Contemporary Research on Anuran Communication
A Symposium Celebrating the Extraordinary Careers and Contributions of
Albert Feng, Carl Gerhardt, Walter Hödl, Darcy Kelley, Peter Narins, & Kent Wells
Wednesday, August 6, 2014
Hunter College, New York, NY
Schedule of Talks
9:00 – 9:15
Josh Schwartz, Introduction to the Symposium
9:15 – 10:00
Mike Ryan, Six Answers to Tinbergen’s Four Questions
10:00 – 10:20 Mark Bee, Three Facets of the Frog’s Cocktail Party Problem
10:20 – 10:40 Break
10:40 – 11:00 Ryan Taylor, Multimodal Signaling
11:00 – 11:20 Alex Baugh, Auditory Induction
11:20 – 11:40 Ham Farris, Thalamic Stimulation Modulates Midbrain Auditory Excitability
11:40 – 12:00 Susan Herrick, Acoustic Interference and Vocal Interactions in Syntopic Species
12:00 – 1:20
Lunch
1:20 – 1:40
Kim Hoke, Causes and Consequences of Repeated Ear Loss and Regain
1:40 – 2:00
Marcos Gridi-Papp, Frequency Tuning in Communication Systems
2:00 – 2:20
Michael Reichert, Evolution of Complex Signal Repertories
2:20 – 2:40
Gerlinde Höbel, Experience-mediated Plasticity of Mate Recognition
2:40 – 3:00
Break
3:00 – 3:20
Phil Bishop, Successful Sexy Small Males
3:20 – 3:40
Kyle Summers, Diversity of Reproductive Strategies in Poison Frogs
3:40 – 4:00
Max Ringler, Population Experiments with a Poison Frog
4:00 – 4:20
Sabrina Burmeister, Natural History as a Compass in Neuroethology
2 No Evidence for Auditory Induction in a Tropical Frog with a Continuous Vocalization
Alexander T. Baugh1*, Michael J. Ryan2,3, Mark A. Bee4
1
Department of Biology, Swarthmore College, Swarthmore PA 19081, USA
Section of Integrative Biology, The University of Texas, Austin, TX 78712, USA
3
Smithsonian Tropical Research Institute, P.O. Box 0843-03092 Balboa Ancón, Republic of Panamá
4
Department of Ecology, Evolution and Behavior, University of Minnesota, St. Paul MN 55108
2
Under real-world conditions, incomplete or masked acoustic scenes are common challenges
encountered in many acoustically communicating animals. This is particularly problematic in lekbreeding organisms, including many species of anuran amphibians. In humans and some nonhuman vertebrates, an auditory object containing brief segments of silence can be rendered
perceptually continuous by inserting noise in these gaps. This ‘auditory induction’ or the
‘continuity illusion’ induces the perception of complete auditory objects despite fragmentary
acoustic stimulation. Previous tests of auditory induction in two species of North American
treefrogs (Hyla versicolor and H. chrysoscelis) have demonstrated an absence of this
phenomenon. These treefrog species produce pulsatile (non-continuous) vocalizations, whereas
studies in other taxa, including humans, have used continuous auditory objects (e.g. tonal
glides). Therefore, we tested for auditory induction in a tropical leptodactylid species
(Physalaemus pustulosus) with a continuous advertisement vocalization. Using two-choice
phonotaxis tests, we created a set of stimuli that included, among other variations, stimuli with
silent gaps filled with band-limited and spectral intensity-matched noise. Our results did not
demonstrate strong evidence to support auditory induction in this species. In combination with
previous research, these findings suggest that anuran receivers cope with interrupted or
masked acoustic stimulation using alternative mechanisms.
Staying Relevant to Human Hearing: Three Facets of the Frog’s Cocktail Party Problem
Mark A. Bee
Department of Ecology, Evolution and Behavior, University of Minnesota, St. Paul MN 55108
People with impaired hearing have tremendous difficulty solving the “cocktail party problem,”
that is, understanding speech in noisy social environments. Hearing aids and cochlear implant
devices typically provide their users with limited benefits in such settings. One way to improve
these devices looks to nature to discover how evolution has solved biologically analogous
problems in other animals. Frogs are among the best examples of nonhuman animals that have
evolved reproductive and social systems involving vocal communication in noisy environments.
Understanding the problems frogs encounter by communicating in dense and noisy choruses,
and the solutions that evolve to overcome these challenges, have been two of the major
research goals in the careers of this symposium’s honorees. In this talk, I will describe three
distinct facets of the problem that frogs and humans experience in noisy settings, including
energetic masking, informational masking, and sound source perception. I will also provide
examples of past and present efforts investigating each of these facets in frogs to demonstrate
how all three are relevant to understanding the mechanisms, function, and evolution of frog
communication systems. I will also suggest a new framework based on these facets in frogs as
a way for future research on these animals to remain relevant to current problems in biomedical
research on human hearing and speech communication. With their internally-coupled middle
ears, inner ears with multiple sensory papillae, and brains that lack an auditory cortex, frogs can
continue to serve as important alternatives to mammals in modern hearing research.
3 Successful Sexy Small Males Ignore Female Preferences in the Red-eyed Tree Frog
(Litoria chloris)
Phil J. Bishop*,1, Peter M. Narins2,3, Ikkyu Aihara4, Michel E. Ohmer5, and Jean-Marc Hero6
1
Department of Zoology, University of Otago, Dunedin 9054, New Zealand
Department of Integrative Biology and Physiology, UCLA, Los Angeles, CA 90095, USA
3
Department of Ecology and Evolutionary Biology, UCLA, Los Angeles, CA 90095, USA
4
Brain Science Institute, RIKEN, Saitama 351-0198, Japan
5
School of Biological Sciences, University of Queensland, Brisbane, QLD 4072, Australia
6
Griffith School of Environment, Griffith University, Southport, QLD 4215, Australia
2
Many anuran studies have shown that females select the bigger males in a chorus and this
choice is largely based on using acoustic parameters of the call. Previous studies of the redeyed tree frog (Litoria chloris) and orange-thighed frog (Litoria xanthomera), both endemic to
Australia, have shown that amplectant pairs consist of females and the smaller males of the
chorus. It was suggested that smaller males may spend more time in the chorus and hence had
a higher probability of encountering a female by chance alone. An alternative hypothesis, based
on female choice, suggests that females actively choose smaller males using their call
characteristics. We conducted phonotaxis experiments and discovered that, like most anurans,
L. chloris females preferentially approach lower frequency calls thereby suggesting that their
‘preference’ for small males is not driven by acoustic cues alone. To determine why smaller
males were more successful we then turned our attention to the spatio-temporal structures of
their choruses. Using a purpose built sound-imaging device called Firefly, which consisted of a
microphone and an LED that illuminates when capturing nearby sounds, we analyzed the
spatio-temporal structures of different L. chloris choruses. This enabled us to determine that
chorus leadership was highly variable in this species. To unravel this mystery further studies are
underway that combine a modification of the Fireflies with acoustic sensor technology, coupled
with non-invasive hormone assays to determine levels of reproductive and stress hormones,
and in situ phonotaxis experiments using known individual males.
Natural History as a Compass in Neuroethology: Understanding How Frogs Hear and See
the World
Sabrina S. Burmeister
Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA
When I began studying frog communication, I had no idea who the giants in the field were but,
during the arc of my education, my research traced the paths of many of those giants: What is
the significance of the sounds that males produce (Wells and Gerhardt)? How do hormones
change the brain and behavior (Kelley)? Do auditory responses predict behavioral responses
(Feng and Narins)? At the center of these questions is an effort to understand the brain and
behavior in the context of ecology and evolution. Recent work in my lab has expanded to
include questions about how frogs remember locations in space. Using simple mazes, we find
that túngara frogs and green and black poison dart frogs differ in the types of cues they
remember during spatial navigation. Túngara frogs depend on cues that are directly associated
with a goal while dart frogs are able to remember complex spatial associations. Furthermore,
dart frogs can modify previously learned associations in a highly flexible manner. These species
differences in spatial cognition can be predicted from species differences in natural history:
While túngara frogs breed in lek-like aggregations that pose little demand on their spatial
4 memory, dart frogs have evolved elaborate parental behaviors that require them to revisit
locations multiple times during a breeding bout. Our findings suggest that the evolution of
parental care in dart frogs promoted the evolution of complex spatial cognition and they hint that
túngara frogs and dart frogs see the world in very different ways.
Sound-by-sound Thalamic Stimulation Modulates Midbrain Auditory Excitability and
Relative Binaural Sensitivity in Frogs
Hamilton Farris
Neuroscience Center and Kresge Hearing Labs, Louisiana State University Health Sciences Center, New Orleans,
LA 70112, USA
Using frogs, the honorees have elucidated numerous fundamental concepts in bioacoustics.
Now, building upon that work, current research is tackling arguably the most important goal in
the field: understanding the mechanisms of auditory scene analysis. Most research on stimulus
sorting has focused on ascending auditory filtering. However, ascending sensitivity is modulated
by descending input. This study examined how descending mechanisms affect auditory
sensitivity in the frog torus semicircularis (TS). During awake in vivo single unit recordings, two
different modes of electrical stimulation to the dorsal thalamus were used to test whether TS
auditory sensitivity could be modulated over longer periods of time (i.e., minutes) or on a soundby-sound basis. Following long-term electrical stimulation (3-10 s), sensitivity (spikes / acoustic
stimulus) decreased 32% and then gradually (600 s) returned to control sensitivity. In contrast,
sound-by-sound electrical stimulation using a single 2-ms duration pulse 25 ms before each
acoustic stimulus caused faster and varied forms of modulation: modulation lasted < 2 s and, in
different cells, excitability either decreased or increased. Within cells, modulation from soundby-sound electrical stimulation varied with acoustic stimuli, including male calls, suggesting
modulation is specific to certain stimulus attributes. For binaural units, modulation depended on
the ear of input, as sound-by-sound electrical stimulation preceding dichotic acoustic stimulation
caused asymmetric modulation. This caused a change in the relative difference in binaural
sensitivity. Thus, sound-by-sound electrical stimulation revealed fast and ear-specific auditory
modulation that is potentially suited to shifts in attention during sound segregation in the
auditory scene.
Frequency Tuning in the Communication System of Túngara Frogs (Engystomops
“Physalaemus” pustulosus)
Marcos Gridi-Papp
Department of Biological Sciences, University of the Pacific, Stockton, CA 95211, USA
In acoustic communication, vertebrate brains interface with the external environment through
vocal apparatuses and ears that should evolve with matched tuning for optimal function.
Evolutionary changes in body size bias the tuning of both vocal folds and middle ears in the
same direction, as larger structures resonate at lower frequencies than smaller ones. To better
understand the evolution of tuning, we examined túngara frogs, which are outliers in the anuran
body-size vs. call frequency relationship, for being small but communicating at low frequencies
(~750 Hz). They produce low frequency signals with an unusually large larynx containing long
vocal folds. Midbrain recordings have revealed maximal sensitivity at ~750 Hz with a secondary
5 peak sensitivity at ~2200 Hz, in agreement with the tuning of the calls. The eardrums and the
thoracic body wall, however, are tuned to ~2200 Hz, as expected for frogs of their size, and their
sensitivity at 750Hz is ~20 dB lower than at 2200 Hz. Measurements involving awake animals or
repositioning of the head and mandible failed to reveal increased low frequency sensitivity at the
eardrum. The tuning of the middle ear, therefore, matches the expectation for body size,
whereas the calls and the midbrain are tuned together to lower frequencies. The evolution of
this mismatch in auditory tuning could reduce the distance from which females can be attracted
to calls and potentially translate into directional selection for increased male call intensity.
Noisy Neighbors: Acoustic Interference and Vocal Interactions Between Two Syntopic
Species of Ranid Frogs, Rana catesbeiana and Rana clamitans.
Susan Z. Herrick
Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT 06269, USA
American bullfrogs (Rana catesbeiana) and green frogs (R. clamitans) share ranges and
breeding seasons, are ecologically similar, and often occupy the same breeding ponds
throughout the summer. Males of both species use vocalizations to defend territories and
attract females. However, bullfrogs have louder, longer calls than green frogs. This could
effectively silence green frogs, exacting a heavy cost on their ability to attract females to the
pond. Nevertheless, in natural settings where these species co-occur, green frogs reproduce
successfully. This suggests that green frogs respond to the calling patterns of bullfrogs in ways
that maximize green frog signal-to-noise ratio. By adapting to bullfrog calling behavior in ways
that reduce acoustic interference, green frogs may increase their breeding success on mixedspecies ponds. I investigated the influence of bullfrog calling patterns on the vocal activity of
green frogs via audio recordings of activity on a breeding pond and of focal interspecific
interactions. Bullfrog chorusing causes a reduction in green frog chorusing. Green frogs
increase chorusing activity in brief windows of bullfrog inactivity and they avoid acoustic overlap
by decreasing calling during bouts of bullfrog vocalizations. These patterns can be detected at
fine timescales as well as between focal interspecific pairs.
Experience-mediated Plasticity of Mate Recognition in Green Treefrogs
Gerlinde Höbel
Department of Biological Sciences, University of Wisconsin-Milwaukee, Milwaukee, WI 53201, U.S.A.
Reproductive character displacement (RCD) is a pattern of geographic variation in sexual traits
in which differences between species are more pronounced in areas of sympatry than in areas
of allopatry. When testing for RCD, geographic variation in signals and preferences is usually
interpreted as representing genetic divergence. However, if experience with different
communication environments (conspecific / heterospecific signals) induces or enhances species
recognition, then patterns of geographic variation resembling RCD may also arise from plasticity
in the expression of sexual traits. In a previous study (Höbel & Gerhardt 2003) I had
documented RCD in the acoustic communication system of green treefrogs, Hyla cinerea.
Here, I extend this study by exposing H. cinerea females from allopatric and sympatric sites to
playbacks of simulated conspecific or heterospecific communication environments before
testing their preferences. I found that there is plasticity in the expression of female mate
6 preferences, and that there is geographic variation in this plasticity: exposure to heterospecific
signals enhanced species recognition in females from a far-allopatric site, but not from a farsympatric one. These findings suggest that species recognition is not entirely genetic, but partly
influenced by experience.
Causes and Consequences of Repeated Ear Loss and Regain in Toads
Kim L. Hoke1.*, Molly C. Womack1, Jakob Christensen-Dalsgaard2
1
2
Department of Biology, Colorado State University, Fort Collins, CO 80523, USA
Department of Biology, University of Southern Denmark, 5230 Odense M, Denmark
Various hypotheses have been proposed to explain why some anuran species lack outer and
middle ear structures. Explanations typically invoke either directional selection for low frequency
vibration sensitivity or relaxed selection on ear structures or hearing ability. We describe the
extensive lability in ear structures in bufonids and highlight how phylogenetically informed
comparisons can reveal the role of relaxed selection, directional selection, and pleiotropy in
driving the repeated losses and regains of ear structures. Species differ in hearing sensitivity
and in the extent of extratympanic hearing. We present initial results relating morphological
evolution to changes in acoustic sensitivity, and suggest that the relative importance of relaxed
selection, directional selection, and pleiotropy in shaping ear transitions may vary within the
bufonid clade.
Static and Dynamic Traits and the Evolution of Complex Signal Repertories
Michael Reichert
Department of Behavioral Physiology, Institute of Biology, Humboldt University-Berlin, 10115 Berlin, Germany
Patterns of variation in signal characteristics can give important insights into their function and
evolution. For instance the concept of static and dynamic traits has greatly advanced our
understanding of sexual selection in both anurans and other organisms. My aim is to use this
framework to understand variation in signal characteristics across multiple signal types. Many
animals use qualitatively different signal types in different contexts, for example the
advertisement and aggressive calls of many anurans. When these signals share a common
production mechanism, this may constrain the magnitude and variability of signal characteristics
within each signal type. I examined patterns of variation in signals within and between
individuals and across signal types in two species, Dendropsophus ebraccatus and Hyla
versicolor. In D. ebraccatus, there were surprisingly high correlations between values of several
call characteristics measured within an individual’s advertisement calls and those within its
aggressive calls. Furthermore, there were strong positive correlations for within-individual
variability of the two different call types. In H. versicolor, there were few correlations in either
means or variances of call characteristics in these two call types. I tentatively hypothesize that
species whose advertisement and aggressive signals are similar in structure (like D.
ebraccatus) will show stronger correlations across call types than those with widely divergent
call structures in their repertoires (like H. versicolor). More significantly, I argue that considering
patterns of variability across multiple signal types is essential to understand the evolution of
signal structure and the diversification of complex signal repertoires.
7 Island of the Frogs - Population Experiments with the Poison Frog Allobates femoralis
Max Ringler*, Andrius Pašukonis, and Eva Ringler
Department of Integrative Zoology, University of Vienna, 1090 Vienna, Austria
Amphibians hold a unique position as the only vertebrate group where basically all members
feature complex live cycles with two distinct, free-living stages that have to face entirely different
challenges in their respective environment. In our current project we investigate determinants of
fitness in the Neotropical frog Allobates femoralis by exploring the effects of parental
relatedness and parental investment on individual reproductive success at various life cycle
stages and by analyzing the associated patterns of space use. To this end we have installed an
experimental population of A. femoralis on a ~5 ha river island by releasing 1800 genotyped
tadpoles into artificial pools. The released tadpoles were taken from a nearby population on the
mainland where we have been conducting research on Allobates femoralis since 2008.
Additionally, we are conducting behavioral experiments with an ex-situ breeding population at
the University of Vienna. The combined approach of controlled field studies under natural
conditions and laboratory experiments allows us to assess the effects of parental relatedness on
fertilization success, larval survival in the clutch, and survival of post-metamorphic juveniles. At
the same time, the island population and experiments in captivity allow us to address questions
on patterns of juvenile dispersal and adult spatial behavior, as well as the use of spatial, visual,
and acoustic information for parental behavior and space use in males and females. The
overarching approach of our research originates in the credo of one of the honorees of this
symposium, Walter Hödl: “Let your animals ask the questions!”
"Froggy Went a-Courtin’" and Now We Know Why: Six Answers to Tinbergen’s Four
Questions
Michael J. Ryan
Section of Integrative Biology, University of Texas, Austin, TX 78712, USA
Studies of anuran communication have been anchored solidly at the proximate and ultimate
ends of analysis, owing especially to the pioneering neuroscience studies of Robert Capranica
and the behavioral-evolutionary studies of W. Frank Blair and Murray Littlejohn. But the
intervening intellectual space has not been left vacant, and the field of anuran communication is
one of the most truly integrative pursuits in organismal and evolutionary biology. The vigorous
and healthy state of the field owes much to the scientists being honored in this symposium:
Albert Feng, Carl Gerhardt, Walter Hödl, Darcy Kelley, Peter Narins, and Kent Wells. As a
group these researchers have made fundamental contributions to our understanding of how
frogs develop, produce, and analyze acoustic signals and to the functional, ecological, and
evolutionary significance of these signals, especially in the context of sexual selection and
speciation. In addition, they have all contributed critically to the integration of anuran
communication by building intellectual bridges across research specializations, which in other
fields sometime serve as intellectual barriers. In this context I review some of the major
achievements of each of the honorees
8 Diversity of Reproductive Strategies in Poison Frogs
Kyle Summers
Department of Biology, East Carolina University, Greenville, NC 27858, USA
Dendrobatid frogs show a diversity of parental care and mating strategies, which provide
multiple avenues for the evolution of communication. In this talk, I will review research on
reproductive behavior in poison frogs with male, female, and biparental care, with a focus on
communication among adults and between adults and offspring. In some species with male
care, elaborate forms of tactile, acoustic and visual communication have evolved in the context
of intrasexual and intersexual interactions, including the evolution of deceptive strategies. In
species with biparental care, males and females also engage in multimodal communication,
particularly in the context of tadpole care and feeding. In species with both female care and
with biparental care, extended tadpole care involving egg feeding has evolved. This has
enhanced the importance of parent-offspring communication, and I review recent research on
tadpole deposition by adults and on begging behavior by tadpoles in the context of parentoffspring conflict and honest signaling theory.
Multimodal Signaling in the Túngara Frog
Ryan C. Taylor
Department of Biological Sciences, Salisbury University, Salisbury, Maryland 21801, USA
Courtship communication in anurans often occurs in noisy chorus environments, analogous to
human cocktail parties. Female frogs express strong mating preferences for particular male
vocalizations, but how they identify and assess individual callers within the chorus remains
unclear. One possible mechanism is cross-modal integration, whereby females attend to both
acoustic and visual cues (male vocal sac inflation). Using a robotic frog with an inflatable vocal
sac, we conducted experiments to examine how the addition of a visual cue influences female
responses to male acoustic signals. In nature, male túngara frogs produce a two-note courtship
call, the whine and chuck, and the vocal sac inflates synchronously during the production of
both notes. We tested female mating preferences when we artificially varied the temporal
synchrony of the vocal sac inflation relative to the whine and chuck. Some combinations elicited
a strong preference from females, some combinations generated a strong aversive response,
and other combinations were neutral. Interestingly, the temporal combinations that elicited
positive, negative, or neutral responses were not predictive in an additive fashion. The use of
the visual cue likely arose as a mechanism to reduce discrimination error in noisy
communication environments. Our data suggest however, that substantial plasticity exists in
how females perceive various audio-visual combinations; this plasticity likely provides an
important basis for positive selection on the evolution of multimodal signals.
9