Journal of Mammalogy, XX(X):1–9, 2020

DOI:10.1093/jmammal/gyaa141

Downloaded from https://academic.oup.com/jmammal/advance-article/doi/10.1093/jmammal/gyaa141/6007685 by University of New England user on 28 November 2020

Trophic relationships within the genus Carollia (Chiroptera,
Phyllostomidae) in a premontane forest of central Peru
Juan J. Pellón, Jorge Rivero, Marta Williams,*, and Mercedes Flores
Departamento de Mastozoología, Museo de Historia Natural, Universidad Nacional Mayor de San Marcos, Av. Arenales 1256,
Lima 11, Lima, Perú (JJP)
Laboratorio de Fisiología Animal y Biorremediación Luis Basto Acosta, Universidad Nacional Agraria La Molina, Av. La Molina
s/n La Molina, Lima 12, Lima, Perú (JJP, JR, MW)
Herbario MOL-Weberbauer, Universidad Nacional Agraria La Molina, Av. La Molina s/n La Molina, Lima 12, Lima, Perú (MF)
*Correspondent: mwilliams@lamolina.edu.pe

Assemblages of Neotropical frugivorous bats are structured as a function of the fruit diets of species; however,
ecological relationships among closely related species largely remain unknown. This study evaluated the trophic
relations among three species of Carollia in a premontane forest of central Peru. To accomplish this, we first
determined the diet composition of frugivorous bats to build a bat–fruit interaction network. We then assessed
the trophic structure of the bat assemblage using a modularity analysis in the network. Carollia brevicauda and
Carollia perspicillata were grouped apart from Carollia benkeithi. This partition occurred because the diet of
C. benkeithi was more specialized, characterized by two Piper species, a Cyclanthaceae species, and Banara
guianensis. Moreover, C. benkeithi, in contrast to its congeners, did not consume fruits of Ficus or Cecropia
(canopy resources). This result and available information on the ecology of Carollia species suggest that small
species of Carollia are more likely to carry out most of their feeding activities in the understory than are large
species of the genus.

Key words:  assemblage, Carollia benkeithi, diet, frugivorous bats, interaction networks, modularity, plant–animal interactions,
species-level relationships, trophic structure, vertical stratification

Los ensambles de murciélagos frugívoros Neotropicales se estructuran en función de los frutos que consumen las
especies; sin embargo, las relaciones ecológicas entre especies estrechamente relacionadas siguen escasamente
conocidas. En este estudio se evaluaron las relaciones tróficas entre tres especies de Carollia en un bosque
premontano del centro del Perú. Para ello, primero determinamos la composición de la dieta de los murciélagos
frugívoros para después construir una red de interacciones murciélago-fruto. A continuación, evaluamos
la estructura trófica en el ensamble de murciélagos usando un análisis de modularidad aplicado a la red de
interacciones. Encontramos que Carollia brevicauda y Carollia perspicillata se agrupan aparte de Carollia
benkeithi. Esta segregación se produjo porque la dieta de C. benkeithi resultó ser más especializada: caracterizada
por dos especies de Piper, una de Cyclanthaceae, y Banara guianensis. Además, C. benkeithi, a diferencia de sus
congéneres, no consumió frutos de Ficus o Cecropia (recursos del dosel). Este resultado, junto con la información
disponible sobre la ecología de las especies de Carollia, sugieren que en comparación con especies más grandes,
las especies de Carollia pequeñas se alimenten principalmente en el sotobosque.

Palabras clave:  Carollia benkeithi, dieta, ensamble, estratificación vertical, estructura trófica, interacción planta-animal,
modularidad, murciélagos frugívoros, redes de interacción, relaciones a nivel de especies

Neotropical frugivorous bats (family Phyllostomidae) con- are important in fundamental ecological processes such
stitute an abundant and diverse group of mammals and as seed dispersal (Muscarella and Fleming 2007). Within

© The Author(s) 2020. Published by Oxford University Press on behalf of the American Society of Mammalogists, www.mammalogy.org.

1
2 JOURNAL OF MAMMALOGY
the family Phyllostomidae, subfamilies Rhinophyllinae,
Stenodermatinae, and Carolliinae have evolved adapta-
tions to feed mainly on fruits; however, members of other
subfamilies (e.g., Glossophaginae, Lonchophyllinae,
Phyllostominae) are considered facultative frugivores (Rojas
et al. 2011). Besides this diversity of evolutionary lineages,
frugivorous phyllostomid bats display a great variation in
morphology (Dumont 2003; Cirranello et al. 2016), foraging
(Heithaus et al. 1975; Bonaccorso and Gush 1987), digestion
(Schondube et  al. 2001; Saldaña-Vázquez 2014), olfaction
(Eiting et al. 2015; Parolin et al. 2015), and other ecological
characters, favoring the development of numerous distinct
feeding strategies among this group.
Since the research of Fleming (1986), many trophic studies
have supported the suggestion that species in assemblages of
frugivorous phyllostomid bats frequently feed on core plant taxa
based on their feeding strategies (Andrade et al. 2013; Saldaña-
Vázquez 2014; Sánchez and Giannini 2018). This tendency cre-
ates bat–fruit relationships that define an organization in the
assemblages known as trophic structure. The three principal
known relationships in the Neotropics between frugivorous
bats and fruits are: 1) Ectophyllini (sensu Gardner 2007)–Ficus
and Cecropia; 2)  Carollia–Piper; and 3)  Sturnira–Solanum
and Piper (Giannini and Kalko 2004; Gonçalvez da Silva et al.
2008; Andrade et al. 2013; Parolin et al. 2016; Castaño et al.
2018; Sánchez and Giannini 2018).
A meta-analysis by Saldaña-Vázquez (2014) suggested that
the main drivers of the aforementioned relationships are body
mass of bats and nutrient digestibility (intrinsic factors), and
food availability (extrinsic factor). The latter highly influences
fruit preferences of bats, causing temporal and geographic var-
iations in their diets. Some phyllostomids shift their diets in
relation to the seasonal availability of food resources (Heithaus
et al. 1975; Mello et al. 2004; Sánchez et al. 2012a; Alviz and
Pérez-Torres 2020). In some ecosystems, fruit preferences
of bats deviate from their expected core plant taxa, probably
because these plants are absent or uncommon (e.g., montane
forests—Sánchez et  al. 2012b; Morales-Rivas 2016; Castaño
et al. 2018; dry forests—Novoa et al. 2011; Turcios-Casco et al.
2019). In addition, certain frugivorous bat species occasionally
consume a large variety of fruits while acting as generalist fruit
feeders; however, the preference on their respective core plant
taxa usually remains (e.g., Sturnira—Galindo-González et al.
2000; Carollia—Arias and Pacheco 2019). Hence, there re-
mains much to uncover about variability in the diet of frugivo-
rous bats in many Neotropical ecosystems.
Information on trophic relationships of frugivorous
phyllostomid bats at the species level is sparse; only a few
species have been evaluated to untangle these relations within
genera. For the genus Artibeus, Amaral et al. (2016) found al-
most no diet overlap between two large species: A. lituratus
and A. planirostris. In Sturnira, Giannini (1999) found no dif-
ferences between the diets of S. lilium and S. erythromos, but
Sánchez and Giannini (2018) suggested that S. tildae differ-
entiates its diet from that of S. lilium by consuming fruits of
root-climbing plants (Araceae and Cyclanthaceae). York and
Billings (2009) found a trophic stratification among species
of Carollia based on their consumption of insects. Moreover,
C. castanea and C. subrufa are hypothesized to be more spe-
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cialized on fruits of Piper compared to larger species such as
C. perspicillata (Fleming 1991; Giannini and Kalko 2004).
Thus, trophic relationships at the species level remain unclear in
most genera of phyllostomids and the coexistence mechanisms
of congeneric bat species consequently remain poorly known.
Three species of Carollia coexist, and are usually abundant,
in the premontane forests of central Peru (Mena 2010; Carrasco
2011; Refulio 2015; Zegarra 2019). These forests therefore rep-
resent suitable areas to study differences in the feeding habits
of Carollia species. In light of the foregoing, the main objective
of this study was to evaluate the trophic relationships among
three species of Carollia (C. benkeithi, C. brevicauda, and
C. perspicillata) in the premontane forest of Fundo Santa
Teresa, in Satipo, Peru. Our specific objectives were: 1) to de-
termine the diet of fruit-eating bats in the study area; 2) to as-
sess the trophic structure in the assemblage of frugivorous bats;
and 3) to assess trophic relationships within the genus Carollia
based on the structure obtained.
Materials and Methods
Study area.—The present study was carried out in Fundo
Santa Teresa, an experimental station of Universidad Nacional
Agraria La Molina located in the district of Río Negro, province
of Satipo, department of Junín, Peru (11°12′30″S, 74°41′15″W;
ca. 800–1,000 m a.s.l.). The field station has an extension of ap-
proximately 203 ha and is divided into two main zones: field
crops of pineapple and chili pepper, and a secondary forest clas-
sified as a humid tropical premontane forest (bh-PM) following
the Holdridge life zone system (Marcelo-Peña and Reynel 2014).
The forest is predominantly composed of Guatteria hyposericea
(Annonaceae), Pourouma minor (Urticaceae), Alchornea
glandulosa (Euphorbiaceae), Vochysia venulosa (Vochysiaceae),
Henriettella sylvestris (Melastomataceae), Jacaranda glabra
(Bignoniaceae), and Miconia splendens (Melastomataceae), a
composition that suggests that the forest is in a transition from
early to late stages of a secondary succession process (Fernández-
Hilario et  al. 2012; Marcelo-Peña and Reynel 2014). Annual
temperature and rainfall fluctuate from 20 to 28°C and 1,500
to 2,000 mm, respectively. Based on annual data of the Satipo
local station of SENAMHI (Servicio Nacional de Meteorología e
Hidrología del Perú), the rainy season starts in October and ends
in March while the dry season extends from April to September.
Field sampling.—We carried out a pilot study from January
to March 2015 during the data collection for the study of
Zegarra (2019; see study for details). Based on that study, we
established sites for high potential bat capture rates along the
edge of the forest. We used 12 understory mist nets (12 m long
and 2.5 m height) and carried out, on a monthly basis, one-
night bat sampling events in May 2015 and from November
2015 to September 2016. Mist nets were set up (every month
at the same locations) for 6 h after the sunset and were checked
every 30 min. Considering all the sampling events, including
 PELLÓN ET AL.—GENUS CAROLLIA TROPHIC RELATIONSHIPS
the pilot study, we achieved a total sampling effort of 45,360
square meters of mist net-hours (Straube and Bianconi 2002).
Captured frugivorous bats were placed in individual clean canvas
bags for 30 min to obtain their feces. After this time interval, fecal
pellets from each bat were collected, preserved in microcentrifuge
tubes with 70% ethanol, and considered as a single sample unit (1
fecal sample). Bats were taxonomically identified then released.
We determined the species of all individuals using the keys of
Pacheco and Solari (1997), Gardner (2007), and Díaz et al. (2011).
Species names are reported considering Sturnira giannae rather
than Sturnira lilium (Velazco and Patterson 2019). All the field-
work procedures described complied with the guidelines of the
American Society of Mammalogists (Sikes et al. 2016).
Diet determination.—Examination of fecal samples was
carried out through direct observation using a stereoscope
(Zeiss Stemi 305). Seeds found in the fecal pellets were iden-
tified taxonomically using the seed collection of the herbarium
MOL-FCF of Universidad Nacional Agraria La Molina (which
contains specimens of the study forest) and using specialized
bibliography (Lobova et al. 2009; Cornejo and Janovec 2010;
Linares and Moreno-Mosquera 2010). A  single fecal sample
could contain more than one type of seed; we considered the
number of different fecal samples containing each identified
seed morphotype as “seed occurrences” (1 occurrence = pres-
ence of 1 seed morphotype in a fecal sample).
Trophic structure.—Using the seed occurrence records, we
obtained an incidence matrix of B × P dimensions (B: number
of bat species, P: number of plant species) filled with the fre-
quencies of occurrence of each plant species in the diet of each
bat species. These can be also interpreted as frequencies of inter-
actions between bats and plants (bat–fruit interactions). Then, the
incidence matrix was represented as a weighted interaction net-
work, being bat and plant species the nodes and the incidences
of fruit consumption, the edges. To assess the trophic structure,
we used the DIRTLPAwb+ modularity optimization algorithm
(Beckett 2016) in the interaction network. This algorithm works
as an ordination tool that finds the most modular pattern in an
interaction network. Such pattern is the result of grouping nodes
(in this case, bat and plant species) in modules, which are sub-
groups of nodes more strongly connected to one another than to
other nodes of the same network (Mello et al. 2019). In addition,
the algorithm calculates a modularity score (Q) which is the de-
gree of compartmentalization in the topology of the network.
Table 1.—Percentage of consumption of the main fruit items in the diet of the frugivorous bats in the premontane forest of Fundo Santa Teresa,
Satipo, Peru, from January to March 2015, May 2015, and November 2015 to September 2016; considering the whole assemblage of frugivorous
bats, bat species of the genera Carollia and Sturnira, and bats of the tribe Ectophyllini (Artibeus, Mesophylla, Platyrrhinus, and Uroderma). Total
number of seed occurrences (n) is indicated in parenthesis.
Plant taxon Assemblage (n = 256) Carollia (n = 195)
Piper 46.48 58.46
Solanaceae 14.06 10.26
Cecropia 13.67 6.15
Ficus 5.86 1.54
Vismia 4.30 5.64
Cyclanthaceae 3.91 5.13
Banara 3.91 5.13
Others 7.81 7.69
3
Network indices usually depend on network size, the
number of links, and the total number of interactions ob-
served; hence, it is recommended to test the significance of
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the obtained parameters using null models (Dormann et  al.
2009; Thébault 2013). We ran the null model suggested by
Vázquez et al. (2007) 1,000 times; this model creates matrices
conserving the observed connectance and the total number
of interactions, and probabilistically conserves the marginal
sums. We then compared the observed modularity score with
the values expected based on the null model using z-scores
(ZQ—Dormann and Strauss 2014). Because z-scores are as-
sumed to be normally distributed, a ZQ value above 2 indi-
cates that the network is significantly modular (Dormann
and Strauss 2014). All analyses were carried out using the R
package bipartite (Dormann et al. 2008).
Results
We captured 410 frugivorous bats of 27 species and obtained
245 fecal samples. The samples with seeds (198) corresponded
to 14 bat species, and in those, we recorded 256 seed occur-
rences (Appendix I). Seeds belonged to 33 morphotypes: 20
were identified to the species level, six to genus, six to family,
and one was unidentified. All records corresponded to complete
seeds found in feces, except the Cissampelos sp. record which
was evidenced by seed remains (seed predation).
The most frequent fruit item in the diet of the assemblage of
frugivorous bats was Piper (46.48%). Solanaceae (14.06%) and
Cecropia (13.67%) fruits also were frequently consumed, while
remaining items individually represented less than 6% in the
diet of the assemblage (Table 1). Bats of the tribe Ectophyllini
(Artibeus, Mesophylla, Platyrrhinus, and Uroderma) displayed
a diet predominantly based on fruits of the genera Cecropia
(57.50%) and Ficus (30%). Sturnira species consumed mainly
fruits of the family Solanaceae (76.19%). Piper represented
the main fruit item in the diet of Carollia species (58.46%).
Carollia perspicillata and C. brevicauda displayed similar
diets: both consumed a high variety of fruits but maintained
Piper as their most frequent resource (Table  2). Carollia
benkeithi also fed mainly on Piper fruits; however, compared
to the other two Carollia species, its diet consisted of higher
proportions of a Cyclanthaceae species and Banara guianensis,
and it did not include Cecropia or Ficus in its diet (Table 2).
Ectophyllini (n = 40) Sturnira (n = 21)
5.00 14.29
0.00 76.19
57.50 0.00
30.00 0.00
0.00 0.00
0.00 0.00
0.00 0.00
7.50 9.52
4 JOURNAL OF MAMMALOGY

All fruits consumed by C.  benkeithi also were consumed by module along with two species of Piper, B.  guianensis, and
C. perspicillata and C. brevicauda (Appendix I). Cyclanthaceae 1.
For the trophic structure analysis, we did not include any spe-

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cies for which we only had one fecal record containing seeds
(Appendix I). Our modularity analysis considered only nine Discussion
bat species and determined four modules (Fig.  1). The mod- Diet composition.—Most of the main fruits registered in the
ularity score was 0.35 and ZQ was 6.213395 (ZQ > 2); hence, diet of the overall assemblage correspond to the core plant taxa
the network was significantly modular (Dormann and Strauss of frugivorous phyllostomid bats: Piper, Solanum, Cecropia,
2014). The first module grouped bats of the tribe Ectophyllini Ficus, and Vismia (Lobova et al. 2009). Although B. guianensis
and was predominantly composed of species of Cecropia and and the family Cyclanthaceae are not considered as core plant
Ficus. The second one comprised the species of Sturnira and taxa, their fruits are frequently noted in the diet of Neotropical
mainly plants of the family Solanaceae. Carollia perspicillata frugivorous bats (Lobova et al. 2009; Geiselman and Younger
and C. brevicauda formed the third module, which was defined 2020). Besides, some fruits represent uncommon or new re-
by most of the Piper species, Vismia sp., and the less frequent cords in the diet of phyllostomid bats (e.g., Cissampelos sp.,
plants in the diet of Carollia species (Palicourea luteovirescens, Bellucia pentamera, Cestrum megalophyllum—Geiselman and
Urera caracasana, etc.). Finally, C. benkeithi formed the fourth Younger 2020).
Trophic structure.—Fruit–frugivore interactions appear more
Table 2.—Percentage of consumption of the main fruit items in
diffuse and less specialized than others (e.g., pollination—
the diet of the frugivorous bats Carollia benkeithi, C.  brevicauda,
and C. perspicillata in the premontane forest of Fundo Santa Teresa,
Blüthgen et al. 2007; Mello et al. 2011a; ant–myrmecophyte—
Satipo, Peru, from January to March 2015, May 2015, and November Blüthgen et  al. 2007; Guimarães et  al. 2007). Hence, if a
2015 to September 2016. Total number of seed occurrences (n) is in- bat–fruit interaction network displays a modular structure, it
dicated in parenthesis. could be expected to have a low modularity score (Guimarães
et al. 2007). As a consequence, the obtained modular pattern
Plant taxon Carollia Carollia Carollia
in the network studied (Q  =  0.35) indicates that bat species
benkeithi (n = 51) brevicauda (n = 51) perspicillata (n = 93)
tend to feed mainly on a determined group of fruits, similar to
Piper 62.75 50.98 60.22
Solanaceae 9.80 13.73 8.60
other bat–fruit networks (Mello et al. 2011a, 2011b; Castaño
Cecropia 0.00 7.85 8.60 et al. 2018). Our results therefore displayed the most common
Ficus 0.00 1.96 2.15 trophic structure in assemblages of frugivorous phyllostomid
Vismia 3.92 9.80 4.30
Cyclanthaceae 11.77 1.96 3.23
bats from the genus to tribe level: Ectophyllini bats focused
Banara 9.80 5.88 2.15 on Cecropia and Ficus fruits, Sturnira on Solanum fruits, and
Others 1.96 7.84 10.75 Carollia on Piper fruits (Fleming 1986; Andrade et al. 2013;

Fig. 1.—Modules of the bat–fruit network of nine frugivorous bat species in the premontane forest of Fundo Santa Teresa, Satipo, Peru, from
January to March 2015, May 2015, and November 2015 to September 2016. The intensity of the color represents the intensity of the interaction.
Bat genera are abbreviated: Artibeus (A), Carollia (C), Platyrrhinus (P), and Sturnira (S).
 PELLÓN ET AL.—GENUS CAROLLIA TROPHIC RELATIONSHIPS
Parolin et al. 2016; Castaño et al. 2018; Sánchez and Giannini
2018). At the species level, although the fruits in the diet of
C. benkeithi were a complete subset of those of C. perspicillata
and C. brevicauda, C. benkeithi was pulled apart in a different
module in the modularity analysis. This result shows a subtle
dietary differentiation within the genus Carollia, specifically
between a small-bodied species (C. benkeithi) and two large-
bodied ones (C. brevicauda and C. perspicillata). These rela-
tionships among Carollia species are discussed in detail in the
next section.
Moreover, it should be noted that the modular topology of
the bat–fruit network has an influence on the seed dispersal
by bats because the different bat species will complement the
richness of the seed rain generated by the overall assemblage.
Therefore, taking into consideration that most plant species
recorded in the assemblage diet are pioneer plants commonly
dispersed by bats (Galindo-González 1998), each bat species is
playing an important role in the regeneration and maintenance
of the studied forest (Muscarella and Fleming 2007).
Trophic relationships within the genus Carollia.—Locally
abundant species of Neotropical frugivorous bats usually dis-
play high connectivity in bat–fruit networks, and thus are
considered to be generalist frugivores; however, bats usually
maintain their core plant taxa as their main food resource
(Laurindo et al. 2020). Although the three Carollia species are
the most abundant frugivorous bats in the understory of the
studied forest (Zegarra 2019; Appendix I), C. benkeithi showed
a more restricted diet than the other two species. Small-sized
Carollia species tend to be more specialized in Piper fruits
compared to larger ones (Fleming 1991). A similar pattern is
observed in several trophic studies in Neotropical forests, even
when C. benkeithi and C. castanea, the smallest species in the
genus, are abundant (e.g., Bonaccorso 1979; Gorchov et  al.
1995; Giannini and Kalko 2004; Lopez and Vaughan 2007).
Instead, in our case, the proportion of Piper in the diet of the
small species did not differ much from those of the large spe-
cies. Nevertheless, C.  benkeithi focused on a reduced subset
of Piper species (two species) according to the modularity
analysis. This partitioning of Piper species within the genus
Carollia has been documented previously between C. castanea
and C.  perspicillata (Thies and Kalko 2004; Andrade et  al.
2013), although Maynard et al. (2019) did not find significant
differences in that aspect.
In addition to its high consumption of Piper fruits, C. benkeithi
showed an association with the fruits of a Cyclanthaceae
species and B.  guianensis, which was one of the main fac-
tors influencing the segregation within the genus Carollia.
Morphologically or ecologically similar bat species sometimes
separate their trophic niches in subtle features, such as their
complementary food resources, to enable coexistence through
exploitative competition (Marinho-Filho 1991; Bonaccorso
et al. 2006; Andrade et al. 2013). Sánchez and Giannini (2018)
suggested that Sturnira tildae differentiates its diet from that of
S. lilium by consuming fruits of Rhodospatha, Thoracocarpus,
and Philodendron. Lopez and Vaughan (2007) found that
Carollia sowelli consumed higher proportions of Araceae
5
fruits than C. perspicillata in a forest of Costa Rica, although
both fed predominantly on Piper fruits. Artibeus gnomus, a
small-bodied species within its genus, mainly consumes fruits
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of Banara; thus, these fruits could be part of the trophic dif-
ferentiation between small and large Artibeus (Sánchez and
Giannini 2018). Moreover, the association of C. benkeithi with
Cyclanthaceae could be similar to the case of Rhinophylla
pumilio, a small-sized bat species previously considered into
the subfamily Carolliinae (e.g., McLellan and Koopman 2007),
which has a diet mostly centered on Cyclanthaceae fruits and
exhibits little diet overlap with Carollia in spite their morpho-
logical similarities (Cockle 2001; Delaval et al. 2005). Carollia
benkeithi has a diet mainly based on Piper, but also it is prob-
ably using some complementary fruit resources (in this case,
Cyclanthaceae and Banara) to avoid competition with larger
species of Carollia.
In our study, C. benkeithi did not consume fruits of Cecropia
or Ficus, plants that usually offer food resources only in the
forest canopy. Although C. perspicillata and C. brevicauda are
known to only consume understory fruits in some localities
(e.g., Ascorra et al. 1996; Lopez and Vaughan 2007), we iden-
tified through a literature search that Ficus and Cecropia fruits
are more frequent resources in the diets of C. brevicauda and
C. perspicillata (10.43%) compared to those of C. benkeithi
and C. castanea (0.92%) (Supplementary Data SD1). In ad-
dition, although all species of Carollia are classified as un-
derstory bats, C.  perspicillata and C.  brevicauda in some
localities use the canopy relatively frequently (e.g., Kalko and
Handley 2001; Vásquez-Parra et  al. 2017; Olaya-Rodríguez
et  al. 2019), in contrast to C.  benkeithi and C.  castanea,
which rarely have been captured in high vertical layers (e.g.,
Ascorra et al. 1996; Pereira et al. 2010). Using stable isotope
analysis, Rex et al. (2011) evaluated the foraging activity of
phyllostomid bats in Costa Rica and Ecuador and found that
C.  castanea foraged at lower heights than C.  perspicillata
in both study sites, but slightly higher than C. brevicauda in
the locality of Ecuador. Available information on the ecology
of Carollia species therefore suggests that C.  benkeithi
and C.  castanea possibly are more likely to perform most
of their feeding activities in the understory compared to
C. perspicillata and C. brevicauda.
Testing the aforementioned differentiation in the use of
vertical layers in forests would contribute to a better under-
standing of the coexistence among species of Carollia be-
cause vertical stratification is considered a mechanism of
resource partitioning in assemblages of frugivorous bats
(Dumont 2003). Supporting this possibility, Bonaccorso
et  al. (2006) suggested that C.  castanea can exploit under-
story resources better than C. perspicillata due to its smaller
body size and lesser wing loading. The existence of this ver-
tical stratification could be expected considering that small
and large Carollia species differ in many ecological aspects
other than their diets, such as echolocation settings (Thies
et  al. 1998), habitat use (Fleming et  al. 1991; Thies 1998;
Bonaccorso et  al. 2006), feeding behavior, and roosting
ecology (Bonaccorso et al. 2006).
6 JOURNAL OF MAMMALOGY
It has been suggested that historical factors have influenced
the dietary diversification of Neotropical frugivorous bats, de-
termining the trophic structure of their assemblages; however,
this hypothesis has only been proven for supraspecific taxa
(genus and subfamily) of fruit-eating phyllostomids (Giannini
and Kalko 2004; Sánchez and Giannini 2018). Taking this
into account, the differences in diet and other ecological fea-
tures between small and large Carollia species also could be
related to their evolutionary history because C. benkeithi and
C. castanea form a clade separated from the larger species in
the genus (Amador et al. 2018). This concept should be empha-
sized in further studies to gain a better understanding of the ori-
gins of the trophic structure in the assemblages of New World
frugivorous bats.
Our results regarding the relationships among coexisting
Carollia species suggest: 1) the possibility that C. benkeithi, in
addition to its diet specialized in Piper, is using other fruits as
complementary food resources (at least in the forest studied) to
decrease the diet overlap with other Carollia species; and 2) a
differential use of the forest vertical layers between small and
large species of Carollia.
Acknowledgments
We are grateful to Rodrigo Medellín, Marília Barros, Daniel
Ramos-H, and two anonymous reviewers for their useful com-
ments on previous versions of this manuscript. We thank all
the people that helped us during the fieldwork, especially:
Mily Valle, Amanda Vílchez, Leonardo Gaspar, Gianlucca
Monteverde, Franco Fernández, Williams Vílchez, Luis
Janampa, Luis Ttito, and Oscar Quispe. Second, to Robin
Fernández-Hilario, Ítalo Revilla, Luis Pillaca, José Alegría,
Carlos Reynel, Marty Condon, and Klauss Cervantes, for their
help determining the identities of some plants consumed by
bats in the study area. We also thank Orlando Zegarra for al-
lowing us to undertake the pilot study during the field evalua-
tion for his bachelor’s thesis. JJP is grateful to Michela Olaya
for her important support during the study. Finally, we thank
Raydo Espinoza, Carlos Marca, and Raúl Blás, for authorizing
us to work on Fundo Santa Teresa.
Supplementary Data
Supplementary data are available at Journal of Mammalogy
online.
Supplementary Data SD1.—Literature search on Ficus
and Cecropia fruits consumption by two small-bodied Carollia
species (C.  benkeithi and C.  castanea) and two large-bodied
ones (C. perspicillata and C. brevicauda). Abbreviations: F/C:
Count of occurrences of Ficus and Cecropia in the diet, T: Total
seed occurrences considered.
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 PELLÓN ET AL.—GENUS CAROLLIA TROPHIC RELATIONSHIPS 9

Appendix I species: A.g.: Artibeus glaucus, A.l.: Artibeus lituratus, A.p.: Artibeus
planirostris, C.b.: Carollia benkeithi, C.br.: Carollia brevicauda,
Number of seed occurrences (i.e., presence of each seed morphotype) C.p.: Carollia perspicillata, M.m.: Mesophylla macconnelli, P.i.:

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in fecal samples of frugivorous bats in the premontane forest of Platyrrhinus incarum, P.m.: Platyrrhinus masu, S.g.: Sturnira
Fundo Santa Teresa, Satipo, Peru, from January to March 2015, May giannae, S.m.: Sturnira magna, S.t.: Sturnira tildae, U.b.: Uroderma
2015, and November 2015 to September 2016. Abbreviations of bat bilobatum, U.m.: Uroderma magnisrostrum.

Plant taxon A.g. A.l. A.p. C.b. C.br. C.p. M.m.a P.i. P.m.a S.g. S.m.a S.t. U.b.a U.m.a
Araceae
  Araceae 1 1
  Araceae 2 1 2
  Araceae 3 1
Cyclanthaceae
  Cyclanthaceae 1 6 1 3
Hypericaceae
  Vismia sp. 2 5 4
Melastomataceae
  Bellucia pentamera 1 2
  Melastomataceae 1 1
Menispermaceae
  Cissampelos sp. 1
Moraceae
  Ficus cf. americana 1 1 2
  Ficus obtusifolia 1 2 1
  Ficus paraensis 3
  Ficus trigona 1 1 1 1
Piperaceae
  Piper arboreum 8 2 6 1
  Piper calvescentinerve 2
  Piper glabribaccum 2 8
  Piper heterophyllum 4 5 11
  Piper hispidum 2 6 11 17
  Piper scabridulicaule 14 5 9 1 1
  Piper sp. 1 1
  Piper sp. 2 1 2
Rubiaceae
  Palicourea luteovirescens 1 1 2
Salicaceae
  Banara guianensis 5 3 2
Solanaceae
  Cestrum megalophyllum 1
  Cestrum racemosum 2
  Solanum grandiflorum 1 2
  Solanum riparium 5 5 6 5 6
  Solanaceae 1 2 1
Urticaceae
  Cecropia polystachya 2 2 4 4 7 1 2 1 1
  Cecropia sciadophylla 1 1 2
  Cecropia sp. 1 3 1 1 1
  Cecropia sp. 2 1
  Urera caracasana 1 2
Undetermined
  Unknown 1 2 1
Total seed occurrences 4 12 15 51 51 93 1 5 1 6 1 14 1 1
Number of bat captures 7 13 16 83 70 162 1 7 3 7 1 16 5 1

Species removed from the modularity analysis.

a