Risks of multimodal signaling:

Bat predators attend to dynamic

motion in frog sexual displays
Wouter Halfwerk, Marjorie M. Dixon, Kristina J. Ottens , Ryan
C. Taylor, Michael J. Ryan, Rachel A. Page and Patricia L.
Jones
OBJECTIVES:
To determine if the fringe-lipped bat (Trichops cirrhosus) detect and
select prey (Tungara frog, Physalaemus pustulosus) by its vocal sac,
To determine if T.cirrhosus prefer dynamic vocal sacs over static ones,
or vise-versa,
To examine the sensory system (both echolocation and vision) used by
T.cirrhosus to detect the vocal sac in a cue isolation experiment; and
To quantify the detection limits of T.cirrhosus visual and echolocation
system.
INTRODUCTION:
Courtship requires animals to produce
complex signals which favors reproductive
success.
Complex dance rituals
Nuptial gifts
Plumage displays
Songs and Calls
Used by females to assess the desirability of
the male as a contributor to the genes of the
progeny
INTRODUCTION:
Tungara Frog (Physalaemus pustulosus)
Commonly distributed on the
Mexican tropics and in Northern
South America
Males produce advertisement calls
to attract females. Calls are
usually accompanied with vocal
sac movement to achieve a novel
response.
Variation in call complexity
determines reproductive success.
 INTRODUCTION:
Tungara frogs produce calls with
two components, a frequency-
modulated whine which can be
produced by itself (simple call) or
followed by 1-7 harmonic burst or
chucks (complex calls).
One chuck apparently increases the
attractiveness of a male fivefold Top, blue illustrations are waveforms and bottom gray-
thus male frogs preference to scale illustrations are spectrograms. The figure
illustrates calls of varying complexity of the same
produce whines with more chucks. male: (top, left) whine, (top, right) whine plus chuck,
(bottom, left) whine plus two chucks, and (bottom,
right) whine plus three chucks.
INTRODUCTION:
However, males are not always observed to produce
whines with chuck. Why?
Acoustic as well as visual signals released by male Tungara frogs is
not only received by its intended receiver (female Tungara) but also
by its predator, the Fringe-lipped bat, which eavesdrops to its
courtship rituals with the female.
Thus, males would do a simple call and a complex call alternatively,
changing them based on the present risk of predation.
This complex behavioral response is influenced by natural and sexual
selection pressures acting on the individual.
INTRODUCTION:
Moreover, production of the sound incidentally creates
ripples on the water surface, and along with the
dynamics of the vocal sac, creates a multimodal cue.
Such incorporation of a signal component into a
multimodal sexual display increase the accuracy of
signal transfer or enhance overall signal efficacy,
increasing the attractiveness of the male to the female.
Thus, it is also of interest if multimodal signals are
used by the predator (Trichops cirrhosus) to assess the
prey quality.
METHODOLOGY:
Experiment 1:
Test whether bat perceive vocal sac and if dynamic
vocal sac was preferred over static ones
Two model frogs was used, one which emits both
acoustic cues and vocal cues while the other one emits
acoustic cues only.
Both model were situated 5 meters from the perch of
T. cirrhosus.
Experimental set-up of the two choice
tests.

(B) Front view showing the robofrog with

inflated vocal sac on the right and the
control model on the left.
(A). Side view of the experimental setup
showing the speaker used to broadcast
acoustic call component with a Plexiglas
screen plus frog model on top. Both the
experimental catheter mimicking the
tngara frog vocal sac as well as the
catheter controlling for sound produced
during catheter inflation are shown in the
enlargement.
Experimental set-up of the two choice
tests.

Stimulus presentation showing

sound playback (whine plus chuck)
in the top channel and the
inflationdeflation of the vocal sac
in the bottom channel. Top view showing the two frog models, the
Plexiglas screen and the holes underneath the
Maximum inflation was reached models to allow for sound transfer. On the
200ms after sound and roughly right side is the bat on the perch, 35 away
150ms after peak amplitude of the from the experimental platform.
whine.
METHODOLOGY:
Experiment 2:
Variation of stimulus presentation
Presentation of vocal sac, sound off on leaving perch, vocal sac off on
leaving perch
Four treatments:
Continuous
Perch only
Dynamic
Static
METHODOLOGY:
Experiment 3:
Use of echolocation to detect vocal sac was examined
Four treatments:
Visual cue only
Echolocation cue only
Both visual and echolocation cue
Visual and echolocation cue absent
RESULTS:

Experiment 1: Naive Responses

Wild-caught bats were given a choice to attack a frog model with a
dynamic vocal sac present (inflatingdeflating in synchrony with sound) or
a control model (with a deflated vocal sac). All bats made their very first
attack on the model with the dynamic moving vocal sac [generalized linear
mixed model (GLMM); N=10, intercept=1, z-score=2.79, P=0.005)].
RESULTS:
Experiment 2: Effect of Stimulus Presentation
The presentation of the sound and the vocal sac was varied to test
whether bats perceived the vocal sac from their perch and whether the
vocal sac had to be dynamically inflated and deflated. Sound and vocal
sac were continuously presented until a bat flew from its perch towards
the frog models. Across all treatments, the average attack rate on the
vocal sac model was 56% higher than that of the control model.
Furthermore, the attack rate depended on the type of presentation
there is a high preference on the dynamic inflating-deflating sac
compared to static inflated sac, which was not attacked by the bat.
RESULTS:
RESULTS:
Bats prefer to attack a frog model with a
dynamically moving vocal sac. Shown are
boxplots derived from the model estimates
per playback treatment (Experiment 2). Bats
preferred to hover over and attack the frog
model with a dynamically inflateddeflated
vocal sac under all playback conditions.
Attack preference did not differ from
chance with a continuous inflated vocal sac
(static treatment). Dashed line indicates
chance level at 50%. n.s., not significant;
P<0.1, *P<0.05, **P<0.01, ***P<0.001.
RESULTS:
Experiment 3: Use of Echolocation to Detect Vocal Sac

The bats were presented with dynamic vocal sac playback

and the sensory environment was manipulated to test what
sensory system was used. During this experiment, bats
showed a significant attack preference for the vocal sac when
both echolocation and visual cues were present as well as
when trials were carried out in complete darkness so only
echolocation cues were present. However, bats showed no
preference when echolocation was blocked by visually
transparent fields or when both visual and echolocation cues
were absent.
RESULTS:
The cue isolation experiment reveals
that bats use echolocation to detect
vocal sac movements. Shown are
boxplots derived from the model estimates
per cue isolation treatment (Experiment
3). Bats preferred to attack the robofrog
when they had only access to echolocation
cues coming from the vocal sac, but not
when they only had access to visual cues.
The control condition refers to the
treatment in which bats had no access to
visual or echolocation cues. Filled circles
are outliers. n.s., not significant.
CONCLUSION:
Bats have very high preference on frogs with a vocal sac that was
dynamically inflated and deflated in synchrony with acoustic call
production. Attack preference depends on the dynamic movement of
the vocal sac and not just size alone, because bats will not attack
static inflated frog models nor the static deflated ones.
The cue isolation experiment showed that bats used echolocation and
not visual cues to detect the frogs vocal sac. Thus, the predation
pressure imposed on the frogs multimodal signal will depend on the
sensory conditions that will affect bats echolocation.
CONCLUSION:
Sexual and natural selection pressures on the same trait are not
always mediated through the same sensory modalities, since
female tungara frogs assess the males vocal sac in the visual
domain, whereas the bat monitor frog vocals using echolocation.
References:

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Halfwerk et al., Crossmodal Comparisons of Signal Components Allow for Relative-Distance

Assessment, Current Biology (2014), http://dx.doi.org/10.1016/j.cub.2014.05.068

Halfwerk et al., Risks of multimodal signaling: bat predators attend to dynamic motion in
frog sexual displays, The Company of Biologists Ltd | The Journal of Experimental Biology
(2014) 217, 3038-3044 doi:10.1242/jeb.107482.

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