Zoosyst. Evol. 96 (2) 2020, 515-525 | DO! 10.3897/zse.96.38770

Ate
BERLIN

A guild classification system proposed for anuran advertisement calls

Mike Emmrich!, Miguel Vences*, Raffael Ernst?, Jorn Kéhler*, Michael F. Barej', Frank Glaw?,
Martin Jansen®, Mark-Oliver Rédel!

Museum fiir Naturkunde, Leibniz Institute for Evolution and Biodiversity Science, Invalidenstr. 43, 10115 Berlin, Germany
Zoological Institute, Technische Universitat Braunschweig, Mendelssohnstr. 4, 38106 Braunschweig, Germany

Museum fir Tierkunde, Senckenberg Natural History Collections Dresden, A.B. Meyer Building, 01109 Dresden, Germany
Hessisches Landesmuseum Darmstadt, Friedensplatz 1, 64283 Darmstadt, Germany

Zoologische Staatssammlung Miinchen (ZSM-SNSB), Miinchhausenstr. 21, 81247 Miinchen, Germany

Senckenberg Gesellschaft fiir Naturforschung, Senckenberganlage 25, 60325 Frankfurt/Main, Germany

DN oR WN

http://zoobank. org/F50B443E-265E-4C93-S8B7D-S55F793075C1F

Corresponding author: Mark-Oliver Rodel (mo.roedel@mfn.berlin)

Academic editor: Rafe Brown # Received 2 August 2019 Accepted 11 June 2020 Published 1 September 2020

Abstract

Zoologists have widely acknowledged the utility of classification systems for characterising variation in anuran egg and clutch types,
tadpole morphotypes, embryonic and tadpole development, amplexus types and reproductive modes. These classification systems
have facilitated unambiguous communication between researchers, often working in completely different fields (e.g. taxonomy, ecol-
ogy, behaviour), as well as comparisons among studies. A syntactic system, classifying anuran call guilds, is so far lacking. Based on
examination of the calls of 1253 anuran species we present a simple, easy to use dichotomous key and guild system for classifying
anuran advertisement calls — the call type most frequently emitted by anurans and studied by researchers. The use of only three call
elements, namely clearly-defined calls, notes, and pulses, plus presence or absence of frequency modulation, allows assigning all cur-
rently known anuran advertisement calls to one of eight distinct call guilds defined here. This novel toolkit will facilitate comparative
studies across the many thousand anuran species, and may help to unravel drivers of anuran call evolution, and to identify ecological
patterns at the level of acoustic communities.

Key Words

Amphibia, Anura, bioacoustics, call guilds

Introduction or evolutionary research questions (Ord et al. 2013; Sch-

iest! and Johnson 2013), and also used data from such

Communication strategies are omnipresent across all
forms of life, ranging from prokaryotes, to plants, fun-
gi, and animals (Miller and Bassler 2001; Bradbury and
Vehrencamp 2011). The reasons why organisms commu-
nicate with each other are, thus, manifold. Essential ele-
ments in all forms of communication are (1) a sender and
a receiver, and (2) a signal of sufficient detectability and
distinctiveness, so as to avoid loss of information or mis-
interpretation by the receiver (Torricelli et al. 1986; Lu-
cass et al. 2016). Researchers from many disciplines have
exploited communication signals to address behavioural,

signals in integrative taxonomic approaches to the study
of various animal groups, including anuran amphibians
(Padial et al. 2010; Kohler et al. 2017).

The form of communication most frequently used by
anurans 1s acoustic (Gerhardt and Huber 2002; for an in-
depth review see Kohler et al. 2017). This form of com-
munication co-evolved presumably along with hearing,
allowing for precise sender—receiver communication sys-
tems to evolve (e.g. Tembrock 1982; Ryan 2001; Desut-
ter-Grandcolas 2002; Gerhardt and Huber 2002). Acoustic
signals have the potential to cover a broad spatial range, to

Copyright Mike Emmrich et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which per-
mits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

516

be characterized by rapid signal transfer rates, and to con-
vey directionality (.e., the location of the sender may be
identifiable to the receiver; Rothganger and Rothganger
2011). Acoustic signals are usually generated by oscillation
of internal (birds, mammals, amphibians, fish), or external
morphological structures (e.g. insects) (Gerhardt and Huber
2002; Bradbury and Vehrencamp 2011). These signals are
mostly transmitted by air but also by using other material as
carrier substrates (e.g. water or soil; Yager 1992; Platz 1993;
Christensen-Dalsgaard and Elepfandt 1995; Seidel 1999;
Lewis et al. 2001; Seidel et al. 2001; Bradbury and Vehren-
camp 2011; Irisarri et al. 2011; Zheng et al. 2011). The main
functions of intra-specific acoustic communication are at-
traction, detection and selection of mates, territoriality, and
/ or exchange of other information (e.g. warning or release;
Bee and Gerhardt 2002; Ballentine et al. 2004; Wollenberg
and Harvey 2010; Stephan and Zuberbuhler 2014).

A considerable diversity of acoustic mating signals ex-
ists in anuran amphibians, and because they are the prima-
ry mate-recognition signals, they are usually species-spe-
cific (Ryan 2001; Gerhardt and Huber 2002; Kohler et al.
2017). Anuran call patterns are assumed to be largely ge-
netically determined (Gerhardt et al. 1980; Duellman and
Trueb 1994; Hédl 1996; Hoskin et al. 2005), with limit-
ed variation among individuals and populations (but see
discussion of intra-specific call variation in Wells 2007
and Kohler et al. 2017). This particularly concerns the so-
called advertisement calls, used (mainly) by males to ad-
vertise their location and to attract females (Mecham 1960;
Zweifel 1968; Forester 1973; Ryan 2001; Gerhardt and
Huber 2002; Wycherley et al. 2002; McLean et al. 2013).

In addition to understanding their function in mate at-
traction, taxonomists have made use of the species-specific
and highly stereotyped nature of advertisement calls (Blair
1955, 1958; Littlejohn 1959; Schiotz 1964, 1967, 1971,
1973), and of their simple characteristics, to identify and
delimit frog species (see Kohler et al. 2017 for review).
However, gaps in our understanding persist, and lead to
questions over which factors drive the evolution of calls
and trigger the differences in advertisement calls among
species. Some properties of anuran advertisement calls are
impacted by morphology. For example, frequency-related
call characters usually correlate with body size (Ryan 2001;
Gerhardt and Huber 2002). Although some call parameters
can be modified by physiology (e.g., a frog’s hormonal
state; Wilczynski and Chu 2001), or temperature (Gerhardt
1978), the main bioacoustic characteristics of anuran calls
are interpreted as fully heritable and only in exceptional
cases shaped by learning (Dawson and Ryan 2009). From
an evolutionary perspective, anuran advertisement calls are
thus controlled by selection: sexual selection is most often
discussed (Bradbury and Vehrencamp 2011), but an addi-
tional, less frequently-explored component is natural se-
lection, due to the abiotic and biotic environment through
which acoustic signals are transmitted (Marten and Maler
1977; Wiley and Richards 1978; Bullen and Fricke 1982;
Forrest et al. 1992; Gerhardt and Huber 2002; Swearingen
and White 2007; Bradbury and Vehrencamp 2011).

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Emmrich, M. et al.: Anuran call guilds

Anuran calls are structurally very variable (Heyer and
Reid 2003; Kohler et al. 2017), leading to a broad range
of definitions of call structures, complicating their com-
parability (Thompson et al. 1994; Gerhardt 1998; Ragge
and Reynolds 1998; Gerhardt and Huber 2002; Kohler et
al. 2017). A unified syntactic (1.e. structural) classification
system, complementing available and widely applied se-
mantic (i.e. functional) classification systems (compare
Tembrock 1982; Gerhardt and Huber 2002) would there-
fore be desirable to facilitate communication among vari-
ous sub-disciplines, eliminate imprecise terminology, and
reduce ambiguity in interactions among researchers from
different backgrounds or disciplines (Littlejohn 2001).

Semantic classification systems for anuran calls were
proposed by Bogart (1960), Littlejohn (1977), and Wells
(1977), and recently reviewed and updated by Toledo et
al. (2015). On the other hand, Littleyohn (2001) suggested
a syntactic classification. While semantic categorisations
are needed to understand a species’ behaviour and com-
munication relative to conspecifics and the environment
(Wells 1977; Toledo et al. 2015), the content of such in-
formation 1s not unique to a species. Syntactic classifica-
tions in contrast, focus on the structure of calls, and tradi-
tionally have been preferred by taxonomists (Thompson
et al. 1994; Ragge and Reynolds 1998). A commonly
used structural approach 1s guild classification. It can be
particularly useful in understanding complex patterns in
evolution and ecology (Wiens 1989; Williams and Hero
1998). Classifying advertisement calls into structural
classes, or guilds, could, for instance, help to improve the
understanding of complex interspecific soundscapes, or
provide objective means of characterising acoustic par-
titioning of diverse species communities (Morton 1975;
Hansen 1979; Rothstein and Fleischer 1987). The use of
an objective, purely structural classification system could
also allow for neutral baselines in the development of
a hypothesis-driven framework to test predictions con-
cerning natural versus sexual selection in call evolution.
Herein, we follow a syntactic, guild-based approach in
describing anuran advertisement calls. We follow the
definition of advertisement calls by Toledo et al. (2015): a
call produced in the “breeding season to attract mates and
to segregate calling individuals”. For other call types and
their definitions see Wells (1977), Toledo et al. (2015) and
Kohler et al. (2017). Our guild classification is based on
the analysis of calls of 1253 anuran species from around
the globe (Suppl. material 1: Table S1).

The aim of this paper is to propose a guild classifica-
tion based on the acoustic properties of anuran advertise-
ment calls. We do this by further developing the syntactic
approach suggested by Littlejohn (2001). We focus on ad-
vertisement calls, because: (1) they are the most frequent-
ly used call type in taxonomic work, (2) they are the most
commonly emitted call of frogs and therefore easy to
collect and most accessible for analyses, and (3) they are
species-specific because they are the primary mate-recog-
nition signal in anuran amphibians. Thus advertisement
calls should be under strong selection. A syntactic guild

Zoosyst. Evol. 96 (2) 2020, 515-525

classification for anuran advertisement calls should there-
fore facilitate addressing evolutionary and functional as-
pects in studies on amphibian biology and ecology.

Material and methods

Data collection

Herein, we aim to simplify and unify syntactic definitions
of advertisement call characters in a way such that they
can unambiguously be applied to mate-recognition acous-
tic signals of all anuran species. To establish an overview
of advertisement call variability, we compiled and anal-
ysed advertisement calls from anuran species from around
the globe. For these baseline data, we used call collections
(Suppl. material 1: References), databases (Suppl. materi-
al 1: Web sources for calls used in this study), published
call descriptions (Suppl. material 1: References), as well
as our own call recordings of species from Africa, Mad-
agascar and Guyana, in an attempt to cover a geographi-
cally and phylogenetically wide range of anuran diversity.

Because our primary goal was to include as much glob-
al frog diversity as possible, we did not apply any stand-
ardised search procedures (e.g., key word searches in Web
of Science or Google Scholar), but simply accessed calls
from freely available call collections, our own sound li-
braries, and published taxonomic papers. We used call
descriptions that were published primarily after 1990, be-
cause earlier publications contained limited acoustic infor-
mation, due to former technical limitations. To get com-
parable recordings, we re-sampled available recordings to
uncompressed wav-format, with a sampling rate of 44.1
kHz. We used the software Soundruler 0.9.6 (Gridi-Papp
2007) to measure call variables and the software package
Seewave (Sueur et al. 2008) for R to visualise waveforms
and frequency spectra (R Core Team 2013). Oscillograms
(waveforms) and audio spectrograms as well as results of
the Fast Fourier Transformation (FFT; frequency spec-
trum) were examined for temporal and spectral charac-
ters, respectively (using 44.1 kHz sample ratio, 16 bits
resolution, FFT window width = 256, window function =
Hanning”). The chosen FFT width represented the best
compromise to achieve usable resolution and informative
visualisation at both the temporal and spectral domain
(Kohler et al. 2017). In cases where we had only published
data available, but not the original recording, we incor-
porated the published data in our data set. Classifying a
call as an advertisement call usually followed the original
assignments of a call description by the respective authors,
but we verified these assignments against the advertise-
ment call definition by Toledo et al. (2015) before adding
a call to our database (Suppl. material 1).

In total, we gathered published calls, call descriptions,
or original recordings for 1426 species from 230 genera
and 43 families. Anuran nomenclature and taxonomy
were obtained directly from databases and publications
(Frost 2019). For further background information and

517

best practices advice, concerning call recording, analyses,
interpretation and presentation, see Kohler et al. (2017).

Definitions of anuran advertisement call units

For the purpose of developing a syntactic classification
system of anuran advertisement call diversity, we estab-
lished a globally applicable scheme that is as simple as
possible but still sufficiently detailed to cover the current-
ly known range of variation in these acoustic signals. To
this aim, we surveyed advertisement calls of all includ-
ed species, comprehensively, striving to identify distinct
structural elements matching the criteria. We incorporated
these elements into a dichotomous key, to allow for objec-
tive assignment of any species’ advertisement call to a dis-
tinct call guild. Following previous definitions of acoustic
units of structural signal variation (Kohler et al. 2017),
we identified three basic elements in common, apparently
sufficient to comprehensively characterise acoustic signal
variability: the call, notes, and pulses.

As the definitions of calls and call series 1s ambigu-
ously dealt with in the literature (Kohler et al. 2017), it
has previously been problematic to articulate an unequiv-
ocal, universal definition of an anuran “call”. However,
such a definition is crucial, because a lack of consistency
among disciplines and individual researchers in terminol-
ogy related to a species’ call, a call series, and note, often
hampers the interpretation and understanding of call de-
scriptions. Previously such standardisations were largely
ignored, resulting in idiosyncratic call descriptions that do
not allow for comparative or meta-analyses. To minimise
these problems, we followed and refined the note-centred
approach suggested by Kohler et al. (2017) to define fun-
damental units of advertisement call variation.

The term call is here used synonymous with advertise-
ment call — the functional signal for mate-recognition,
as the main acoustic unit in frog vocalisation. Calls are
separated from other calls by silent inter-call intervals,
typically longer (often several times longer) than the call
itself. A call series is the temporal repetition of identical
calls, repeated at rather regular intervals, and separat-
ed by larger gaps of silence from other call series (note
that the definitions of our advertisement call guilds below
do not take into account whether calls are arranged in
series or not; only the call unit itself was considered).
Under this definition, a call may be comprised of one or
more subunits (Fig. 1b-e). These may differ in length and
structure and are classified as either notes or pulses.

Calls are often sub-structured into two or more notes.
Notes are subunits separated by intervals of silence (100%
amplitude modulation), with the duration of these intervals
being usually short relative to the duration of the note. Peri-
ods of silence are longer between notes than between pulses
(see below) that form such notes (if pulsed), and shorter
than the periods of silence between calls.

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THA HH-HH-HH
‘HH: HH-HH- HHH
TATA

Time
Figure 1. Basic types of anuran vocalizations based on their temporal structure, shown as schematic waveforms, modified after
Littlejohn (2001): (a) non-pulsed call, (b) pulsed call, (c) call with uniform pulsed notes, (d) complex call containing different note

types, and (e) two complex calls in a call series. Black arrows mark inter-note intervals and red arrow marks inter-call interval.

It must be mentioned that in a call consisting of only
one unit (with or without subunits of the pulse category;
Fig. 1a, b), the definition of a note and a call would apply
simultaneously to the same, making them synonymous
(Kohler et al. 2017). Because we follow this note-centred
approach, we use the term call for the broader, encompass-
ing unit. With this definition, 1t is only necessary to use all
three terms if a call consists of at least three different units,
separated by unequal periods of silence (Fig. 1c—e).

Notes sometimes contain a sub-structure produced by
amplitude modulation within the note. These units are de-
fined as pulses, following Kohler et al. (2017):

A pulse is the shortest, undividable unit in anuran vo-
calisation, with a typical duration of less than 50 ms.

In addition to these formalised syntactical advertise-
ment call units, we included modulation of dominant
spectral frequency. Frequency modulation can be depicted
visually from spectrograms by a clearly visible increase
or decrease in dominant frequency (“dfrq” in Hz). Mod-
ulation can be objectively quantified by subtracting the
end-frequency from the start-frequency, and dividing this
value by call duration (in ms). We calculated dominant
frequency modulation (dfrq/ms) of all species with calls
exhibiting frequency modulation, based on one represent-
ative call of the respective species. Values of > 1/-1 Hz/

Key to anuran Advertisement Call Guilds
(compare Fig. 2 and descriptions below)

1 call consists of only one acoustic Unit .................cceceeeeeee
1’ call contains several acoustic UNITS ....... cece eee ee

ms were considered as a significant change in dominant
frequency and all species were assigned to one of two bi-
nary character states, namely “not frequency modulated”
(< 1/-1 Hz/ms) or “frequency modulated” (> 1/-1 Hz/ms).

After filtering our initial recordings representative of
1426 species and removing calls of insufficient quality
(e.g. call descriptions lacking data for frequency modula-
tion; visualisation only comprising either oscillogram or
spectrogram; figures of insufficient quality; or recordings
consisting of only one single call) from our dataset, we
retained calls of 1253 species for final classification (Sup-
pl. material 1: Table S1). We used these remaining calls
to formalise the advertisement call structural (syntactic)
guild classification presented in the following key.

Results

The combination of call units (call, note, and pulse) and
frequency modulation allowed us to define eight distinct
structural (syntactic) call guilds (Guilds A—H, Table 1).
With a dichotomous key, the advertisement calls of each
of the 1253 species could readily be assigned to one such
guild. Below, we provide the guild classification key (Fig.
2), we summarise call guilds, and provide illustrative ex-
amples (respective spectrograms and waveforms, plus
species identifications in Fig. 3.)

2 dominant frequency without significant change over Call CUraTiON................cccccceseeecceeceeesencesecencoessecsseceeecesceeseereeesseceres
A ee oer Aaa eB rN cen Fh ol SY IR 2» Any ek ae PIT si Call Guild A: “non-frequency modulated, non-pulsed simple call”
2’ dominant frequency with significant change over call Curation ................ccccecsseceseceecoesceccsecesccescoussecceecaseceesenscecseneeseeees

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Call Guild B: “frequency modulated, non-pulsed simple call”

Zoosyst. Evol. 96 (2) 2020, 515-525 519
S Call-COMpPuiSes- OC Ses Ut! POMTOISS:. 252 eir AN Pes Jere esl hee TA Ake noe PANN ce ee Sed ae es Bek ie en a Bn Bek ee Sees BL 4
Siig REA COMM SSS: Se Veal MOM SSC INGLES = a: a aiecebuhtes’ dav rues cerscnars bad etnbe a2 pw assests bitbend Ae eynstnie ipa ee tech Os AA ates ranetnarchh tht dt i wrecaneauennirta 5
4 = dominant frequency without significant change over call duration:...... Call Guild C: “non-frequency modulated pulsed call”
4’ ~~ dominant frequency with significant change over call duration: ............ Call Guild D: “frequency modulated pulsed call”
5 call-camprises several structurally-cmorée-or less) -sSiimi(lat NOTES -9. «slate alee caleetiles #004 cee lde guncesdleble ve Uibdlowid Sade bade etina Pant ldiee 6
5” “callecomipenses-siruetuirallycish Methy CIMTEKENT NOTES), «cet faane segndoocsiss cheng tans bnadl tps ais ve esch tering anie ABbgpeais cicheea afer sme ape dels veceeees 7

6 cominantdrequency Wwiinout- significant change -ever-call CMFATIOR: rect ces) Aa leas 2... SOMOS, Cece, PPO cea) PR ees 22s canbe
a a itd pst ne eeaeteg ie © Hee #8 hart BR ea SRE Latent oben esate vee Call Guild E: “non-frequency modulated call with uniform notes”
G.” “eminent irequency-Withssisrificant-ctriaiige: Over Call=CVatiOne nhs ses a. beara dau ata icceemadealsnseetarang ede stn apes

.... Call Guild F: “frequency modulated call with uniform notes”

7 dominant frequency without significant change over Call CUIraAtiON...........cccccecc ccc ecec eee ece eee ees eeeeeeeeeee eee eeseeeeeeeeeaseeaeeeeeeees

dytediateceatd Call Guild G: “non-frequency modulated complex cal

ji

7’ dominant frequency with significant change over call duration in at least one of the distinct note typeS.............ccceeeeeee

Short description of call guilds with species
examples

Here we summarise the “diagnostic” characters of the dif-
ferent call guilds, give some species examples for each
guild and refer to respective illustrations of selected ex-
emplary calls (Fig. 3). The sources for the specific exam-
ples are summarised in Suppl. material 1: Table S1.

Call Guild A “non-frequency modulated, non-pulsed
simple call”: call consists of one single continuous signal
(which can be of any duration) with no significant change
in dominant frequency. Examples: Alytes cisternasii
(Alytidae), Bombina bombina (Bombinatoridae), E/euth-
erodactylus tonyi (Eleutherodactylidae), Heleophryne de-
pressa (Heleophrynidae), Rana arvalis (Ranidae).

Call Guild B “frequency modulated, non-pulsed sim-
ple call”: call consists of one single continuous signal

Call

Mn dh’ Behe TRON Call Guild H: “frequency modulated complex call”

(which can be of any duration) with a significant change
in dominant frequency. Examples: Rhaebo haematiti-
cus (Bufonidae), Pristimantis bambu (Craugastoridae),
Ameerega pepperi (Dendrobatidae), Kassina senegalen-
sis (Hyperoliidae), Leptodactylus fuscus (Leptodactyl-
idae), Limnodynastes peronii (Limnodynastidae), Aus-
trochaperina fryi (Microhylidae), Strongylopus grayii
(Pyxicephalidae), Chiromantis vittiger (Rhacophoridae).
Call Guild C: “non-frequency modulated, pulsed call”:
call comprised of several similar, but distinguishable acous-
tic signals (pulses). Pulses are arranged in a single group
(note = call), meaning that intervals between pulses are
equally long, but much shorter than inter-call intervals. The
dominant frequency does not change over the call duration.
Examples: Dendropsophus tritaeniatus (Hylidae), Eleuth-
erodactylus toa (Eleutherodactylidae), Hemisus marmora-
tus (Hemisotidae), Cophixalus concinnus (Microhylidae).

een

single multi-unit
one pulsed note multi-note
ff . x / Ke
non- non- non- non-
modulated modulated modulated modulated modulated modulated modulated modulated
wee oonooa
—— $BGSSS Oooanmc i BX BH Mi canal i 8 Bt Sooo eu #

AI iiiititins ition

Guild A Guild B Guild C Guild D

HH HH tA

Guild E Guild F Guild G Guild H

Figure 2. Key to anuran advertisement call guilds (compare text); each guild illustrated by schematic waveform and spectrogram.

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520 Emmrich, M. et al.: Anuran call guilds

"Guild A Guild B
Qo—
& Guild c "| Guild D
|
i | nee
UPPED DEP DD DD
N !
t
x
>
oO
od
o
—
oO
©
LL

T

ne EE EE

B cuild € Guild F

r pei eh vittp ee

XD HDHD. te Rast ob.

8—
Guild G Guild H

fi

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Duration [s]

wr

Figure 3. Examples for all different anuran advertisement call guilds (A—H), with a time scale of 0 to 1 s on x-axis and frequency
scale of 0 to 8 kHz on y-axis (compare text). Guild A) non-frequency modulated, non-pulsed simple call (Bombina bombina; Bom-
binatoridae; dfrq/ms = 0.00 Hz/ms) (based on Schneider 2005); Guild B) frequency modulated, non-pulsed simple call (Leptodacty-
lus fuscus, Leptodactylidae; dfrq/ms = 7.22 Hz/ms) (based on Marquez et al. 2002); Guild C) non-frequency modulated pulsed call
(Hyla meridionalis;, Hylidae; dfrq/ms = 0.67 Hz/ms) (based on Maso and Pijoan 2011); Guild D) frequency modulated pulsed call
(Hyperolius pickersgilli,; Hyperoliidae; dfrq/m = 2.32 Hz/ms) (based on Du Preez and Carruthers 2009); Guild E) non-frequency
modulated call with uniform notes (Sclerophrys mauritanica;, Bufonidae; dfrq/ms = 0.31 Hz/ms) (based on Maso and Pijoan 2011);
Guild F) frequency modulated call, with uniform notes (Pseudopaludicola boliviana, Leptodactylidae; dfrq/ms = 2.38 Hz/ms)
(based on Marquez et al. 2002); Guild G) non-frequency modulated complex call (Smilisca sila, Hylidae; dfrq/m = 0.43 Hz/ms)

(based on Ibanéz 1999); Guild H) frequency modulated complex call (Hyperolius nasutus; Hyperoliidae; dfrq/ms = 1.66 Hz/ms)
(based on Du Preez and Carruthers 2009).

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Zoosyst. Evol. 96 (2) 2020, 515-525

Table 1. Number of species studied (N = 1253) per call guild;
for guild definitions compare text and Fig. 2.

N Percentage
Guild A 130 10.4%
Guild B 198 15.8%
Guild C 454 36.3%
Guild D 247 19.7%
Guild E 81 6.5%
Guild F 22 1.8%
Guild G 93 7AN
Guild H 28 2.3%
Total 1253 100.0%

Call Guild D: “frequency modulated, pulsed call”:
call comprised of several similarly structured, but distin-
guishable acoustic signals (pulses). Pulses are arranged
in a single group meaning that intervals between puls-
es are equally long, but much shorter than inter-call in-
tervals. The dominant frequency changes significantly
over the call duration. Examples: Pristimantis w-nigrum
(Craugastoridae), Acris gryllus (Hylidae), Diasporus
vocator (Eleutherodactylidae), Mantidactylus tricinctus
(Mantellidae), Agalychnis callidryas (Phyllomedusidae),
Ptychadena taenioscelis (Ptychadenidae), Rana muscosa
(Ranidae), Kurixalus appendiculatus (Rhacophoridae).

Call Guild E “non-frequency modulated call with uni-
form notes”: call comprised of several similarly struc-
tured notes. Dominant frequency does not change over the
call duration. Examples: Boana leptolineata (Hylidae),
Blommersia grandisonae (Mantellidae), Leptobrachium
leucops (Megophryidae), Oreophryne clamata (Micro-
hylidae), Mixophyes fleayi (Myobatrachidae), Lithobates
virgatipes (Ranidae).

Call Guild F “frequency modulated call with uniform
notes”: call comprised of several distinguishable notes.
These notes are structurally very similar to each other. Dom-
inant frequency changes significantly over the call duration.
Examples: Boana almendarizae, Osteocephalus yasuni, Sci-
nax nebulosus (Hylidae), Pseudopaludicola boliviana (Lep-
todactylidae), Ptychadena schillukorum (Ptychadenidae).

Call Guild G “non-frequency modulated, complex
call”: call comprised of several notes. The signals are ar-
ranged in several, at least two, structurally different note
types. Dominant frequency does not change over the call
duration. Examples: Melanophryniscus atroluteus (Bufo-
nidae), Hyperolius benguellensis (Hyperoliidae), Boophis
bottae (Mantellidae), Litoria fallax (Pelodryadidae).

Call Guild H “frequency modulated, complex call”: call
comprised of several notes, at least two being structurally
different. Dominant frequency changes significantly over
the call duration in at least one of the distinct note types,
e.g. Smilisca sila (Hylidae), Cochranella granulosa (Cen-
trolenidae), Engystomops pustulosus (Leptodactylidae).

Discussion

Syntactic classification systems allow for unambiguous
communication between researchers and comparisons be-

521

tween studies. For instance, the frequent adoption, appli-
cation, and widespread use of clear definitions of anuran
egg types, tadpole morphotypes, and developmental stages
(Gosner 1960; Altig and Johnston 1989; Altig and McDiar-
mid 2007; Schulze et al. 2015), anuran reproduction modes
(Duellman and Trueb 1994; Haddad and Prado 2005),
modes of amplexus (Carvayal-Casto et al. 2020), and an-
uran call types (Wells 1977; Toledo et al. 2015), have
demonstrated their substantial value for herpetologists.

In this paper, we present a simplified guild classifi-
cation system for anuran advertisement calls. In order
to avoid assignment of individuals from one species to
different guilds, we have not included body size-driven
traits like dominant frequency, temperature-driven traits
like pulse rate, or motivation-driven traits like inter-call
interval duration or call rate. The use of only three call el-
ements (call, note, pulse, plus the presence or absence of
frequency modulation), allows for the unambiguous allo-
cation of any anuran advertisement call currently known
to us to a distinct syntactic, non-functional, call guild.

The number of species investigated by us, although
covering the majority of families, habitats and regions,
represents only a small proportion (about 17%) of the
currently known anuran species (> 7100; Frost 2019; last
accessed 10 March 2020). It is thus possible, or even like-
ly, that advertisement calls discovered in the future may
not perfectly fit our proposed guild system. However,
this system could easily be extended. For example, the
proposed guilds could be divided by differentiating with-
in a guild the maximum of amplitude (initial, centred or
terminal of call), the dominant frequency (low, medium
or high-pitched calls), the direction of frequency modula-
tion (negative or positive), or by the distinction between
pulsatile and tonal calls.

Our definition of call guilds may not only allow for
better comparisons between variable call descriptions, as
suggested by Krause (1987), but a syntactic classification
based on acoustics may also enable improved insight into
the life-history of species. Most anurans behaviourally
select and call from species-specific breeding sites (Du-
ellman and Trueb 1994; Wells 2007). Different calling
behaviour and different habitats both affect signal prop-
agation through call-specific environments in different
ways. Abiotic (e.g., humidity or air pressure) and biotic
factors (e.g., vegetation density or structure) may affect
sound waves (Bradbury and Vehrencamp 2011). Propaga-
tion properties may change due to an individual (usually
male) frog, calling from different substrates or microhab-
itats, such as trees, leaf-litter, from water, underground,
or, if they call singly or in a chorus (Lopez et al. 1988;
Forrest 1994; Lardner and bin Lakim 2002). Intrinsic fac-
tors such as body condition or fatigue can also change
propagation properties (Humfeld 2013; Jansen et al.
2016). Call properties and calling behaviour, thus, may
be adjusted behaviourally to avoid or reduce information
loss or alteration of structure. Many breeding sites share
similar features, such as stagnant versus flowing streams,
open or closed vegetation (Hédl 1977; Kwet 2001;

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522

Schliiter 2005), and characteristics of such microhabitats
may alter sound in specific ways. For instance, torrent
water introduces background noise, which may simply
mask the call (or certain frequency components); dense
vegetation may cause scattering, blurring, or reflections,
particularly of amplitude-modulated calls (Bradbury and
Vehrencamp 2011). Thus, habitat characteristics may
force or select for species living in similar environments
to share specific combinations of call elements. It is pos-
sible that the call guild types presented herein are coupled
to certain behavioural patterns and thus allow predictions
about the behaviour of species. Several correlations be-
tween bioacoustics and habitat, behaviour, or morphol-
ogy have already become known in frogs, as well as in
other animals (Etges 1987; Krause 1987; Hodl 1996;
Martins et al. 2006; Vasconcelos and Rossa-Feres 2008;
Both and Grand 2012; Sinsch et al. 2012). For example,
Neotropical birds living in dense understorey show less
frequency modulations than birds of more open habitats
(Morton 1975). However, it is unlikely that call proper-
ties are determined by single factors; acoustic signals will
be, apart from phylogeny, shaped by various environmen-
tal and species-specific characters (Goutte et al. 2018).

By classifying calls according to structural elements,
our syntactic call guilds might assist in detecting such
general correlations between call characteristics and nat-
ural history, or habitat. Based on the calls of the 1253
Species considered in this study, the most common call
guilds were guilds C and D, followed by guilds A and B
(Table 1). Calls with more complex structures, like guilds
E to H, were less frequent. Frequency modulation was
most often associated with simple and relatively short
calls, whereas complex calls were less likely to consist of
frequency modulated elements.

Our guild system is not suited to discriminate between
closely related species or to describe species; it is, thus,
not a tool for taxonomy. However, it might be used as a
first “sorting step” for an acoustic characterisation in call
descriptions, and it may help to facilitate the understand-
ing of anuran advertisement call evolution. For example,
a semantic classification of advertisement calls assumes
that similar calls comprise the same information (Wells
1977; Toledo et al. 2015). However, the informational
content of advertisement calls often differs (Ryan 2001;
Gerhardt and Huber 2002). An increase in call complexi-
ty may be related to more, or different, social interactions,
like in Engystomops pustulosus (Ryan et al. 1982; Ryan
1985; Ryan and Rand 1990; Baugh and Ryan 2010). The
ultimate adaptive significance for such reduction or addi-
tion of information may be indicative of interactions of
species with their abiotic and biotic environments. The
simple classification of call guilds based on structure may
facilitate interpretation of these acoustic interactions and
help clarify the origin of call components or structures.
Finally, we envision that our syntactic call guide classi-
fication scheme will be a useful tool set for future me-
ta-analyses and comparative studies concerning the evo-
lution of anuran acoustic signals. However, inclusion of

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Emmrich, M. et al.: Anuran call guilds

questions relating to how the environment, morphology,
life-history and phylogeny shape anuran advertisement
calls, remains a challenge for forthcoming studies.

Acknowledgments

We thank Franco Andreone, Roberto Alonso, Rainer
Gunther, Axel Kwet, Rafael Marquez and Gongalo M.
Rosa for providing sound recordings, Ariel Rodriguez for
fruitful collaboration and productive discussions, the ed-
itor Rafe Brown and two anonymous reviewers for their
constructive critique and suggestions.

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925

Supplementary material |

Database for the definition of anuran call
guilds

Authors: Mike Emmrich, Miguel Vences, Raffael Ernst,
Jorn Kohler, Michael F. Barej, Frank Glaw, Martin
Jansen, Mark-Oliver Rodel

Data type: DOCX file

Explanation note: Table $1: List of 1253 anuran species
with advertisement calls; References (literature and
CDs) for anuran calls used in this study; Web sources
for anuran calls used in this study.

Copyright notice: This dataset is made available under
the Open Database License (http://opendatacommons.
org/licenses/odbl/1.0/). The Open Database License
(ODbL) is a license agreement intended to allow us-
ers to freely share, modify, and use this Dataset while
maintaining this same freedom for others, provided
that the original source and author(s) are credited.

Link: https://doi.org/10.3897/zse.96.38770.suppl 1

zse.pensoft.net