processes involved in how and why animals communicate have
long held veritable fascination for scientists (Darwin, 1871; Darwin,
1886). Nonetheless, since the first attempts at discovery of mechanisms
of communication, the research methods into animal vocalizations have
still not been standardized. New concepts and methods to better assess
voice communication of various species are still being developed.
Previous attempts to analyze sound signals are based on three main
scientific approaches (Garcia and Favaro, 2017). The oldest and most
commonly used research type is based on attempts at classification,
description and subsequent analysis of vocalizations used in different
contexts by various animal species. This allows to later determine
which groupings of sounds are most characteristic of the given species
in the selected behavioral situation. The second approach to bioacoustic
research is to combine individual sound signals issued by animals with
a behavioral context and subsequent attempts to understand how the
sounds affected the behavior and emotions of the receiver. The third
and latest type of research is investigating the sound production me-
chanisms involved in vocalization processes. Here, the main emphasis is
placed on anatomy and movement of the vocal tract characteristic of
various taxa. It is important to remember that only a combination of all
of the above-mentioned frameworks allows to understand the full vocal
abilities of animals (Garcia and Favaro, 2017).
The main purpose of the present study is to raise and discuss some
issues related to the relationship between animals, their sounds and
ecology, including presentation of emerging new recording technolo-
gies and methods of their analysis. A better understanding of the re-
lationship between the studied animals will allow for development of a
better framework for future research, as well as a better grasp of in-
teractions between different organisms, including humans (Vallee,
2018). The paper summarizes selected previous bioacoustic studies in
the field of animal communication, discusses the significance of
acoustic research in animal ecology and points its possible applications
in the future.
2. Bioacoustics as a science
Countless organisms, including crustaceans, arachnids, insects, fish,
amphibians, reptiles, birds and mammals, produce species-specific
acoustic signals during their daily activities (Bradbury and
Vehrencamp, 1998). Such signals are a great information trail that can
be recorded to determine the presence of various animal species and
many aspects of their ecology and behavior (Obrist et al., 2010). Animal
acoustic signals serve communication purposes and most often contain
species-specific information as well as individual information that can
be used by receivers, making bioacoustics perfectly suited to monitor
biodiversity. Acoustic signals can be received at various distances,
which permits discreet detection and observation of their senders.
Acoustic observations are a well-established research method, e.g. in
the case of birds, insects, amphibians, bats or whales. Depending on the
type of signals and the way they are processed, it is possible to identify
species, estimate numbers or perform a behavioral assessment of the
individuals involved in signal exchange (Obrist et al., 2010).
Bioacoustics is an interdisciplinary field combining biological and
acoustic sciences, which uses sound technologies to record, store and
analyze large collections of animal communication data. It is rooted in
the transmission of sound in flexible, often organic, media, and cen-
tered on sound interpretation and perception by animals, including
humans. This means that neurophysiological and anatomic abilities of
sound emission and reception are within its field of interest. In addition,
bioacoustics deals with the study of dependence of sound signal prop-
erties on the type of medium in which it propagates, what allows to
2
Ecological Complexity 43 (2020) 100847
obtain information about the course of evolution of acoustic mechan-
isms, and thus the evolution of animals that developed them.
Early research into animal signals relied on the use of standard re-
cordings and phonetic rendering. However, over the past 30 years,
technological advances and falling device prices (e.g. portable spec-
trophotometers, high-speed digital cameras or self-service magnetic
recorders) have led to an explosion of research into diversity of signals
in nature (Ryan et al., 2013). A breakthrough in the history of bioa-
coustics was the invention of the spectrograph recorder in the mid-20th
century, which helped improve animal vocalization studies by visua-
lizing sound and consequently inaugurated the field of bioacoustics
(Mundy, 2009). Although for most of the 20th century this science was
used as a method for identifying species, it has now also been adapted
to collect crisis data and perform environmental monitoring by
studying biovariation and biodiversity.
Typical bioacoustic equipment starts with a microphone or hydro-
phone and a recording device. Progressively more specialized material
like directional microphones or parabolas may come into use. For ul-
trasound generated by bats, insects and marine mammals species,
specialized equipment for the recording of ultrasounds are needed.
Finally, recordings require hard- and software for replay, visualization
and analysis.
2.1. Bioacoustic monitoring in species biodiversity research
Human activity causes the disappearance of various animal species
at an alarming rate, leading to a new crisis related to eradiation of
biodiversity (Barnosky et al., 2011). Many of the critically endangered
species are very rare, mysterious animals that live in hiding, which will
probably die out before they are fully documented (Wilson, 2017). In
such circumstances, the only way to register their sojourn on the planet
is to use automatic recorders.
In the face of this urgent challenge, scientists need alternatives to
replace the need for human presence in the field and still allow for
proper documentation of biodiversity of an area (Wilson, 2017). Studies
methods using automated bioacoustic recorders offer significant pro-
mise, especially for species whose behavior or ecology reduces their
detectability using traditional methods. Individual recognition by
means of the acoustic features of vocalizations can be achieved in
several animal taxa, from frogs to mammals and birds, and is one of the
best examples of the application of acoustic analysis to population.
Bioacoustic monitoring is a rapidly developing tool in nature pro-
tection, supported by the latest technological and analytical achieve-
ments (Snaddon et al., 2013). Unlike the related field of eco-acoustics,
bioacoustics is behavior-focused and focuses on acoustic signals of in-
dividuals and species, rather than on wider ecological processes or
habitats (Sueur and Farina, 2015). The usefulness of bioacoustical
material collected is very high, because it can be used when analyzing
all species of sound-producing animals, especially those rare and diffi-
cult to observe (Williams et al., 2018; Wrege et al., 2017). Currently,
bioacoustic monitoring is becoming increasingly popular in measuring
indicators such as presence-absence of given animals (Sebastián-
González et al. 2015), richness of species diversity (Celis-Murillo et al.,
2012), numbers (counts) (Borker et al., 2014) and density of occurrence
(Rogers et al., 2013; Stevenson et al., 2015). Conducting long-term
acoustic research, researchers are able to observe new, previously un-
known behaviors of some animal species. For example, in situ activity
patterns of any species of elephant were poorly known prior to bioa-
coustic studies (Wrege et al., 2017).
This kind of research is becoming increasingly popular in bird bio-
diversity research. There are many reasons why these animals are dif-
ficult to record visually. Their fear of human, masking colors, rare oc-
currence, and protected areas that are difficult to get to make
bioacoustics the only way to study them. For example, sounds of Cory's
shearwaters (Calonectris diomedea) are most detectable at night. This,
combined with their tendencies to breed on inaccessible cliff faces on
W. Penar, et al.
remote islands, complicates monitoring (Williams et al., 2018). Vocal
monitoring birds can help to understand the seasonal concentrations
and movements during migration too, providing insight on what geo-
graphic features are particularly important for migratory species
(Pamuła et al., 2017).
Bioacoustic research can also be used on smaller animal taxa, which
are difficult to see in the natural environment. Amphibians are the most
threatened vertebrate taxon of modern times. Baseline data and af-
fordable methods to monitor populations are absent for many frog
species. Furthermore, some species are visually cryptic, and detection
often relies upon male advertisement calls (Willacy et al., 2015).
For some time, bioacoustic tools have also been used to study insect
biodiversity. Insect identification is a primary need of entomologists
both for research applications and for pest control. Different kinds of
insects can emit sound to attract, repel, or threaten members of their
own species and to startle and evade predators. The same bioacoustic
methods in this case are a good way to study animals that are small and
difficult to find.
2.2. Bioacoustic monitoring in measurement of environmental pollution
Interestingly, bioacoustics can also be used for purposes other than
measuring species biodiversity. Research conducted by Kloepper and
Simmons (2014) proves that bioacoustic monitoring can be a good in-
dicator of climate change. Increases in global temperature can cause
changes in vast areas, including melting of glaciers, decreases in Arctic
ice cover, weather changes (droughts/floods) and increased disease risk
(Neftel et al., 1985; IPCC, 2013). These biotic and abiotic effects of
climate change can also affect environmental acoustics and thus change
communication between animals. This in turn leads to changes in entire
soundscapes and affects biodiversity, as some species are unable to
adapt quickly to changes in the environment (Peck et al., 2004).
One of the better known effects of climate change affecting acoustics
is due to increasing acidification of the oceans. Burning of fossil fuels
has fueled emissions of CO2 into the atmosphere for years. At present,
however, only about half of these emissions are still in the atmosphere,
the rest - due to precipitation - was absorbed by the seas and oceans,
affecting their acidification (Kloepper and Simmons, 2014).
Sound naturally attenuates in the ocean - a phenomenon known as
acoustic absorption. As a result of absorption, energy of a wave passing
through the medium is reduced, causing the medium's internal energy
to increase. Sound absorption depends on temperature, pressure, sali-
nity and, amongst others, acidity. In the case of ocean acidification, this
natural damping ability may be further compromised. Absorption
changes that depend on pH occur at frequencies below 3 kHz.
Miller et al. (2014) proved that for a pH of 7.5, the difference in ab-
sorption between low- (500 Hz) and high-frequency tone (5 kHz) is
about 2.5 dB, but at pH 8.5 the difference in absorption can be as sig-
nificant as 4.5 dB. At present, the average global pH of ocean surface is
around 8.0, but continued failure to tackle problems related to CO2
emissions will reduce it by 0.3 or more by the end of this century
(Orr et al., 2005). Climate forecasts estimate that future carbon dioxide
emissions will continue to acidify water, which is expected to reduce
sound absorption, especially at low frequencies, by up to 40% in 100
years (Hester et al., 2008). Reduced absorption of sound in the ocean
means that sounds, both natural and anthropogenic, will travel further.
An increase in anthropogenic sound levels will contribute to more
“background” noise in the ocean that will affect the behavior (including
acoustic behavior) of various marine animals. Studies conducted on
whales show that in noisy environments, animals increase the duration
of their sounds, their intensity and modulate their frequency
(Miller et al., 2014; Kloepper and Simmons, 2014). Furthermore, an-
thropogenic noises also affect whale behavior changes such as inter-
ruptions in foraging or migrations (Aguilar Soto et al., 2006). Research
conducted by Nowacek et al., 2004 showed that beaked whales sub-
jected to anthropogenic sounds are susceptible to decompression
3
Ecological Complexity 43 (2020) 100847
sickness caused by too fast ascent. In the worst cases in areas where
deep waters occur in close proximity to shallow waters, beaked whales
may swim into shallow waters to avoid certain sounds and could strand
if they are unable to navigate back to deeper waters (Parks et al., 2014).
Bioacoustics highly effectively serves as a tool for measuring the
impact of human activities on the environment not only in the waters.
Also on land we can estimate changes in the ecosystem by recording
and analyzing sounds.
Birds are among the most-studied organisms on earth and constitute
an important indicator group demonstrating effects of climate change
in particular as concerns changes in tropical ecosystems
(Şekercioğlu et al., 2012). Most tropical birds are endemic, sedentary
species, isolated either in tropical mountains or lowlands without ac-
cess to hills (Şekercioğlu et al., 2012). Climate warming is the main
factor causing loss of natural habitats at higher altitudes, while pre-
cipitation is destroying the habitats of birds living in the lowlands
(Enquist, 2002). Bioacoustic studies conducted in such areas may be
used to observe and assess the level of climate change by monitoring
the animals which live there.
Among places most vulnerable to global warming and rising sea and
ocean levels are coastal ecosystems (Waycott et al., 2009). Most bays
are located less than three meters above sea level – such altitudes are
also preferred by sea birds. Such places may in the future be flooded
during high water periods, and even during high tide
(Şekercioğlu et al., 2012). By recording and analyzing the sounds of the
most vulnerable taxa, we are able to determine changes in the number
of individuals and see how climate change affects biodiversity.
Changes in the structure of atmospheric precipitation caused by
environmental pollution also significantly affect animal sounds; either
by changing humidity and thus absorption of sound by the atmosphere,
or by changing the seasons and parameters of their vocalization. Snell-
Rood (2012) noted that in the same species of bats, acoustic commu-
nication differed between the rainy and dry seasons. In the rainy sea-
sons, when atmospheric precipitation and humidity were high and
sound absorption was higher by 0.58 dB/m than in the dry season, the
echolocation sounds of bats were of longer duration and lower fre-
quency.
Information on the current and projected impact of environmental
pollution on climate change can be used to create appropriate practices
in nature protection. Physiological, ecological and biogeographic fea-
tures that increase vulnerability of birds to climate change also occur in
other animals. Current conservation methods aimed at reducing the
risks posed by climate change for different bird species could also help
species from other taxa in the future. To start protecting the species
most vulnerable to climate change in a timely manner, reliable and
proven methods are needed to track habitat modification and perform
animal counts. Application of bioacoustic monitoring, relevant to any
taxa with recognized vocalizations seems to be an excellent solution.
Information‐rich bioacoustic recordings can facilitate the investigation
of multiple traits of birdsong as well as other cryptic behaviors that may
be relevant to individual fitness affected by climate changing. More
research in this way provides a viable solution for standardized long‐-
term automated monitoring of animal populations and behaviors in
endangered environment.
2.3. Bioacoustics in research on extinct ecosystems
In addition to the current applications of bioacoustics, acoustic
monitoring can also serve to create bioacoustic time capsules (Sugai
and Llusia, 2019). Collecting acoustic recordings around the world can
help create the benchmark for upcoming research, helping us under-
stand the magnitude and direction of changes in ecosystems.
Some of the analyzed recordings found in biological collections
belong to already extinct animal species, such as Yellow Warbler
(Vermivora bachmanii) or Darwin's frog from Chile (Rhinoderma
rufum). According to paleontological terminology, such recordings can
W. Penar, et al.
be referred to as trace fossils, i.e. records of past biological activity
(Seilacher, 2007) of already extinct animals. Creating such record col-
lections helps preserve evidence of existence of many animal species,
and can be invaluable in the future. Such recordings best demonstrate
the speed of changes in the ecosystems.
In addition, collections of sound recordings of various animals to-
gether with existing knowledge in the field of anatomy and ethology
can be used by scientists attempting to reconstruct the sounds of extinct
animal species based on their morphological and behavioral features.
Paleontologists have attempted to recreate the sounds of extinct
crickets (Gu et al., 2012), dinosaurs (Diegert and Williamson, 1998)
and hominids (Barney et al., 2012).
Such use of bioacoustics provides historical information on the
structure and dynamics of past ecosystems, and creates registers of
extinct animals for future generations. Furthermore, it allows for a
better understanding of ongoing changes in the environment and better
protection of endangered animal species.
3. Summary
In this review, we have provided an overview of bioacoustics
monitoring for ecology and conservation, and the effects of anthro-
pogenic noise on animal species. Many terrestrial and aquatic species,
including insects, frogs, birds and mammals use vocalizations as part of
their social and reproductive behavior (Bradbury and
Vehrencamp, 1998). The recording of their sounds and subsequent
analysis allows for a better understanding of species biodiversity –
however, it is also is a good measure of changes in ecosystems.
Passive acoustic monitoring of biological sounds allows to non-in-
vasively collect long-term and standardized data on ecosystem biodi-
versity. Such research is increasingly used in both terrestrial and
aquatic ecosystems (Linke et al., 2018). The presented studies show that
using bioacoustics can also be more effective and beneficial than the
traditional methods used so far. The recording of sounds from different
environments and geographic areas offers the possibility to make
comparisons between habitats, to show how they change over the years
because of climate change. Some environments, such as deep oceans or
tropical forests, represent a true challenge posed to traditional research.
The placement of autonomous acoustic recording stations allows the
collection of important information, especially over long periods.
Vocalizations of every acoustically communicating animal are
threatened by climate change. For marine animals, the source of
changes in vocalization abilities is ocean acidification and increased
ambient noise, which can affect communication and foraging behavior.
For terrestrial animals, changes in precipitation and temperature may
result in modifications of the sounds emitted, as well as certain mod-
ifications to the auditory system. Together with changes in species
distribution due to environmental parameters, cumulatively these fac-
tors can cause changes in the entire landscape of acoustics ecosystems.
Thanks to acoustic biomonitoring, we can understand how the sounds
of entire habitats and acoustic ecosystems will change in response to the
changing climate and how it will affect bioacoustics on a global scale
(Kloepper and Simmons, 2014).
Funding
This research did not receive any specific grant from funding
agencies in the public, commercial, or not-for-profit sectors.
Declaration of Competing Interests
The authors declare that they have no know competing financial
interests ro personal that could have appeared to influence the work
reported in this paper.
4
Ecological Complexity 43 (2020) 100847
Supplementary materials
Supplementary material associated with this article can be found, in
the online version, at doi:10.1016/j.ecocom.2020.100847.
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