0% found this document useful (0 votes)
43 views12 pages

Terrestrial Acoustic Monitoring Review

Uploaded by

Nátaly Danndara
Copyright
© © All Rights Reserved
We take content rights seriously. If you suspect this is your content, claim it here.
Available Formats
Download as PDF, TXT or read online on Scribd
0% found this document useful (0 votes)
43 views12 pages

Terrestrial Acoustic Monitoring Review

Uploaded by

Nátaly Danndara
Copyright
© © All Rights Reserved
We take content rights seriously. If you suspect this is your content, claim it here.
Available Formats
Download as PDF, TXT or read online on Scribd
You are on page 1/ 12

See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/329321912

Terrestrial Passive Acoustic Monitoring: Review and Perspectives

Article in BioScience · November 2018


DOI: 10.1093/biosci/biy147

CITATIONS READS

448 3,184

4 authors:

Larissa Sayuri Moreira Sugai Thiago Sanna Freire Silva


Cornell University University of Stirling
28 PUBLICATIONS 1,216 CITATIONS 148 PUBLICATIONS 4,164 CITATIONS

SEE PROFILE SEE PROFILE

José Wagner Ribeiro Jr Diego Llusia


WildMon Autonomous University of Madrid
21 PUBLICATIONS 835 CITATIONS 76 PUBLICATIONS 1,878 CITATIONS

SEE PROFILE SEE PROFILE

All content following this page was uploaded by Larissa Sayuri Moreira Sugai on 12 February 2019.

The user has requested enhancement of the downloaded file.


Overview Articles

Terrestrial Passive Acoustic


Monitoring: Review and
Perspectives

Downloaded from https://academic.oup.com/bioscience/article-abstract/69/1/15/5193506 by guest on 12 February 2019


LARISSA SAYURI MOREIRA SUGAI, THIAGO SANNA FREIRE SILVA, JOSÉ WAGNER RIBEIRO JR.,
AND DIEGO LLUSIA

Passive acoustic monitoring (PAM) is quickly gaining ground in ecological research, following global trends toward automated data collection
and big data. Using unattended sound recording, PAM provides tools for long-term and cost-effective biodiversity monitoring. Still, the extent
of the potential of this emerging method in terrestrial ecology is unknown. To quantify its application and guide future studies, we conducted
a systematic review of terrestrial PAM, covering 460 articles published in 122 journals (1992–2018). During this period, PAM-related studies
showed above a fifteenfold rise in publication and covered three developing phases: establishment, expansion, and consolidation. Overall, the
research was mostly focused on bats (50%), occurred in northern temperate regions (65%), addressed activity patterns (25%), recorded at
night (37%), used nonprogrammable recorders (61%), and performed manual acoustic analysis (58%), although their applications continue to
diversify. The future agenda should include addressing the development of standardized procedures, automated analysis, and global initiatives
to expand PAM to multiple taxa and regions.

Keywords: audio recorders, auditory monitoring, automated data collection, bioacoustics, ecoacoustics, faunal survey, soundscapes

W ildlife monitoring has undergone a remarkable


transformation in the twenty-first century, with the
development and introduction of technologies that greatly
this reason, auditory surveys have become the basis for
many biodiversity assessment programs, such as the North
American Amphibian Monitoring Program (Weir and
expand the possibilities for biodiversity assessment and eco- Mossman 2005) and several terrestrial bird survey initia-
logical research (e.g., remote sensing, camera trapping, DNA tives (Rosenstock et al. 2002).
barcoding; Pimm et al. 2015). These methods have allowed In addition to these properties, sounds can be reliably
us to better track the effects of a rapidly changing environ- recorded by analog or digital devices. Historically, the devel-
ment on biodiversity, including the impacts of habitat loss, opment of portable tape recorders enabled researchers to
species introductions, and climate change (Llusia et al. 2013, record animal sounds in the field, providing new oppor-
Schmeller et al. 2017). Among these cutting-edge technolo- tunities for faunal surveys (Parker 1991, Vielliard 1993,
gies, automated audio recorders have recently revolutionized Haselmayer and Quinn 2000). A subsequent milestone
traditional faunal survey methods based on auditory detec- was the release of digital audio recorders, which supplied
tion (Obrist et al. 2010, Blumstein et al. 2011). researchers with affordable and smaller devices, maintain-
Terrestrial environments are typically replete with sounds ing high fidelity to analog signals and optimizing auditory
from multiple sources, particularly from animals (McGregor surveys (Obrist et al. 2010). More recently, early autonomous
2005). Animal sounds are highly informative. In addition to recorders provided additional innovations by allowing unat-
their use as characteristics for species identification, they tended recording over long periods, with longer battery life
also convey cues about abundance, position, body size, and and programmable recording schedules (Sueur et al. 2012,
motivation of emitters (Bradbury and Vehrencamp 1998, Digby et al. 2013). These advances translate into several
Wilkins et al. 2013). Additionally sounds can propagate advantages for species surveys, including broader temporal
in multiple directions, through physical obstacles, and and spatial sampling, reduced observer bias, and long-term
over relatively long distances; therefore, vocal animals are storage of field recordings, which can later be digitally ana-
generally more easily detectable by hearing than by see- lyzed and checked for dubious vocalizations. Therefore, pas-
ing (Rosenthal and Ryan 2000, Heinicke et al. 2015). For sive acoustic monitoring (PAM) now stands as a powerful

BioScience 69: 15–25. © The Author(s) 2019. Published by Oxford University Press on behalf of the American Institute of Biological Sciences. All rights
reserved. For Permissions, please e-mail: [email protected].
doi:10.1093/biosci/biy147 Advance Access publication 29 November 2018

https://academic.oup.com/bioscience January 2019/ Vol. 69 No. 1 • BioScience 15


Overview Articles

tool for biodiversity monitoring, supporting a variety of sciences, zoology, ornithology, and evolutionary biology. In
ecological, behavioral, and conservation applications (Farina addition, to include potentially meaningful articles absent
and Gage 2017, Wrege et al. 2017, Linke et al. 2018). from the reviews in WoS, complementary searches were per-
Wildlife surveys based on passive acoustics have been formed using Google Scholar on 15 September 2017 and 27
widely applied in marine environments to detect species September 2018, using the keyword combination ((wildlife
presence, estimate population dynamics, measure home acoustic) AND (passive acoustic monitoring)).
ranges, and determine activity patterns and movement The literature search procedure resulted in more than
routes (Mellinger et al. 2007). Similarly, this technique 10,000 articles. From this initial list, we excluded those unre-
offers ample possibilities for faunal surveys in terrestrial lated to this review (false positives)—that is, articles that did
environments, because acoustic sensors allow noninvasive not employ PAM to survey biological aspects of terrestrial
data collection for a wide range of animals emitting detect- fauna, such as underwater environments (for a review, see

Downloaded from https://academic.oup.com/bioscience/article-abstract/69/1/15/5193506 by guest on 12 February 2019


able acoustic signals (Browning et al. 2017). Moreover, PAM Mellinger et al. 2007); environmental sound pressure level
can increase the temporal and spatial coverage of monitoring assessments (see Lynch et al. 2011, Shannon et al. 2016);
programs while providing favorable cost–benefit trade-offs and the use of acoustic lures, playbacks, and call–broadcast
for wildlife surveys in relation to traditional survey methods surveys without joint use of passive acoustics (see McGregor
(Ribeiro et al. 2017, Wrege et al. 2017). Nevertheless, the use 2000, Suraci et al. 2017). Articles aimed at estimating spe-
of PAM in terrestrial-monitoring programs is still relatively cies density and movement by acoustic location systems
incipient when compared with its use for marine fauna, and using microphone arrays were also excluded, because several
it has only recently gathered significant attention (Servick comprehensive reviews have been published on these meth-
2014). By understanding the current trends, limitations, and ods (see Marques et al. 2013, Stevenson et al. 2015, Measey
challenges of terrestrial PAM, we can better guide future et al. 2017). This filtering finally led to a final data set of 460
applications and the progress of this emergent method in selected articles (see the supplemental information).
ecological research. From each article found in this literature search, we
In the present article, we provide a comprehensive review extracted key information to characterize PAM-based
and synthesis of the use of passive acoustic monitoring for research: publication year, monitoring year, journal of pub-
terrestrial wildlife survey. First, we characterize the his- lication, research topic, monitored taxa, geographical coor-
torical evolution and expansion of PAM-based studies across dinates of the recorded sites, recording settings (type of
research topics, focal organisms, geographical locations, and recorder and daily recording period), and acoustic analysis
methodological procedures. Second, we synthesize current applied to derive biological information from the passive
applications, trends, key shortfalls, and future challenges, recordings (table 1).
drawing attention to the potential of PAM to support of
global initiatives and citizen science projects, through the Overview of passive acoustic monitoring in
adoption of standardized procedures and coordinated moni- terrestrial ecosystems
toring of multiple taxa and regions using common monitor- Studies using PAM in terrestrial ecosystems started in the
ing stations. 1990s and have exponentially increased in the last decades,
at an average rate of 2.8 articles per year in the 1990s (from
Reviewing the literature of terrestrial passive 0 to 11 per year), 10.8 in the 2000s (from 3 to 19 per year),
acoustic monitoring and 42.5 in the 2010s (from 28 to 62 per year; figure 1a).
We conducted a systematic review of passive acoustic moni- Noticeably, the number of articles increased more than
toring on terrestrial ecosystems using complementary litera- fifteenfold during this period, with the peak in 2017 (i.e.,
ture searches in the Thomson Reuters Web of Science (WoS) the last complete year spanned by this review). The actual
platform, spanning all years on record (1900–2018). The first monitoring reported in these articles has a similar pat-
search was performed on 24 August 2017, with the following tern to the publication trend, with a 3–4-year lag between
keywords: (((sound* OR acoustic* OR call* OR song* OR sing* monitoring and publication; the peak was in 2012, and 50%
OR vocal*) AND (monito* OR passive OR record* OR survey of the recordings were made after 2008 (figure 1b). This
OR sampl* OR automat* OR activit*)) AND (wildlife OR prominent rise in PAM-based research has mostly resulted
biodiversit* OR animal* OR soundscape* OR ecoacoustic* OR from the increased availability of automated audio recorders,
vertebrate* OR mammal* OR bird* OR avian* OR anura* OR whose use has risen from 2 to 48 articles per year since their
amphibia* OR frog* OR toad* OR insect* OR artropod* OR commercial release in 2007. So far, this type of recorder rep-
orthoptera OR cricket* OR cicada*)). A second search was resents 39% of all published articles, whereas nonprogram-
performed on 9 September 2017, using ((call* OR acoustic*) mable audio recorders represent 61% (figure 1a).
AND (survey OR activit*)). To update our database, the two Overall, we could delimit three general developing phases
previous literature searches were repeated on 27 September of terrestrial PAM: establishment, during which the first
2018. These searches were restricted to 13 WoS subject areas: studies using ad hoc acoustic methods to assist faunal inven-
biology, biodiversity conservation, environmental sciences, tories and investigate species activity and habitat use were
remote sensing, ecology, entomology, acoustic, behavioral published (before 2000); expansion, which is represented by

16 BioScience • January 2019/ Vol. 69 No. 1 https://academic.oup.com/bioscience


Overview Articles

Table 1. Description of items compiled in this review and used to characterize publication and research trends in passive
acoustic monitoring in terrestrial ecosystems from 1992–2018.
Items Classes Categories Description
Publication Publication year
Journal of publication
Data collection Monitoring year Years when the acoustic monitoring was conducted
Study sites Geographical coordinates of the sites at which the acoustic
monitoring was conducted
Research area Research topics Activity patterns Studies assessing seasonal and diel activity levels of populations
and communities

Downloaded from https://academic.oup.com/bioscience/article-abstract/69/1/15/5193506 by guest on 12 February 2019


Behavior Studies focused on aspects of animal behavioral biology
Community Ecology Studies addressing the determinants of species diversity,
community structure, and assembly
Conservation Biology Studies concerned with the conservation of species, habitats, and
ecosystems
Ecoacoustics Investigations of soundscape patterns and dynamics
Habitat use Studies addressing species preference and selection over distinct
environmental conditions
Signal processing Automated methods for detecting and classifying species in
acoustic recordings
Species assessment Faunal inventories and surveys aiming to document biodiversity
Species distribution/Occupancy Estimates of distribution patterns of species over multiple scales;
imperfect species detectability
Survey technique Protocols, data collection procedures, or comparisons with other
survey methods
Urban Ecology Ecological studies that include urban context
Monitored taxa Bats
Nonflying mammals
Birds
Anurans
Invertebrates
Soundscapes Environmental sounds as a whole that emerge from the landscape
Recording settings Recording system Automated recorder Audio recorders with scheduled recording options
Nonprogrammable recorder
Recording period Continuous Recordings obtained continuously across the day
Dawn Recordings obtained exclusively at dawn
Morning
Afternoon
Dusk
Night
Acoustic analysis Manual Extraction of biological information mostly relied on human effort
(e.g., manual measurement of acoustic parameters, visual or aural
inspection of spectrograms)
Semiautomated Combination of manual and automated methods
Automated Extraction of biological information mostly relied on computing
effort (e.g., built-in software recognizers, ad hoc discriminant
function analyses)
Acoustic indices Estimation of α or b acoustics-based ecological indices (which is a
particular automated method)

a visible increase in the number of studies focusing on the research topics and reaching the highest publication rates in
same earlier topics, followed by an initial diversification of recent years (after 2010; figure 2).
research areas (conservation biology, community ecology, Presently, studies using terrestrial PAM cover a wide
and ecoacoustics, between 2000–2010); and consolidation, range of research areas, studied organisms, surveyed loca-
which is the exponential growth of studies covering multiple tions, and methodological approaches. The 460 articles

https://academic.oup.com/bioscience January 2019/ Vol. 69 No. 1 • BioScience 17


Overview Articles

patterns to estimate thermal tolerances


of calling behavior, with further implica-
tions for the assessment of climate change
impacts. Cryptic, rare, and endangered
species, such as koalas (Ellis et al. 2011)
and elephants (Wrege et al. 2017), have
been monitored to reveal behavioral and
ecological aspects. Applied conserva-
tion programs have also benefited from
PAM, through monitoring of hunting
activities (Astaras et al. 2017), studies

Downloaded from https://academic.oup.com/bioscience/article-abstract/69/1/15/5193506 by guest on 12 February 2019


of species responses to anthropogenic
impacts (Gil et al. 2014), and multitaxa
assessments (Deichmann et al. 2017).
Together, these successful applications
reinforce the ample potential of passive
acoustics for practical applications in
terrestrial ecosystems, contributing to
the toolbox of conservation practitioners
and researchers (Ribeiro et al. 2017).

Monitored taxa. Over the focal organ-


isms investigated with terrestrial
PAM, bats were, by far, the biological
group most studied (50% of the arti-
cles; figure 3a). Likewise, the journal
with the most articles on terrestrial
PAM is fully devoted to this group
(9%, Acta Chiropterologica; figure 1c).
However, most of the articles within
this taxon were based on nonpro-
grammable audio recorders (89%),
with automated devices only recently
appearing (figure 3b). The trajectory
of PAM applications for bat surveys
Figure 1. The publication rates of studies using passive acoustic monitoring in clearly exemplifies the three distinct
terrestrial ecosystems (1992–2018) across (a) years, (b) monitoring periods, developing phases of PAM for ter-
and (c) journals. Only journals with the most number of articles are shown. restrial application: first, focusing on
In the upper panels (a) and (b), the colors represent the recording system methodological issues regarding the
employed: automated audio recorders (white) and nonprogrammable recorders use of ultrasound detectors and early
(gray). applications for species assessment
(Rachwald 1992, Kuenzi and Morrison
identified in our search were published in 122 journals, 1998), followed by an increase in applications and diver-
with 14 journals concentrating 46% (210) of all of the arti- sification of investigated topics, and, finally, consolidating
cles (figure 1c). Across these journals, the main research as a robust method to support a variety of goals including
subjects were divided among taxonomy-oriented studies, species inventory, population/community assessment, and
applied ecology and conservation biology, and method- species conservation (Russo and Jones 2003, Froidevaux
ological studies. Among the research topics investigated et al. 2014).
so far, reports on species activity patterns were the most After bats, birds were the most researched terrestrial group
frequent (25%), followed by habitat use (16%), survey (20%), followed by anurans (12%), nonflying mammals
technique (15%), and species assessment (9%; figure 2). (6%), and invertebrates (5%). Automated recording systems
Terrestrial PAM has become as useful as other well- were more frequently used than nonprogrammable ones for
established survey techniques (e.g., camera traps) to assess all of these groups, except invertebrates (figure 3a). Pioneer
and monitor species, either as a standalone method or as a contributions between 1990 and 2000 mostly reported the
complementary approach (Browning et al. 2017). For exam- efficiency of acoustic methods, discussed the optimization of
ple, Llusia and colleagues (2013) used anuran phenological sampling procedures (e.g., Mohr and Dorcas 1999, Bridges

18 BioScience • January 2019/ Vol. 69 No. 1 https://academic.oup.com/bioscience


Overview Articles

Downloaded from https://academic.oup.com/bioscience/article-abstract/69/1/15/5193506 by guest on 12 February 2019


Figure 2. The research topics of studies using passive Figure 3. The taxa studied in articles using passive acoustic
acoustic monitoring in terrestrial ecosystems (1992–2018): monitoring in terrestrial ecosystems (1992–2018): (a) the
(a) number of published articles per topic, and (b) density number of published articles per focal organism and (b)
plots of articles over time. Vertical black lines represent the density plots of the articles over time. The colors and line
median number of published articles for each topic. types represent the recording system employed: automated
audio recorders (the white boxes and solid lines), and
nonprogrammable recorders (the color boxes and dashed
lines). The vertical black lines represent the median
and Dorcas 2000), and addressed general activity patterns, number of published articles for each taxon.
such as for tropical cricket assemblages (Riede 1993) and
birds (Evans and Mellinger 1999).
Soundscapes (i.e., environmental sounds as a whole that patterns, and this new research program has been garnering
emerge from the landscape) were examined in 7% of the increasing significance in ecological research (Servick 2014,
studies. This recent approach has been fostered by the chal- Gasc et al. 2015, Farina and Gage 2017).
lenge of extracting biological information from the large vol-
umes of acoustic data obtained through PAM, using acoustic Geographical distribution. PAM-based studies have been
indices to synthesize patterns made by vocal organisms, irre- mostly concentrated in the northern temperate zone (65%),
spective of species identity (Sueur et al. 2008). Consequently, primarily in North America and Europe, whereas a mark-
a new research area was created, first formalized as sound- edly smaller number of studies occurred in tropical (25%)
scape ecology and posteriorly as ecoacoustics (Pijanowski and southern temperate zones (10%). To our knowledge,
et al. 2011, Sueur and Farina 2015). Soundscape dynamics large areas of the globe still have no recorded sites with this
have shown promise to represent overall animal activity technique to date, with regions of Asia, western Oceania,

https://academic.oup.com/bioscience January 2019/ Vol. 69 No. 1 • BioScience 19


Overview Articles

Downloaded from https://academic.oup.com/bioscience/article-abstract/69/1/15/5193506 by guest on 12 February 2019


Figure 4. The geographic distribution of the study sites in articles using passive acoustic monitoring in terrestrial
ecosystems (1992–2018) included in this review. The colors represent the focal taxa of each article.

northern Africa, and southern South America standing as and soundscapes were investigated over wider periods
the main gaps (figure 4). Passive recordings of bats, birds, and mainly at dawn (34% and 37%). During the morning
and anurans were more widely distributed than other and afternoon, recordings were collected only in studies
biological groups. PAM of nonflying mammals was con- focused in nonflying mammals, birds, invertebrates, and
centrated on a few focal taxa, such as elephants in Africa, soundscapes (figure 5b).
whereas invertebrate and soundscape studies likely reflect
the geographical location of the main research groups in Acoustic analysis. The main procedure used to extract bio-
Europe and the United States. logical information from PAM recordings has been manual
analysis, which mostly relies on human effort (e.g., manual
Recording periods. Although 19% of the studies using PAM measurement of acoustic parameters, visual or aural inspec-
recorded audio samples throughout the entire day, the tion of spectrograms) and corresponded to 58% of the
majority of studies recorded only during specific periods studies (figure 6a). Fully automated analyses were applied
(figure 5a). Among these, sampling effort was mostly con- in only 19% of the studies, with relatively more frequent use
centrated at night (37%) and dusk (32%), when nonpro- for bat signals (32% of the articles within the group), because
grammable recorders were primarily used (72% and 74%, several software packages contain built-in classification
respectively). This temporal asymmetry was due to the algorithms and libraries for automated recognition of bat
larger contribution of studies focusing on nocturnal spe- species (e.g., Analook and Batsound). For other biological
cies—namely, bats and anurans (figure 5b). The recordings groups, fully automated methods are still being developed
at dawn represented 21% of the recording periods and were and tested (e.g., Digby et al. 2013, Astaras et al. 2017, Ulloa
conducted with both types of recorders in a similar propor- et al. 2018), and there are still relatively few alternatives to
tion (56% with nonprogrammable). Morning and afternoon manual or semiautomated PAM data analysis (Kasten et al.
were the least frequent recording periods (figure 5a), with a 2012, Llusia et al. 2013).
higher proportion of automated recorders being used (68% Semiautomated procedures (i.e., combining both manual
and 74%, respectively). and automated analyses) were applied in 15% of the studies,
As was expected, researchers generally prioritized with more applications than fully automated procedures for
acoustic monitoring on periods coinciding with the high- anurans, birds, and nonflying mammals (figure 6). Acoustic
est activity levels of the species of interest (figure 5b). indices (10.5%) were applied mostly for soundscape stud-
Therefore, bats and anurans were investigated at more ies, which, by definition, rely exclusively on the automated
restricted daily periods, mainly at night (43% and 51%) extraction of these indices to represent overall patterns of
and dusk (38% and 30%, respectively), whereas birds acoustic communities. Interestingly, acoustic indices were

20 BioScience • January 2019/ Vol. 69 No. 1 https://academic.oup.com/bioscience


Overview Articles

Downloaded from https://academic.oup.com/bioscience/article-abstract/69/1/15/5193506 by guest on 12 February 2019


Figure 5. The daily recording periods applied in studies
using passive acoustic monitoring in terrestrial ecosystems Figure 6. The analysis approach applied to acoustic data
(1992–2018): (a) the number of published articles per in studies using passive acoustic monitoring in terrestrial
period (excluding those performed throughout the entire ecosystems (1992–2018): (a) the number of published
day) and (b) the number of articles per period for each articles per type of acoustic analysis and (b) the proportion
taxon. In the upper panel (a), the colors represent the of articles per type for each taxon.
recording system employed: automated audio recorders
(white) and nonprogrammable recorders (gray).

also used as proxies for species diversity by a few studies although some custom passive audio recorders capable of
(figure 6). monitoring the vocal activity of terrestrial fauna were pro-
posed early in the literature (Peterson and Dorcas 1994).
Challenges and future directions for terrestrial PAM Examples of methodological developments include studies
We identified three main challenges for a further expan- providing field recording protocols (Obrist et al. 2010),
sion of PAM-based research in terrestrial ecosystems. designing methods for estimating the detection space of
These shortfalls, which can likely be extended to the PAM stations (Llusia et al. 2011), comparing detection
application of PAM in other environments, are nonstan- accuracy in relation to human observers (Digby et al. 2013,
dardized monitoring procedures, time-consuming acous- Wimmer et al. 2013) and to other survey techniques (Horton
tic analysis, and limited data curation and data sharing et al. 2015, Enari et al. 2017), and evaluations of changes in
resources. detectability given different recording schedules (La and
Research focused on methodological approaches and the Nudds 2016, Madalozzo et al. 2017). In addition, recent
limitations of PAM only substantially appeared during the efforts to promote ecoacoustics as a new discipline have
consolidation phase identified in this review (2010–2018), also generated contributions to PAM through both semiotic

https://academic.oup.com/bioscience January 2019/ Vol. 69 No. 1 • BioScience 21


Overview Articles

and theoretical unifying proposals (Farina 2014, Sueur and Another necessary step forward for increasing the appli-
Farina 2015, Farina and Gage 2017). However, despite these cability of PAM is the development and improvement of
efforts, further formalization of general methods for design- widely available sound repositories for curation, manage-
ing and employing PAM programs remain a challenging ment, and sharing of temporal acoustic data sets, facili-
objective for future research. Such a methodological frame- tating the access and preservation of these sizeable data
work should include, for instance, generalized procedures sets. Existing public sound libraries and repositories are
to estimate species detectability, protocols for determining mostly focused on storing conventional manual audio
adequate recording schedules and sampling efforts, and recordings (i.e., directional recordings), and their infra-
guidelines to optimize the set of audio settings and auton- structure is often not suitable for transferring and storing
omy in PAM stations. These accomplishments would benefit the raw time series of recordings produced by PAM. To fill
forthcoming studies by guiding decision-making in PAM this gap, new repository initiatives have been appearing

Downloaded from https://academic.oup.com/bioscience/article-abstract/69/1/15/5193506 by guest on 12 February 2019


planning and standardizing sampling protocols (Brandes for managing PAM data, such as ARBIMON (Aide et al.
2008, Roch et al. 2016). 2013), Pumilio (Villanueva-Rivera and Pijanowski 2012),
A critical challenge in PAM studies is still the analy- and REAL (Kasten et al. 2012). Ideally, researchers should
sis and handling of very large amounts of acoustic data, archive audio recordings in sound repositories, similar to
especially for programs spanning wide temporal or spa- what is done for museum specimens and DNA sequences,
tial extents (Browning et al. 2017). As the data volumes although this practice is still not ubiquitous (Toledo et al.
resulting from PAM programs often approach the scale 2015). Because bandwidth and storage capabilities have
of big data, automation of essential procedures such as been increasing exponentially, we expect the rapid prolif-
species detection and recognition are desirable. There are eration of acoustic repositories in the next decade, with new
currently several research areas devoted to developing opportunities for collective efforts on managing and analyz-
automated methods to meet this pressing demand (e.g., ing terrestrial PAM data.
signal processing and pattern recognition; Xie et al. 2017,
Ulloa et al. 2018). However, current solutions often require Integrating PAM to global monitoring networks
professional experience and time-consuming supervision. Methods to capture multiple taxa information over broad
An open avenue is the development of analytical solutions spatial and temporal scales have been a central issue for
that are transferable among multiple species and acoustic improving global biodiversity monitoring in the face of
conditions, thus facilitating management and data min- human-driven changes (Schmeller et al. 2017). Worldwide
ing of PAM recordings for wildlife monitoring. Although long-term ecological research and monitoring networks
fully automated solutions are progressing, PAM users have often been supported by methods that enable coor-
and researchers should consider the best balance between dinated, standardized, and scalable projects (Pimm et al.
research goals, measurement accuracy, and time allocated 2015). In this context, we strongly advocate the use of PAM
to analysis of the time series of recordings, with semiauto- as a suitable and standardized method for measuring essen-
mated procedures currently being the preferred solution tial biodiversity variables using sensor networks (Kissling
(Kasten et al. 2012, Llusia et al. 2013). et al. 2017), thus increasing our ability to monitor and pre-
The challenge of extracting biological information is serve global biological diversity.
larger for noisy and complex environments. Manual scan- PAM stations can easily be added to existing monitoring
ning may be valuable when automated procedures show sites and can provide data from vocal animals. Affordable
poor performance, such as recordings containing overlap- commercial or custom-built recorders have become increas-
ping vocalizations or a low signal-to-noise ratio (Hugel ingly available, making acoustic monitoring more accessible
2012, Browning et al. 2017). Still, manual approaches are (e.g., Mennill et al. 2012, Farina et al. 2014, Whytock and
labor intensive and can be unattainable for large amounts of Christie 2017). Moreover, individual research teams should
recordings. These challenges have favored the development pool resources and combine efforts to overcome logistical
and use of acoustic diversity indices to characterize overall limitations and financial costs, benefiting collectively from
acoustic communities, although their biological meaning is extended data collection and improved knowledge of spe-
arguable (Servick 2014). Acoustic indices are more reliable cies natural history, site selection, and signal identification.
in representing general patterns of species vocal activity Coordinated PAM stations may also inspire the develop-
instead of diversity (Gasc et al. 2017) and offer singular ment of more customizable or accessible recording systems
opportunities to track global change impacts on biodiver- adaptable for different research purposes.
sity (Krause and Farina 2016, Sueur and Farina 2015). More Such advances could favor the implementation of PAM
research focused on identifying and understanding the in remote and currently unmonitored areas, meeting the
facets of biodiversity provided by acoustic indices are highly urgent need for tracking unprotected areas at risk (Watson
encouraged, because the acoustic component expressed by et al. 2016), located mostly in the same regions in which
these indices can be related to other biodiversity aspects, spatial gaps in acoustic monitoring have been identified
such as phylogenetic and functional diversity (Gasc et al. by our review. PAM is suitable for surveying threatened
2015). fauna and monitoring their responses to environmental

22 BioScience • January 2019/ Vol. 69 No. 1 https://academic.oup.com/bioscience


Overview Articles

change, contributing to the development of wildlife protec- The main barriers for the expansion of terrestrial PAM
tion strategies under the current global biodiversity crisis. remain in establishing baselines for standardizing acous-
In addition, a wide variety of taxa can be simultaneously tic sampling, and in developing efficient solutions for
monitored with audio recordings. Therefore, worldwide automated signal analysis of long-term acoustic data sets.
efforts to commit to a set of standardized procedures can Another step forward is the improvement of PAM-oriented
be facilitated by the availability of programmable recording sound repositories for data management and sharing. Global
schedules that allow the recording of multiple species in monitoring and citizen science initiatives can find in PAM
PAM (e.g., static ultrasonic detectors for monitoring high- flexible options to coordinate multitaxa assessments over
frequency animal sounds as bats and orthopteran species; varying ecological conditions, providing new procedures for
Newson et al. 2017). data collection over large spatial and temporal extents.
The increasing role of citizen science in providing large-

Downloaded from https://academic.oup.com/bioscience/article-abstract/69/1/15/5193506 by guest on 12 February 2019


scale ecological data also has a large potential to support Acknowledgments
the widespread adoption of PAM. The French national We thank the two anonymous reviewers and Raul Costa
acoustic biodiversity monitoring gathers acoustic data from Pereira for comments on the manuscript. LSMS acknowledges
orthopteran communities over a large extent of France, doctoral fellowships no. 2015/25316–6 and no. 2017/15772–
using passive audio recorders that have been supervised by 0, the São Paulo Research Foundation (FAPESP), and a
volunteers since 2006 (see Jeliazkov et al. 2016). In another Rufford Small Grant from The Rufford Foundation. TSFS
citizen-based program, a long-term integrated system of receives a research productivity grant (no. 310144/2015–9)
audiovisual recordings from Japan provides live streaming from the National Council of Technological and Scientific
from remote areas to online users; participants can identify Development (CNPq). JWRJ acknowledges doctoral fel-
bird species and discuss their identification through social lowship no. 2014/07113–8 and the São Paulo Research
media, improving the efficiency of bird inventories (Saito Foundation (FAPESP). DL acknowledges Global Marie S.
et al. 2015). Ritts and colleagues (2016) worked with First Curie fellowship no. EAVESTROP–661408 and postdoc-
Nations in Canada to deploy automated sound sensors and toral grant Atracción de Talento Investigador (no. 2016-T2/
interpret sounds along a potential shipping corridor and AMB-1722), granted by the European Commission (pro-
to determine its impacts on the population. Even before gram no. H2020) and the Comunidad de Madrid (CAM,
the expansion of passive acoustics, the volunteer-based Spain), respectively, and funding provided by Ministerio de
wildlife acoustic survey proposed by the North American Economía, Industria y Competitividad (research project no.
Amphibian Monitoring Program had already demonstrated CGL2017-88764-R, MINECO/AEI/FEDER, Spain).
the synergistic potential between citizen since and acoustic
monitoring (Cosentino et al. 2014). Supplemental material
Supplementary data are available at BIOSCI online.
Conclusions
Our review traces the emergence and progress of terrestrial References cited
PAM, a burgeoning toolbox for animal surveys. The use Aide TM, Corrada-Bravo C, Campos-Cerqueira M, Milan C, Vega G,
of PAM in terrestrial ecology has been growing exponen- Alvarez R. 2013. Real-time bioacoustics monitoring and automated
tially since the 1990s, reaching widespread adoption and a species identification. PeerJ 1: e103.
Astaras C, Linder JM, Wrege P, Orume RD, Macdonald DW. 2017. Passive
wide range of applications, with unprecedented publication
acoustic monitoring as a law enforcement tool for Afrotropical rainfor-
rates. Bats have been the most researched group until now, ests. Frontiers in Ecology and the Environment 15: 233–234.
mainly supported by nonprogrammable audio recorders. Blumstein, et al. 2011. Acoustic monitoring in terrestrial environments
Nevertheless, new technologies for the automated record- using microphone arrays: Applications, technological considerations
ing of animal sounds have fostered the consolidation of this and prospectus. Journal of Applied Ecology 48: 758–767.
Brandes ST. 2008. Automated sound recording and analysis techniques for bird
emerging method, especially since the 2010s, expanding
surveys and conservation. Bird Conservation International 18: S163–S173.
applications to a large variety of ecological and conservation Bridges AS, Dorcas, ME. 2000. Temporal variation in anuran calling behav-
studies focused on several terrestrial organisms and sur- ior: Implications for surveys and monitoring programs. Copeia 2000:
passing the use of nonprogrammable recorders. The devel- 587–592.
opment of innovative analytic tools for automated signal Bradbury JW, Vehrencamp SL. 1998. Principles of Animal Communication.
Sinauer.
detection and the computation of acoustic diversity indices
Browning E, Gibb R, Glover-Kapfer P, Jones KE. 2017. Passive Acoustic
have opened new avenues for PAM applications in commu- Monitoring in Ecology and Conservation. World Wildlife Fund
nity ecology and other scientific areas. However, our review Conservation Technology Series no. 1.
also unveiled important gaps in terms of both geographical Cosentino BJ, et al. 2014. Citizen science reveals widespread negative
coverage and temporal design of PAM programs. Monitored effects of roads on amphibian distributions. Biological Conservation
180: 31–38.
areas have been mostly concentrated in a few regions of the
Deichmann JL, Hernandez-Serna A, Delgado JA, Campos-Cerqueira M,
northern temperate zone, whereas recording efforts mainly Aide TM. 2017. Soundscape analysis and acoustic monitoring docu-
focused at dusk and night, because of the larger contribution ment impacts of natural gas exploration on biodiversity in a tropical
of studies on nocturnal species. forest. Ecological Indicators 74: 39–48.

https://academic.oup.com/bioscience January 2019/ Vol. 69 No. 1 • BioScience 23


Overview Articles

Digby A, Towsey M, Bell BD, Teal PD. 2013. A practical comparison of of calling temperatures in ectotherms. Global Change Biology 19:
manual and autonomous methods for acoustic monitoring. Methods in 2655–2674.
Ecology and Evolution 4: 675–683. Llusia D, Márquez R, Bowker R. 2011. Terrestrial sound monitoring
Ellis W, Bercovitch F, FitzGibbon S, Roe P, Wimmer J, Melzer A, Wilson R. systems, a methodology for quantitative calibration. Bioacoustics 20:
2011. Koala bellows and their association with the spatial dynamics of 277–286.
free-ranging koalas. Behavioral Ecology 22: 372–377. Lynch E, Joyce D, Fristrup K. 2011. An assessment of noise audibil-
Enari H, Enari H, Okuda K, Yoshita M, Kuno T, Okuda K. 2017. Feasibility ity and sound levels in U.S. National Parks. Landscape Ecology 26:
assessment of active and passive acoustic monitoring of sika deer popu- 1297–1309.
lations. Ecological Indicators 79: 155–162. Madalozzo B, Santos TG, Santos MB, Both C, Cechin S. 2017. Biodiversity
Evans W, Mellinger D. 1999. Monitoring grassland birds in nocturnal assessment: Selecting sampling techniques to access anuran diversity in
migration. Studies in Avian Biology 19: 219–229. grassland ecosystems. Wildlife Research 44: 78–91.
Farina A, Gage SH. 2017. Ecoacoustics: The Ecological Role of Sounds. Marques, et al. 2013. Estimating animal population density using passive
Wiley. acoustics. Biological Reviews 88: 287–309.

Downloaded from https://academic.oup.com/bioscience/article-abstract/69/1/15/5193506 by guest on 12 February 2019


Farina A. 2014. Soundscape Ecology: Principles, Patterns, Methods, and McGregor PK. 2000. Playback experiments: Design and analysis. Acta
Applications. Springer. Ethologica 3: 3–8.
Farina A, James P, Bobryk C, Pieretti N, Lattanzi E, McWilliam J. 2014. McGregor PK. 2005. Animal communication networks. Cambridge
Low cost (audio) recording (LCR) for advancing soundscape ecology University Press.
towards the conservation of sonic complexity and biodiversity in natu- Measey GJ, Stevenson BC, Scott T, Altwegg R, Borchers DL. 2017. Counting
ral and urban landscapes. Urban Ecosystems 17: 923–944. chirps: Acoustic monitoring of cryptic frogs. Journal of Applied Ecology
Froidevaux JSP, Zellweger F, Bollmann K, Obrist MK. 2014. Optimizing 54: 894–902.
passive acoustic sampling of bats in forests. Ecology and Evolution 4: Mellinger DK, Stafford KM, Moore SE, Dziak RP, Matsumoto H. 2007. An
4690–4700. overview of fixed passive acoustic observation methods for cetaceans.
Gasc A, Francomano D, Dunning JB, Pijanowski BC. 2017. Future direc- Oceanography 20: 36–45.
tions for soundscape ecology: The importance of ornithological contri- Mennill DJ, Battiston M, Wilson DR, Foote JR, Doucet SM. 2012. Field
butions. Auk 134: 215–228. test of an affordable, portable, wireless microphone array for spatial
Gasc A, Pavoine S, Lellouch L, Grandcolas P, Sueur J. 2015. Acoustic indi- monitoring of animal ecology and behaviour. Methods in Ecology and
ces for biodiversity assessments: Analyses of bias based on simulated Evolution 3: 704–712.
bird assemblages and recommendations for field surveys. Biological Mohr JR, Dorcas ME. 1999. A comparison of anuran calling patterns at two
Conservation 191: 306–312. carolina bays in South Carolina. Journal of the Elisha Mitchell Scientific
Gil D, Honarmand M, Pascual J, Perez-Mena E, Macias Garcia C. 2014. Society 115: 63–70.
Birds living near airports advance their dawn chorus and reduce overlap Newson SE, Bas Y, Murray A, Gillings S. 2017. Potential for cou-
with aircraft noise. Behavioral Ecology 26: 435–443. pling the monitoring of bush-crickets with established large-scale
Haselmayer J, Quinn JS. 2000. A comparison of point counts and sound acoustic monitoring of bats. Methods in Ecology and Evolution 8:
recording as bird survey methods in Amazonian southeast Peru. The 1051–1062.
Condor 102: 887–893. Obrist MK, Pavan G, Sueur J, Riede K, Llusia D, Marquez R. 2010.
Heinicke S, Kalan AK, Wagner OJJ, Mundry R, Lukashevich H, Kühl HS, Bioacoustics approaches in biodiversity inventories. Abc Taxa 8:
Jones K. 2015. Assessing the performance of a semi-automated acoustic 68–99.
monitoring system for primates. Methods in Ecology and Evolution 6: Parker TA. 1991. On the use of tape recorders in avifaunal surveys. Auk
753–763. 108: 443–444.
Horton KG, Shriver WG, Buler JJ. 2015. A comparison of traffic estimates Peterson CR, Dorcas ME. 1994. Automated data acquisition. Pages 47–57 in
of nocturnal flying animals using radar, thermal imaging, and acoustic Heyer WR, Donnelly MA, McDiarmid RW, Hayek LC, Foster MS, eds.
recording. Ecological Applications 25: 390–401. Measuring and Monitoring Biological Diversity: Standard Methods for
Hugel S. 2012. Impact of native forest restoration on endemic crickets and Amphibians. Smithsonian Institution Press.
katydids density in Rodrigues island. Journal of Insect Conservation Pijanowski BC, Villanueva-Rivera LJ, Dumyahn SL, Farina A, Krause BL,
16: 473–477. Napoletano BM, Gage SH, Pieretti N. 2011. Soundscape ecology: The
Jeliazkov A, Bas Y, Kerbiriou C, Julien J-F, Penone C, Le Viol I. 2016. Large- science of sound in the landscape. BioScience 61: 203–216.
scale semi-automated acoustic monitoring allows to detect temporal Pimm SL, et al. 2015. Emerging technologies to conserve biodiversity.
decline of bush-crickets. Global Ecology and Conservation 6: 208–218. Trends in Ecology and Evolution 30: 685–696.
Kasten EP, Gage SH, Fox J, Joo W. 2012. The remote environmental assess- Rachwald A. 1992. Habitat preference and activity of the noctule bat
ment laboratory’s acoustic library: An archive for studying soundscape Nyctalus noctula in the Bialowieza Primeval Forest. Acta Theriologica
ecology. Ecological Informatics 12: 50–67. 37: 413–422.
Kissling WD, et al. 2017. Building essential biodiversity variables (EBVs) of Ribeiro JW, Sugai LSM, Campos-Cerqueira M. 2017. Passive acous-
species distribution and abundance at a global scale. Biological Reviews tic monitoring as a complementary strategy to assess biodiver-
93: 600–625. sity in the Brazilian Amazonia. Biodiversity and Conservation 26:
Krause B, Farina A. 2016. Using ecoacoustic methods to survey the 2999–3002.
impacts of climate change on biodiversity. Biological Conservation 195: Riede K. 1993. Monitoring biodiversity: Analysis of amazonian rainforest
245–254. sounds. Ambio 22: 546–548.
Kuenzi AJ, Morrison ML 1998. Detection of bats by mist-nets and ultra- Ritts M, Gage SH, Picard CR, Dundas E, Dundas S. 2016. Collaborative
sonic sensors. Wildlife Society Bulletin 26: 307–311. research praxis to establish baseline acoustic conditions in Gitga’at
La VT, Nudds TD. 2016. Estimation of avian species richness: Biases in Territory. Global Ecology and Conservation 7: 25–38.
morning surveys and efficient sampling from acoustic recordings. Roch MA, et al. 2016. Management of acoustic metadata for bioacoustics.
Ecosphere 7: e01294. Ecological informatics 31: 122–136.
Linke S, et al. 2018. Freshwater ecoacoustics as a tool for continuous Rosenstock SS, Anderson DR, Giesen KM, Tony L, Carter MF. 2002.
ecosystem monitoring. Frontiers in Ecology and the Environment 16: Landbird counting techniques: Current practices and an alternative.
231–238. Auk 119: 46–53.
Llusia D, Márquez R, Beltrán JF, Benítez M, do Amaral JP. 2013. Calling Rosenthal GG, Ryan MJ. 2000. Visual and acoustic communication in non-
behaviour under climate change: Geographical and seasonal variation human animals: A comparison. Journal of Biosciences 25: 285–290.

24 BioScience • January 2019/ Vol. 69 No. 1 https://academic.oup.com/bioscience


Overview Articles

Russo D, Jones G. 2003. Use of foraging habitats by bats in a Mediterranean Watson JEM, et al. 2016. Persistent disparities between recent rates of
area determined by acoustic surveys: Conservation implications. habitat conversion and protection and implications for future global
Ecography 26: 197–209. conservation targets. Conservation Letters 9: 413–421.
Saito K, et al. 2015. Utilizing the Cyberforest live sound system with social Weir LA, Mossman MJ. 2005. North American Amphibian Monitoring
media to remotely conduct woodland bird censuses in central Japan. Program (NAAMP). Pages 307–313 in Lanoo M, ed. Amphibian
Ambio 44: 572–583. Declines: The Conservation Status of United States Species. University of
Schmeller DS, et al. 2017. Building capacity in biodiversity monitoring at California Press.
the global scale. Biodiversity and Conservation 26: 2765–2790. Whytock RC, Christie J. 2017. Solo: An open source, customizable and
Servick K. 2014. Eavesdropping on ecosystems. Science 343: 834–837. inexpensive audio recorder for bioacoustic research. Methods in
Shannon G, et al. 2016. A synthesis of two decades of research documenting Ecology and Evolution 8: 308–312.
the effects of noise on wildlife. Biological Reviews 91: 982–1005. Wilkins MR, Seddon N, Safran RJ. 2013. Evolutionary divergence in acous-
Stevenson BC, Borchers DL, Altwegg R, Swift RJ, Gillespie DM, Measey GJ. tic signals: Causes and consequences. Trends in Ecology and Evolution
2015. A general framework for animal density estimation from acoustic 28: 156–166.

Downloaded from https://academic.oup.com/bioscience/article-abstract/69/1/15/5193506 by guest on 12 February 2019


detections across a fixed microphone array. Methods in Ecology and Wimmer J, Towsey M, Roe P, Williamson I. 2013. Sampling environmen-
Evolution 6: 38–48. tal acoustic recordings to determine bird species richness. Ecological
Sueur J, Farina A. 2015. Ecoacoustics: The ecological investigation and Applications 23: 1419–1428.
interpretation of environmental sound. Biosemiotics 8: 493–502. Wrege PH, Rowland ED, Keen S, Shiu Y. 2017. Acoustic monitoring for con-
Sueur J, Gasc A, Grandcolas P, Pavoine S. 2012. Global estimation of animal servation in tropical forests: Examples from forest elephants. Methods
diversity using automatic acoustic sensors. Pages 101–119 in Le Galliard in Ecology and Evolution 8: 1292–1301.
JF, Guarini JM, Gail F, eds. Sensors for Ecology: Towards Integrated Xie J, Towsey M, Zhu M, Zhang J, Roe P. 2017. An intelligent system for esti-
Knowledge of Ecosystems. CNRS Editions. mating frog community calling activity and species richness. Ecological
Sueur J, Pavoine S, Hamerlynck O, Duvail, S. 2008. Rapid acoustic survey Indicators 82: 13–22.
for biodiversity appraisal. PLOS ONE 3 (art. e4065).
Suraci JP, Clinchy M, Mugerwa B, Delsey M, Macdonald DW, Smith JA,
Wilmers CC, Zanette LY. 2017. A new automated behavioural response
system to integrate playback experiments into camera trap studies. Larissa Sayuri Moreira Sugai ([email protected]) and José Wagner
Methods in Ecology and Evolution 8: 957–964. Ribeiro Jr. are affiliated with the Universidade Estadual Paulista,
Toledo LF, Tipp C, Márquez R. 2015. The value of audiovisual archives. Instituto de Biociências, in São Paulo, Brazil. Larissa Sayuri Moreira
Science 347: 484–484. Sugai and Thiago Sanna Freire Silva are affiliated with the Instituto de
Ulloa JS, Aubin T, Llusia D, Bouveyron C, Sueur J. 2018. Estimating animal Geociências e Ciências Exatas at the Universidade Estadual Paulista,
acoustic diversity in tropical environments using unsupervised multi- Ecosystem Dynamics Observatory, in São Paulo. Diego Llusia is affili-
resolution analysis. Ecological Indicators 90: 346–355. ated with the Laboratório de Herpetologia e Comportamento Animal, in
Vielliard J. 1993. Recording wildlife in tropical rainforest. Bioacoustics 4: the Departamento de Ecologia, at the Instituto de Ciências Biológicas,
305–311. Universidade Federal de Goiás, in Goiás, Brazil. Larissa Sayuri Moreira
Villanueva-Rivera LJ, Pijanowski BC. 2012. Pumilio: A web-based manage- Sugai and Diego Llusia are affiliated with the Terrestrial Ecology
ment system for ecological recordings. The Bulletin of the Ecological Group, in the Departamento de Ecología, Universidad Autónoma de
Society of America 93: 71–81. Madrid, Spain.

https://academic.oup.com/bioscience January 2019/ Vol. 69 No. 1 • BioScience 25

View publication stats

You might also like