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Revista
Mexicana
de
Biodiversidad
www.ib.unam.mx/revista/
Revista
Mexicana
de
Biodiversidad
87
(2016)
1407–1411
Research
note
New
records
and
range
extension
of
Promops
centralis
(Chiroptera:
Molossidae)
Nuevo
registro
y
ampliación
de
la
distribución
de
Promops
centralis
(Chiroptera:
Molossidae)
Tania
P.
González-Terrazasa,∗,
Luis
R.
Víqueza,b,
Ana
Ibarra-Macíasb,
Adrián
Tonatiuh
Ruízc,
Leonora
Torres-Knoopb,
Kirsten
Junga,
Marco
Tschapkaa,d,
Rodrigo
A.
Medellínb
aInstitute
of
Evolutionary
Ecology
and
Conservation
Genomics,
Albert-Einstein
Allee
11,
D-89069
Ulm,
Germany
bInstituto
de
Ecología,
Universidad
Nacional
Autónoma
de
México,
Tercer
Circuito
s/n,
Ciudad
Universitaria,
04318
Ciudad
de
México,
Mexico
cInstitute
of
Neural
Information
Processing,
University
of
Ulm,
Albert-Einstein
Allee
11,
D-89069
Ulm,
Germany
dSmithsonian
Tropical
Research
Institute,
PO
Box
0843-03092,
Balboa,
Panama
Received
4
May
2016;
accepted
16
August
2016
Available
online
15
November
2016
Abstract
We
captured
Promops
centralis
and
recorded
its
echolocation
calls
in
Bahía
de
Kino,
Sonora,
which
represents
the
first
record
of
this
species
for
the
state
of
Sonora,
Mexico.
Our
new
record
extends
the
distribution
of
P.
centralis
at
least
1,300
km
northwest
from
the
northernmost
known
locality,
Cuautla,
Jalisco.
Until
now,
there
was
no
evidence
of
the
occurrence
of
P.
centralis
in
the
deserts
of
northern
Mexico.
These
new
records
are
ecologically
significant
as
they
show
that
this
species
also
occurs
in
extreme
dry
areas
such
as
the
Sonoran
Desert.
Our
findings
suggest
that
P.
centralis
may
be
more
widely
distributed
than
previously
thought.
©
2016
Universidad
Nacional
Autónoma
de
México,
Instituto
de
Biología.
This
is
an
open
access
article
under
the
CC
BY-NC-ND
license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
Keywords:
Aerial
insectivores;
Bahía
de
Kino;
Echolocation;
Molossids;
Northern
Mexico
Resumen
Se
capturó
al
murciélago
Promops
centralis
y
se
grabaron
sus
llamadas
de
ecolocalización
en
la
localidad
de
Bahía
de
Kino,
Sonora;
este
es
el
primer
registro
de
la
especie
para
el
estado
de
Sonora,
México.
Este
nuevo
registro
amplía
la
distribución
de
P.
centralis
por
lo
menos
1,300
km
al
noroeste
de
la
localidad
más
norte˜
na
previamente
conocida,
Cuautla,
Jalisco.
Hasta
ahora
no
existía
evidencia
de
la
presencia
de
P.
centralis
en
los
desiertos
del
norte
de
México.
Este
nuevo
registro
es
de
importancia
ecológica
ya
que
por
primera
vez
se
muestra
que
esta
especie
puede
subsistir
en
áreas
extremadamente
secas
como
el
Desierto
de
Sonora.
Nuestro
hallazgo
sugiere
que
P.
centralis
puede
estar
más
ampliamente
distribuido
de
lo
que
se
pensaba
con
anterioridad.
©
2016
Universidad
Nacional
Autónoma
de
México,
Instituto
de
Biología.
Este
es
un
artículo
Open
Access
bajo
la
licencia
CC
BY-NC-ND
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
Palabras
clave:
Insectívoros
aéreos;
Bahía
de
Kino;
Ecolocalización;
Molósidos;
Norte
de
México
The
Molossidae
is
a
diverse
group
of
bats
(fourth
largest
bat
family,
ca.
100
species),
with
most
of
the
species
occurring
in
tropical
and
subtropical
regions
(Simmons,
2005).
Molossids
are
∗Corresponding
author.
E-mail
address:
tania.gonzalez@uni-ulm.de
(T.P.
González-Terrazas).
Peer
Review
under
the
responsibility
of
Universidad
Nacional
Autónoma
de
México.
typical
open
space
bats
that
hunt
high
up
in
the
air
and
roam
over
large
distances.
They
are
rarely
captured
in
mist
nets
so
there
is
a
general
lack
of
information
on
many
species.
The
genus
Pro-
mops
is
restricted
to
the
New
World
and
currently
encompasses
3
species
(Gregorin
&
Chiquito,
2010):
Promops
centralis,
Pro-
mops
nasutus
and
Promops
davisoni.
P.
centralis
is
the
most
widely
distributed,
from
Mexico
(Jalisco
to
Yucatán)
through-
out
South
America,
from
Colombia,
Ecuador,
and
Peru,
to
the
http://dx.doi.org/10.1016/j.rmb.2016.10.008
1870-3453/©
2016
Universidad
Nacional
Autónoma
de
México,
Instituto
de
Biología.
This
is
an
open
access
article
under
the
CC
BY-NC-ND
license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
1408
T.P.
González-Terrazas
et
al.
/
Revista
Mexicana
de
Biodiversidad
87
(2016)
1407–1411
Figure
1.
(A)
Artificial
pond
where
we
captured
Promops
centralis.
(B)
The
pond
(red
dot)
is
mainly
surrounded
by
crops.
This
area
is
very
dry
and
these
water
bodies
are
the
only
source
of
fresh
water
nearby.
Amazon
basin
in
Brazil,
western
Bolivia,
Paraguay,
northeast-
ern
Argentina
and
the
northern
coast
of
Brazil,
Guianas,
and
Venezuela
(Eger,
2008;
Pacheco,
Cadenillas,
Salas,
Tello,
&
Zeballos,
2009;
Simmons,
2005).
Despite
its
large
distributional
range,
little
is
known
about
the
ecology
of
this
species.
Like
most
molossids,
P.
centralis
possesses
long
and
narrow-tipped
wings
(high
wing
loading
and
aspect
ratio)
which
are
well
suited
to
fly
at
high
speed
but
are
less
suited
for
high
maneuverability
(Freeman,
1981;
Norberg
&
Rayner,
1987).
In
accordance,
these
bats
are
known
to
forage
in
open
areas
above
the
forest
canopy
or
in
open
landscapes
(Jung,
Molinari,
&
Kalko,
2014;
Kalko,
Estrada-Villegas,
Schmidt,
Wegmann,
&
Meyer,
2008).
P.
cen-
tralis
occurs
in
a
very
diverse
range
of
habitats
such
as
rain
forest,
tropical
dry
forest
and
pine-oak
(Arita,
1997;
Sánchez-Cordero,
Bonilla,
&
Cisneros,
1993;
Simmons
&
Voss,
1998),
pastures
(MacSwiney,
Bolivar,
Clarke,
&
Racey,
2006),
and
has
even
been
reported
in
urban
areas
(Jung
&
Kalko,
2011;
Regueras
&
Maga˜
na-Cota,
2008).
The
echolocation
calls
of
P.
centralis
are
very
conspicuous
as
they
are
characterized
by
upward
fre-
quency
modulation
similar
to
the
genus
Molossops
(Jung
et
al.,
2014).
Within
sequences
up-
and
downward
modulated
calls
can
alternate
irregularly.
Species-specific
variation
of
echolocation
calls
has
been
previously
described
in
detail
(while
assigning
it
to
Cynomops
mexicanus
by
MacSwiney
et
al.,
2006).
In
Mexico,
this
species
has
been
recorded
from
Jalisco
south-
ward
throughout
the
west
coast
to
the
Yucatán
Peninsula.
We
report
here
the
capture
of
this
species
for
the
first
time
in
the
extreme
north
of
Mexico,
in
the
state
of
Sonora,
where
there
was
no
record
of
this
species
in
the
northern
desert
habitats
of
Mexico.
Field
work
was
conducted
on
the
nights
of
the
8th
and
9th
of
April
2014
in
Bahía
de
Kino,
Sonora.
Our
study
site
was
one
of
the
few
artificial
water
reservoirs
in
this
area
(28◦501.09 N,
111◦3557.20 W).
The
pond
had
a
size
of
ca.
90
m
×
90
m
with
some
palm
trees
close
to
the
edge
of
the
water
and
mainly
surrounded
by
crops
(Fig.
1).
However,
the
pond
is
relatively
close
to
the
natural
vegetation
typical
for
the
Sonoran
Desert,
dominated
by
small
shrubs
and
columnar
cacti
(Mexican
giant
cardon:
Pachycereus
pringlei,
saguaro:
Carnegiea
gigantea,
organ
pipe
cactus:
Stenocereus
thurberi)
(Van
Devender,
2002).
We
used
mist
nets
for
capturing
bats
and
acoustic
monitor-
ing
to
record
the
echolocation
calls
of
all
the
bats
flying
near
the
study
site.
Captured
bats
were
identified
using
a
bat
iden-
tification
guide
(Medellín,
Arita,
&
Sánchez-Herrera,
2008).
Acoustic
recordings
were
obtained
using
a
real
time
acoustic
ultrasound
recording
device
(batcorder,
ecoObs
GmbH,
Nürn-
berg,
Germany)
located
at
1.5
m
above
the
ground.
Both,
mist
netting
and
use
of
the
acoustic
recording
device
started
at
sun-
set
and
ended
at
midnight.
We
followed
the
guidelines
for
the
use
of
wild
mammal
species
in
research
as
recommended
by
the
American
Society
of
Mammalogists
(Sikes
&
The
Animal
Care
and
Use
Committee
of
the
American
Society
of
Mammalogists,
2016).
All
captures
were
carried
out
under
permission
of
the
Secretaría
de
Medio
Ambiente
y
Recursos
Naturales,
Mexico
(FAUT-0001).
In
total
we
captured
12
individuals
of
2
bat
families
(Ves-
pertilionidae
and
Molossidae).
We
identified
2
individuals
of
P.
centralis,
1
in
each
capture
night,
both
individuals
presented
the
characteristic
morphological
features
of
P.
centralis:
upper
lip
without
grooves
(Fig.
2A),
forearm
less
than
56
mm,
dark
pelage
(darker
in
the
dorsal
part
than
in
the
ventral
part)
and
the
incisors
protruding
substantially
from
the
front
of
the
canines
(Fig.
2B).
The
first
captured
individual
was
an
adult
male,
repro-
ductively
inactive,
with
a
forearm
of
54.8
mm,
the
time
of
capture
was
around
22:00
h.
The
collected
individual
was
deposited
in
the
National
Collection
of
Mammals,
UNAM,
Mexico
(catalog
number
47626).
The
second
individual,
captured
around
20:00
h
and
released
after
taking
measurements
and
photographs,
was
an
adult
male,
reproductively
inactive
with
a
forearm
of
55.4
mm.
We
analyzed
13
echolocation
sequences
(n
=
206
upward
modulated
echolocation
calls)
of
P.
centralis.
Corroborating
with
previous
publications,
this
species
has
very
particular
echolocation
calls
(Jung
et
al.,
2014),
which
are
easily
identi-
fied
using
acoustic
recordings
for
species
inventory.
Contrary
to
most
molossids,
their
search
calls
are
upward
modulated
quasi-
constant
frequency
calls
with
a
variable
upward
modulated
T.P.
González-Terrazas
et
al.
/
Revista
Mexicana
de
Biodiversidad
87
(2016)
1407–1411
1409
Figure
2.
(A)
Side
view
of
one
of
the
individuals
of
Promops
centralis.
The
upper
lip
does
not
present
vertical
groves.
(B)
The
most
remarkable
characteristic
of
P.
centralis
are
the
incisors
that
protrude
substantially
from
the
front
of
the
canines
(red
arrow).
FM-component
at
the
beginning
(i.e.,
the
start
frequency
is
lower
than
the
end
frequency).
Call
sequences
are
character-
ized
by
interspersed
downward-modulated
signals,
especially
before
prey-capture
attempts.
Upward
and
downward
modu-
lated
signals
do
not
overlap
in
frequency
range.
The
upward
modulated
search
calls
of
P.
centralis
are
long,
low
frequency
quasi-constant
calls
with
the
highest
energy
in
the
first
harmonic
(Fig.
3;
Table
1).
Our
new
records
of
P.
centralis,
besides
being
the
first
for
the
state
of
Sonora,
extend
the
distributional
range
of
this
species
by
1300
km
northwesterly.
So
far,
the
northernmost
records
of
P.
centralis
were
from
Cuautla,
Jalisco
(Watkins,
Jones,
&
Genoways,
1972)
and
one
recent
record
from
the
city
of
Guana-
juato
(Regueras
&
Maga˜
na-Cota,
2008).
Additionally,
this
is
the
Table
1
Call
parameters
of
the
upward
modulated
calls
(mean
±
SD)
of
Promops
cen-
tralis.
We
analyzed
a
total
of
206
calls
from
13
different
sequences.
Search
calls
(n
=
206)
Call
duration
(ms) 20.6
±
3.90
Peak
frequency
(kHz) 24.7
±
0.57
Start
frequency
(kHz)
23.0
±
0.72
End
frequency
(kHz)
25.6
±
0.47
Bandwidth
(kHz)
2.7
±
0.56
first
record
of
P.
centralis
for
the
Sonoran
Desert
(xeric
shrub-
lands).
This
type
of
habitat
covers
large
part
of
northwestern
Mexico
and
southwest
of
the
United
States,
with
an
approxi-
mate
area
of
260,000
km2(Phillips
&
Comus,
2000).
The
xeric
shrublands
of
the
northern
Mexican
deserts
covered
originally
approximately
40%
of
the
Mexican
territory
(Rzedowski,
1978;
Fig.
4B),
nowadays
they
cover
only
ca.
30%
of
the
country
(Inegi,
2005).
Our
finding
of
the
occurrence
of
P.
centralis
in
this
type
of
habitat
suggests
that
the
potential
distribution
of
this
species
(Fig.
4A)
may
cover
a
much
larger
area
than
previously
thought.
In
addition
to
the
2
captures,
we
also
recorded
many
echolo-
cation
passes
of
P.
centralis
during
the
2
nights
of
acoustic
monitoring.
The
measurements
of
the
call
parameters
in
this
study
are
similar
to
those
previously
reported
for
P.
centralis
(Jung
et
al.,
2014;
MacSwiney
et
al.,
2006).
In
contrast
to
most
molossids,
which
demonstrate
a
high
variability
in
echoloca-
tion
call
frequencies,
hampering
acoustic
species
identification
(Gillam
et
al.,
2009;
Kalko
et
al.,
2008)
echolocation
calls
of
P.
centralis,
are
very
characteristic
and
thus
a
reliable
indica-
tor
for
the
occurrence
of
this
species.
Thus
acoustic
monitoring
can
be
an
important
tool
to
enhance
our
knowledge
about
the
ecology
of
this
species.
In
dry
habitats,
where
water
is
limited,
the
few
available
water
bodies
are
hot
spots
of
activity
of
the
regional
fauna.
We
recorded
echolocation
calls
and
captured
P.
centralis
while
the
animals
were
approaching
the
pond
for
drinking
or
capturing
insects
gathered
near
the
water.
With
extensive
monitoring
efforts,
com-
bining
acoustic
and
mist
netting
techniques
at
similar
locations
it
may
be
possible
to
record
this
species
at
additional
localities
in
the
northern
deserts
of
Mexico
where
this
species
has
not
yet
been
found.
Our
results
indicate
that,
more
than
ever
before,
standardized,
careful
acoustic
surveillance
is
rapidly
becoming
an
essential
tool
for
biodiversity
monitoring.
mV
Freq. (kHz)
0
–200
0.2 0.4 0.6
20 ms
Time (s)
30
200
Figure
3.
Three
upward
modulated
echolocation
calls
of
a
search
sequence
of
Promops
centralis.
Sonogram
was
created
using
a
fast
Fourier
transform
(FFT)
with
512
point,
a
Hamming
window
and
an
overlap
of
75%.
1410
T.P.
González-Terrazas
et
al.
/
Revista
Mexicana
de
Biodiversidad
87
(2016)
1407–1411
120ºW 110ºW 100ºW 90ºW
120ºW
110ºW
100ºW
90ºW
30ºN25ºN20ºN15ºN30ºN25ºN20ºN15ºN
30ºN25ºN20ºN15ºN30ºN25ºN20ºN15ºN
90ºW100ºW110ºW
Model consensus
A
B
Pine-oak forest
Thorn forest
Cloud forest
Tropical deciduous
Tropical evergreen forest
Tropical semi-deciduous forest
Xeric scrub
Grasslands
Acuatic and underwater vegetation
1-2
0
250
500 Km
0
250
500 Km
3-4
5-7
8-10
90ºW100ºW110ºW
Figure
4.
(A)
Potential
distribution
of
Promops
centralis
in
Mexico
(modified
from
Ceballos,
Blanco,
González
y
Martínez,
2006).
Light
green
shading
indicates
the
current
known
distribution
of
this
species
in
Mexico
(modified
from
Medellín
et
al.,
2008).
The
red
star
represents
the
location
of
the
new
records
reported
in
this
study.
(B)
Potential
vegetation
of
Mexico
(modified
from
Rzedowski,
1990).
These
captures
were
in
a
type
of
habitat
(xeric
shrublands)
where
P.
centralis
was
considered
to
be
absent.
This
habitat
type
is
extensively
distributed
in
the
north
of
Mexico,
therefore,
this
species
may
be
more
widely
distributed
than
previously
thought.
We
want
to
thank
all
the
people
who
contributed
to
the
field
work.
Scientific
collecting
permits
were
provided
to
R.A.M.
by
the
Secretaría
del
Medio
Ambiente
y
Recursos
Naturales
(FAUT-0001).
This
study
was
supported
by
a
joint
DFG-Conacyt
Bilateral
Cooperation
program
under
the
num-
ber
190901
[to
R.A.M]
and
TS
81/8-1
and
8-2
[to
M.T.
and
K.J.]
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