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Oup Accepted Manuscript 2020 PDF
Oup Accepted Manuscript 2020 PDF
DOI:10.1093/jmammal/gyaa141
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.
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the family Phyllostomidae, subfamilies Rhinophyllinae, Billings (2009) found a trophic stratification among species
Stenodermatinae, and Carolliinae have evolved adapta- of Carollia based on their consumption of insects. Moreover,
tions to feed mainly on fruits; however, members of other C. castanea and C. subrufa are hypothesized to be more spe-
the pilot study, we achieved a total sampling effort of 45,360 Network indices usually depend on network size, the
square meters of mist net-hours (Straube and Bianconi 2002). number of links, and the total number of interactions ob-
Captured frugivorous bats were placed in individual clean canvas served; hence, it is recommended to test the significance of
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) Ectophyllini (n = 40) Sturnira (n = 21)
Piper 46.48 58.46 5.00 14.29
Solanaceae 14.06 10.26 0.00 76.19
Cecropia 13.67 6.15 57.50 0.00
Ficus 5.86 1.54 30.00 0.00
Vismia 4.30 5.64 0.00 0.00
Cyclanthaceae 3.91 5.13 0.00 0.00
Banara 3.91 5.13 0.00 0.00
Others 7.81 7.69 7.50 9.52
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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-
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 5
Parolin et al. 2016; Castaño et al. 2018; Sánchez and Giannini fruits than C. perspicillata in a forest of Costa Rica, although
2018). At the species level, although the fruits in the diet of both fed predominantly on Piper fruits. Artibeus gnomus, a
C. benkeithi were a complete subset of those of C. perspicillata small-bodied species within its genus, mainly consumes fruits
It has been suggested that historical factors have influenced Literature Cited
the dietary diversification of Neotropical frugivorous bats, de- Alviz, Á., and J. A. Pérez-Torres. 2020. Difference between sexes:
termining the trophic structure of their assemblages; however,
Díaz, M. M., L. F. Aguirre, and R. M. Bárquez. 2011. Clave de Kalko, E. K. V., and C. O. Handley. 2001. Neotropical bats in the
identificación de los murciélagos del cono sur de Sudamérica. canopy: diversity, community structure, and implications for con-
Centro de Estudios en Biología Teórica y Aplicada. Cochabamba, servation. Plant Ecology 153:319–333.
Olaya-Rodríguez, M. H., J. Pérez-Torres, and M. C. Londoño- mammals in research and education. Journal of Mammalogy
Murcia. 2019. Use of forest strata by bats according to wing mor- 97:663–688.
phology and habitat complexity in a fragment of tropical dry forest Straube, F. C., and G. V. Bianconi. 2002. Sobre a grandeza e a
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.:
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