First report of a hard fruit in the diet of Centurio senex (Chiroptera

Journal of Mammalogy, 94(3):628–631, 2013
First report of a hard fruit in the diet of Centurio senex (Chiroptera:
Phyllostomidae) in Mexico
SERGIO M. MADRID-L ÓPEZ, ALEJANDRO A. CASTRO-LUNA,
AND
JORGE GALINDO-GONZÁLEZ*
Instituto de Biotecnologı́a y Ecologı́a Aplicada (INBIOTECA), Universidad Veracruzana, Avenida de las Culturas
Veracruzanas #101, Colonia Emiliano Zapata, Xalapa, Veracruz, CP 91090, México
* Correspondent: jorgegalin@gmail.com; jgalindo@uv.mx
Key words:
bat
frugivorous bat, fruit hardness, seed dispersal, Sideroxylon capiri, subdeciduous forest, Veracruz, wrinkle-faced
Ó 2013 American Society of Mammalogists
DOI: 10.1644/12-MAMM-A-218.1
The wrinkle-faced bat, Centurio senex (Phyllostomidae:
Stenodermatinae), is a medium-sized bat (total length: 55–70
mm, forearm body mass: 41–45 mm, 17–28 g), characterized
by a broad, flat face that has numerous hairless skin folds, and a
jaw that juts forward. There is no true nose leaf, and there are
glands in the neck that probably secrete an odoriferous
substance (Nowak 1994). When roosting, males of this species
cover their face with a chin fold that extends from the neck
over the ears and over the top of the head (Hill and Smith 1984;
Nowak 1994). C. senex inhabits a wide variety of ecosystems,
from tropical rain forests and agroecosystems to sites with
xerophilous vegetation (Watkins et al. 1972). The species is
distributed from central Mexico south to western Venezuela,
over elevations ranging from sea level up to 2,230 m above sea
level (Snow et al. 1980; Naranjo and Espinoza 2001).
Centurio senex is a strict frugivore (Snow et al. 1980;
Dumont et al. 2009) and it has been suggested that it sucks the
pulp from soft fruit such as Ficus sp. (Elizalde-Arellano et al.
2004), Musa sp., and Asimina triloba (Goodwin and Greenhall
1961). Little is known about most aspects of the biology of C.
senex (Dumont et al. 2009). In the wild, C. senex eats Spondias
radlkoferi (Anacardiaceae—Bonaccorso 1979), Drypetes lateriflora (Putranjivaceae—Snow et al. 1980), Ficus sp.
(Moraceae—Gardner 1977), Guettarda foliacea (Rubiaceae—
Giannini and Kalko 2004), Vitex mollis (Lamiaceae—Ramı́rezPulido and López-Forment 1979; Ceballos and Oliva 2005),
and Maclura tinctoria (Moraceae—Dumont et al. 2009).
Recently, it was proposed that C. senex is a frugivore
specializing on hard fruit. Compared to other frugivores of
similar size (e.g., Carollia perspicillata with a bite strength of
5.6 newtons [N] 6 1.69 SE—Freeman and Lemen 2010), C.
senex possesses a stronger bite (10.9 6 0.85 N—Dumont et al.
2009). This specialization, however, has not been tested. We
report for the 1st time that Sideroxylon capiri (Sapotaceae)
forms part of the diet of C. senex, and provide evidence that
supports the hypothesis that C. senex eats harder fruit than do
other frugivorous bat species.
MATERIALS
AND
METHODS
From June 2009 to March 2010 we carried out a study of the
bat assemblage composition (research permit FLO.FAU-026)
in patches of semideciduous seasonal forest (sensu Miranda
and Hernández-X. 1963) and agroecosystems in the municipality of Tlaltetela, Veracruz, Mexico (19817 0 52.083 00 N,
96842 0 27.313 00 W—Madrid-López 2010). The elevation of the
study area is 523 m above sea level and the climate in the area
is type Aw 00 (W)(i)g (Garcı́a 1981), which is a warm subhumid
climate with summer rains and a dry season from November to
March (Servicio Meteorológico Nacional 2000). With a
sampling effort of 28,080 m2h (Straube and Bianconi 2002),
we captured 907 bats, 9 of which were C. senex (7 females and
2 males). Seven of these were caught in semideciduous
seasonal forests and 2 were in mango (Mangifera indica) and
www.mammalogy.org
628
Downloaded from http://jmammal.oxfordjournals.org/ by guest on November 18, 2016
Recently it was proposed that Centurio senex specializes on hard fruit because of its strong bite compared to
other similar-sized frugivorous bats; however, this hypothesis has not been tested. We tested the hardness of 5
fruit species eaten by bats, including Sideroxylon capiri (Sapotaceae), here reported for the 1st time as part of the
diet of C. senex. Results show that S. capiri is the hardest fruit of the species evaluated. This is the 1st evidence
of C. senex eating hard fruit in the wild, which supports the theory of a skull adapted to eating hard fruit.
June 2013
629
MADRID-LÓPEZ ET AL.—CENTURIO SENEX EATING SIDEROXYLON CAPIRI
RESULTS
FIG. 1.—Penetrometer designed to measure the hardness of fruit
eaten by bats. A) Container with fine sand; B) plunger to catch the
sand and transfer weight onto the fruit via C) the point (diameter ¼ 1
mm); D) container for the fruit; E) fruit; and F) digital balance.
sapodilla (Manilkara zapota) agroecosystems. We documented
every aspect of the biology of the bats captured, including
those fruits that were carried by the bats into the nets.
Following capture all bats were released at their capture site.
We handled all animals in accordance with guidelines
approved by the American Society of Mammalogists (Sikes
et al. 2011).
To compare the hardness of S. capiri relative to that of the
fruit eaten by other frugivorous bat species, we simultaneously
collected the ripe fruit from species of plants reported to be part
On 22 January 2010 we captured several species of bats,
including Artibeus lituratus, Artibeus phaeotis, and Desmodus
rotundus, and a lactating female C. senex that was carrying a
fruit of S. capiri in her mouth. This is the 1stt report of a fruit of
Sapotaceae being eaten by C. senex. The fruits of S. capiri are
fleshy, ovoid berries with a smooth, hard epicarp that ends in a
fine point. These berries are 30–50 mm long and weigh, on
average, 17.5 g (Table 1). When ripe, the fruit turns yellow and
then red; each fruit has a single ovoid seed, 17.5–24 mm long,
that is brown, with a hard, smooth, shiny seed coat.
We collected the fruits of 4 plant species (Table 1) reported to
have been eaten by bats, along with the fruit of S. capiri, for
which there were no previous records of it as part of the diet of
bats. Fruit hardness differed among species (F4,44 ¼ 59.88, P ,
0.01), with S. capiri the hardest of the 5. There were 3 degrees of
hardness: Spondias purpurea and Brosimum alicastrum had the
softest fruit (Fig. 2), whereas fruits of S. capiri were the hardest.
DISCUSSION
The fruits of S. capiri have a soft juicy mesocarp, but the
epicarp is hard. Inclusion of S. capiri in the diet of C. senex
TABLE 1.—Epicarp hardness of fruit eaten by bats. Sample size (n) and mean and standard deviation of the measurements taken from 10 fruits of
each species are given. Hardness is expressed in newtons (N). With the exception of Sideroxylon capiri, the species were confirmed as having
been eaten by bats based on the criteria of Geiselman et al. (2002). Sp pu, Spondias purpurea; Br al, Brosimum alicastrum; Ph sp, Physalis sp.; So
um, Solanum umbellatum; Si ca, Sideroxylon capiri.
Plant species
n
Sp pu
Br al
Ph sp
So um
Si ca
10
9
10
10
10
Mass (g)
6.20
4.88
1.60
1.40
17.5
6
6
6
6
6
1.13
1.05
0.51
0.51
5.38
Length (mm)
25.77
21.43
15.01
12.76
38.95
6
6
6
6
6
1.03
0.77
1.42
1.48
4.33
Width (mm)
21.76
18.34
13.58
12.30
29.41
6
6
6
6
6
1.31
0.92
1.77
1.43
2.90
Hardness (N)
0.80
0.82
1.41
1.66
2.23
6
6
6
6
6
0.15
0.32
0.19
0.22
0.28
Downloaded from http://jmammal.oxfordjournals.org/ by guest on November 18, 2016
of the diet of frugivorous bats (Geiselman et al. 2002). The
species were identified by comparing specimens with those in
the XAL herbarium at the Instituto de Ecologı́a, A. C. Fruit
hardness was defined as the force necessary to pierce the epicarp
of the fruit with a blunt point 1 mm in diameter. We designed a
penetrometer (Fig. 1) to record the mass in grams necessary for
the point to puncture the fruit’s epicarp. The value obtained in
grams was converted to newtons (N) using the formula: F ¼ m 3
a, where F is the force in newtons, m is mass in kilograms, and a
is acceleration in meters per seconds squared (m/s2); we used the
value of acceleration due to gravity (9.806 m/s2).
To determine differences in hardness, the fruits were
weighed, measured (width and length), and tested with the
penetrometer. Three trials were run for each individual fruit
and the mean of these was used as the representative value for
each fruit. Ten fruits were used for each of the 5 plant species.
A 1-way analysis of variance and Tukey’s test were used to
detect any differences in fruit hardness among species (Zar
1999). All analyses were performed in R-system software (R
Development Core Team 2007).
630
Vol. 94, No. 3
JOURNAL OF MAMMALOGY
agrees with the suggestion made by Dumont et al. (2009).
Based on bite strength and observations of foraging by C.
senex in captivity, Dumont et al. (2009) suggested that the diet
of this species could include hard fruits that would separate the
diet of this species from that of other frugivores. Our results
also support the proposal by Freeman (1988), who stated that
the shape of the cranium of C. senex suggests that this species
may reflect a durophagous mode of feeding. It is quite probable
that the powerful mandibles of this bat, together with the long
cutting edges of its molars, are able to penetrate the epicarp of
hard fruits such as those of S. capiri. The bat can then squeeze
out the pulp, extract the sugar-rich juice, and spit out the
indigestible fiber; however, this strategy requires verification
(Morrison 1980; Freeman 1988; Dumont et al. 2009). This
ability would give C. senex access to resources that are in less
demand and a certain advantage when food is scarce. Other bat
species deal with this by switching from frugivory to
insectivory, or from nectarivory to insectivory (Gardner
1977), or by migrating to different feeding sites.
Moreover, the observation of C. senex transporting a fruit of
S. capiri indicates that, like other phyllostomids, this species is
capable of transporting the fruit it eats to nocturnal feeding
refugia that are generally at some distance (20–250 m) from the
tree where the fruit was picked up (Galindo-González 1998).
This implies that C. senex is likely to be a disperser of seeds of
S. capiri. The mean mass of fruit of S. capiri (17.5 g; Table 1)
is equivalent to at least 60% of the body mass of an adult C.
senex (17–28 g—Nowak 1994), and is indicative of this
species’ capacity to carry heavy loads relative to its size. This
finding refutes the idea that C. senex is a bat that only eats very
ripe, extremely soft or even rotting fruit (Bonaccorso 1979), or
that it must eat this fruit directly from the ground or from the
plant because of its inability to transport the fruits (Paradiso
1967; Freeman 1988).
RESUMEN
Recientemente se planteó que Centurio senex se especializa
en frutos duros, ya que posee una fuerte mordida comparada
con otros murciélagos frugı́voros de talla similar; aunque no se
ha probado. Pusimos a prueba la dureza de 5 especies de frutos
consumidos por murciélagos, incluyendo Sideroxylon capiri
(Sapotaceae), que reportamos por primera vez en la dieta de C.
senex. Los resultados muestran que S. capiri es la especie con
semilla más dura de las estudiadas. Esta es la primera evidencia
del consumo de un fruto duro por C. senex en la naturaleza, lo
cual apoya la teorı́a de un cráneo adaptado para el consumo de
frutos duros.
ACKNOWLEDGMENTS
We thank A. Tepatlán and N. Hernández for their valuable help
with the fieldwork. We are thankful to the inhabitants of the Coetzala
community, especially A. Durán, for their hospitality. The Instituto de
Biotecnologı́a y Ecologı́a Aplicada of Universidad Veracruzana
provided logistical support. R. A. Medellı́n and V. J. Sosa provided
insightful comments that improved the quality of the manuscript. This
study was partly funded by the Universidad Veracruzana awarded to
JG-G for being in the Sistema Nacional de Investigadores (National
Researches System) and a Consejo Nacional de Ciencia y Tecnologı́a
(National Council for Science and Technology) postdoctoral scholarship to AAC-L.
LITERATURE CITED
AGUIRRE, L. F., A. HERREL, R. VAN DAMME, AND E. MATTHYSEN. 2002.
Ecomorphological analysis of trophic niche partitioning in a
tropical savannah bat community. Proceedings of the Royal Society
of London, B. Biological Sciences 269:1271–1278.
BONACCORSO, F. J. 1979. Foraging and reproduction in a Panamanian
bat community. Bulletin of the Florida State Museum. Biological
Sciences 24:359–408.
CEBALLOS, G., AND G. OLIVA (coords.). 2005. Los mamı́feros silvestres
de México. Fondo de Cultura Económica—Comisión Nacional Para
Downloaded from http://jmammal.oxfordjournals.org/ by guest on November 18, 2016
FIG. 2.—Hardness (X̄ 6 SE) of the fruit belonging to 5 species
eaten by bats in the region of Apazapan, Veracruz, Mexico. Different
letters indicate significant differences (P , 0.01). Sp pu, Spondias
purpurea; Br al, Brosimum alicastrum; Ph sp, Physalis sp.; So um,
Solanum umbellatum; Si ca, Sideroxylon capiri.
It is important to highlight the fact that there is only 1 report
of fruit of S. capiri being eaten by A. jamaicensis, when S.
capiri was known by its synonym Mastichodendron capiri
(Orozco-Segovia and Vázquez-Yañes 1982). This is a
potentially important point, because no other frugivore is
known to do so. A. jamaicensis weighs 36–48 g (Ortega and
Castro-Arellano 2001), more than double the weight of C.
senex. The strength of its bite also is greater than that of C.
senex (24.96 6 8.53 N—Aguirre et al. 2002), and thus is
strong enough to pierce the epicarp of this fruit.
Our results demonstrate that C. senex is capable of eating
fruits that are harder than the mean hardness of the fruit eaten
by similar-sized phyllostomid frugivores. This supports the
proposal that this species has a skull adapted to eating hard
fruit, which confers an advantage on C. senex concerning niche
separation from other frugivorous bats when food is scarce and
eventually toward the specialization of eating fruits with hard
epicarp, and also means that C. senex is a genuine disperser of
seeds of S. capiri.
June 2013
MADRID-LÓPEZ ET AL.—CENTURIO SENEX EATING SIDEROXYLON CAPIRI
MORRISON, D. W. 1980. Efficiency of food utilization by bats.
Oecologia 45:270–273.
NARANJO, E. J., AND E. ESPINOZA. 2001. Los mamı́feros de la Reserva
Ecológica Huitepec, Chiapas, México. Revista Mexicana de
Mastozoologı́a 5:58–67.
NOWAK, R. M. 1994. Walker’s bats of the world. Johns Hopkins
University Press, London, United Kingdom.
OROZCO-SEGOVIA, A., AND C. VÁZQUEZ-YAÑES. 1982. Plants and fruit
bat interactions in a tropical rain forest area, southeastern Mexico.
Brenesia 19/20:137–149.
ORTEGA, J., AND I. CASTRO-ARELLANO. 2001. Artibeus jamaicensis.
Mammalian Species 662:1–9.
PARADISO, J. L. 1967. A review of the wrinkle-faced bat (Centurio
senex Gray) with description of a new subspecies. Mammalia
31:595–604.
RAMÍREZ-PULIDO, J., AND W. LÓPEZ-FORMENT. 1979. Additional records
of some Mexican bats. Southwestern Naturalist 24:541–544.
R DEVELOPMENT CORE TEAM. 2007. R: a language and environment for
statistical computing. R Foundation for Statistical Computing,
Vienna, Austria. http://www.R-project.org. Accessed 26 July 2012.
SERVICIO METEOROLÓGICO NACIONAL. 2000. Normales climatológicas
1971–2000. Estación: 00030367 Apazapan (CFE). Servicio Meteorológico Nacional, Veracruz, Mexico.
SIKES, R. S., W. L. GANNON, AND THE ANIMAL CARE AND USE COMMITTEE
OF THE AMERICAN SOCIETY OF MAMMALOGISTS. 2011. Guidelines of
the American Society of Mammalogists for the use of wild
mammals in research. Journal of Mammalogy 92:235–253.
SNOW, J. L., J. K. JONES, JR., AND W. D. WEBSTER. 1980. Centurio
senex. Mammalian Species 138:1–3.
STRAUBE, F. C., AND G. V. BIANCONI. 2002. Sobre a grandeza e a
unidade utilizada para estimar esforço de captura com utilição de
redes-de-neblina. Chiroptera Neotropical 8:150–152.
WATKINS, L. C., J. K. JONES, JR., AND H. H. GENOWAYS. 1972. Bats of
Jalisco, Mexico. Special Publications, The Museum, Texas Tech
University 1:1–44.
ZAR, J. H. 1999. Biostatistical analysis. 4th ed. Prentice-Hall Inc.,
Upper Saddle River, New Jersey.
Submitted 29 August 2012. Accepted 21 January 2013.
Associate Editor was Victor Sánchez-Cordero.
Downloaded from http://jmammal.oxfordjournals.org/ by guest on November 18, 2016
el Conocimiento y Uso de la Biodiversidad, México, Distrito
Federal, México.
DUMONT, E. R., A. HERREL, R. A. MEDELLÍN, J. A. VARGAS-CONTRERAS,
AND S. E. SANTANA. 2009. Built to bite: cranial design and function
in the wrinkle-faced bat. Journal of Zoology (London) 279:329–
337.
ELIZALDE-ARELLANO, C., E. URÍA-GALICIA, AND J. C. LÓPEZ-VIDAL.
2004. Estructura anatómica e histológica de la lengua del
murciélago frugı́voro Centurio senex (Chiroptera: Phyllostomidae).
Acta Zoológica Mexicana (Nueva Serie) 20:31–37.
FREEMAN, P. W. 1988. Frugivorous and animalivorous bats (Microchiroptera)—dental and cranial adaptations. Biological Journal of
the Linnean Society 33:249–272.
FREEMAN, P. W., AND C. A. LEMEN. 2010. Simple predictors of bite
force in bats: the good, the better, and the better still. Journal of
Zoology (London) 282:284–290.
GALINDO-GONZÁLEZ, J. 1998. Dispersión de semillas por murciélagos:
su importancia en la conservación y regeneración del bosque
tropical. Acta Zoológica Mexicana (Nueva Serie) 73:57–74.
GARCÍA, E. 1981. Modificaciones al sistema de clasificación climático
de Köppen. Offset Larios, México, Distrito Federal, México.
GARDNER, A. L. 1977. Feeding habits. Pp. 293–350 in Biology of bats
of the New World family Phyllostomatidae, part II (R. J. Baker, J.
K. Jones, Jr., and D. C. Carter, EDS.). Special Publications, The
Museum, Texas Tech University 13:1–364.
GEISELMAN, C. K., S. A. MORI, AND F. BLANCHARD. 2002. Database of
Neotropical bat/plant interactions. Updated 2007. http://www.nybg.
org/botany/tlobova/mori/batsplants/database/dbase_frameset.htm.
Accessed 29 February 2012.
GIANNINI, N. P., AND E. K. V. KALKO. 2004. Trophic structure in a large
assemblage of phyllostomid bats in Panama. Oikos 105:209–220.
GOODWIN, G. G., AND A. M. GREENHALL. 1961. A review of the bats of
Trinidad and Tobago. Bulletin of the American Museum of Natural
History 122:191–301.
HILL, J. E., AND J. D. SMITH. 1984. Bats, a natural history. University of
Texas Press, Austin.
MADRID-LÓPEZ, S. M. 2010. Abundancia, diversidad y composición de
murciélagos en fragmentos de selva mediana subcaducifolia y
cultivos de árboles frutales en la región de Apazapan, Veracruz.
B.S. thesis, Universidad Veracruzana, Veracruz, Mexico.
MIRANDA, F., AND E. HERNÁNDEZ-X. 1963. Los tipos de vegetación de
México y su clasificación. Boletı́n de la Sociedad Botánica de
México 28:29–179.
631