doi: http://dx.doi.org/10.15446/caldasia.v36n2.47494
http://www.icn.unal.edu.co/
CaldasiaMantilla-Meluk
36(2):373-388. et
2014
al.
GEOGRAPHIC AND ECOLOGICAL AMPLITUDE IN
THE NECTARIVOROUS BAT ANOURA FISTULATA
(PYHLLOSTOMIDAE: GLOSSOPHAGINAE)
Amplitud geográfica y ecológica en el murciélago nectarívoro
Anoura fistulata (Pyhllostomidae: Glossophaginae)
HUGO MANTILLA-MELUk
Programa de Biología, Universidad del Quindío. Carrera 15 Calle 12 Norte, Armenia,
Quindío, Colombia. hugo.mantilla-meluk@gmail.com
LIzETTE SILES
Texas Tech University, Department of Biological Sciences and The Museum of Texas Tech
University Lubbock TX, 79409-1313, U.S.A.
LUIS F. AGUIRRE
Centro de Biodiversidad y Genética, Universidad Mayor de San Simón, casilla 538,
Cochabamba, Bolivia.
ABSTRACT
The wide range of feeding habits among phyllostomid bats has resulted in the
selection of unique and contrasting morphological attributes. It has been suggested
that nectarivorous bat species co-evolve with the plants they use as primary source of
food, and changes in morphology and behavior in the bat, are in some way directed
by changes in morphology and phenological cycles of the plants. The nectarivorous
bat Anoura fistulata (Pyhllostomidae: Glossophaginae) has the longest tongue in
proportion to body size among mammals; feature that apparently allows the species
to take nectar from flowers with long corollas, some of them typical of highland
ecosystems. In spite of this unique morphological adaptation, little is known on the
ecological requirements of the species. Herein, Geographic Information System-based
analyses and niche modeling techniques were applied to investigate the geographic
and ecological niche breath of A. fistulata. We also introduce the first Bolivian record
of the species collected at Hernando Siles, Department of Chuquisaca (20°10’0.0’’
S, 64°15’0.00’’ W, at 1,524 m), which represents a remarkable extension in the
distribution of the species of more than 7°. Our analyses revealed that A. fistulata
occurs in contrasting ecosystems, from Andean montane and pre-montane moist forest
in Western Ecuador and Central Colombia, up to arid and semiarid environments in
southern Colombia and Bolivia. Anoura fistulata occurs across a wide elevational
range between 1,175 and 2,510 m, which is well represented along the geologic unit
of the Batholith of Ecuador. A constriction of this elevational belt along the Peruvian
Punas and Yungas was suggested as a natural barrier for the establishment of A.
fistulata. The Peruvian Punas and Yungas isolate A. fistulata of Bolivia from records
in the northern range of the distribution of the species.
Key words. Anoura fistulata, Bolivia, distribution extension, morphology, new
record.
373
Geographic range of Anoura fistulata
RESUMEN
El amplio espectro de hábitos alimentarios entre los murciélagos filostómidos ha
resultado en la selección de atributos morfológicos únicos y contrastantes. Se ha
sugerido que las especies de murciélagos nectarívoros han co-evolucionado con las
plantas que usan como fuente principal de alimento y que cambios en la morfología y
el comportamiento de los murciélagos son, de alguna manera, dirigidos por cambios en
la morfología y los ciclos fenológicos de las plantas. El murciélago nectarívoro Anoura
fistulata (Pyhllostomidae: Glossophaginae) posee la lengua más larga en comparación
a su tamaño corporal entre los mamíferos, característica que aparentemente le permite
utilizar flores de corolas largas, algunas de ellas típicas de ecosistemas de alta montaña.
A pesar de esta adaptación morfológica única, poco se sabe de los limitantes ecológicos
de la especie. En este estudio se aplicaron Sistemas de Información Geográfica en
combinación con técnicas de modelamiento de nicho para investigar la amplitud de
nicho de A. fistulata a escala geográfica y ecológica. También presentamos el primer
registro de la especie para Bolivia, recolectado en Hernando Siles, Departamento
de Chuquisaca (20°10’0.00’’ S, 64°15’0.00’’ W, at 1,524 m), el cual representa una
extensión considerable de la distribución de la especie en 7° de latitud. Nuestros
análisis revelan que A. fistulata existe en ecosistemas contrastantes que incluyen
desde bosques andinos premontanos y montanos en el occidente de Ecuador y centro
de Colombia, hasta ambientes áridos y semiáridos en el sur de Colombia y Bolivia.
Anoura fistulata existe en un amplio intervalo de elevaciones entre 1,175 y 2,510
m, intervalo bien representado en la unidad geológica del batolito de Ecuador. Una
constricción de este cinturón de elevaciones a lo largo de las Punas peruanas y las
Yungas se identifica como una barrera natural para el establecimiento de A. fistulata.
Las Punas y las Yungas peruanas aíslan A. fistulata de Bolivia de registros en la parte
norte del área de distribución de la especie.
Palabras clave. Anoura fistulata, Bolivia, extensión de distribución, morfología,
nuevo registro.
INTRODUCTION
The charismatic nectar feeding bat Anoura
fistula Muchhala et al. (2005) (Pyhllostomidae:
Glossophaginae) is characterized by some of
the most extreme morphological adaptations
for nectar consumption, including the longest
tongue in proportion to body size among
mammals. Such a remarkable adaptation has
been interpreted as a specialization for the
consumption of resources difficult to exploit
by other sympatric nectar feeders (Muchhala,
2006). Dietary studies conducted by Muchhala
(2006) suggested that the overextended tongue
of A. fistulata is an evolutionary adaptation
that enables this species to take nectar from
flowers characterized by extremely elongated
374
corollas (9–12 cm) such as Centropogon
nigricans (Campanulaceae), which apparently
is not visited by the sympatric congeneric
species Anoura caudifer (Geoffroy) and A.
geoffroyi Gray. The implied co-evolutionary
relationship between C. nigricans and A.
fistula suggests that morphological variation
in this nectar-feeding species is the result of
a process of adaptive specialization (sensu
Gould and Vbra, 1982). It has been accepted
that highly specialized feeding strategies are
usually accompanied by a reduction of species
niche breadth (Page and Swofford, 1984).
Anoura fistulata is only known from less than
20 localities in northern South America, the
majority of them within adjacent bioregions
Mantilla-Meluk et al.
in Colombia, Ecuador, and Peru (Muchhala,
2005; Muchhala et al. 2005; Lee et al., 2008,
2010; Mantilla-Meluk and Baker, 2008;
Mantilla-Meluk et al., 2009; Pacheco et
al., 2009). However, new records extended
the distribution of the species into the
southern portion of Peru in the region of Puno
(Chacaneque, Ollachea district, Carabaya
province), close to the border with Bolivia
(Garate-Bernardo and Carrasco-Rueda,
2011).
During an appraisal of museum specimens
of Anoura deposited at the Field Museum
of Natural History (FMNH), we found a
female specimen of A. fistulata (FMNH
106088) collected in the Bolivian Department
of Chuquisaca, which represents the first
documented record of this species for
the country. We present a comparative
morphometric analysis of this specimen
to evaluate and describe its morphometric
variation and phenetic similarities with other
species of the genus.
In this work we investigate the environmental
variability associated with A. fistulata recorded
localities. We proposed two competing
hypotheses regarding niche breath of A.
fistulata: 1) if extreme morphological
adaptations in A. fistulata increase the
opportunity of the species to exploit a wider
variety of plant resources, then we expect
a high environmental variability across
its distributional range, and 2) if extreme
morphological adaptations in A. fistulata
are an evolutionary response to the use of
specific plant resources, then we expect a
greater environmental homogeneity across its
distributional range. To test these hypotheses,
we evaluate the niche breadth of A. fistulata
across its distributional range using niche
modeling and Geographic Information
Systems (GIS)-based analyses.
MATERIALS AND METHODS
Morphological and morphometric
characterization.- Skull morphology of
specimen FMNH 106088 was contrasted
against 374 adult specimens including the
following taxa: 46 A. aequatoris (Bolivia
2; Colombia 33, Ecuador 10, and Peru 1);
2 A. cadenai (Colombia); 31 A. caudifer
(Bolivia 1; Brazil 29; Colombia 1), 29 A.
cultrata Handley (Colombia 18; Costa Rica
10; Peru 1); 4 A. fistulata (Colombia); 34 A.
geoffroyi (Brazil 3, Trinidad 31), 5 A. latidens
Handley (Venezuela); 11 A. luismanueli
Molinari (Colombia 9; Venezuela 2); and
212 A. peruana (Bolivia 10, Colombia 172,
Ecuador 6, Peru 24) deposited in the following
institutions: Instituto de Ciencias Naturales of
the Universidad Nacional de Colombia (ICN);
Field Museum of Natural History (FMNH);
Museo de Historia Natural de la Universidad
de Caldas (MHNUC), Southwestern Biology
Collection of the University of New Mexico
(MSB); and the Museum of Texas Tech
University (TTU). To evaluate and describe
the morphometric variation and phenetic
similarities of the newly introduced record
of A. fistulata from Bolivia, a principal
component analysis (PCA) was performed
on 11 craniodental variables recorded from a
selected group of female specimens (N=179),
including all recognized species of Anoura,
except A. cadenai (only represented by male
specimens), in the statistical package PAST
(ver. 2.17) available at (http://folk.uio.no/
ohammer/past/index.html).
Ecological and geographic analyses.- To
assess the environmental affinities among
A. fistulata collecting localities, a PCA and
a Cluster Analysis (CA) were performed
based on four environmental variables
including: Elevation, Maximum Temperature
of the Warmest Month of the Year, Minimum
375
Geographic range of Anoura fistulata
Temperature of the Coldest Month of the Year,
and Precipitation. Environmental data were
derived from raster layers available at (http://
www.worldclim.org/bioclim) by applying
the extract values to point tool of the Spatial
Analyst extension in ArcGIS 9.3.1. Variables
were log-transformed and statistical analyses
were performed in the statistical package
PAST (ver. 2.17), available at (http://folk.uio.
no/ohammer/past/index.html).
Ecological niche modeling.- An ecologicalniche model was produced to evaluate
the suitable habitat for A. fistulata using
the maximum entropy machine learning
algorithm in the software MaxEnt (Phillips
et al., 2006, 2008). MaxEnt estimates a
target probability distribution based on
environmental information in the study
area associated to presence-only data. The
model generates a probability distribution
that respects a set of constraints (expressed
in terms of environmental variables) derived
from the occurrence data (Phillips et al.,
2006, 2008).
Nineteen sampling localities including records
reported by Muchhala et al. (2005) (N=10);
Lee et al. (2008) (N=1), Lee et al. (2010)
(N=1), Mantilla-Meluk and Baker (2008)
(N=1), Mantilla-Meluk et al. (2009) (N=3),
Garate-Bernardo and Carrasco-Rueda (2011)
(N=1); Pacheco et al. (2009) (N=1), and the
new record from Bolivia introduced in this
work were used as input. Sampling localities
were tested for duplicated occurrence data
within the same 1 km2 grid cell using ENM
tools (Warren et al., 2008). This procedure
allowed us to have only one point per grid cell,
and each remaining point was moved to the
center of its grid cell. Collecting localities used
to develop the MaxEnt model are contained
in Appendix II. A total of 19 bioclimatic
parameters of the current climate conditions
were used in the model (WorldClim data set,
from Hijmans et al., 2005). The data layers
used were generated through interpolation of
376
average monthly climate data from weather
stations on a 30 arc-second resolution grid (~1
km2 resolution). General accuracy of model
was evaluated by the Area Under the Curve
(AUC) of Receiver Operating Characteristic
(ROC plots) as a measure of prediction
success (Fielding and Bell, 1997). Models
providing AUC values in the range > 0.9 are
considered highly accurate, between 0.7 – 0.9
useful, and lower than 0.7 poorly accurate
(according to Sweets, 1988).
RESULTS
First record of A. fistulata for Bolivia.Adult Female (FMNH 106088) collected
by R. S. Crossin, (collectors number: 7275)
on November, 26, 1972 at the Department
of Chuquisaca, Azero, Hernando Siles
(Misspelled “Hernando Silez” on tag), 16
Km N Monteagudo, Bolivia, 20°10’0.00’’
S, 64°15’0.00’’W, at 1,524 m, preserved as
skull extracted, in good condition (Fig. 1a),
and body in fluid (Fig. 1b). We were not able
to determine if the name Azero on the tag of
specimen FMNH 106088 refers to the older
name of Hernando Siles, or to the River
Azero.
Diagnostic characters.- Specimen FMNH
106088 corresponds to a medium-sized
Anoura (forearm 39.0 mm), characterized
by an elongated, tubelike lower lip (Fig. 1b)
extending beyond the upper lip; interfemoral
membrane relatively wide (3.5 mm) with an
inverted V-shaped margin as described for A.
fistulata (Muchhala et al., 2005). Muchhala
et al. (2005) identified the length of the
tongue among the most important diagnostic
characters of A. fistulata; unfortunately, the
tongue of specimen FMNH 106088 was
partially removed as part of the procedure
of skull extraction (previously performed)
preventing us from determining its actual
length. However, the remaining portion of
the basal part of the tongue in our specimen
follows the anatomical description of A.
Mantilla-Meluk et al.
fistulata’s tongue in Muchhala (2006). In
specimen FMNH 106088, the basal part of
the tongue passes back through the throat
into the thoracic cavity and it is inserted at
the base of the sternum (Fig. 1b). At its base,
the tongue is distinctively surrounded by
a sleeve of connective tissue, described as
a glossal tube by Muchhala (2006), which
follows the ventral position of the trachea
(Fig. 1b). The placement of the tongue in
a deeper position between the sternum and
the heart, as well as the presence of a glossal
tube are claimed as autopomorphies of A.
fistulata (Muchhala et al., 2006), contrasting
the typical placement of the tongue at the base
of the oral cavity of other nectarivorous bats
(Griffiths, 1982), or at the upper part of the
sternum as in other choeronycterines, such
as Choeronycteris mexicana, as confirmed
based on the dissections of specimens of this
taxon (N=3).
Skull comparisons.- Skull of A. fistulata
FMNH 106088 is greater than that in A.
aequatoris and A. lusimanueli, and falls
within the morphometric ranges reported for
A. caudifer and A. fistulata (Mantilla-Meluk
and Baker, 2006; Muchhala et al., 2005)
(Table 1). The first upper molar has the typical
enlarged anteroexternal cusp and a reduced
associated cristid, characters identified as
synapomorphies of the A. caudifer complex
(Griffiths and Gardner, 2008; Mantilla-Meluk
and Baker, 2010 Fig. 8 Pg. 15). This character
differentiates A. fistulata from A. carishina,
A. geoffroyi, and A. peruana (Mantilla-Meluk
and Baker, 2010). Additionally, A. fistulata has
complete zygomata, differentiating it from A.
peruana and A. latidens. In A. fistulata, the
upper canines have a smooth anterior face with
no sulci; first lower premolar not enlarged and
bladelike shape as in A. cultrata (Handley,
1960). The dentary in A. fistulata is straight
Figure 1. A) Skull views of Anoura fistulata FMNH 106088, from Chuquisaca, Bolivia,
showing characters included in A. fistulata description (Muchhala et al. 2005): protruded
mandibular synphisis, elongated, straight and slender dentary, gap between the lower 1st and
2nd premolars; and the short postpalatal spine; B) insertion of the tongue (Tn) at the base of
the sternum, glossal tube (Gt) that follows the trachea (Tr), as well as the elongated lower lip
tubelike structure (Lp).
377
Geographic range of Anoura fistulata
and slender resembling that of A. caudifer from
Brazil and contrasting the most robust and
curved dentary of A. aequatoris from Bolivia,
Colombia, and Peru. Although the dentary in
A. cadenai is also straight, it is more robust
than that of A. fistulata. In A. fistulata the lower
tooth row is characterized by a noticeable gap
between the 1st and 2nd lower premolars (0.61
mm), a character present in six specimens
analyzed by Muchhala et al. (2005) (0.54 mm),
which is absent in A. cadenai. Although a gap
between the 1st and 2nd lower premolars was
also present in A. caudifer specimens from
Brazil (N=8), it was less noticeable (< 0.6
mm) than in A. fistulata. The mandible of A.
fistulata is also characterized by a protrusion
at the mandibular suture (mandibular keel)
that is absent in A. cadenai, and less developed
in other species of the genus such as A.
aequatoris, A. caudifer from Brazil and A.
luismanueli (Mantilla-Meluk and Baker, 2006,
Fig. 6, Pg. 12).
Principal components analysis of
morphometric data.- Most of the skull
variation in our dataset was explained by the
first two components (PC1 = 83.84% and PC2
= 5.30%) with greater loadings associated
with GSL and CBL. Although specimens
with GSL greater than 23.0 mm largely
overlap in the morphospace of our PCA (Fig.
2), A. fistula proved to be morphometrically
independent from other members of the A.
caudifer complex (A. aequatoris, A. caudifer,
and A. luismanueli) and closely related in
skull morphology to A. carishina and small
A. peruana in the northern range of the
distribution of this species in Colombia.
Table 1. Skull measurements of a selected group of specimens of Anoura in all recognized
species in the genus. All specimens correspond to females except those of A. cadenai (*),
represented by only males. Measurements of specimen A. fistulata FMNH 10688 from
Chuquisaca, Bolivia are also included. Description of the measurements are included in
Appendix I.
GSL
CB
PAL
PO
MB
BCW
BCH
TR
M-M
C-C
Mand
22.00
21.32
11.65
4.53
8.34
8.83
6.85
8.11
5.46
3.95
15.54
8.49
0.55
0.67
0.67
0.19
0.34
0.39
0.33
0.34
0.20
0.18
0.49
0.25
23.47
22.51
12.46
4.92
8.43
9.23
8.34
8.75
5.68
4.31
16.67
9.16
0.33
0.31
0.30
0.36
0.15
0.25
0.17
0.15
0.16
0.10
0.34
0.10
24.04
23.31
11.98
4.86
8.88
9.55
7.22
8.98
5.99
4.11
16.58
9.47
0.00
0.04
0.29
0.19
0.27
0.35
0.37
0.07
0.15
0.06
0.12
0.03
22.7
22.1
12.5
4.7
8.4
8.9
6.9
8.3
5.4
4.3
16.2
8.6
0.6
0.6
0.5
0.2
0.2
0.2
0.3
0.2
0.2
1.2
0.5
0.4
24.26
22.45
12.17
5.02
9.05
9.65
7.64
8.38
5.78
4.77
16.91
8.87
0.58
3.08
0.44
0.16
0.17
0.22
0.22
0.23
0.32
0.14
0.36
0.32
24.14
23.50
12.86
4.61
8.58
9.21
8.02
8.83
5.75
4.20
16.08
9.15
0.66
0.66
0.80
0.15
0.45
0.32
0.41
0.55
0.19
0.19
1.52
0.50
FMNH 106088
23.75
23.09
12.72
4.56
8.1
8.74
8.0
8.5
5.78
3.96
16.31
8.76
A. geoffroyi
24.90
24.05
13.25
5.17
9.20
9.76
7.54
9.46
6.23
4.46
17.39
9.77
0.358
0.34
0.48
0.21
0.27
0.25
0.36
0.18
0.19
0.14
0.29
0.28
24.23
23.50
12.18
22.30
9.09
9.61
6.87
9.23
6.10
4.25
77.76
9.34
0.57
0.74
0.48
93.61
0.23
0.23
0.29
0.19
0.18
0.17
315.81
1.12
24.74
24.22
13.49
4.97
9.14
9.69
7.26
9.56
6.00
4.28
17.52
9.80
0.38
0.42
0.28
0.19
0.12
0.12
0.08
0.42
0.20
0.14
0.32
0.36
21.51
20.77
11.16
4.53
8.27
9.01
6.62
7.58
4.75
4.01
15.29
8.48
0.42
0.26
0.28
0.21
0.07
0.16
0.26
0.41
0.29
0.29
0.33
0.28
25.16
24.22
13.10
4.89
9.13
9.68
7.31
9.39
5.97
4.33
17.44
9.76
1.18
1.16
1.46
0.19
0.22
0.22
0.51
0.30
0.20
0.16
0.67
0.59
A. aequatoris
N= 17
StDv
A. cadenai*
N= 4
StDv
A. carishina
N= 4
StDv
A. caudifer
N= 13
StDv
A. cultrata
N= 11
StDv
A. fistulata
N=4
N= 11
StDv
StDv
A. latidens
N= 29
StDv
A. lasyopiga
N= 4
StDv
A. luismanueli
N= 3
StDv
A. peruana
N= 87
378
StDv
ManTR
379
Mantilla-Meluk et al.
Figure 2. Principal Component Analysis of 11 craniodental variables of 179 female specimens: A. aequatoris (8); A. carishina (4); A. caudifer
(26); A. cultrata (9); A. fistulata (6); A. geoffroyi geoffroyi (5); A. g.lasiopyga (4); A. latidens (26); A. luismanueli (3); A. peruana (88). Anoura
fistulata specimen FMNH 106088, from Bolivia is marked by a black star.
Geographic range of Anoura fistulata
Range extension of A. fistulata.- Anoura
fistulata was described from Condor Mirador,
near the Destacamento Militar (3°38’08” S,
78°23’22” W) on the Cordillera del Condor,
1,750 m, Zamora Chichipe Province, Ecuador
(Muchhala et al., 2005). Besides the type
locality, the authors recorded the species in
eleven other localities in Ecuador, two of them
on the western versant of the Andes. Lee et
al. (2010) reported an additional record from
western Ecuador from Imbabura (0°19’51’’ N,
78°55’55’’ W), which represents the lowest
elevation reported for the species (702 m).
Mantilla-Meluk and Baker (2008) extended
the distribution of A. fistulata into the
Colombian territory based on a specimen from
Llorente, Nariño (0°49’0.00” N, 77°15’0.00”
W), with a posterior extension of the range
of the species into the northern portion of
the Colombian Andes by Mantilla-Meluk et
al. (2009) based on a specimen collected in
Pueblo Rico, Department of Risaralda, on the
road to La Bocatoma (5°14’18” N, 76°2’11”
W) at 2,460 m. In the southern part of its range,
the distribution of the species was extended by
Jiménez et al. (2008) into the Peruvian territory
based upon a specimen collected at Playa
Colorada, District Huicungo, Department of
San Martin (7°16’60” S, 76°47’60” W) at
1,704 m. Pacheco et al. (2009) also reported
A. fistulata for the Abiseo River, San Martín
(not specific locality provided by the authors),
deposited at the Museo de la Universidad
de San Marcos (MUSM 7213, 7215) and
proposed that the species is likely to be
present in southern localities along the Andes.
Later Gárate-Bernardo and Carrasco-Rueda
(2011) reported the species for Puno, southern
Peru (13°39’42” S, 70°28’56” W). Herein,
we present the morphological evidence
associated with the first record of A. fistulata
from Bolivia, which also constitutes the
southernmost known locality of the species.
The locality is part of the Bolivian montane
dry forest (Olson et al., 2001), which encloses
the Bolivian Inter-Andean dry forest (Ibish et
al., 2003).
380
Analysis of environmental variation.- In our
PCA the first component accounted for most
of the variation among A. fistulata collecting
localities (PC1 65.86 %, PC2 20.67), with
Minimum Temperature (-0.834), Mean
Annual Precipitation (-0.427), and Maximum
Temperature (-0.290) having a negative
loadings and Elevation (0.191) having
positive loading.
In our PCA and CA, Puno, Peru and Llorente,
Serranía de los Churumbelos in Colombia,
represented the most divergent localities
in terms of the environmental variables
analyzed. Puno, Peru had the lowest minimum
temperature; while Llorente had the highest
precipitation among analyzed localities (Mean
Annual Precipitation>2,490 mm). The rest of
the environmental variation was grouped into
a single cluster, subdivided into four clusters
without geographic structure (Fig. 5).
MaxEnt algorithm niche model.- Areas of
high suitability for the species represented
by probability values greater than 75%
were located in the northern portion of the
Andean Region of southern Colombia and
Ecuador (Figure 3). In our niche model, the
northernmost known locality for the species
in Pueblo Rico, Risaralda, Colombia, the
westernmost locality at Imbabura, Ecuador;
while the southernmost record in that reported
for Puno, Peru. In our MaxEnt model,
the locality of Puno was associated with
predictive values greater than 45%; while
the newly reported record from Hernando
Siles, Chuquisaca, Bolivia fell within an
area characterized by probability values
lower than 5%. Additionally, the area of
Chuquisaca, Bolivia, is isolated from suitable
environments in the northern range of the A.
fistulata distribution by the Bolivian Yungas
which were represented by probability values
lower than 5% (Fig. 3).
Mantilla-Meluk et al.
Figure 3. MaxEnt niche model constructed for A. fistulata based on the 19 known localities for
the species. Areas with high probability of species occurrence in warm colors, areas enclosing
low probability values in cool colors. Locality enclosed by the circle represents the new record
of A. fistulata from Chuquisaca, Hernando Siles, Bolivia.
381
Geographic range of Anoura fistulata
382
Figure 4. Scatter plot of the PCA and minimum spam tree of four environmental variables (Elevation, Mean Annual Maximum Temperature,
Mean Annual Minimum Temperature, and Mean Annual Precipitation) analyzed among known collecting localities of A. fistulata. Abbreviations
used to designate the localities: BOLIVIA: Hernando Siles (BoHS); COLOMBIA; Génova (CoGe); Llorente (CoLl); Pueblo Rico (CoPR);
Serranía de Los Churumbelos (CoCh); ECUADOR: Bellavista (EcBv); Condor Mirador (EcCM); Cotundo (EcCo); Chinapinza (EcCh),
1,700 m; Cuevas de Numbala (EcCvN); Imbabura (EcImb); El Salado (EcES); Guajalito (EcGj); La Herradura (EcLH); Pahuma (EcPh); Río
Cristalino (EcRC); Uunsuants (EcUt); Volcán Sumaco (EcVS); Yanayacu (EcYn); PERU: Playa Colorada (PePC); Puno (PePu).
Mantilla-Meluk et al.
DISCUSSION
Elevation explained most of the variation
among A. fistulata collection localities. Anoura
fistulata occurs between 702 and 2,517 m
(mean = 1,846 m, standard deviation 335 m),
altitudinal belt which is well represented along
the Andean unit constituted by the Batholith
of Ecuador and associated areas in Colombia
and Peru. This area is part of three adjacent
but ecologically contrasting bioregions: the
Eastern Cordillera real montane forest, the
Northwestern Andean montane forest, and
the Ucayali moist forest (Olson et al., 2001).
The elevational belt delimited by maximum
and minimum elevations reported for A.
fistulata, experiences a substantial reduction
in area at central and southern Peru where
the Andes are steeper (Fig. 3). Although we
agree with Pacheco et al. (2009) and believe
that the absence of A. fistulata in central
Peru may be an artifact of sampling, and
lack of detailed analyses of specimens, the
reduction in area of suitable elevations for
A. fistulata at this portion of the country may
constitute an ecological limiting factor for the
establishment of the species, and may be an
alternative explanation for the gap of records
between San Martin and Puno.
The northern range of the distribution of
A. fistulata enclosed the most divergent
environments for the analyzed variables. In
this portion of its distribution A. fistulata
inhabits three adjacent but ecologically
contrasting bioregions: the Eastern Cordillera
real montane forest, the Northwestern Andean
montane forest, and the Ucayali moist forest
as defined by Olson et al. (2001). In both
our PCA and CA the Andean montane moist
forests of Western Ecuador and Central
Colombia, represented by the localities of
Imbabura and Serranía de los Churumbelos,
respectively, as well as the premontane
forests of Southern Colombia in Llorente
were classified in independent groups in our
cluster analysis (Fig. 5). This result reflects
the great variety of environments inhabited
by A fistulata.
One of the most significant results of this study
is the latitudinal extension of the distribution
of A. fistulata by more than 7º into Hernando
Siles in Bolivia. In both our PCA and CA, the
geographically isolated A. fistulata Bolivian
locality clustered with those in the northern
portion of the distribution of the species (Figs.
4 and 5). The A. fistulata Bolivian locality
at the Bolivian Inter-Andean dry forests
biome (Ibish et al. 2003) is characterized by
a marked seasonality with a dry period of
8 to 10 months, and the area is dominated
by xerophytic dwarf forests (chaparral),
columnar, and terrestrial cacti (Ibish et
al. 2003). Although not representing arid
enclaves, Ecuadorian collecting localities of:
Chinapinza, Cuevas de Numbala and Condor
Mirador shared low Precipitation values and
high Minimum and Maximum Temperature
and cluster with A. fistulata Bolivian locality
(Figs. 4 and 5).
Areas identified as arid enclaves in southern
Colombia and Ecuador were also included
in our A. fistulata MaxEnt model. With
a disjunctive distribution, arid enclaves
are relatively common along the Andean
System from Venezuela south to Chile
and glossophagine bats and particularly
representatives of the genus Anoura are a
typical component of their faunas (Soriano
and Ruiz 2002, Sanchez et al. 2006). Pollen
of the cacti Opuntia dillenii, Pilosocereus
sp., and Stenocereus griseus has been found
in the guts of the congeneric A. carishina
(Mantilla-Meluk and Baker 2010) from
arid enclaves in the southern Andes of
Colombia, enclosed within areas associated
with A. fistulata intermediate presence
probabilities (>35%) in our MaxEnt model
(Fig. 3). Several studies have pointed on
the co-evolutionary relationship that exists
between glossophagine bats and columnar
cacti characterizing chiropterophylic
383
Geographic range of Anoura fistulata
Figure 5. Cluster analysis of A. fistulata collecting localities based on euclidian distances of
four environmental variables (Elevation, Mean Annual Maximum Temperature, Mean Annual
Minimum Temperature, and Mean Annual Precipitation). Abbreviations used to designate A.
fistulata localities: BOLIVIA: Hernando Siles (BoHS); COLOMBIA; Génova (CoGe); Llorente
(CoLl); Pueblo Rico (CoPR); Serranía de Los Churumbelos (CoCh); ECUADOR: Bellavista
(EcBv); Condor Mirador (EcCM); Cotundo (EcCo); Chinapinza (EcCh), 1,700 m; Cuevas de
Numbala (EcCvN); Imbabura (EcImb); El Salado (EcES); Guajalito (EcGj); La Herradura
(EcLH); Pahuma (EcPh); Río Cristalino (EcRC); Uunsuants (EcUt); Volcán Sumaco (EcVS);
Yanayacu (EcYn); PERU: Playa Colorada (PePC); Puno (PePu).
384
Mantilla-Meluk et al.
syndromes that consist of anatomical and
behavioral adaptations of both cacti and
bats to promote and facilitate bat pollination
(Baker et al. 2012, Fleming et al. 2009,
Nassar et al. 1997, Rivera-Marchand
and Ackerman 2006, Ruiz et al. 1997,
Soriano and Ruiz 2006, Valiente-Banuet
et al. 1997). The co-evolutionary history
between Neotropical nectar feeders and
cacti supports their existence in relatively
wide latitudinal gradients across divergent
bioregions enclosing arid enclaves.
Anoura fistulata proved to exist in a wide
altitudinal range in divergent bioregions
enclosing ecologically contrasting localities.
Most of the ecological variation among known
localities is associated with the northern
portion of the species distribution. The
prevalence of A. fistulata along the geologic
unit of the Batholith of Ecuador as well as
the absence of the species across Central
and Southern Peru is apparently explained
by differences in steepness and its effect
on the area of the elevational belt between
1,175 m and 2517 m. A reduction of this
elevational belt in Central and Southern Peru
may constitute an ecological barrier for the
establishment of A. fistulata in that region,
isolating the arid environments inhabited
by the species in the southern portion of its
distribution in Bolivia.
Although there is not a unified definition
that makes specialization comparable
across study systems (Lara et al., 2002),
the term “specialized” is used to describe
species that possess unique attributes
(Hintzpeter and Bauer 1986) or a restricted
ability to respond to varying environmental
parameters (Klopfer and MacArthur, 1960;
Endler, 1986), or both (Westoby, 1978;
Leisler, 1980; Benkman, 1988; Futuyma
and Moreno, 1988). Although other species
of nectarivorous bats have long tongues,
the size of the tongue in A. fistulata is
remarkably longer when compared with
other sympatric congeneric species. To date,
there is no a detailed analysis on A. fistulata
diet, but the data presented herein revealed
that the species can occur in contrasting
ecosystems presumably having differences
in plant compositions, and thus suggesting
that unique attributes of A. fistulata do
not necessitate stereotypy. Altogether
our results support our first hypothesis
that interprets extreme adaptations of A.
fistulata as features that allow the species
to survive in contrasting ecosystems across
its distributional range.
Table 2. Loadings of collecting localities
in the four axes of our PCA for the four
environmental variables analyzed.
Axis 2
Axis 3
EcUt
Locality
Axis 1
0,25038
0,029171
0,095396
Axis 4
-0,01022
EcRC
0,15734
0,17249
0,13645
-0,015108
-0,013053
0,0018196
EcCo
-0,09162
0,02774
EcES
-0,068289
0,014477
0,0085036 -0,0030054
EcBv
-0,12227
-0,13693
0,0027879
-0,019774
EcGj
-0,10363
-0,073067
0,012319
-0,010255
-0,098027
0,024233
EcPh
-0,15274
0,02953
EcYn
0,044443
-0,10837
EcLH
0,058591
-0,071609
EcCh
0,078192
EcCvN
-0,019381 -0,0071039
0,041699
0,04323 -0,0067959
-0,020912
0,022955
0,13687
-0,022277
-0,037474
0,019495
CoLl
-0,31288
0,10048
-0,073593
-0,042427
PeSM
-0,048248
0,2043
-0,074622
0,027683
BoHS
0,15572
0,077378
0,013545
0,0075025
CoGe
-0,012502
0,015025 -0,0029493
-0,048665
CoCh
0,24473
-0,15828
-0,038114
0,010245
CoPR
0,030977
-0,063196
-0,11623
0,008585
EcCM
PePu
0,14327 -0,0056678 -0,0098785
-0,38833
-0,07443
0,17942
0,013256
0,041696
Abbreviations used to designate collecting localities:
BOLIVIA: Hernando Siles (BoHS); COLOMBIA;
Génova (CoGe); Llorente (CoLl); Pueblo Rico
(CoPR); Serranía de Los Churumbelos (CoCh);
ECUADOR: Imbabura (EcImb); Uunsuants
(EcUt); Río Cristalino (EcRC); Cotundo (EcCo);
El Salado (EcES); Bellavista (EcBv); Guajalito
(EcGj); Pahuma (EcPh); Yanayacu (EcYn); La
Herradura (EcLH); Chinapinza (EcCh), 1,700 m;
Cuevas de Numbala (EcCvN); Condor Mirador
(EcCM); PERU: Playa Colorada (PePC); Puno
(PePu).
385
Geographic range of Anoura fistulata
ACkNOWLEDGEMENTS
This work would not be possible without
the invaluable efforts devoted by the
Field Museum of Natural History to the
understanding of the mammalian biodiversity
of the Andes represented in their collections.
We specially thank B. D. Patterson, L. R.
Heaney, and R. Banasiak. We thank R. J.
Baker, J. Dunnum, J. Cook, H. López, G. D.
Amat, J. Aguirre, K. Helgen, D. Wilson, and
A. L. Gardner whom facilitated our visit to the
collections of the Natural Science Research
Laboratory of the Texas Tech Museum, the
Southwestern Collection of the University
of New Mexico, the Instituto de Ciencias
Naturales of the Universidad Nacional de
Colombia, and the National Museum of
Natural History. We particularly thank N.
Muchhala for his valuable comments. This
work was funded by the Field Museum of
Natural History Fellowship. Finally we thank
H. York and R. Cadenillas for critical review
of the manuscript.
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Recibido: 15/10/2012
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Appendix II. Collecting localities of A. fistula analyzed
BOLIVIA: Chuquisaca: Azero, Hernando Siles, 16 Km; N Monteagudo, 1,524 m, 20°10’0.00’’
S, 64°15’0.00’’ W. COLOMBIA; Nariño: Génova, Municipio de Colón, Vereda Bordo Alto,
1,979 m, 1° 38’47’’ N, 77° 1’27’’ W; Llorente, 2,088 m, 0°49’0.00’’ N, 77°15’0.00’’ W;
Risaralda: Pueblo Rico, on the road to La Bocatoma, 2,460 m, 5°14’18’’ N, 76°2’11’’ W;
Cauca: Serranía de Los Churumbelos, Municipio de Santa Rosa, Vereda La Petrolera, Tataui,
2,100 m, 1°14’32.32’’ N, 76°30’28.34’’ W; ECUADOR: Imbabura: 10 km east of Santa
Rosa, 702 m 0°19’51’’ N, 78°55’55’’ W; Morona Santiago: Uunsuants, 1,300 m, 2°33’’09’’
S, 77°53’48’’ W; Río Cristalino, 1,061 m, 3°31’12’’ S, 78°25’48’’ W; Napo: Cotundo, 1,870
m, 0°38’30’’ S, 77°50’15’’ W; El Salado; Alto Coca, 1,800 m, 0°15’0.00’’ S, 77°41’0.00’’ W;
Pichincha: Bellavista, 2,200 m, 0°00’08’’ S, 78°41’02’’ W; Guajalito, 2,000 m, 0°13’09’’
S, 78°48’00’’ W; Pahuma, 2,275, 0°01’04’’ S, 78°38’00’’ W; Yanayacu, 2,075 m, 0°35’03’’
S, 77°52’08’’ W; Zamora Chichipe: La Herradura, 1,750 m, 4°02’02’’ S, 78°34’12’’ W;
Chinapinza, 1,700 m, 4°02’19’’ S, 78°35’40’’ W; Cuevas de Numbala, 1,890 m, 4°32’48’’ S,
79°04’05’’ W; Destacamento Militar, Condor Mirador, 1,750 m, 3°38’08’’ S, 78°23’22’’ W;
Volcán Sumaco, 0º34’19’’ S, 77º35’64’’ W; PERU: Puno: the village of Chacaneque, Ollachea
district, Carabaya province, 13°39’42” S, 70°28’56” W; San Martin: District of Huicungo;
Playa Colorada, 1,704 m, 7°16’60’’ S, 76°47’60’’ W.
388