Acta Chiropterologica, 5(2): xxx–xxx, 2003
PL ISSN 1508-1109 © Museum and Institute of Zoology PAS
SHORT NOTES
First description of a tent used by Platyrrhinus helleri
(Chiroptera: Phyllostomidae)
JOSE G. TELLO and PAUL M. VELAZCO
Department of Zoology, The Field Museum, Chicago, IL 60605 and Department of Biological Sciences,
University of Illinois at Chicago, Chicago, IL 60607, USA, E-mail of JGT: [email protected]
Key words: Manu, Peru, roost, tent, Platyrrhinus helleri, Eirmocephala megaphylla
White-lined Fruit bats of the genus
Platyrrhinus
Saussure
(Chiroptera:
Phyllostomidae) are found from southern
Mexico south to southeastern Peru, Bolivia,
Paraguay, Uruguay, and southern Brazil,
where they live in mature and disturbed
lowland rainforest, gardens, clearings and
plantations, cloud forest, deciduous forest
and Caatinga (Sanborn, 1955; Emmons and
Feer, 1999). Ten species are commonly recognized in Platyrrhinus (Nowak, 1999), although a recent study has suggested that this
number is an underestimate (Velazco,
2002).
Heller’s broad-nosed bat, Platyrrhinus
helleri Peters is the most common and
widespread Platyrrhinus species (Nowak,
1999). This species ranges from southern
Mexico southward to Central America, and
South America to Peru, Bolivia, and
Amazonian and Central Brazil, and
Trinidad (Ferrell and Wilson, 1991).
Platyrrhinus bats roost in caves or tunnels, culverts or under bridges, foliage or
under branches, hollow trees, buildings, and
under large leaves or palm fronds (Tuttle,
1976; Willig and Hollander, 1987; Ferrell
and Wilson, 1991; Albuja, 1999; Nowak,
1999). Peracchi and Albuquerque (1971)
observed smaller groups of P. lineatus
roosting under leaves of the palm, Livistona oliviformis (Arecaceae), and larger
groups roosting under Syagrus picrophylla
(Arecaceae) leaves. Taddei (1973) observed
eight individuals roosting beneath a Dracaena (Agavaceae) (approximately 3 m in
height), and two individuals in a bromeliad
(Bromeliaceae) 12 m off the ground. In
Trinidad, Goodwin and Greenhall (1961)
reported one individual of P. helleri roosting
in a hollow olivier tree (Chuncoa obovata,
Combretaceae) in association with Saccopteryx leptura Schreber, Micronycteris megalotis Gray, M. minuta Gervais, and
Carollia perspicillata Linnaeus. They also
reported two individuals roosting under
leaves of the carat palm (Sabal glaucensens,
Arecaceae).
No detailed descriptions of the roosts
have ever been published for any Platyrrhinus species. In this study we present
the first description of the tent of P. helleri
in an undisturbed lowland wet forest at
Cocha Cashu Biological Station (11°54’S,
2
Short Notes
Fig. 1. (A) Conical tent of Platyrrhinus helleri in an Eirmocephala megaphylla shrub. (B) Three adult
males of P. helleri roosting in the tent
71°18’W), elevation ca. 400 m, Manu
National Park, Department of Madre de
Dios, southeastern Peru. Mean temperature
at the station is 23° to 24°C, and rainfall averages about 2000 mm annually (Terborgh
et al., 1990). Rainfall is concentrated during
a 5-mo rainy season extending from late
November to early May. On average, less
than 100 mm of rain falls monthly during
the dry season. More complete descriptions
of the area and its ecology are presented by
Terborgh (1983), Foster et al. (1986), and
Gentry and Terborgh (1990).
Bat tent observations were made from
12 August to 16 September 1994 during
a study on diurnal vertebrates using Ficus
spp. (Moraceae) at Cocha Cashu. On 12
August 1994, JGT found three adult males
of P. helleri roosting (Fig. 1A) in a tent
of Eirmocephala megaphylla (Asteraceae:
Short Notes
Vernonieae). The bats were captured,
weighed (13.5, 14.0, and 15.5 g), and then
released. The shrub was located in terra
firme forest near a fruiting Ficus pertusa
sensu lato tree. On 12 August two tents
were found in the same plant, but only one
of them was being used by bats as a diurnal
roosting place. That tent was used by these
bats for at least 35 days, when the observations ended. A third tent was built on 15
August in an adjacent shrub of the same
species approximately 10 m from the previous one. These observations strongly suggest that P. helleri was the actual tent
builder.
The tent architecture was ‘conical’, as
described by Kunz et al. (1994; see Fig.
1B). The tents were formed by the leaves
drooping downward after severe damage to
the midrib caused by the bats chewing on
it; the fallen tip forms a conical-shaped enclosure under which the bats roost. Bats
severed the midrib near the base of the petiole (approximately 3 cm), and no damage
was observed on the leaf surface. The main
tent was located at the tip of one of the
stems of the 2.40 m-height Eirmocephala
shrub. This tent was formed by 15 leaves
that formed the sides of the tent, with the
following dimensions (in cm): roost height
= 240, tent length = 49, diameter of tent entrance = 49. The second tent, located in the
same shrub, was formed by 11 leaves, with
the following dimensions (in cm): roost
height = 195, tent length = 50, diameter of
tent entrance = 37.5. The third tent, located
in a 2.44 m-height Eirmocephala shrub, was
formed by 12 leaves, with the following dimensions (in cm): roost height = 244, tent
length = 50, diameter of tent entrance =
23.2.
This study constitutes the first description of the tent of P. helleri. It also constitutes the first record of phyllostomid bats
using a plant species in the family
Compositae. Among Microchiroptera, only
3
the phyllostomid bat Uroderma bilobatum
Peters is known to construct conical tents
(Kunz et al., 1994). Convergently, conical
tents have also been reported for the
Megachiropteran bat, Cynopterus brachyotis Müller (Kunz et al., 1994). The general
architecture of conical tents among these
three species does not differ greatly, which
may be explained by the overall similarities
in leaf shape (elliptical) and leaf distribution
(radial and alternate) of the plants used by
them to build their tents. At least 15 species
of phyllostomid bats have been reported to
modify leaves of plants to construct tents as
roosts (Kunz et al., 1994). With the exception of one species, the Carolliinae bat Rhinophylla pumilio Peters, all the reported
species belong to the subfamily
Stenodermatinae (Kunz et al., 1994). Kunz
et al. (1994) assignment of R. pumilio as a
tent-maker was based on CharlesDominique (1993) report on tent-use by this
species. However, Charles-Dominique
(1993) concluded that R. pumilio might not
be the tent-builder, but rather using tents already built by other species of bats.
Occupancy of tent roosts built by other
species might not be infrequent, as has been
reported by Simmons and Voss (1998) who
found individuals of R. pumilio using tents
previously occupied by Ectophylla macconnellii Thomas. This finding suggests
that tent building in Microchiroptera has
evolved only once in the Phyllostomidae (in
the subfamily Stenodermatinae) and not
twice as previously thought.
Dermanura Gervais and Uroderma Peters, two genera close related to Platyrrhinus, are known to build up to seven different types of tents (Kunz et al., 1994), and it
may be that, Platyrrhinus has the same ability to build different tent types as these other genera. Further studies searching for
roosting sites in this, and other species, are
necessary to understand roosting site preferences and roosting behavior in general.
4
Short Notes
ACKNOWLEDGEMENTS
Thanks to the Instituto Nacional de Recursos
Naturales (INRENA) for facilitating JGT permits to
work in Manu National Park. JGT’s fieldwork was
possible thanks to grants from the International
Center of Tropical Ecology at the University of
Missouri-St. Louis (UMSL) and World Wildlife Fund
through J. Terborgh. Thanks to P. Nuñez and J. Pruski
for assistance with plant identification. We also thank
B. D. Patterson, E. Davion and D. Willard for useful
comments on improving this manuscript. J. Blake, B.
Loiselle, J. Perez, S. Brugada, and E. Joern supplied
support and hospitality to JGT during his years at
UMSL.
LITERATURE CITED
ALBUJA, L. 1999. Murciélagos del Ecuador. Escuela
Politécnica Nacional, Quito, ii+288 pp.
CHARLES-DOMINIQUE, P. 1993. Tent-use by the bat
Rhinophylla pumilio (Phyllostomidae: Carolliinae) in French Guiana. Biotropica 25: 111–116.
EMMONS, L. H., and F. FEER. 1999. Neotropical
Rainforest Mammals: a field guide. University of
Chicago Press, Chicago, Illinois, xvi + 307 pp.
FERREL, C. S., and D. E. WILSON. 1991. Platyrrhinus
helleri. Mammalian Species, 373: 1–5.
FOSTER, R., J. ARCE, and T. S. WACHTER. 1986.
Dispersal and sequential plant communities in
Amazonian Peru flood plain. Pp. 357–370, in
Frugivores and seed dispersal (A. ESTRADA and
T. H. FLEMING, eds.). Dr. W. Junk Publishers,
Dordrechht, The Netherlands, xiii + 392 pp.
GENTRY, A. H., and J. TERBORGH. 1990. Composition
and dynamics of the Cocha Cashu “mature” flood
plain forest. Pp. 542–564, in Four Neotropical
rainforests (A. H. GENTRY, ed.). Yale University
Press, New Haven, Connecticut, xiii + 627 pp.
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: 187–302.
KUNZ, T. M., M. S. FUJITA, A. P. BROOKE, and G. F.
MCCRACKEN. 1994. Convergence in tent architecture and tent-making behavior among Neotropical and Paleotropical bats. Journal of
Mammalian Evolution, 2: 57–78.
NOWAK, R. M. 1999. Walker’s Mammals of the
World, Sixth edition, Vol. 1. The John Hopkins
University Press, Baltimore, 836 pp.
PERACCHI, A. L., and S. T. DE ALBUQUERQUE. 1971.
Lista provisoria dos quirópteros dos estados do
Rio de Janeiro e Guanabara, Brasil (Mammalia,
Chiroptera). Revista Brasileira de Biologia, 31:
405–413.
SANBORN, C. C. 1955. Remarks on the bats of the
genus Vampyrops. Fieldiana (Zoology), 37:
403–413.
SIMMONS, N. B., and R. S. VOSS. 1998. The mammals
of Paracou, French Guiana: a Neotropical lowland rainforest fauna. Part I. Bats. Bulletin of the
American Museum of Natural History, 237:
1–219.
TADDEI, V. A. 1973. Phyllostomidae da Região Norteoccidental do Estado de Sao Paulo. Ph.D. Thesis,
Universidade Estadual Paulista de Sao Jose do
Rio Preto, Sao Paulo, 249 pp.
TERBORGH, J. 1983. Five new world primates.
Princeton University Press, Princeton, 260 pp.
TERBORGH, J., S. ROBINSON, T. PARKER III, C. MUNN,
and N. PIERPONT. 1990. Structure and organization of an Amazonian forest bird community.
Ecological Monographs, 60: 213–238.
TUTTLE, M. D. 1976. Collecting techniques. Pp.
71–88, in Biology of bats of the New World family Phyllostomidae. Part I (R. J. BAKER, J. K.
JONES, JR., and D. C. CARTER, eds.). Special
Publications, The Museum, Texas Tech
University, 10: 1–218.
VELAZCO, P. M. 2002. Análisis filogenético del
género Platyrrhinus (Chiroptera: Phyllostomidae). M.Sci Thesis, Universidad Nacional
Mayor de San Marcos, Lima, xii + 129 pp.
WILLIG, M. R. and R. R. HOLLANDER. 1987.
Vampyrops lineatus. Mammalian Species, 275:
1–4.
Received 06 January 2003, accepted 30 April 2003
Short Notes
5
Leaf modifying behavior in Artibeus lituratus
MARIANA MUÑOZ-ROMO1, 2 and EMILIO A. HERRERA1
1Departamento
de Estudios Ambientales, Universidad Simón Bolívar, Apartado 89.000,
Caracas 1080-A, Venezuela
2
Grupo de Ecología Animal B, Departamento de Biología, Universidad de Los Andes, Apartado 786,
Mérida, Estado Mérida, Venezuela; E-mail: [email protected]
Key words: Artibeus lituratus, leaf modification, tent-making behavior, roosts, Venezuela
INTRODUCTION
Fourteen species of Neotropical and
four species of Paleotropical bats are
throught to construct tents, by modifying
large leaves and other plant parts in order
to use them as diurnal roosts (Kunz and
McCracken, 1996). These authors argue
that the kinds of cuts on palm leaves and the
architecture of the resulting tent are determined more by the general shape of the leaf
than by the behavior of the bat species
thought to be responsible for the construction of the tent. There is increasing evidence
that some tent-making bats tend to have
polygynous mating systems (Brooke, 1990;
Kunz and McCracken 1996; Tan et al.,
1997; Storz et al., 2000; reviewed in Kunz
and Lumsden, 2003).
Kunz and McCracken (1996) have suggested that tent making may be the result
of nocturnal activity by a single male. Once
a tent is completed, other females join the
male and a harem is established (Kunz,
1994; Kunz and McCracken, 1996; Tan et
al., 1997). The male defends the tent he has
built, and, as females join him, he also defends them (Balasingh et al., 1995). A significant number of cases of apparent resource defense polygyny in frugivorous,
tent-making species from Central and South
America, all in the phyllostomid subfamily
Stenodermatinae (Timm and Mortimer
1976; Timm 1987; Brooke 1990; Kunz
1994; Kunz and McCracken 1996; Stoner
2000). Females seem to depend on the male
to find a roost and this may have conditioned the establishment of harems, because
the result is always an association between
a group of females with a male who displays defensive behavior (Kunz and McCracken, 1996). In this report, we describe a
new example of leaf modification, rather
than tent making, in the big fruit-eating bat,
Artibeus lituratus.
MATHERIALS AND METHODS
During a study of social behavior (Muñoz-Romo,
2003), two groups of A. lituratus were found roosting
beneath leaves of the palm Washingtonia sp. in a residential area in Mérida (08°36’N, 71°11’W, 1400 m
a.s.l.), Venezuela, in 2001. The trees were planted in
a row along the sidewalk, at approximately 2 meter
intervals. The trees were 12 m tall and the leaves were
about 130 cm wide and 90 cm long. One colony was
located in a tree at eight meters and the other at 6 m
above the ground.
On 27 July 2001, using a mechanical ladder, six
animals from one group (1 ; and 5 ::) were captured and three from the other (1 ;and 2 ::). An
estimated five more bats were present in the groups
on that day but were not captured; others joined later
during the observation period so the total number of
males confirmed to be regular attendants at the locality was three, while the number of females varied between one and 13th. All captured bats were measured,
weighed, and a colored, individually numbered tag
(Gey Band & Tag Co, Norristown, PA; style 374, size
4) was placed on the left (;;) and right (::) forearms. During the months of November-2001 to
January-2002, roosting bats were observed for 11
nights from 19:30 to 00:30 h using a video camera
(Sony DCR-TRV 110P) and an infrared light source
(Sony HVL-IRC). Fifty-five hours of video were
recorded. These were later observed and analyzed
6
Short Notes
using scan sampling and focal animal sampling methods (Martin and Bateson, 1993), noting all behavior
patterns observed. On sixty-four occasions the groups
were also observed during the day, using 10 × 25
binoculars.
RESULTS
During the three months of observation,
leaf modifying behavior was recorded
six times, and on each occasion it was
a male. During the recording period
(19:30–00:30), tent modification behavior
was observed between 20:00 and 22:00 h
four times by male A and twice by male B.
On one occasion male A was observed perforating the leaf from which he was hanging
on three different times. The general pattern
observed in both males was as follows.
Several times each night, a male would
return to the palm tree to feed on the fruits
that were brought back from a foraging
bout. As the male hung from the leaf, he
was observed perforating the leaf from
which he was hanging. To accomplish this,
the male appeared to firmly fix his thumbs
to the veins of the leaf before proceeding
to bite at it. As he shut his mouth to apply
the bite, he moved his head from side
to side, apparently to make sure the leaf was
perforated. On five of six occasions,
the behavior lasted a short time (18 ± 14 s),
but once, male A spent 220 seconds biting
at the leaf. The perforated leaf did not appear different from an intact leaf, except for
the roughly circular or ellipsoidal array of
holes (about 2 mm diameter) around
the center of the leaf near the rachis, and apparently avoiding the veins (Fig. 1). The
pattern of perforations can be described
as pleurocostal-elliposidal on the medial region of the lamina. We propose the term
‘aggregate ellipsoidal’ for the perforation
pattern observed (Fig. 1). We did not
observe perforations near the edges of
the leaves: always close to the medial section.
DISCUSSION
This is the first report of leaf modification by A. lituratus. We prefer the term “leaf
modification” in this case, as opposed to
“tent making” because the leaf did not
change shape as a result of the bats' behavior. However, we believe this is a deliberate
action on the part of a male A. lituratus and
he appears to modify the leaf for a ‘purpose’. The purpose seems to be to produce
a number of points from which females can
attach themselves more securely to the leaf.
During the day, strong winds can badly
shake the leaf, and if the animals are not securely attached to it, they could fall off.
Perhaps the perforations, which do not conform to any of the patterns described by
Kunz et al. (1994) for tent making bats
(conical, palmate umbrella, pinnate, apical,
bifid, boat, paradox, stem), also allow for a
certain amount of air circulation on hot
days.
It is noteworthy that the leaves do not
appear withered around the edges of perforations and the male clearly makes the holes
on the flat portion of the leaf rather than on
the veins, which presumably keeps the leaf
healthy, and therefore the roost can last
longer, as Kunz and McCracken (1996) and
Cholewa et al. (2001) have pointed out.
Since palms are extremely slow growing
trees and leaves are not often renewed
(Stoner, 2000), it becomes even more important to maintain a roost in good shape.
This is also the first report of a direct observation of a bat modifying a leaf, and it allows us to confirm that it is the male who
performs the behavior. Although we cannot
rule out the possibility that females also participate (Kunz and McCracken, 1996) in the
modification of leaves (especially between
00:30–06:30), the fact that we only observed this behavior at night (the only behaviors observed in daytime were grooming, sleeping, change of position, shaking,
Short Notes
stretch the wings, etc.) and that the males
were the only ones ever to be observed returning to the roost at night, suggests very
strongly that it is only males who perform
this activity. This is consistent with observations reported for the Old World mega-
7
chiropteran, Cynopterus sphinx (Balasingh
et al., 1995).
The fact that only males were observed
modifying the leaf also suggests that the
kind of polygyny observed in this species
could be associated with resource defense
Fig. 1. Illustration of the perforation produced by a male of Artibeus lituratus on a palm leaf (Washingtonia sp.)
(Drawing by Iván Akirov R.)
Short Notes
(Kunz and McCracken, 1996). This is further corroborated by the observation of
male A shaking his wings from side to side
when an unmarked male flew close to his
roost, apparently to drive the intruder away,
on one night when he was unaccompanied.
Tent making, or more generally, leaf
modifying behavior seems to be limited to
small bat species, because heavy bats cannot be supported by leaves (Kunz et al.,
1994). The latter authors point out that
the Neotropical tent-making bats weigh between 5 and 50 g, and the heaviest species
belongs to the megachiropteran genus Cynopterus, weighing in at 60 g. With an adult
body mass averaging 70 g (;;: 63 g and
::: 76 g; Davis, 1984), A. lituratus is the
heaviest leaf-modifying bat thus far described.
ACKNOWLEDGEMENTS
We are grateful to Dr. Thomas H. Kunz for many
helpful suggestions and corrections which improved
the manuscript. We also wish to thank an anonymous
reviewer for comments on the manuscript. Illustration
were skillfully rendered by Iván Akirov and digitalized by J. F. Burgos. This research was partially supported by Convenio de Postgrados Integrados en
Ecología (FONACIT).
LITERATURE CITED
BALASINGH, J., J. KOILRAJ, and T. H. KUNZ. 1995.
Tent construction by the short-nosed fruit bat,
Cynopterus sphinx (Chiroptera: Pteropodidae) in
southern India. Ethology, 100: 210–229.
BROOKE, A. P. 1990. Tent selection, roosting ecology
and social organization of the tent-making bat,
Ectophylla alba, in Costa Rica. Journal of Zoology (London), 221: 11–19.
CHOLEWA, E., M. J. VONHOF, S. BOUCHARD, C. A.
PETERSON, and M. B. FENTON. 2001. The pathways of water movement in leaves modified into
tents by bats. Biological Journal of the Linnean
Society, 72: 179–191.
8
DAVIS, W. B. 1984. Review of the large fruit-eating
bats of the Artibeus ‘lituratus’ complex (Chiroptera: Phyllostomidae) in middle America.
Occasional Papers The Museum Texas Tech University, Lubbock, (93): 1–16.
KUNZ, T. H. 1994. The world of tent-making bats.
Bats, 12: 6–12.
KUNZ, T. H., and L. F. LUMSDEN. 2003. Ecology of
cavity and foliage roosting bats. Pp. 3–89, in Bat
ecology (T. H. KUNZ and M. B. FENTON, eds.).
University of Chicago Press, Chicago, 779 pp.
KUNZ, T. H., and G. F. MCCRACKEN. 1996. Tents and
harems: apparent defence of foliage roost by tentmaking bats. Journal of Tropical Ecology, 12:
121–137.
KUNZ, T. H., M. S. FUJITA, A. P. BROOKE, and G. F.
MCCRACKEN. 1994. Convergence in tent architecture and tent-making behavior among neotropical and paleotropical bats. Journal of Mammalian Evolution, 2: 57–78.
MARTIN, P., and P. BATESON. 1993. Measuring behaviour: an introductory guide. 2nd ed. Cambridge
University Press, Cambridge, 222 pp.
MUÑOZ-ROMO, M. 2003. Comportamiento y estructura social en agrupaciones de Artibeus lituratus.
M.Sci. Thesis, Universidad Simón Bolívar, Caracas, 91 pp.
STONER, K. E. 2000. Leaf selction by the tent-making
bat Artibeus watsoni in Asterogyne martiana
palms in southwestern Costa Rica. Journal of
Tropical Ecology, 16: 151–157.
STORZ, J. F., H. R. BHAT, and T. H. KUNZ. 2000. Social
structure of a polygynous tent-making bat,
Cynopterus sphinx (Megachiroptera). Journal of
Zoology (London), 251: 151–165.
TAN, K. H., A. ZUBAID, and T. H. KUNZ. 1997. Tent
construction and social organization in Cynopterus brachyotis (Muller) (Chiroptera: Pteropodidae) in Peninsular Malaysia. Journal of Natural
History, 31: 1605–1621.
TIMM, R. M. 1987. Tent construction by bats of the
genera Artibeus and Uroderma. Pp. 187–212, in
Studies in Neotropical mammalogy: essays in
honor of Philip Hershkovitz (B. D. PATTERSON
and R. M. TIMM, eds.). Fieldiana: Zoology (N.S.),
39: 1–506.
TIMM, R. M. and, J. MORTIMER. 1976. Selection of
roost sites by Honduran white bats, Ectophylla
alba (Chiroptera: Phyllostomidae). Ecology, 57:
385–389.
Received xx.yy 200c, accepted aa.bb 200c