It's time to listen: There is much to be learned from the sounds of tropical ecosystems

Abstract

Knowledge that can be gained from acoustic data collection in tropical ecosystems is low‐hanging fruit. There is every reason to record and with every day, there are fewer excuses not to do it. In recent years, the cost of acoustic recorders has decreased substantially (some can be purchased for under US$50, e.g., Hill et al. 2018) and the technology needed to store and analyze acoustic data is continuously improving (e.g., Corrada Bravo et al. 2017, Xie et al. 2017). Soundscape recordings provide a permanent record of a site at a given time and contain a wealth of invaluable and irreplaceable information. Although challenges remain, failure to collect acoustic data now in tropical ecosystems would represent a failure to future generations of tropical researchers and the citizens that benefit from ecological research. In this commentary, we (1) argue for the need to increase acoustic monitoring in tropical systems; (2) describe the types of research questions and conservation issues that can be addressed with passive acoustic monitoring (PAM) using both short‐ and long‐term data in terrestrial and freshwater habitats; and (3) present an initial plan for establishing a global repository of tropical recordings.

Full text

COMMENTARY
It’s time to listen: there is much to be learned from the sounds of tropical ecosystems
Jessica L. Deichmann
1,16
, Orlando Acevedo-Charry
2,3
, Leah Barclay
4
, Zuzana Burivalova
5
, Marconi Campos-Cerqueira
2
,
Fernando d’Horta
6
, Edward T. Game
7
, Benjamin L. Gottesman
8
, Patrick J. Hart
9
, Ammie K. Kalan
10
, Simon Linke
11
,
Leandro Do Nascimento
12
, Bryan Pijanowski
8
, Erica Staaterman
13,14
,and T. Mitchell Aide
2,15
1
Center for Conservation and Sustainability, Smithsonian Conservation Biology Institute, National Zoological Park, Washington, DC, USA
2
Sieve Analytics, San Juan, PR, USA
3
Colecci
on de Sonidos Ambientales, Instituto de Investigaci
on de Recursos Biol
ogicos Alexander von Humboldt, Bogot
a, Colombia
4
Queensland Conservatorium Research Centre, Griffith University, Nathan, Qld, Australia
5
Woodrow Wilson School of Public and International Affairs, Princeton University, Princeton, NJ, USA
6
Graduate Program in Genetics, Conservation and Evolutionary Biology, INPA, Manaus, AM, Brazil
7
Global Science, The Nature Conservancy, Brisbane, Qld, Australia
8
Department of Forestry and Natural Resources, Purdue University, West Lafayette, IN, USA
9
Department of Biology, University of Hawaii at Hilo, Hilo, HI, USA
10
Department of Primatology, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany
11
Australian Rivers Institute, Griffith University, Nathan, Qld, Australia
12
Department of Wildland Resources and Ecology Center, Utah State University, Logan, UT, USA
13
Bureau of Ocean Energy Management, Office of Environmental Programs, Sterling, VA, USA
14
Beneath the Waves, Inc., Herndon, VA, USA
15
Department of Biology, University of Puerto Rico, San Juan, PR, USA
ABSTRACT
Knowledge that can be gained from acoustic data collection in tropical ecosystems is low-hanging fruit. There is every reason to record
and with every day, there are fewer excuses not to do it. In recent years, the cost of acoustic recorders has decreased substantially
(some can be purchased for under US$50, e.g., Hill et al. 2018) and the technology needed to store and analyze acoustic data is contin-
uously improving (e.g., Corrada Bravo et al. 2017, Xie et al. 2017). Soundscape recordings provide a permanent record of a site at a
given time and contain a wealth of invaluable and irreplaceable information. Although challenges remain, failure to collect acoustic data
now in tropical ecosystems would represent a failure to future generations of tropical researchers and the citizens that benefit from
ecological research. In this commentary, we (1) argue for the need to increase acoustic monitoring in tropical systems; (2) describe the
types of research questions and conservation issues that can be addressed with passive acoustic monitoring (PAM) using both short-
and long-term data in terrestrial and freshwater habitats; and (3) present an initial plan for establishing a global repository of tropical
recordings.
Key words: conservation technology; ecoacoustics; passive acoustic monitoring; soundscape.
“The universe is your orchestra. Let nothing less be the terri-
tory of your new studies”Raymond Murray Schafer (1969)
In an era of rapid environmental change, remote sensing
methods are particularly important for ecology and conservation
biology because they produce consistent data streams that can be
analyzed over different spatial and temporal scales (Kerr &
Ostrovsky 2003; Nagendra et al. 2013; Turner et al. 2003). Pas-
sive acoustic monitoring (PAM) is one way to characterize and
evaluate ecosystems remotely using sounds. First developed for
use in the marine realm (Tavolga 2012), autonomous recordings
can detect a range of sounds produced by natural and physical
phenomena (Krause 1987). The ‘soundscape’includes all sounds
emanating from any given habitat, which can be classified with
respect to their source: geophony (climate and geography), bio-
phony (all wildlife), and anthrophony (human activities;
Received 21 February 2018; revision accepted 8 June 2018.
16
Corresponding author; e-mail: deichmannj@si.edu
ª2018 The Association for Tropical Biology and Conservation 1
BIOTROPICA 0(0): 1–6 2018 10.1111/btp.12593

Pijanowski et al. 2011). Analysis and monitoring of these various
contributions to a soundscape can permit rapid assessment of
biodiversity as well as the health and stability of an ecosystem
(e.g., Blumstein et al. 2011, Pijanowski et al. 2011, Fuller et al.
2015, Bertucci et al. 2016, Burivalova et al. 2017, Deichmann
et al. 2017, Staaterman et al. 2017).
APPLICATIONS OF ECOACOUSTICS IN THE
TROPICS
Many tropical biologists have been startled by the sound of a
nearby treefall, while others have been warned of an oncoming
storm by croaking toucans or the presence of a predator by
screeching squirrel monkeys; yet many of us have never consid-
ered that these sounds are data that can be harnessed to answer
questions about tropical ecosystems. Here are a few examples of
the types of questions that can be answered using sounds:
POPULATION DYNAMICS AND ACTIVITY PATTERNS.—We know very lit-
tle about natural activity fluctuations within tropical forest commu-
nities, and perhaps even less in tropical freshwater systems. Thus, it
is difficult to precisely assign causal relationships between human
activities and changes in biodiversity (Thompson 2003). For exam-
ple, is the decline in abundance of a hornbill species in an Indone-
sian forest a part of a naturally occurring seasonal and superannual
fluctuation pattern, or is the population actually decreasing due to
hunting, logging, and habitat loss? If measurements are taken during
a‘low’part of an undetected cycle, small population numbers could
make the impact of an otherwise-sustainable hunting practice appear
catastrophic. Alternatively, unsustainable hunting rates could be seen
as deceivingly benign if measurements were taken during a peak
time. Recording soundscapes regularly to span the natural cycles of
animal activity helps us correctly understand these patterns (Bridges
et al. 2000, Towsey et al. 2014, Linke et al. 1999), which otherwise
would be extremely difficult to decipher using traditional biodiver-
sity monitoring methods.
BROAD SPATIAL SCALES.—Our current methods for comparing bio-
diversity of multiple habitats (beta diversity) are insufficient. This
task is notoriously difficult in tropical forests and streams due to
the sheer number of species present and the amount of sampling
necessary. The ability to deploy multiple acoustic sensors across
landscapes in a short period of time enables simultaneous record-
ing, which allows researchers to make meaningful comparisons
and tackle elusive patterns in tropical forest and freshwater fauna
(e.g., Bormpoudakis et al. 2013, Gasc et al. 2013, Rodriguez et al.
2014). For instance, PAM can improve our understanding of eco-
logical processes across entire elevational gradients helping us to
track the impact of climate change on animal distributions (Cam-
pos-Cerqueira et al. 2017).
RAPID INVENTORIES AND SPECIES OF CONSERVATION CONCERN.—The
presence of rare and cryptic species in tropical habitats is difficult
to detect in short trips to the field (Thompson 2003, Plaisance
et al. 2011), but PAM methods have been successfully used to
detect such animals in densely forested habitats, producing results
that would otherwise require massive search efforts by field
crews. For example, PAM has been used to estimate the presence
and abundance of African forest elephants (Loxodonta cyclotis)
inhabiting dense rain forests of Central Africa (Wrege et al. 2017)
as well as cryptic fish in tropical coastal habitats (Staaterman et al.
2017) and an endemic and threatened bird in Puerto Rican
mountains (Campos-Cerqueira & Aide 2016). Invasive species
such as fish (Rountree & Juanes 2017) and pest insects (Mankin
et al. 2011) have also been detected using PAM. Likewise, PAM
can detect the recovery of species extirpated from a site after nat-
ural disaster, disease, or other perturbation (Butler et al. 2016).
The ability for PAM data to be collected rapidly from many
places but analyzed later makes it a valuable tool for rapid inven-
tories (Sueur et al. 2008, Ribeiro et al. 2017), which tend to be
costly and difficult to fund.
HUMAN IMPACTS AND SHIFTING BASELINES.—Comparing sound-
scapes in areas under different management regimes allows for a
rapid understanding of the intensity of impact caused by different
human activities (e.g., Alvarez-Berrıos et al. 2016, Burivalova et al.
2017, Deichmann et al. 2017). Examples include changes in habi-
tat structure (Tonolla et al. 2010, Geay et al. 2017) or levels of
hunting activity in protected areas (Astaras et al. 2017). Further-
more, acoustic data collected over the long-term can be used to
answer broader questions regarding the effects of environmental
change on species abundance, phenology, distribution (Campos-
Cerqueira & Aide 2017, Campos-Cerqueira et al. 2017), and
behavior (Llusia et al. 2013, Narins & Meenderink 2014). For
example, acoustic monitoring has been used to demonstrate
changes in the seasonal onset of birdsong (Buxton et al. 2016),
which may be indicative of climatic influences on the timing of
reproduction. Acoustic ‘time-capsules’—measurements made in
the past or the present—will be critically important for similar
observations in the decades to come.
ADVANTAGES OF PASSIVE ACOUSTIC
MONITORING
Using PAM, rather than traditional methods, to monitor and ana-
lyze biodiversity will help us do a better job of understanding and
conserving tropical terrestrial and freshwater ecosystems. Netting,
trapping, distance sampling, visual transects, etc. are labor-intensive,
expensive, and logistically impractical in many places—often even
more so in the tropics than in the temperates. In addition, most
observations of animal behavior are influenced by human presence
and limited to daylight hours. Crucially, the autonomous nature of
acoustic sensors permits continuous collection of PAM data with-
out biases from the ‘observer effect’(Shonfield & Bayne 2017).
PAM can cover broad spatial and temporal scales, including simul-
taneous and long-term monitoring, which is simply not possible
with traditional methods (Linke et al. 2018). This can even be done
in real time (e.g., Van Parijs et al. 2009, Aide et al. 2013), providing
researchers and managers with information necessary for immedi-
ate decision making, and make adaptive management more feasible.
2 Deichmann et al.

Finally, collection of big data through PAM creates permanent
records that can be reanalyzed when new analytical tools become
available, when additional research questions arise, or to compare
past to present conditions.
The related technique of camera trapping has greatly improved
our capacity to estimate species composition, abundance, and den-
sity of medium to large-bodied mammals and birds—groups that
are difficult to study using traditional methods—in terrestrial (Bur-
ton et al. 2015) and arboreal habitats (Gregory et al. 2014). That
said, camera trapping is restricted to this subset of species (but see
Hobbs & Brehme 2017) and the detection range is relatively lim-
ited. PAM has the additional benefit of having broader detection
ranges [e.g., maximum 1 km detection radius calculated for primate
sounds (Kalan et al. 2015); up to many km depending on fre-
quency, microphone height, and habitat type (Darras et al. 2016)]
and sampling a wider range of taxonomic groups (Aide et al. 2017).
We consider camera trapping and acoustic monitoring to be com-
plementary in terms of taxonomic groups and advocate the use of
both methods where possible.
CHALLENGES
While PAM holds many advantages over other methods, it would
be remiss not to recognize that challenges do exist. For example,
as with other methods that result in the collection of big data,
PAM faces the challenge of data storage and management. Stor-
ing recordings on multiple hard drives is not expensive, but it is
not a particularly effective way to encourage their use in analyses
by the broader community. Furthermore, extracting meaningful
biological information from recordings is complex. Automated
detection tools for species-level analyses have advanced signifi-
cantly over the last decade (e.g., Aide et al. 2013, Kalan et al.
2015, de Camargo et al. 2017). Still, there are limitations to auto-
matic approaches because they can be initially time-consuming
and they require training data to create different classifiers for
different species as well as programming or signal processing
expertise to develop automated species identification models. At
the soundscape level, many acoustic indices and soundscape anal-
ysis methods have been proposed and used for the assessment of
biodiversity (e.g., Sueur et al. 2008, Pieretti et al. 2011, Villanueva-
Rivera et al. 2011, Gasc et al. 2013, Fuller et al. 2015, Vega et al.
2016, Aide et al. 2017, Rankin & Axel 2017), yet there is no con-
sensus to date as to which are most effective, primarily due to
the difficulties in generalizing across taxa and ecosystems (Buxton
et al. 2018). Existing indices can also be sensitive to geophony
such as rain, wind, and river flow, or can be skewed by certain
acoustically dominant species (Staaterman et al. 2017, Linke et al.
1999). Most also lack measures of uncertainty (e.g., detection
probabilities)—an issue likely to be exacerbated in highly diverse
tropical habitats. Nevertheless, collection of acoustic data now
opens up the possibility of analyzing long time series of sounds
in the future as analytical methods become more advanced and
standardized—a possibility that can only be realized if we start
recording now.
BROADER IMPACTS OF ECOACOUSTICS
In addition to serving as permanent records of ecosystem health
and providing data for scientific research, animal sounds can
serve as an alluring tool for engaging public audiences. Camera
trapping has been successful for many reasons, but chief among
them is the charismatic nature of the resulting photographs—
who doesn’t smile when they see wildlife ‘selfies’or animals
caught in the act of defiling a camera? We argue that sounds
can be just as captivating—many of us have seen public audi-
ences become wide-eyed when we play them a unique, previ-
ously unknown animal sound. Ecoacousticians have successfully
enlisted the help of citizen scientists to gather data on bats (e.g.,
Bat Detective: www.batdetective.org) and birds (e.g., eBird: ebir-
d.org) and to record soundscapes on a global scale (Record the
Earth: www.recordtheearth.org). Italian sound artist David
Monacchi’sFragments of Extinction project, initiated in 2001,
records the world’s undisturbed primary equatorial forests to
highlight disappearing soundscapes and brings attention and
urgency to the ongoing loss of a ‘sonic heritage of millions of
years of evolution’(Monacchi & Krause 2017). Ecological sound
art is an effective medium for science dissemination, and immer-
sive experiences of soundscapes can engage listeners on an emo-
tional level. This acts as a powerful and accessible tool for
inspiring public awareness about the value of ecoacoustics and
ecosystem health in general (Monacchi & Krause 2017), and its
efficacy in driving behavior changes is another interesting topic
for scientific investigation.
A WAY FORWARD
With the increasing popularity of PAM and rapid flurry of analyt-
ical tools, it is now necessary to take advantage of obvious
opportunities for acoustic data collection, to develop standards
for data collection that allow cross-site comparisons and to create
an open repository to store, visualize, and share recordings.
COLLECT MORE DATA.—Just as a meteorological station has
become a standard and invaluable accessory at biological field
stations, there should also be a permanent acoustic recorder.
Anyone can put out a recorder, and researchers with long-term
field programs are in a particularly good position to conduct
passive acoustic monitoring for biodiversity. Long-term research
sites typically have metadata related to vegetation composition
and structure, faunal richness and abundance, and/or physical
landscape variables that can be used together with acoustic
data to create and validate population, community, and sound-
scape monitoring models. Detailed methods for collecting ecoa-
coustic data and a review of available hardware can be found
in WWF’s guide to acoustic monitoring (Browning et al. 2017);
we encourage researchers to consult this report and take
advantage of their field sites by beginning to compile invaluable
long-term acoustic datasets that will contribute to creating a
global database.
It’s Time to Listen 3

STANDARDIZED ACOUSTIC DATA COLLECTION.—To build a compre-
hensive PAM program, one needs to acquire the necessary hard-
ware and software, develop a method for data collection, and
determine a plan for storage of acoustic data files and associated
metadata. While we understand that every PAM project will have
specific requirements to address the research questions of inter-
est, the best way to maximize the utility of any PAM effort is to
follow a standard storage and metadata protocol. We strongly
encourage researchers to use the data storage and metadata stan-
dards proposed by Roch et al. (2016). When acoustic data are
organized and annotated in a uniform way, it allows other
researchers (present-day or future) to utilize the data for addi-
tional questions.
AGLOBAL DATABASE.—With global data being increasingly publicly
available in the ecological sciences (e.g., TRY, GBIF, GenBank,
BOLD, eMammal), only a limited fraction meets the best prac-
tices standards defined by Joppa et al. (2016). Ideally, data should
be freely available at high spatial resolution, up-to-date, user-
friendly and assessed for accuracy, thereby increasing our ability
to answer broad questions and improve its utility for conserva-
tion management. The Macaulay Library (https://www.macaulayli
brary.org/) and xeno-canto (https://www.xeno-canto.org/) are
two large databases that house bioacoustic data, but only the lat-
ter allows full-soundscape recordings to be uploaded. Existing
ecoacoustics databases include ARBIMON (https://arbimon.sie
ve-analytics.com/home), the Remote Environmental Assessment
Laboratory (REAL, http://lib.real.msu.edu/), Ecosounds (http://
ecosounds.org), and the Center for Global Soundscapes
(https://centerforglobalsoundscapes.org), although only the first
allows users to upload their own data. For marine acoustic data,
there is support across US federal agencies to archive PAM
recordings at the National Center for Environmental Information
(NCEI); terrestrial and freshwater ecologists must follow suit. A
free platform for soundscape storage to enable future temporal
and spatial comparisons is absolutely necessary to advance tropi-
cal ecology and conservation.
CONCLUSION
We are convinced that PAM is a powerful tool that can be used
to assess biodiversity over a range of spatial and temporal scales
and can detect rare species, human impacts, and climatic shifts.
Just as a plant or animal voucher specimen can provide informa-
tion on diet, disease, and evolutionary relationships, so too can a
sound recording provide information on species occurrence, den-
sity, distribution, phenology, inter- and intraspecific communica-
tion, and much more. The rapid proliferation of acoustic
recorders and analysis algorithms makes this an exciting frontier
in tropical ecology, yet we urge scientists to create standards in
our approach to data collection, analysis, and archiving that will
amplify the utility of recordings. What PAM can reveal will be
invaluable in future decades as tropical ecosystems continue to
change.
ACKNOWLEDGMENTS
We thank the participants and attendees of the ‘Quantitative
acoustic ecology: Using sound in tropical biodiversity
research and conservation’symposium at the ATBC meeting
in Merida, 2017, for insightful presentations and discussion
of the need for documenting soundscapes in tropical ecosys-
tems. We also thank two anonymous reviewers for providing
feedback that improved the commentary. JLD was supported
by the Center for Conservation and Sustainability at the
Smithsonian Conservation Biology Institute; MCC acknowl-
edges the support of the Brazilian Ministry of Education
(CAPES); AKK was supported by the Max Planck Society;
LDN was supported by the Brazilian National Council of
Scientific and Technological Development (CNPq) 203230/
2015-9 and Ecology Center USU; BCP has been supported
by funds from Purdue University, the Office of the Execu-
tive Vice President for Research and Engagement, College of
Agriculture Deans Office, NSF Coupled Natural and Human
Systems Program, NSF Advancing Informal STEM Learning,
and the USDA McIntire-Stennis Program; BLG has been
supported by the Lynne Fellowship Program, Graduate
School, Purdue University, and the Wright Forestry Fund,
Department of Forestry and Natural Resources, Purdue
University; SL was supported by the Australian Research
Council DECRA DE130100565.
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