A blind climber: The first evidence of ultrasonic echolocation in arboreal mammals

Abstract

The means of orientation is studied in the Vietnamese pygmy dormouse Typhlomys chapensis, a poorly known enigmatic semi-fossorial semi-arboreal rodent. Data on eye structure are presented, which prove that Typhlomys (translated as "the blind mouse") is incapable of object vision – the retina is folded and retains no more than 2 500 ganglion cells in the focal plane, and the optic nerve is subject to gliosis. Hence, Typhlomys has no other means for rapid long-range orientation among tree branches other than echolocation. Ultrasonic vocalization recordings at the frequency range of 50–100 kHz support this hypothesis. The vocalizations are represented by bouts of up to 7 more or less evenly-spaced and uniform frequency-modulated sweep-like pulses in rapid succession. Structurally, these sweeps are similar to frequency-modulated ultrasonic echolocation calls of some bat species, but they are too faint to be revealed with a common bat detector. When recording video simultaneously with the ultrasonic audio, a significantly greater pulse rate during locomotion compared to that of resting animals has been demonstrated. Our findings of locomotion-associated ultrasonic vocalization in a fast-climbing but weakly-sighted small mammal ecotype add support to the "echolocation-first theory" of pre-flight origin of echolocation in bats. This article is protected by copyright. All rights reserved

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Integrative Zoology 2017; 12: 172–184 doi: 10.1111/1749-4877.12249
ORIGINAL ARTICLE
A blind climber: The rst evidence of ultrasonic echolocation in
arboreal mammals
Aleksandra A. PANYUTINA,1,2 Alexander N. KUZNETSOV,2 Ilya A. VOLODIN,2,3 Alexei V.
ABRAMOV4,5 and Irina B. SOLDATOVA2
1Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow, Russia, 2Department of Vertebrate Zoology,
Faculty of Biology, Lomonosov Moscow State University, Moscow, Russia, 3Scientic Research Department, Moscow Zoo,
Moscow, Russia, 4Zoological Institute, Russian Academy of Sciences, Saint Petersburg, Russia and 5Joint Vietnam–Russian Tropical
Research and Technological Centre, Hanoi, Vietnam
Abstract
The means of orientation is studied in the Vietnamese pygmy dormouse Typhlomys chapensis, a poorly known
enigmatic semi-fossorial semi-arboreal rodent. Data on eye structure are presented, which prove that Typhlo-
mys (translated as “the blind mouse”) is incapable of object vision: the retina is folded and retains no more than
2500 ganglion cells in the focal plane, and the optic nerve is subject to gliosis. Hence, Typhlomys has no oth-
er means for rapid long-range orientation among tree branches other than echolocation. Ultrasonic vocalization
recordings at the frequency range of 50–100 kHz support this hypothesis. The vocalizations are represented by
bouts of up to 7 more or less evenly-spaced and uniform frequency-modulated sweep-like pulses in rapid suc-
cession. Structurally, these sweeps are similar to frequency-modulated ultrasonic echolocation calls of some bat
species, but they are too faint to be revealed with a common bat detector. When recording video simultaneous-
ly with the ultrasonic audio, a signicantly greater pulse rate during locomotion compared to that of resting an-
imals has been demonstrated. Our ndings of locomotion-associated ultrasonic vocalization in a fast-climbing
but weakly-sighted small mammal ecotype add support to the “echolocation-rst theory” of pre-ight origin of
echolocation in bats.
Key words: arboreal locomotion, reduced eyes, Rodentia, Typhlomys, ultrasonic echolocation
Correspondence: Aleksandra A. Panyutina, Severtsov Institute
of Ecology and Evolution, Russian Academy of Sciences,
Moscow, 119071, Russia.
Email: myotis@mail.ru
INTRODUCTION
Solid surfaces reflect both light and sound, which
gives animals an opportunity to perceive out-of-touch
surroundings using vision or echolocation. Use of vi-
sion is much more common because life on Earth is full
of sunlight. Only under poor light conditions are ani-
mals forced to expend their own metabolic energy to

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Bat-like echolocation in arboreal rodent
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emit sounds and listen to echoes instead of using vision.
To approach acuity of vision echolocation calls must be
composed of as short as possible wavelengths to come
into ultrasonic range. Among mammals, ultrasonic echo-
location is used in water by odontocetes, from dolphins
up to pygmy sperm whale (Madsen et al. 2005), and is
used on land by chiropterans (excluding most fruit bats
[Pteropodidae]) (Jones & Teeling 2006). Beyond these
species no other mammal has yet been shown to rely on
ultrasonic echolocation as the main means of orienta-
tion, either in water or on land.
Early reports on ultrasonic echolocation in shrews
(Gould et al. 1964; Tomasi 1979; Forsman & Malmquist
1988) were subject to doubt (Konstantinov & Movchan
1985). Indeed, ultrasonic echolocation is likely disad-
vantageous as compared to touch in the typical environ-
ment of shrews. Inside leaf-bedding the high-frequency
calls would be reected as noise from all the nearby ob-
stacles, which are readily accessible to vibrissae. These
calls would not pass beyond these obstacles to pro-
vide far-away echoes for long-range orientation. New-
er studies have failed to show ultrasonic echolocation in
shrews (Catania et al. 2008; Siemers et al. 2009; Volo-
din et al. 2012, 2015; Zaytseva et al. 2015). It has been
argued that lower-frequency calls (audible clicks and
twitters) must be more appropriate for echolocation in
cluttered substrates, and can be used by shrews to gain
echoes for orientation (Siemers et al. 2009; Volodin et
al. 2015; Zaytseva et al. 2015).
All available speculations on echolocation regarding
small rodents come from behavioral experiments: dor-
mice, hamsters, voles and rats were vision-deprived and
forced to look for food (see review by Thomas & Jali-
li 2004). The only instance of potential ultrasonic echo-
location was seen in Norway rats [Rattus norvegicus
(Berkenhout, 1769)]. However, there was very limited
acoustic analysis provided in the study (Thomas & Jalili
2004). The study concluded that the calls were echo-lo-
cating based on weak evidence including the pulse-like
waveform of the calls, and on the fact that they were
produced by rats left alone in the dark.
Therefore, neither shrews nor typical rodents aid to
portray how a quadrupedal mammal can rely on ul-
trasonic echolocation. The issue is interesting not only
by itself, but also because such an animal, if discov-
ered, could serve as a model for the hypothesized ances-
tral state of bat echolocation. There are three current-
ly debated theories on how echolocation in bats may
have evolved (Speakman 2001; Jones & Teeling 2006;
Simmons 2008; Maltby et al. 2010). According to the
“ight-rst theory,” echolocation arose in bats after ac-
quisition of ight ability (Speakman 2001, 2008; Sim-
mons et al. 2010). The “echolocation-first theory” in-
sists that echolocation was acquired earlier than flight
by quickly moving small mammals adapted to complex
but poorly-lit environments (Fenton et al. 1995; Jones
& Teeling 2006; Teeling 2009; Teeling et al. 2012). Ac-
cording to the “tandem theory,” the ight and echoloca-
tion developed simultaneously (Schnitzler et al. 2003).
The “ight-rst theory” is best supported by current ev-
idence due to the fact that there is an absence of extant
examples of non-volant mammals using ultrasonic echo-
location. Followers of the “echolocation-first theory”
must nd a peculiar prototype: a mammal that has ac-
quired ultrasonic echolocation and lives in an environ-
ment more appropriate as a runway for flight than the
depth of leaf-bedding.
Zoologists have identified many mammals with re-
duced eyes and many fast-climbing mammals, but no
mammal except the poorly studied Typhlomys (Fig. 1)
combines these extreme features together. Typhlomys,
which means “the blind mouse,” belongs to an enigmat-
ic rodent family, Platacanthomyidae (Jansa et al. 2009).
The genus Typhlomys consists of two species, of which
Typhlomys chapensis Osgood, 1932 (the Vietnamese
pygmy dormouse) lives in northern Vietnam and Typh-
lomys cinereus Milne-Edwards, 1877 lives in southern
China (Abramov et al. 2014). The pygmy dormice in-
habit subtropical forests at the altitudes of 360–2000-m
Figure 1 Vietnamese pygmy dormouse Typhlomys chapen-
sis. Its reduced eyes are reected in the generic name, which
means “the blind mouse.”

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a.s.l. (Smith 2008; Abramov et al. 2012). The biology
of these rodents is poorly studied; they are reported to
be both terrestrial and burrowing (Smith 2008), and we
trapped T. chapensis by live cage-traps not only on the
ground but on tree branches too (Abramov et al. 2014),
which indicates they have climbing ability. Keepers at
the Moscow Zoo, which obtained 2 of these animals,
conrm their outstanding agility, especially in an arbo-
real environment, and also report their strictly nocturnal
activity and the absence of any vocalizations. One can
hypothesize that with reduced eyes, the arboreal mobil-
ity in the dark and silence could be guided by ultrasonic
echolocation.
In this study we have conducted the following exper-
iments to provide evidence for use of ultrasonic echo-
location in Typhlomys: (1) checked vision quality using
histology to study the morphology of the eye structure;
(2) investigated the presumed existence of ultrasonic
vocalization with sensitive acoustic equipment and; (3)
upon nding ultrasonic vocalization we used video and
audio recordings to correlate vocalization with locomo-
tion in an environment that is difcult to navigate using
non-visual orientation.
MATERIALS AND METHODS
Eye morphology
Two ethanol-preserved adult specimens of T. chapen-
sis from the Zoological Institute of the Russian Acade-
my of Science (Saint Petersburg, Russia) were studied.
They were collected in northern Vietnam in the moun-
tain tropical forest in 2010–2012 by live cage-traps set
up either on branches or on the ground. These speci-
mens are: a 16.7-g female (ZIN 101563) and a 18.3-g
male (ZIN 101566). In each specimen, both eyes were
excised, and the eyeball axial length was measured ex-
ternally with a vernier caliper (precision 0.1 mm) under
a Stereomicroscope Carl Zeiss Stemi SV 11.
The expected eyeball axial length was calculated us-
ing an equation from Howland et al. (2004) for mam-
mals in general:
Log (eye axial length in mm) = 0.9354+ 0.225*Log
(body mass in kg), (1)
with coefcient of determination R2 = 0.835.
In addition, we calculated the regression equation
separately for rodents, using data on 28 rodent species
from Howland et al. (2004) as:
Log (eye axial length in mm) = 0.9243+ 0.2161*Log
(body mass in kg), (2)
with R2 = 0.650.
We calculated the regression equation for bats, using
data on 11 bat species from Howland et al. (2004) as:
Log (eye axial length in mm) = 0.9566+ 0.3255*Log
(body mass in kg), (3)
with R2 = 0.745.
After measurements were taken, all 4 eyeballs with
a bit of surrounding tissues were embedded in parafn,
cut into 4 or 5-μm thick serial sections and stained ac-
cording to Mallory or with hematoxylin and eosin using
standard procedures. Sections were studied under a Lei-
ca DM 2500 M microscope.
Experimental design
Two adult males of T. chapensis (#1 and #2) were
studied experimentally at the Scientific Department of
the Moscow Zoo (Moscow, Russia). Like the speci-
mens used in eye morphology research, they were col-
lected in northern Vietnam in the mountain tropical for-
est in 2010–2012 by live cage-traps set up either on the
branches or on the ground. In the Moscow Zoo, they
were kept for 10 months before the acoustic experi-
ments, under a natural light regime and room tempera-
ture (24–26 °C); individuals were isolated in glass-and-
wire-mesh cages 40 × 40 × 80 cm with mulch bedding
and various shelters and branches. The animals were fed
with small rodent chow and water ad libitum.
Ultrasound-and-video recordings were carried out on
2 days in July 2013. Two adult males (#1 and #2) were
tested singly in a separate room without other animals.
Tests were performed in the experimental chamber (30
× 50 × 100 cm) having the back 50 × 100-cm wall made
of smooth plastic, the front 50 × 100-cm wall and one
30 × 50-cm wall made of glass, and the other 30 × 50-
cm and both 30 × 100-cm wall made of wire mesh (10
× 10 mm). The chamber contained straight and furcat-
ed dry branches 0.5–5.0-cm thick and the mulch bed-
ding. During test trials the cage was set either vertically
(see Supplementary_1.mov video) or horizontally (in re-
spect of direction of its 100-cm side), with the branches
being re-positioned from time to time (when explorato-
ry activity of the animal ceased) so that the test animal
remained unfamiliar with the environment. This was
aimed at sustaining exploratory activity of the animals.
In total, 13 test trials (7 with male #1 and 6 with male
#2) were conducted. A test trial lasted 2 to 12 min, de-
pending on the behavior of the subject animal. All the
test trials were performed between 1400 and 1800 hours
at temperatures of 24–26 °C; there were two trials with

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natural light from windows and 11 trials with bright
light of halogen lamps (1.5 kWt in total) for better qual-
ity high-speed video recording. The test trials were au-
dio and video recorded with an ultrasonic recorder and
two camcorders simultaneously; the recordings were
synchronized by clicker signals.
The Pettersson D 1000X recorder with a built-in mi-
crophone (Pettersson Elektronik AB, Uppsala, Swe-
den) was used for audio recording (sampling rate 768
kHz, 16 bit; frequency response from 5 to 235 kHz).
During recordings, the distance from the hand-held mi-
crophone to a test animal varied from 10 to 50 cm. The
microphone was oriented as far as possible directly to
the muzzle of tested animal because the sector for ultra-
sound recording is rather narrow (see Supplementary_2.
mov video). Each test trial was recorded as a WAV-le.
The total duration of audio recordings was 62 min (30
min from male #1 and 32 min from male #2).
Two camcorders were used simultaneously for vid-
eo recording: the JVC GC-PX10 camcorder (Vic-
tor Company of Japan, Yokohama, Japan) was used
for a high-definition video (HD-video, 50 fps, shut-
ter speed 1/1000 s, frame size 1920 × 1080 pixels, with
soundtrack) and the Casio EX-F1 camcorder (Casio
Computer, Tokyo, Japan) was used for a high-speed vid-
eo (HS-video, 299.7 fps, shutter speed 1/2000 s, frame
size 512 × 384 pixels, no soundtrack).
Acoustic analysis
All acoustic les were inspected for the presence of
ultrasound by means of the Avisoft SASLab Pro soft-
ware (Avisoft Bioacoustics, Berlin, Germany). Next,
540 pulses of good quality (325 pulses from male #1
and 215 pulses from male #2) were selected for acoustic
analysis. After a high-pass ltration at 10 kHz (sampling
frequency 768 kHz, Hamming window, FFT 512 points,
frame 50%, overlap 93.75%, frequency resolution 1500
Hz, time resolution 0.04 ms), the maximum fundamen-
tal frequency (fmax) and the minimum fundamental fre-
quency (fmin) were measured for each pulse, and the
pulse bandwidth as bandw = fmax–fmin (Fig. 2b) was
calculated. The pulse duration (dur), the duration to the
pulse maximum amplitude in percentage of the entire
pulse duration (disttomax) (Fig. 2b) and the peak fre-
quency of a pulse (fpeak) (Fig. 2c) were measured by
applying the automated parameter measuring option of
Avisoft. The periods between pulses (period), from the
beginning of a pulse to that of the next pulse (Fig. 2a)
Figure 2 The waveforms, spectrograms
and power spectrum (c) representing
acoustic patterns and acoustic variables
measured from the vocal pulses of Typh-
lomys chapensis. (a) Natural sequence of
pulses, of which the rst 4 comprise a typi-
cal bout; period, the period between pulses.
(b) and (c) A pulse without echo; fmax, the
maximum fundamental frequency; fmin,
the minimum fundamental frequency;
bandw, the pulse bandwidth; dur, the pulse
duration; disttomax, the duration to the
pulse maximum amplitude; fpeak, the peak
frequency. (d) A pulse with weak echo. (e)
A pulse with strong echo.

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were also measured. Measurements were exported auto-
matically to Microsoft Excel software (Microsoft, Red-
mond, WA, USA) for further processing.
As the study sample (only 2 animals) was too small
for individual-based statistical analysis, we used the
pooled samples from both individuals according to
Leger and Didrichsons (1994). Analysis was carried out
with STATISTICA v. 8.0 software (StatSoft, Tulsa, OK,
USA). Signicance levels were set at 0.05, and 2-tailed
probability values were tested. Means are given as mean
± SD.
Video analysis
To estimate the probable bearing of orientation of ex-
perimental animals on the uncovered ultrasonic puls-
es, the relationship between vocalization and locomo-
tion was studied. The respective ultrasonic audio-tracks
and video-tracks were superimposed by using Virtu-
alDub (http://www.virtualdub.org/) and AviSynth (http://
sourceforge.net/projects/avisynth2/) software. Ultra-
sonic audio tracks and HD-video tracks were superim-
posed based on clicker signals. The HD-video tracks
and HS-video tracks were superimposed based on ani-
mal postures. The total duration of the resulting HD-vid-
eo or HS-video clips with the ultrasonic audio track was
57 min (see Online Resources Video for example).
The recordings were sampled by selecting the first
0.5-s fragment from every 5-s interval. Each selected
0.5-s fragment was classied into locomotion or resting
state of the animal by viewing the video track in Vir-
tualDub software. The audio track was analyzed using
Syrinx software (http://www.syrinxpc.com/). The num-
ber of ultrasonic pulses was counted and their arrange-
ment in bouts was registered for each 0.5-s fragment
(detailed denition of a bout is presented in the Results
section). The corresponding pulse rates (pulses per sec-
ond) and numbers of single pulses and 2-pulse, 3-pulse
etc. bouts per second were calculated. Fragments, in
which the animal was beyond the video frame or in
which ultrasonic pulses were overlapped with clicker
strikes or other noises, were excluded from the analysis.
In total, 531 0.5-s fragments (247 fragments from male
#1 and 284 fragments from male #2) were analyzed.
To compare the pulse rates in the 0.5-s fragments
during rest and locomotion, we used the online Kolm-
ogorov–Smirnov test (http://www.physics.csbsju.edu/
stats/KS-test.html). In addition, the medians ± quartiles
were estimated for the 0.5-s fragments containing pulses
(pulse rate >0).
Some ultrasonic pulses together with their echoes
could have been missed by the microphone due to the
narrow beam of ultrasound propogation and the move-
ment of the subject animal outside of the audio record-
ing reach. At the same time, virtually all pulses emitted
by resting animals were collected. However, some un-
derestimation of the pulses emitted during locomotion is
unlikely to affect the validity of the present results.
RESULTS
Eye morphology
In each of the 2 studied specimens with an average
body mass of 17.5 g, the eyeball axial length was mea-
sured as 1.4 mm. According to Equation (1), the expect-
ed eye axial length for a 17.5-g mammal should be 3.5
mm. According to Equation (2), the expected eye axi-
al length for a 17.5-g rodent should also be 3.5 mm. Ac-
cording to Equation (3), the expected eye axial length
for a 17.5-g bat should be 2.4 mm. Thus, the eye axi-
al length of Typhlomys is very small, not only compared
to an average mammal or rodent, but even to an average
bat.
The measurement of the total eyeball inevitably in-
cluded some soft tissue at its posterior side. Measure-
ments on histological sections (Fig. 3) give even a
smaller value of approximately 1 mm for the net eye-
ball diameter. The lens front surface, which faces the
pupil, is somewhat irregular (Fig. 3b1). The lens matter
is very damaged on our histological sections, but looks
rather normally everywhere except for the pupil-facing
portion, which is filled with irregularly packed fibers
(Fig. 3b2).
Our histological sections show very restricted, if any,
vitreous chamber between the lens and retina. Some
parts of the retina tightly adjoin the lens, and the other
parts form irregular folds (Fig. 3a). These folds are de-
nitely not an artifact of hard ethanol xation but the nat-
ural condition of the live animal, as is shown by the spe-
cic structure of the nerve ber layer in the deep folds
(Fig. 3b3). If they were an artifact the nerve ber lay-
er would be folded together with the other layers of ret-
ina to form a double lamina. Contrary to that, axons of
ganglion cells converge from the opposite walls of the
fold to form, inside it, a single lamina of the nerve fi-
ber layer; if one decided that it was an artifact and tried
to spread the fold, these axons would be inevitably torn.
In the retina, ganglion cells are widely spaced from each
other. In our series of sections, we did not nd any local

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concentrations of ganglion cells. The section represent-
ed on Fig. 3b2 allows one to count them 1 by 1. Their
number in this section is as few as 70–75, including 21–
23 ganglion cells in the retinal fold. In accordance with
the very small amount of the ganglion cells, the nerve
ber layer is very thin too (see again the nerve bers in
the deep retinal fold represented in Fig. 3b3). Finally,
the optic nerve of Typhlomys is characterized by an ir-
regular arrangement of nuclei inside it (Fig. 3c), whose
pattern is indicative of reactive gliosis. We found no
blood vessels supplying retina inside the optic nerve.
Locomotor behavior
In captivity, Typhlomys likes to dig in mulch and, at
the same time, shows evidence of arboreal adaptation.
Its agile movements over branches seem to indicate
that its eyes function well (this cannot be true, howev-
er, with the given eye morphology). It moves with con-
dence in an unfamiliar environment over sloping and
vertical branches, while also making rapid aimed leaps
from branch to branch over gaps several times great-
er than the tactile reach of its vibrissae (see Supplemen-
tary_1.mov video). It can also upwardly jump 30–40
cm (body length being 7–9 cm, and vibrissae not lon-
ger than 5 cm). From time to time, the animal hangs for
a while upside-down on its hind limbs and, detecting an
appropriate surface below, beyond the reach of vibris-
sae, jumps down onto it (see Supplementary_3.mov vid-
eo).
Acoustics
Almost all recordings, which we obtained in various
experiments with Typhlomys, were surprisingly full of
soft ultrasonic vocalizations composed of rather uniform
units (Fig. 2). These units are pulses represented in most
recordings by the fundamental frequency band only; the
second (harmonic) frequency band was pronounced in
less than 1% of pulse records. The fundamental frequen-
cy band shows a descending pattern of frequency modu-
lation from the maximum at 127.3 ± 6.3 kHz to the min-
imum at 64.1 ± 4.6 kHz, resulting in pulse bandwidth of
63.2 ± 7.3 kHz. The pulse peak frequency is 93.4 ± 7.4
kHz, the pulse duration is 0.68 ± 0.15 ms, and the pulse
amplitude reaches a maximum in the middle of the pulse
(51.6% ± 11.1% from the start).
Single pulses alternate with double-pulse bouts (dy-
ads), triple-pulse bouts (triads), and up to 7-pulse bouts.
Bouts can be distinguished by shorter silent intervals
between the pulses: intra-bout intervals were always
shorter than 23 ms, while inter-bout intervals were al-
ways longer than 26 ms. In fact, an essential bout spec-
icity exists (Fig. 2a): if there are 3 or more pulses in a
bout, they are evenly spaced, so that the intervals are al-
most equal or change gradually differing from each oth-
Figure 3 Eye structure in Typhlomys chap-
ensis. (a) Section parallel to the optic axis
stained according to Mallory represents
extensive folding of retina. (b) Section
through the optic axis stained according to
Mallory at different magnifications: (b1)
general eye composition, (b2) close-up
view of the retina and (b3) close-up view
of the retinal fold. (c) Longitudinal section
of the optic nerve at its exit out of retina
stained with hematoxylin–eosin shows gli-
osis of the optic nerve. AC, anterior cham-
ber; Ch, choroid; Co, cornea; GCL, gan-
glion cell layer; I, iris; INL, inner nuclear
layer; L, lens; NFL, nerve ber layer; ON,
optic nerve; ONL, outer nuclear layer (rod
nuclei); P, pigment epithelium; R, retina; S,
sclera. Scale bars 0.1 mm.

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er only fractionally; contrary to that, the intervals before
and after the bout are several times longer, reaching the
full bout duration or exceeding it. The criterion of sub-
equal intra-bout intervals is inapplicable to dyads, but
they are well distinguished from 2 single pulses in that
the total duration of the true dyad is less than that of tri-
ad and so on (Fig. 2a). The mean period in a bout is
13.02 ± 3.00 ms, with the minimum and maximum val-
ues of 8.70 and 23.27 ms, respectively. Further analysis
of bouts is beyond the scope of this study.
Vocal activity
In 432 of the 531 0.5-s fragments, analyzed for a re-
lationship between vocalization and locomotion, the
test animals were resting, whereas in 99 fragments
they were moving. At rest, vocal pulses were scored in
only 10.6% of fragments (n = 46), whereas during lo-
comotion the pulses were scored in two-thirds of frag-
ments (n = 66) (Fig. 4a). At rest, the mean pulse rate
was less than 1.0 pulse per second, whereas during lo-
comotion it was more than 12.5 pulses per second. Fi-
nally, at rest, the maximum pulse rate was 38 pulses per
second, whereas during locomotion it was 64 pulses per
second. There is a significant correlation between in-
creased pulse rate and locomotion (Kolmogorov–Smirn-
ov P-value < 0.001). The Kolmogorov–Smirnov D-val-
ue reaches its maximum of 0.56 when the pulse rate is
zero. Simply speaking, even at pulse rates as low as 1,
the animal is likely to be in motion rather than at rest.
On the whole, the vocal activity during locomotion is
convincingly greater than at rest.
This does not simply mean that the more the animal
moves, the more it vocalizes: the composition of calls
changes abruptly with locomotion. We have compared
the rest and locomotion pulse distributions in the sub-
set of fragments where vocal activity was present (pulse
rate > 0) (Fig. 4b,c). In this subset, the mean pulse rate
at rest was 9.1 pulses per second (Fig. 4b), of which on
average 5 pulses were single, 2 pulses were combined
in a 2-pulse bout (dyad) and longer bouts were rare
(Fig. 4c). Contrary to that, the mean pulse rate during
locomotion was 18.8 pulses per second (Fig. 4b), of
which on average less than 4 pulses were single, 6 puls-
es were combined in three 2-pulse bouts, another 6 puls-
es were combined in two 3-pulse bouts (triads), and a
4-pulse bout (tetrad) was rather frequent too (Fig. 4c).
In the dataset considered, the top pulse rate (64 pulses
per second) was registered in male #1, which produced
three 4-pulse bouts and four 5-pulse bouts (pentads)
during half a second.
DISCUSSION
Degree of blindness
Presented data on eye morphology (Fig. 3) strong-
ly suggest vision degeneration in Typhlomys, which can
be best appreciated by comparison with subterranean
blind mammals such as the mole Talpa (Carmona et al.
2008; Carmona et al. 2010; Quilliam 1966) and the na-
ked mole rat Heterocephalus glaber Ruppell, 1842 (Ni-
kitina et al. 2004). Contrary to mice and similar to more
mature naked mole rats (Nikitina et al. 2004), the lens
surface in Typhlomys shows some wavy irregularities.
The lens matter in Typhlomys looks rather similar to that
in the mouse and the naked mole rat; it is denitely not
as bad for light conduction as in the mole, whose lens
is entirely lled with disorganized bers and cell nuclei
(Carmona et al. 2008; Quilliam 1966). In Typhlomys,
the lens bers are disorganized at the pupil-facing side
Figure 4 Relationship between vocalization and locomotion in
Typhlomys chapensis. (a) Proportion of 0.5-s fragments with-
out vocal pulses (white bars) and with pulses (grey or black
bars) at rest and during locomotion. (b) Total pulse rates and (c)
pulse rate distributions in different bouts, from single pulse to
a 5-pulse bout (pentad), at rest (grey bars) and during locomo-
tion (black bars) in 0.5-s fragments where the vocalization was
present (pulse rate > 0). On (b) central points show medians,
boxes show rst and third quartiles, and whiskers show mini-
mum and maximum values.

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only and no cell nuclei are visible. On the whole, the
lens of Typhlomys is diminished approximately like that
in the mole rat but less than in the mole.
Irregular retinal folds are even more extensive in Ty-
phlomys than in the naked mole rat (Nikitina et al.,
2004). Such folds protrude beyond the focal plane; they
are ineffective with respect to object vision and destroy
continuity of image projection on the retina. The reduc-
tion of vitreous chamber resulting in too short a distance
between lens and retina is detrimental for focusing.
Notably, the mole eye appears better suited for focus-
ing than the eyes of Typhlomys and the naked mole rat
in that it retains big depth of the vitreous chamber and
does not have image-destructive retinal folds (Quilliam
1966; Carmona et al. 2008).
The acuity of the retina can be estimated by the num-
ber of its ganglion layer cells. Mice possess a single lay-
er of tightly packed ganglion cells (Nikitina et al. 2004;
Carmona et al. 2010). In the Iberian mole, a nearly
blind rodent, this layer does not differentiate structurally
from neuroblasts even in adults (Carmona et al. 2010).
The naked mole rat (Nikitina et al. 2004) and Typhlo-
mys show an intermediate state: the ganglion cell layer
is present, but its cells are widely spaced from each oth-
er because their number is reduced. Our data allow us to
roughly estimate that the retina of Typhlomys spread on
a plane must have an area of a square of 50 × 50 gangli-
on cells, if the visually useless retinal folds are exclud-
ed. Therefore, in total there are approximately 2500 vi-
sually useful ganglion cells in the eye of Typhlomys. To
appreciate the poor image quality of such an eye, imag-
ine a digital photographic camera with a 2.5-kilopixel
sensor which is pressed against the back surface of the
lens. Note also that the common mole’s eye is not much
worse in this respect, bearing about 2000 ganglion cells
(Quilliam 1966).
Typically, axons of the ganglion cells converge into
the optic nerve over the concave lens-facing surface of
the retina, lining it with a nerve ber layer. Reduction
of the ganglion cells’ number in Typhlomys results in
a very thin nerve ber layer. In the naked mole rat, the
nerve ber layer tends to disappear after birth (Nikitina
et al. 2004). As for the optic nerve, its normal structure
is characterized by regular arrangement of glial cells,
characterized by longitudinal rows of their nuclei (e.g.
in a mouse; Nikitina et al. 2004). In the naked mole rat,
as well as Typhlomys (Fig. 3c), this regular pattern is de-
stroyed, and the optic nerve corridor is plugged with
cluttering nuclei indicating reactive gliosis (Nikitina et
al. 2004). In contrast, the optic nerve of moles looks
more normal, with the blood vessels in the middle and
nerve bers on the periphery (Quilliam 1966).
On the whole, the type of eye diminishment observed
is rather similar in Typhlomys and the naked mole rat.
This is in contrast to the mole eye, which has a more de-
stroyed light entrance (the lens) but has better retained
those parts that are located downstream in respect of
the signal propagation. We can conclude that Typhlo-
mys, like the two subterranean mammals mentioned
above, cannot focus on an obstacle or target such as a
tree branch; at best, its eyes can distinguish dark from
light or help photoperiodicity, like in the mole (Carmo-
na et al. 2010). The retention of eyes for photoperiod-
icity may be crucial for survival of Typhlomys as an aid
in avoiding vision-relying predators. Indeed, observa-
tions by the Moscow zookeepers indicate that Typhlo-
mys avoids coming out of the shelter when the darkness
is incomplete. Adhering to complete darkness, which
was noticed by keepers in the Moscow Zoo, may help it
in the wild to avoid any vision-relying predators.
Possible evolutionary scenario of Typhlomys
Generally, reduced eyes are characteristic of small
subterraneous or leaf-bedding dwellers, who mainly rely
upon smelling with whisking for orientation (Deschenes
et al. 2012; Catania 2013) and also rely upon seismic
sensitivity (Narins et al. 1997; Kimchi et al. 2005; Ma-
son & Narins 2010). Therefore, the degenerated eyes
along with the Typhlomys’ digging ability suggest that
this lineage may have evolved from a semi-fossorial an-
imal residing in the leaf-bedding of tropical forests.
A peculiarity of Typhlomys is its unique juxtapo-
sition of fossorial and scansorial adaptations. We hy-
pothesize that the eyes of Typhlomys lost visual acui-
ty in its leaf-bedding but non-arboreal ancestor, as in the
mole rat. However, we can also hypothesize with con-
dence that high-frequency hearing did not degrade as it
did in subterranean rodents and moles (Konstantinov &
Movchan 1985; Heffner et al. 2006; Heffner & Heffner
2008). Once the chance to invade the arboreal niche in
the tropical forest appeared, the almost blind emigrant
from a leaf-bedding environment would only be able to
crawl slowly, caring not to lose tactile contact with the
tree surface. The re-acquisition of vision from a mole-
rat-like degree of blindness is likely to have been dif-
cult. If so, ultrasonic echolocation would have become
the only available replacement of vision for long-range
orientation and agile locomotion in the complex 3-D
environment full of branches, which can suddenly be-
come footholds or obstacles. Indeed, the denite posi-

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tive correlation of ultrasound production with acrobatics
on branches, as well as the serial arrangement of these
short ultrasonic calls is denitively echolocation.
The ultrasonic vocalization of Typhlomys is reminis-
cent of bats’ echolocation signals. Both are represent-
ed by pulses produced with very high peak frequency
(93 kHz) and combined in bouts. Structurally, the pulses
are most similar to frequency-modulated (FM) calls of
bats, which are relatively short sweeps with fast descent
of frequency from the start to the end (Schnitzler Kalko
2001; Maltby et al. 2010). In Typhlomys the frequency
descends from 127 to 64 kHz during 0.68 ms. Yet, the
sweeps of Typhlomys are much more faint than in bats,
which is revealed by the fact that the vocalizations can-
not be noticed at all with a common bat detector. The
low intensity of echolocation sweeps may be explained
by their use in relatively short-range orientation only, of
approximately a few decimeters in front of the animal (it
is a short range as compared to bat echolocation, but a
long range as compared to the length of vibrissae). Note
that signals of the so called “whispering bats” hunting
among tree branches are poorly audible with a common
bat detector as well (e.g. Grifn 2004).
Though faint, the sweeps of Typhlomys are much ad-
vanced with respect to their high frequency and, espe-
cially, in their frequency-modulated and bout-organized
structure, which was yet unknown beyond bats. Typh-
lomys’ sound-producing apparatus seems to have un-
dergone some peculiar specialization in respect of the
available frequency range. It has likely entirely lost the
ability to produce any calls audible to the human ear.
This follows from the fact that during several years in
captivity neither keepers nor ourselves ever heard any
calls of Typhlomys, which is in sharp contrast with the
well-known ability of other small rodents, as well as
bats, for both sonic and ultrasonic vocalizations.
The peak frequency of 93 kHz is just above the nor-
mal hearing range of non-chiropteran mammals of
the size of Typhlomys, such as shrews, mice and dor-
mice (Konstantinov & Movchan 1985; Heffner & Heff-
ner 2008). These animals can hear well only at the low-
er end of Typhlomys’ calls and echoes. It is known that
the rise of call frequencies in bats is accompanied by re-
spective improvement of high-frequency hearing sensi-
tivity (Heffner et al. 2006), and the same must be neces-
sary to Typhlomys to make use of the energy-expensive
calls at the 93-kHz peak frequency. In this study, the
perception of frequencies around 90 kHz by Typhlomys
has not been shown directly: this could be the subject of
future studies.
The higher the perceived echo frequency, the closer
the use of sonar approaches vision with respect to acu-
ity. Therefore we can denitely conclude that the ultra-
sonic activity of this unique rodent is rather advanced.
Its ancestors could hardly hear above 70–90 kHz, like
shrews (70 kHz limit), mice (80 kHz limit) and com-
mon dormice (90 kHz limit) (Konstantinov & Movchan
1985). They could have used primitive and less pre-
cise echolocation in the low ultrasonic range from 20 to
70 kHz, or even human-audible twittering as shrews in
a leaf-bedding environment use (Siemers et al. 2009).
The rise of produced and perceived frequencies must
have accompanied the ascension from leaf-bedding onto
trees: fossorial-to-scansorial transition.
Rethinking the evolutionary scenario of bats
Ultrasonic echolocation calls have never been dis-
covered and recorded in any climbing mammals before.
More than that, Typhlomys is the rst non-volant mam-
mal, which relies on on-air ultrasonic echolocation for
long-range orientation during locomotion more than on
any other senses. Thus, our nding allows us to recon-
sider a possible evolutionary scenario of bats; name-
ly, the circumstances of echolocation origins. Based on
molecular grounds, it is now clear that microbats, which
are all characterized by echolocation, are paraphylet-
ic relative to the almost exclusively non-echolocating
megabats (Tsagkogeorgasend et al. 2013; see also pure
molecular trees supplementary to O’Leary et al. [2013]).
This new fact, that non-echolocating megabats are root-
ed inside echolocating microbats, should now be tak-
en into account when answering an old question of
whether or not the rst ancestral bat, capable of apping
flight, was already able to echolocate. There two sce-
narios are possible: (1) the origin of echolocation fol-
lowed that of ight several times in parallel and the ab-
sence of the former in megabats is plesiomorphic, or (2)
echolocation was already developed in the ying ances-
tral bat and then secondarily lost in megabats. The Typh-
lomys’ precedent seems to be good evidence in favor of
the second alternative; that is, the so-called “echoloca-
tion-rst theory.” This theory implies that the origin of
echolocation was in small quadrupedal mammals adapt-
ed to fast locomotion in complex but poorly-lit environ-
ments (Fenton et al. 1995; Teeling et al. 2012). Simi-
lar to Typhlomys, the non-ying bat ancestor could have
been an arboreal animal with previously reduced eyes
(most probably not impaired structurally as in Typhlo-
mys), which developed ultrasonic echolocation for com-
pensation. It must have been of great advantage when

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leaping and gliding as a means to nd the best surface
to land upon in the dark. The initial function of echolo-
cation was orientation rather than prey detection. First,
this is due to the fact that for prey detection perfect
echolocation is necessary, while even the most primitive
usage of echoes, such as in humans (Rice et al. 1965) or
in the piebald shrew (Volodin et al. 2012), is enough to
aid orientation. The second reason is that the prey can
effectively be detected by echo in a homogeneous me-
dium, such as air or water. On solid surfaces, such as
ground or branches, even bats must detect prey by other
means than echolocation. Namely, most of the gleaning
bats use echolocation for orientation, but locate the prey
on the substrate by sounds produced by prey itself (e.g.
Arlettaz et al. 2001; Jones et al. 2003). As to the hearing
ability of ultrasonic echoes, the current understanding
in the eld is exemplied by this statement: “the typi-
cal high-frequency sensitivity of small non-echolocat-
ing mammals would have been sufcient to support ini-
tial echolocation in the early evolution of bats” (Heffner
et al. 2006, p. 17).
In the course of flight development in the first true
bats, the power of ultrasonic echolocation calls must
have increased in order to satisfy the new speed of pro-
gression; ight is much faster than running or jumping
over branches and so sensing echoes from the more dis-
tant obstacles would have become crucial. The second-
ary loss of ultrasonic calls, which we propose for Ptero-
podidae, may have directly resulted from their transition
to the fruit diet. This is due to the associated increase of
body size with this diet and of the larynx in particular.
This results in a corresponding decrease of fundamental
frequency of laryngeal vocalization, preventing echolo-
cating. However, some of them (e.g. the cave-living ge-
nus Rousettus) developed ultrasonic vocalization again
based on different morphological structure: by using
brief, broadband tongue clicks, instead of laryngeal calls
(Yovel et al. 2011). Note that non-echolocating Pteropo-
didae possess their best hearing sensitivities around 8–10
and 20–25 kHz (Heffner et al. 2006), while in Rousettus
the second optimum of the hearing prole is shifted to
45 kHz (Yovel et al. 2011).
CONCLUSION
The major limitations of our study were the small
number of live individuals to experiment with and the
poor quality of dead specimens for histology. This is
due to the extreme rarity of the Vietnamese pygmy dor-
mouse, or “blind mouse” in nature. That is why our con-
clusions, although rather convincing, are still prelimi-
nary. Additional research is required to describe in detail
the acoustic patterns of ultrasonic pulses and bouts in
Typhlomys and to compare them with the known acous-
tics of bats and with non-echolocation ultrasonic calls
of other rodents. A remaining question is the mechanism
of signal production: Is it located in the larynx? In ad-
dition, is the animal entirely incapable of communicat-
ing in the human-audible range? It will be of interest to
investigate the degree of eye degeneration and develop-
ment of echolocation in a closely related and very sim-
ilar species, the Chinese pygmy dormouse, Typhlomys
cinereus.
The next very interesting direction of research is as-
sociated with the closest, and almost as rare, extant rela-
tive of Typhlomys: the Malabar spiny dormouse Platac-
anthomys. Scarce scientic data suggest their nocturnal
activity in spite of rather small eyes and arboreal capa-
bilities (Mudappa et al. 2001; Jayson & Jayahari 2009).
Taken together, these traits are similar in the 2 related
genera; this suggests that Platacanthomys may too use
echolocation as a means for orientation. However, the
eyes in this genus, although small, are much larger than
in Typhlomys, judging from available photos. Therefore,
there is a chance of nding a more basal stage of echo-
location development. Perhaps Platacanthomys pro-
duces vocalizations in the low-ultrasonic or even the
human-audible range, and its calls may not be yet orga-
nized in bouts. If this was true, Platacanthomys would
ll the “evolutionary gap” at the very beginning of the
suggested evolutionary scenario for Typhlomys, as well
as of the grand scenario for bats.
ACKNOWLEDGMENTS
The eld works in Vietnam were possible due to sup-
port of the Joint Vietnam–Russian Tropical Research
and Technological Centre. We are sincerely grateful to
V. V. Rozhnov for substantial organization efforts which
allowed us to undertake this study, to A. V. Shchinov,
Nguyen Dang Hoi and Vu Van Lien for their great help
and scientific expertise during the field works, to the
staff of the Scientic Department of the Moscow Zoo,
and especially to O. G. Ilchenko, for the animal and
room supply, to E. L. Yakhontov for assistance in ex-
periments and work with literature, to B. D Vasiliev for
his kind transport support in the crucial situation on the
rainy 15 July 2013, our rst shooting day, to A. G. Bush
and E. D. Pavlov for assistance with microscopes, to O.
Yu. Orlov and T. V. Khokhlova for consulting regarding
eye morphology, to Al. B. Savinetsky for consulting in

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© 2016 International Society of Zoological Sciences, Institute of Zoology/
Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd
statistics, to A. A. Lissovsky for help with Syrinx soft-
ware usage, to C. Voigt and D. N. Lapshin for valuable
discussion on echolocation, to E. V. Volodina for partic-
ipation in English translation of the initial Russian text,
and to M. Kaczmarek, D. V. Logunov and S. V. Koval-
sky for improving the English of the nal draft.
In all experiments we adhered to the “Guidelines for
the treatment of animals in behavioural research and
teaching” (2012, Animal Behaviour, 83, 301–309). This
study was approved by the Committee of Bio-ethics of
the Lomonosov Moscow State University (research pro-
tocol no. 2011-36). Video processing was performed
with support of the Russian Science Foundation (project
14-50-00029 “Scientific basis of the national biobank
– depository of the living systems”). Acoustic analysis
was supported by the Russian Science Foundation (proj-
ect 14-14-00237) and the Program of Basic Research
of the Presidium of the Russian Academy of Scienc-
es “Wildlife: Current Status and Problems of Develop-
ment.”
All the other work, including experimental setting
and recording, eye morphology research and manuscript
preparation, was financed by the Russian Foundation
for Basic Research (projects 14-04-01132 and 15-04-
05049).
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SUPPLEMENTARY MATERIALS
Supplementary_1.mov
Typical exploratory behavior of the Vietnamese pyg-
my dormouse Typhlomys chapensis (male #1) in the ex-
perimental cage set vertically. Natural speed playback,
50 fps. Note especially, 2 jumps from branch to branch.
Supplementary_2.mov
Blind climbing of the Vietnamese pygmy dormouse
Typhlomys chapensis male #2. Soundtrack recorded at
768 kHz sampling rate is synchronized with videotrack
recorded at 50 fps. Together, they are slowed down 10-
fold, so that the resulting sampling rate is 76.8 kHz, fps
is 5 and the peak frequency (fpeak) of ultrasonic pulses
appears audible at approximately 9 kHz.
Supplementary_3.mov
Nine seconds of blind climbing of the Vietnam-
ese pygmy dormouse Typhlomys chapensis male #1.
Soundtrack recorded at 768 kHz sampling rate is syn-
chronized with videotrack recorded at 299.7 fps. At the
beginning the record is reproduced at normal speed;
then videotrack and soundtrack are slowed down 20-
fold, so that the resulting sampling rate is 38.4 kHz, fps
is 14.985 and the peak frequency (fpeak) of ultrasonic
pulses appears audible at approximately 4.5 kHz. Note
especially, the non-stop vocalization of the animal hang-
ing upside-down on its hind limbs.
Panyutina AA, Kuznetsov AN, Volodin IA, Abramov AV, Soldatova IB (2017). A blind climber: The rst evidence
of ultrasonic echolocation in arboreal mammals. Integrative Zoology 12, 172–84.
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