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ISSN Versión impresa: 1992-2159; ISSN Versión electrónica: 2519-5697
Biotempo, 2017, 14(2), jul-dec.: 87-95.
Biotempo (Lima)
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
COMPARATIVE ANATOMY OF THE BONY LABYRINTH OF THE BATS
PLATALINA GENOVENSIUM (PHYLLOSTOMIDAE, LONCHOPHYLLINAE)
AND TOMOPEAS RAVUS (MOLOSSIDAE, TOMOPEATINAE)
ANATOMÍA COMPARADA DEL LABERINTO ÓSEO DE LOS MURCIÉLAGOS
PLATALINA GENOVENSIUM (PHYLLOSTOMIDAE, LONCHOPHYLLINAE) Y
TOMOPEAS RAVUS (MOLOSSIDAE, TOMOPEATINAE)
Paúl M. Velazco1 & Camille Grohé1
1 Division of Paleontology, American Museum of Natural History, Central Park West at 79th Street, New York, NY 10024, USA.
E-mails: pvelazco@amnh.org; cgrohe@amnh.org
ABSTRACT
e bony labyrinth inside the temporal bone houses the inner ear, sensory organ of hearing and balance. Variations in
the three components of the bony labyrinth (cochlea, vestibule, and semicircular canals) give insight into the physiology
and evolution of the di erent groups of mammals. Based on high resolution micro-Computed Tomography (µCT), we
reconstructed the digital endocasts of the bony labyrinths of Platalina and Tomopeas. We found that both species exhibit
unique characteristics among bats, that were mainly located in the cochlea, including the aspect ratio of the cochlear
spiral, cochlear width rela tive to that of the basicranial region, number of cochlear spiral turns, among others. Finally we
highlight the need of more morphological comparative studies of the bony labyrinth.
Key words: Cochlea – Chiroptera – Inner ear – Phyllostomidae – Molossidae
RESUMEN
El laberinto óseo dentro del hueso temporal protege el oído interno, órgano sensorial para la audición y balance. La
variación en los tres componentes del laberinto óseo (cóclea, vestíbulo y canales semicirculares) ofrece un alcance sobre la
siología y evolución de los diferentes grupos de mamíferos. Usando la tomografía micro-computarizada de alta resolución
(µCT), reconstruimos los moldes digitales internos de los laberintos óseos de Platalina y Tomopeas. Encontramos que
ambas especies presentan características únicas entre los murciélagos, que están principalmente localizadas en la cóclea,
entre ellos la proporción del espiral de la cóclea, ancho de la cóclea con respecto al ancho de la región de la base del
cráneo, número de espirales cocleares. Finalmente, resaltamos la necesidad de más estudios de morfología comparada del
laberinto óseo.
Palabras clave: Cóclea – Chiroptera – Oído interno – Phyllostomidae – Molossidae
LIMA - PERÚ
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INTRODUCTION
Bats are the only mammals capable of ying and most
of them use echolocation to orientate and move in
complete darkness. Echolocation is the production
of high-pitched sounds, which returning echoes are
analyzed by the brain and help these bats detecting
obstacles and prey without the use of vision. Most bats
produce echolocation signals in the larynx, while a few
species echolocate with sounds produced by tongue
clicks, and one species may use wing claps (Veselka et
al., 2010). Echolocating bats exhibit a unique set of
anatomical, neurological, and behavioral characteristics
that allow them to send and receive high-frequency
sounds. Among the anatomical structures involved in
echolocation are three bones in the skull: stylohyal,
malleus, and cochlea (Simmons et al., 2008, 2010;
but see Veselka et al., 2010). e cochlea, along with
the vestibule and the semicircular ducts, form the
inner ear, which is surrounded by the bony labyrinth
(osseous structure preserved after the desiccation of
the soft tissues). Variation in the bony labyrinth shape
and dimensions provide insights into the physiology,
morphology, and evolution of the dierent groups of
mammals (Ekdale, 2013).
e long-snouted bat Platalina genovensium omas,
1928, is the largest member of the phyllostomid
subfamily Lonchophyllinae (Gregorin & Ditcheld,
2005; Cirranello et al., 2016). It occurs in elevations
from near sea level up to 2566 m, from localities west
of the Andes, from northern Peru to southern Chile
and from two localities in central Peru (Griths &
Gardner, 2008; Ossa et al., 2016; Velazco et al., 2013).
P. genovensium is a highly specialized bat that feeds
primarily on nectar and pollen from ve plant families
(e.g., Cactaceae, Bromeliaceae, Solanaceae; Sahley &
Baraybar, 1996; Baraybar, 2004; Aragón & Aguirre,
2007; Zamora et al., 2013; Maguiña & Amanzo,
2016). e echolocation calls of Platalina consist of
frequency-modulated (FM), short duration (1.98 ±
0.11 ms) calls with repetitions spaced up to 90.08 ±
13.79 ms. e harmonics range from 42.2 kHz to
111.9 kHz (Ossa et al., 2016).
e enigmatic blunt-eared bat Tomopeas ravus Miller,
1900, is an insectivorous bat endemic to the coastal
desert of central and northern Peru, with an elevational
range from near sea level to near 2300 m (Velazco et
al., 2013; Zamora et al., 2014). e phylogenetic
anities of this bat have been a matter of debate
since its description by Miller (1900), where it was
placed as a member of Vespertilionidae. Shortly after
its description, it was placed under its own subfamily,
Tomopeatinae, still under the family Vespertilionidae
(Miller, 1907). Many years later, Sudman et al. (1994),
who used cytochrome-b sequences and protein
electrophoretic data, demonstrated that Tomopeas
should be allocated to the family Molossidae instead of
the family Vespertilionidae. is placement is currently
followed and has been supported by morphological
analyses (Gregorin & Cirranello, 2016). e
characteristics of the echolocation calls of Tomopeas are
unknown.
In the present report, we describe and compare the bony
labyrinths of P. genovensium and T. ravus. ese are the
rst descriptions of the bony labyrinths of members
of the subfamilies Tomopeatinae (Molossidae) and
Lonchophyllinae (Phyllostomidae).
MATERIAL AND METHODS
CT data acquisition
Two adult females were included in this study. Both
specimens are housed in the mammal collection of
the Department of Mammalogy of the American
Museum of Natural History (AMNH) in New York,
USA. Skulls of P. genovensium (AMNH 278520)
and T. ravus (AMNH 278525) were scanned using
a high-resolution GE Phoenix V|tome|x s240 micro-
CT scanner at the Microscopy and Imaging Facility
(MIF) of the AMNH. Platalina and Tomopeas skulls
were digitized at a resolution of 37.29 and 19.40 µm
(voxel size), respectively. For each bat skull, 1200 slices
(X-ray projections) with dimensions of 990 × 1000
pixels were recorded over the 180° sample rotation.
We reconstructed the volume data from those X-ray
projections and exported a stack of 2D images
corresponding to coronal sections of the volume data
in TIFF format using Phoenix datos|x 2 reconstruction
version 2.3.2 and VGStudio MAX version 3.0 (Volume
Graphics GmbH, Heidelberg, Germany).
3D reconstruction and measurements
After importing the TIFF images in MIMICS 16.0
(Materialise NV, Belgium), we segmented and created
a 3D rendering of the right bony labyrinths of
Platalina and Tomopeas. We calculated the volumes of
the cochlear and inner ear systems and the proportions
of the cochlea and basicranium in MIMICS. Our
measurements of cochlear and basicranial widths were
Running title: Bony labyrinths of Platalina and Tomopeas
89
plotted along the measurements of other bats collected
by Simmons et al. (2008). Cochlear size is known to
be correlated with echolocation behavior, where non-
echolocating bats tend to have smaller cochlea relative
to bats able to echolocate (Simmons et al., 2008).
We followed the protocol of Davies et al. (2013a)
to measure the length of the basilar membrane. We
used ISE-Meshtools 1.3 (Lebrun, 2014; http://
morphomuseum.com/meshtools) to import the
surface les of the 3D bony labyrinths (STL format)
and to place 100 equidistant semi-landmarks along
the secondary bony lamina, from the outer edge of
the round window to the apex of the cochlea (see
Davies et al., 2013a: additional le 5, gure S1A-B
for illustrations). We exported the 3D landmarks
coordinates and calculated the sum of the Euclidean
distances between landmarks in Excel to obtain the
length of the basilar membrane (see Davies et al.,
2013a for the formula). e basilar membrane length
of our two specimens were then combined with the
measurements of other bats compiled by Davies et
al. (2013a: table S2), to investigate the relationship
between linear measurements of basilar membrane
length and body mass. e body mass of the studied
specimens of Platalina and Tomopeas were measured
on the eld by P.M.V. after the bats were captured
(Velazco et al., 2013). To plot the basilar membrane
length (mm) versus the cube root of the body mass, all
the values were log10 transformed to explore the linear
relationship between the two variables.
Finally, we followed West (1985) to measure the
number of cochlear spiral turns in both bats. From
an apical view of the cochlea, a line was drawn from
the round window to the apex. e number of turns
was calculated by the number of times the line was
crossed by the path of the canal, plus the nearest one
quarter of a complete turn. Our measurements were
then combined with the bat measurements compiled
by Davies et al. (2013a: table S2). Cochlear coiling
is correlated with the presence of elongated auditory
sensory membranes. We investigated the correlation
between the number of turns of our specimens and the
relative basilar membrane length. All measurements of
Platalina and Tomopeas are presented in Table 1.
Bony labyrinth 3D models of Platalina (AMNH
278520) and Tomopeas (AMNH 278525) are available
at MorphoMuseuM.com (Velazco & Grohé, 2017).
e angles between the planes of the semicircular
canals were measured using 3D PDF models.
RESULTS
ree distinct components of the bony labyrinth can
be distinguished on the digital endocasts of Platalina
and Tomopeas (Figure 1): the cochlea, vestibule, and
the three semicircular canals. Selected measurements
of Platalina and Tomopeas bony labyrinths are provided
in Table 1. e width of the cochlea relative to the
basicranium in Platalina is intermediate among other
bats (Figures 2A, B), while, in Tomopeas, it is grouped
among the smallest (Figures 2A, C). e contribution
of the cochlear volume to the whole bony labyrinth is
similar in both taxa: 69.7% in Platalina and 68.6% in
Tomopeas (Table 1). e coiling of the cochlear canal
completes 2.25 turns in Platalina and 2 in Tomopeas
(Figure 1, Table 1). e estimated height of the spiral
of the cochlea is 2 mm in Platalina and 1.07 mm
in Tomopeas (Table 1), so that the cochlea is atter
in Tomopeas, than in Platalina (Figure 1). ere is a
large apical lacuna at the apex of the cochlear spiral
in Tomopeas, whereas an apical lacuna is absent in
Platalina (Figure 1). e basal turn becomes thicker
when approaching the vestibule in both Platalina and
Tomopeas (Figure 1). e second turn of the cochlear
spiral overlies partially the basal turn in those bats,
but the width of the second turn in Tomopeas is much
narrower than its basal turn while it is only slightly
narrower in Platalina.
Revista Biotempo: ISSN Versión Impresa: 1992-2159; ISSN Versión electrónica: 2519-5697 Velazco & Grohé
90
Figure 1. Right (mirrored) bony labyrinths of
Platalina genovensium (AMNH 278520; left) and
Tomopeas ravus (AMNH 278525; right). A, labeled
digital endocast in anterolateral view; B, labeled digital
endocast in dorsal view; C, labeled digital endocast
in posterolateral view. Abbreviations: aa, anterior
ampulla; ac, anterior semicircular canal; ant, anterior
direction; av, bony channel for vestibular aqueduct; cc,
canaliculus cochleae for cochlear aqueduct; co, cochlea;
cr, common crus; dor, dorsal direction; er, elliptical
recess of vestibule; fc, fenestra cochleae; fv, fenestra
vestibuli; la, lateral ampulla; lat, lateral direction; lc,
lateral semicircular canal; med, medial direction; pa,
posterior ampulla; pc, posterior semicircular canal;
pl, primary bony lamina; pos, posterior direction; ps,
outpocketing for perilymphatic sac; sl, secondary bony
lamina; sr, spherical recess of vestibule; ventr, ventral
direction.
Table 1. Body mass and dimension of the skull and
bony labyrinth of Platalina and Tomopeas.
Platalina Tomopeas
BLV (mm3) 5.37 2.71
CV (mm3) 3.74 1.86
CV % 69.65 68.63
CH (mm) 2.00 1.07
WBT (mm) 2.21 1.90
SICS (index) 0.90 0.56
CST (Nº) 2.25 2.00
WB (mm) 11.02 6.91
BML (mm) 12.61 9.40
BM (g) 14.50 3.00
Abbreviations: BLV, bony labyrinth volume; BM, body
mass; BML, basilar membrane length; CH, height of
spiral of the cochlea; CV, cochlear volume; CV %,
cochlear volume percentage of bony labyrinth; CST,
number of cochlear spiral turns; SICS, shape index of
cochlear spiral (CH/WBT); WB, width basicranium;
WBT, width of the basal turn of the cochlea.
A secondary bony lamina is present in both species
(Figure 1; Ekdale, 2013). e secondary bony lamina
is visible on the outer edge of the rst turn in Tomopeas
and on the two rst turns in Platalina (sl in Figure
1). In Platalina, the aspect ratio of the cochlear spiral
(height of the spiral divided by width of the basal turn)
is the greatest in bats and the second largest among
placental mammals, after the rodent Cavia (Table 1;
Ekdale, 2013: table 2). e aspect ratio for Tomopeas
is average among bats (Table 1; Ekdale, 2013: table
2). A canaliculus cochlea is observed in both Platalina
and Tomopeas posterodorsally to the wide fenestra
cochleae (cc in Figure 1). e canaliculus in Tomopeas
is located and oriented similarly to the one in Tadarida
(cc in Figure 1; Ekdale, 2013: gure 48C). e plane
of the basal turn of the cochlea of Platalina forms an
angle with the plane of the lateral semicircular canal
(lc in Figure 1) that is similar to the one exhibited
by other phyllostomids (e.g., Trachops; Davies et al.,
Running title: Bony labyrinths of Platalina and Tomopeas
91
2013a: gure 2). is angle in Tomopeas is similar to
the angle measured in the molossid Tadarida (Figure
1; Ekdale, 2013: gure 48). e fenestra vestibuli is
elliptical in both Platalina and Tomopeas (fv in Figure
1). e elliptical and spherical recesses are separated
in Platalina and Tomopeas (er and sr in Figure 1).
e vestibule of both Platalina and Tomopeas exhibit
an anterior excavation for the anterior and lateral
ampullae and a posterior excavation for the posterior
ampulla and common crus (aa, la, pa, and cr in Figure
1). e ampullae in both Platalina and Tomopeas
are well dierentiated (aa, la, and pa in Figure 1). In
Platalina, the spherical recess and the elliptical recess
are separated by a shallow furrow, whereas in Tomopeas
they are separated by an almost imperceptible furrow
(er and sr in Figure 1A).
Figure 2. Relationship between the cochlear width
(mm) vs. basicranial width (mm) in A, echolocating
(y = 0.16393x + 0.82697, r2 = 0.3402) versus non-
echolocating bats (y = 0.091462x + 1.0756, r2 = 0.8193
[Pteropodidae]); B, Platalina genovensium and other
species of the family Phyllostomidae (y = 0.13661x
+ 0.69954, r2 = 0.844); and C, Tomopeas ravus and
other species of the family Molossidae (y = 0.17273x +
0.73879, r2 = 0.891).
e common crura of Platalina and Tomopeas are
shorter and wider compared to other bats (cr in Figure
1; tall and slender in Nycteris, Rhinolophus, Tadarida:
Ekdale, 2013). e bony channel for the vestibular
aqueduct in Tomopeas leaves the inner ear medial and
anterior to the vestibular aperture of the common
crus similar to the condition observed in Tadarida
(av in Figure 1; Ekdale, 2013: gure 48B, C). e
channel gently curves and opens on the surface of the
petrosal near the dorsal end of the common crus (av
in Figure 1C). e bony channel for the vestibular
aqueduct in Platalina could not be determined because
the resolution of the volume was not appropriate to
reconstruct the structure.
e posterior limb of the lateral semicircular canal
opens directly into the vestibule between the posterior
ampulla and the base of the common crus in both
Platalina and Tomopeas (lc and pa in Figure 1). It is
Revista Biotempo: ISSN Versión Impresa: 1992-2159; ISSN Versión electrónica: 2519-5697 Velazco & Grohé
92
located more dorsally than the ventral limb of the
posterior semicircular canal, the dorsoventral separation
between the lateral and posterior semicircular canals
being greater in Tomopeas than in Platalina (lc and
pc in Figure 1). e angle between the planes of the
posterior and anterior semicircular canals is 95º in
both Platalina and Tomopeas (Figure 1B). e angle
between the anterior and lateral semicircular canals is
perpendicular (90º) in Platalina, where it is smaller
(75º) in Tomopeas (Figure 1A). e angle between the
posterior and lateral semicircular canals is perpendicular
(90º) in Platalina, where it is larger (107º) in Tomopeas
(Figure 1C). e semicircular canals are slightly
narrower in Platalina than in Tomopeas (Figure 1).
e semicircular canals of Platalina are mostly planar,
whereas in Tomopeas the anterior and lateral canals
deviate substantially from their planes (out-of-plane
curvature) and the posterior canal is mostly planar
(Figure 1). e anterior semicircular canal is more
extended dorsally than the posterior semicircular
canal in both species, but the anterior and posterior
semicircular canals are more compressed dorsoventrally
in Tomopeas than in Platalina (ac and pc in Figure 1).
e lateral semicircular canal has an oval shape in dorsal
view that is similar in both species (lc in Figure 1). e
anterior semicircular canal extends more anteriorly
than the lateral semicircular canal in Platalina, while
the anterior and lateral semicircular canals extend at
the same level anteriorly in Tomopeas (ac and lc in
Figure 1).
In comparison with other extant bats, the basicranial
region of Platalina indicates that it has a relatively
small cochlea that falls into the zone of overlap of
echolocating and non-echolocating bats (Figure 2A),
while it is known that Platalina is an echolocating bat
(Malo de Molina et al., 2011). e cochlear width of
Platalina (compared to that of the basicranium) is of
medium size when compared with other species of
phyllostomids, but it is one the largest when compared
to other phyllostomid bats with similar feeding behavior
(Glossophaginae and Lonchophyllinae; Figure 2B). e
lonchophylline sample size is small (n = 3) but it shows
that the other two species (Lionycteris spurrelli omas,
1913 and Hsunycteris thomasi (Allen, 1904)) have the
smallest relative cochlear widths in the family, clearly
distinguishing them from Platalina (Figure 2B).
e basicranial region of Tomopeas in turn indicates
that it has a small cochlear width and falls on the
regression line of echolocating bats (Figure 2A). When
compared with other molossids, Tomopeas has one the
smallest cochlear widths in the family (Figure 2C).
e plot of the log basilar membrane length versus the
log body mass0.33 showed that Platalina and Tomopeas
grouped within the dierent families of echolocating
bats (Figure 3A). Platalina falls in the middle of the
variation for its family (Phyllostomidae), whereas
Tomopeas falls on the lower end for both variables
when compared to its family (Molossidae) and all the
bats (Figure 3A).
Figure 3. Log basilar membrane length (mm) vs. log of
the cube root of body mass (g) plotted across 16 families
of bats. A, overall dispersal of the dierent families (y
= 0.1988x + 1.0324, r2 = 0.05849): Craseonycteridae
(lled black triangle), Emballonuridae (lled blue
diamond), Hipposideridae (lled gray diamond),
Megadermatidae (lled green inverted triangle),
Miniopteridae (red diamond), Molossidae (lled black
circle), Mormoopidae (empty black circle), Natalidae
(asterisk), Noctilionidae (plus), Nycteridae (empty
Running title: Bony labyrinths of Platalina and Tomopeas
93
black square), Phyllostomidae (lled black square),
Pteropodidae (x), Rhinolophidae (lled black inverted
triangle), Rhinopomatidae (empty black inverted
triangle), yropteridae (lled black diamond),
Vespertilionidae (empty black diamond), Platalina
genovensium (lled blue square), Tomopeas ravus (lled
blue circle); and B, with circles sized according to the
number of cochlear spiral turns.
Both, Platalina and Tomopeas, present the shortest
number of cochlear spiral turns in their respective
families (Figure 3B). Platalina has 2.25 cochlear
spiral turns while the other 7 phyllostomid species in
the sample range from 2.5 to 3.25 turns (Figure 3B).
With 2 cochlear spiral turns, Tomopeas has the smallest
number of turns among the echolocating bats, along
with Cardioderma cor (Peters, 1872), Nycteris thebaica
É. Georoy St.-Hilaire, 1818, and Plecotus auritus
(Linnaeus, 1758). e only other bats with a shorter
number of cochlear spiral turns are members of the
non-echolocating family Pteropodidae with 1.75
cochlear spiral turns (Figure 3B). e other molossids
presented in the sample (n = 5) have a cochlear spiral
turns range from 2.5 to 3.0 (Figure 3B).
DISCUSSION
e morphological description of the bony labyrinths
of Platalina and Tomopeas presented here represents
the rst study of inner ear bats of the subfamilies
Lonchophyllinae and Tomopeatinae. e cochlear
attributes of both species demonstrated unique
characteristics. Platalina presents the greatest aspect
ratio of the cochlear spiral in bats, and among
placental mammals it is second only to rodents of the
genus Cavia. Also, it has a medium-size cochlear width
when compared with other phyllostomids, but it is
one the largest when compared to other phyllostomid
bats with similar feeding behavior (Glossophaginae
and Lonchophyllinae). Additionally, both Platalina
and Tomopeas have the shortest number of cochlear
spiral turns in their respective families and among
echolocating bats. Tomopeas is also characterized by
having one the smallest cochlear width relative to that
of the basicranial region among the Molossidae. From
the four bats described by Ekdale (2013), Tomopeas is
morphologically closer to Tadarida, both are members
of the same family.
e study of the dierent aspects of the bony labyrinth
in bats is mainly based on histological cross sections,
x-ray images, and fossilized petrosals (e.g., Pye, 1966a,
b, 1967, 1970; Hinchclie & Pye, 1968; Habersetzer
& Storch 1992; Simmons et al., 2008; Odendaal &
Jacobs, 2011; Carter & Adams, 2015; Czaplewski,
2017). However, the recent availability to researchers
of new technology like Computed Tomography
(CT) to study the internal morphology of biological
structures without damaging the specimens allows
the reconstruction of structures that were impossible
to observe on their entirety before. One of these
structures is the bony labyrinth, but most studies
using 3D models of inner ears in bats are focused on
using measurements from these models to explore the
evolution of ight, echolocation, etc. (e.g., Davies
et al., 2013a, b; Pfa et al., 2015). Only one study
provides detailed descriptions of the bony labyrinth
morphology of bats (non-echolocating Pteropus lylei
Andersen, 1908 and echolocating Nycteris grandis
Peters, 1865, Rhinolophus ferrumequinum (Schreber,
1774), and Tadarida brasiliensis (I. Georoy St.-
Hilaire, 1824)) using 3D models (Ekdale, 2013).
ere is a clear need for more comparative data on the
bony labyrinth morphology of bats and more eort
should be devoted to the use of the 3D data available
from repositories of digital data (e.g., DigiMorph
http://www.digimorph.org/; MorphoSource http://
morphosource.org/; MorphoMuseuM.com; www.
phenome10k.org etc.).
ACKNOWLEDGEMENTS
We would like to thank Morgan Hill and Henry
Towbin of the Microscopy and Imaging Facility at
AMNH for assistance with instrumentation; Carlos
Tello for providing bibliography; Kerry Kline, Ricardo
Moratelli, and one anonymous reviewer for comments
on an early version of the manuscript; Gregg F.
Gunnell, Jörg Habersetzer, and Nancy B. Simmons for
sharing the data used in gure 2.
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94
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Received July 7, 2017.
Accepted August 16, 2017.
