Investigation of Roosting Habitat of Art;beus watson; and Vampyressa nymphaea in Costa Rica An Honors Thesis (Honors 499)
Julia A. Nawrocki
Timothy C. Carter
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In the spring of 20 11, I travelled down to Costa Rica for a semester study abroad
program. I had chosen to go to Costa Rica because not only is it a beautiful country but it
is also home to a plethora of unique species. This level of diversity can be seen in the
approximately 113 species of bats, compared to only 45 species in the United States.
One group of bats particularly caught my attention. There are only twenty-two bat species
that demonstrate the distinct behavior of modifying leaves to create tents in which to
roost (known as tent-making bats). Knowledge of this behavior and preferences of tent­
making species is poorly understood, yet crucial to the protection and understanding of
species. The objective of this study was to examine the habitat surrounding the tent
roosts of Vampyressa nymphaea (Big Yellow-eared bat) in Potalia turbinata plants and
of Artibeus watsoni (Thomas' Fruit-eating bat) in Asterogyne plants and to uncover any
preferences these species might have. Asterogyne and Potalia plants with and without
bat tents were located within Tirimbina Biological Reserve, Heredia, Costa Rica. Habitat
measurements were taken on each plant and the surrounding vegetation. Vampyressa
nymphaea showed the most selective preference for the height of the plant and the
distance to the closest tree. Artibeus watsoni displayed a preference towards height of the
plant and canopy cover. Because bats have a highly sensitive and selective attitude
towards their habitat, these results may have direct implications on conservation efforts in
the tropics.
1
Acknowledgements
I would like to thank my Ball State University advisor Dr. Timothy Carter for all
of his support and advice throughout this project. He has helped me not only complete
this project but has also guided me well throughout the past four years. I would also like
to thank my field advisor Dr. Bernal Rodriguez-Herrera, who helped with the
development and execution of this project in Costa Rica. Emmanuel Pequeno also served
as a big help with the daunting task of identifying tropical plants and data collection. I
would also like to thank Mark Pyron and Stephen Jacquemin for their assistance and
allowing me to learn from their vast knowledge of multivariate statistics. Michael Whitby
also assisted with statistics and read through many drafts to help me edit this work.
Lastly I would like to thank my family and friends that have been so supportive
and encouraging during the pursuit of my education especially Charlene, Daniel, Nate,
and Giovanna.
2
Table of Contents
Author's Statement ................................................................................ 4 Part 1: Literature Review ...................................................................... 6 Figures ................................................................... 11 Part 2: Manuscript for Publication ...................................................... 13 Abstract ..................................................................................... 14 Keywords .................................................................................. 14 Introduction ............................................................................... 15 Materials and Methods ............................................. 17 ResuJts ................................................................ 18 Discussion ................................................................................. 19 Acknowledgements ................................................................... 21 Literature Cited ......................................................................... 22 Tables and Figures .................................................................... 24 3
Author's Statement
I chose this project on tent-making bats because I thought I would fully utilize my
study abroad experience by conducting research in the tropics, which is a biological
haven. Costa Rica is famous for its vast amount of biodiversity and the idea that there are
around 113 species of bats in that tiny country is simply outstanding (compared to 45
species in all of the U.S.A.). I was already somewhat familiar with bats, as I have been
working with North American species for about two or three years, but the bats in Costa
Rica are so different. One of the most attractive factors about them is how little we know
about many of the species. There are so many questions that could be asked and
examined. I chose to conduct a study on two species of tent-making bats that occur in
Costa Rica mostly due to availability of resources and time restraints.
The two species, Thomas' fruit-eating bat and the Big yellow-eared bat, are
among 22 other species that are known to modify foliage into roosts. This means that
these bats actively chew on the leaves of live plants, so that they fold down into a type of
tent that provides a protect structure where the bats spend their days. They are often able
to do this without killing the leaf so that roosts can be maintained for an extended period
of time. In simple terms, my project examines the idea of whether or not the different
species of tent-making bats select sites to roost based upon the various measured habitat
components or if the sites are simply randorrtly selected based upon availability. These
often are not differences between individuals, but instead species level preferences. This
information is important to understanding the life history of each species and providing
information to properly manage them. Many of the private tropical reserves actively
manage for wildlife species by selective cutting vegetation. The information from this
4
study could also be used for educational purposes to make visitors to the reserves more
informed about things that they encounter on the trails.
Along with providing valuable knowledge to the scientific community, I also
gained a lot of personal experience from the situation. I learned to work in a climate very
different from what I call home and soon discovered you can't take "rain days" in a
rainforest or everyday would be one. I found out that wearing large rubber boots not only
keeps your feet dry but also acts as an extra layer of protection if you ever were to step on
the plentiful snakes that I commonly encountered. I learned to work with other biologists
who knew a lot about tropical ecology of bats and plants. All of my research took place
at the Tirimbina Biological Reserve in the Heredia Province of Costa Rica and because
this is a hotspot for research, I got to directly interact with many other biologist and
researchers from various parts of the world. One of the toughest parts of conducting this
project was working with my field assistant who spoke no English whatsoever. He
would be trying to explain the complex characteristics of some tropical plant and I would
have to keep saying, "GQue? Repita mas lento por favor?" (translation: "What? Could
you repeat that slower please?") I am sure it was frustrating at times for him as well but
we worked through it and became good friends. This experience has opened my eyes to
all the benefits, as well as challenges, that one faces when attempting to conduct
international research. And I will definitely consider undertaking international research
in the future.
5
Part 1: Literature Review
6
Costa Rica is a small country located in the Neotropical region of Central
America and is bordered by Panama, Nicaragua, as well as, the Atlantic and Pacific
Oceans. Within this small country there is an incredible amount of biodiversity. In an
area of only 52,100 km2 (0.00035% of the world), Costa Rica has representatives of
about 40/0 of the total species estimated worldwide (National Biodiversity Institute, 2012).
Tirimbina Biological Reserve is located in the northeastern Caribbean lowlands
of Costa Rica in the Heredia province. It boundaries encompasses approximately 345 ha
of forest and a large section of the Sarapiqui River. It was declared a Wildlife Refuge in
2001 and is part of the San Juan- La Selva Biological Corridor. The main objectives of
Tirimbina Biological Reserve and Rainforest Center are to conserve the ecosystems and
maintain biodiversity, to promote scientific research, ecotourism, and provide educational
programs to the comnlunity (Tirimbina Biological Reserve, 2010). More than 300
species of birds, 65 species ofherptiles, and 89 species of mammals (with 59 of those
being species of bats) have been documented on the reserve (Tirimbina Biological
Reserve, 2010).
Bats make up approximately one-fifth of all mammal species with over 1,200
species (Bat Conservation International, 2012). Bats exhibit an incredible amount of
diversity that includes all different sizes from a 2 gram Microchiropteran to a 1,500 gram
Megachiropteran, various morphological adaptations including elaborate facial
ornamentation, and inhabit most areas of the planet (Altringham, 1996; Bat Conservation
International, 2012; Feldhamer et aI., 2007; Nowak, 1994). The group contains
frugivores, nectivores, insectivores, and carnivores (Altringham, 1996; Nowak, 1994;
Feldhamer et aI., 2007). They also exhibit a variety of roosting behaviors that include
7
roosting in tree cavities, abandoned bird nests, foliage, caves, and actually modifying
plants to construct tent-like structures (Altringham, 1996; Kunz and Lumsden, 2003;
Nowak, 1994).
Roosting sites are important locations for bats because they are often sites for
protection, mating, raising young, and can often facilitate social interactions between
individuals. They also play vital roles in microclimate regulation, energy conservations,
and minimize risks of predation (Kunz and Lumsden, 2003). Roosting habits of bats can
be influenced by such factors as availability of roosts, abundance and location of food
sources, and energy regulation dictated by body size and external environmental factors
(Altringham, 1996; Kunz and Lumsden, 2003).
Tent-making bats were first discovered in 1932 in Panama by Thomas Barbour, a
naturalist from Harvard University's Museum of Comparative Zoology (Barbour, 1932.)
In that same year, a naturalist from the American Museum of Natural History named
Frank Chapman made similar observations and coined them tents because he found them
to resemble the tents made by people (Chapman, 1932.) These tents are energetically
expensive to construct and therefore must yield benefits to the individual bats. It has
been suggested that tents play important roles in microclimate regulation, protection
against rain, wind and sun, predator avoidance, parasite avoidance, and sexual selection
(Altringham, 1996; Kunz and Lumsden, 2003; Nowak, 1994; Rodriguez-Herrera et aI.,
2007)
There are multiple different architectural styles of tents; however they are
ultimately constructed in a similar manner. The bat selects a large, broad leaf and chews
through the veins of the midrib causing the leaf to collapse over itself, making a "tent"
8
for the bat to roost under (Altringham, 1996). The different styles of tents include
conical, bifid, pinnate, umbrella, apical, boat, and boat/apical (Rodriguez-Herrera et aI.,
2007). These variations are differentiated by the number of leaves involved, where the
cuts are located, the shape of the leaf, and the shape of the cuts made by the bat
(Rodriguez-Herrera et aI., 2007). Some tents may be constructed overnight while others
may take days to construct. Still little is known about which individuals construct the
tents, for example do males strictly build the tents to attract females? It is also unknown
whether all bats found in tent roosts were involved in the construction of the roosts or if
they simply moved into a vacant tent (Rodriguez-Herrera et aI., 2007; Kunz and
Lumsden, 2003).
The two species of bats examined in this study were Artibeus watsoni and
Vampyressa nymphaea. A. watsoni is a frugivourous bat that occurs in Mexico, Central
America, and Columbia. In Costa Rica, it is a fairly common bat and has been found to
use 41 different species of plants and construct five different architectural styles of tents
(Rodriguez-Herrera et aI., 2007). It is also known that A. watsoni will use tents
constructed by other species of bats, such as Ectophylla alba (Rodriguez-Herrera et al.,
2007). In this study A. watsoni was examined in its relationship with Asterogyne spp.
plants, where it builds bifid style tents (Figure 1). V nymphaea is also a frugivorous bat.
It is more rare than A. watsoni and little is known about its feeding behavior, roost sites,
and social system. It often builds umbrella style tents in palm-like species, such as
Potalia turbinata (Figure 2). Because it is often difficult and time consuming to directly
capture these bats, plants are often examined to detennine presence or absence.
Literature Cited
9
ALTRINGHAM, J. D. 1996. Bats Biology and Behavior. Oxford University Press Inc. New
York, New York, USA.
BARBOUR, T. 1932. A peculiar roosting habit of bats. Quarterly Review of Biology,
7:307-312.
BATCONSERVATION INTERNATIONAL. 2012 All about bats.
<www.batcon.orglindex.php/all-about-bats.html>.
CHAPMAN, F. M. 1932. A home making bat. Natural History (New York), 32:555.
FELDHAMER, G. A., L. C. DRICKAMER, S. H. VESSEY, 1. F. MERRITT AND C. KRAJEWSKI.
2007. Mammalogy. 3rd ed. The Johns Hopkins University Press, Baltimore,
Maryland, USA.
KUNZ, T. H. AND L. F. LUMSDEN. 2003. Roosting Ecology in Bat Ecology. Pp 3-89. The
University of Chicago Press. Chicago, Illinois, USA.
NATIONAL BIODIVERSITY INSTITUTE. 2012. Biodiversity in Costa Rica.
<http://www.inbio.ac.cr/enlbiodlbio_biodiver.htm>
NOWAK, R. M. 1994. Walker's Bats of the World. The Johns Hopkins University Press,
Baltimore, Maryland, USA.
RODRiGUEZ-HERRERA B., R. A. MEDELLIN, AND R. M. TIMM. 2007. Murcielagos
neotropicales que acampan en hojas. Instituto Nacional de Biodiversidad
(INBio). Costa Rica.
TIRIMBINA BIOLOGICAL RESERVE. 2010. Conservation efforts.
<http://www.tirimbina.org/conservation.html>.
10
Figure 1. Asterogyne martiana plant containing two bifid tents. Pink arrows show the
leaves involved in tent construction.
11
Figure 2. Potalia turbinata plant with an umbrella tent. The majority of the leaves are
bitten at the base and fold down forming a closed umbrella-like structure.
12
Part 2: Manuscript for Publication
*Following the guidelines of Acta Chiropter%gica
13
Roosting Micro-Habitat preferences of tent-roosting bats
Vampyressa nymphaea and Artibeus watson; in Costa Rica
Julia A. Nawrocki
Ball State University Muncie, IN 47306
janawrocki@bsu.edu
ABSTRACT
Twenty-two bat species demonstrate the distinct behavior of modifying leaves to
create tents in which to roost. Knowledge of this behavior and preferences of species that
use tents is poorly understood, yet crucial to the protection and understanding of species.
The objective of this study was to examine the habitat surrounding the tent roosts of Big
Yellow-eared bat (Vampyessa nymphaea) in Potalia turbinata plants and of Thon1as'
Fruit-eating bat (Artibeus watsoni) in Asterogyne martian a plants and uncover any
preferences these species might have. Micro-habitat measurements on Asterogyne spp.
and P. turbinata plants with and without bat tents were taken within Tirimbina Biological
Reserve, Heredia, Costa Rica. Each data set was then analyzed using individual
MANOV As to detennine if overall differences were present. Principal components
analysis was used to ordinate relationships and post hoc two sample t-tests were used to
test for differences among sites with tents and sites without tents along resulting PCA
axes. V. nymphaea showed the most selective preference for plants that were farther
away from all surrounding trees and for plants that were of greater height. A. watsoni
displayed a preference for fewer trees in the surrounding area and taller plants.
Furthennore, these bats have a similar selective attitude towards their roosting habitat,
these results may have direct implications on conservation efforts in the tropics.
14
KEy WORDS: Costa Rica, Tent-making bats, Vampyressa nymphaea, Potalia turbinata,
Artibeus watsoni, Asterogyne, roost selection, conservation
INTRODUCTION
There are more than 1100 spp of bats in the world, but currently just 22 species of
bats are known to modify the leaves of live plants to construct roosts (Chapman, 1932;
Rodriguez-Herrera et al., 2008). Tents are thought to provide protection from wind and
rain, regulate microclimate, and protection from predators (Kunz and McCracken, 1996;
Stoner,2000). These tents are temporary roosting sites and bats may change at
seemingly random intervals for both suspected and unknown reasons (Rodriguez-Herrera
et al., 2007). Chaverri and Kunz (2006) found that Artibeus watsoni tend to have low
tent fidelity and individual bats often change between roosts in the surrounding area. The
main reason for these shifts appears to be predation pressure, once flushed by a potential
predator the bat may not return to that tent for many days to weeks. It has also been
suggested that tents may also help reduce ectoparasites, when parasites are present in
roosts (Lewis, 1995).
When bats construct a new tents they may be highly selective in which habitat
they occupy. Understanding this selection can be important information from a
conservation standpoint (Kunz and Lumsden, 2003; Stoner, 2000). Important features of
tent roosts may include the physical strength of the leaves, the height of the plant, the
angle of the leaf, and proximity to food resources (Kunz and Lumsden, 2003). For
example Stoner (2000) found that, A. watsoni often selected Asterogyne martiana palms
that were taller and possessed longer leaves with thicker rachises.
15
Vampyressa nymphaea is a medium-sized frugivorous bat that occurs from
southern Nicaragua to northern Ecuador (Rodriguez-Herrera et ai., 2007). These bats
generally roost in groups of two to four, consisting of one male and multiple females
(Rodriguez-Herrera et aI., 2007; LaVal and Rodriguez-Herrera, 2002). One of the plants
that this species uses commonly is P. turbinata, a small palm-like tree only 2-3 meters in
height found throughout Costa Rica and Panama (Rodriguez-Herrera et aI., 2007).
Vampyressa nymphaea use the long leaves of P. turbinata to construct umbrella shaped
tents, in which all leaves are chewed at the base and fold downward uniformly around the
stem (Fig. 1; Rodriguez-Herrera et aI., 2007).
Artibeus watsoni occurs across central America from Veracruz, Mexico to
Columbia. A. watsoni has been recorded to use 41 species of plants to construct tents,
more than any other species (Rodriguez-Herrera et aI., 2007). They commonly use plants
from the genus Asterogyne, which contains five species in Central America and northern
South America. The plant is typically only 1-2 meters tall and has a blade length ranging
from 0.7 to 1.0 n1eters (Stoner, 2000). This species is also capable of constructing
multiple different styles of tent (Rodriguez-Herrera et aI., 2007; LaVal and Rodriguez­
Herrera, 2002), the one examined in this study was the bifid tent, in which the bat cuts a
"j-shaped" cut away from the midvein causing the leaf tips to fold down and form a
cavity below (Fig. 2; Rodriguez-Herrera et aI., 2007).
The objective of this study was to examine the micro-habitat surrounding roosts
of the Big Yellow-Eared bat (Vampyressa nymphaea) in Potalia turbinata plants and of
Thomas' Fruit-eating bat (A. watsoni) in Asterogyne martiana. plants and to discover any
16
habitat preferences the bats might have, as well as to examine similarities between bat
speCIes.
MATERIALS AND METHODS
We located Potalia turbinata and Asterogyne martiana. plants with and without
tents in the Tirimbina Biological Reserve, Heredia Province, Costa Rica from January­
April 2011. We established a 10m radius (area of 79 m 2) vegetation plot around each
plant. Within these vegetation plots, we measured (1) height of plant; (2) density of trees,
measured by counting the number of surrounding trees in the area with a diameter at
breast height (DBH) greater than 10 cm; (3) canopy cover, measured using a densiometer
(Model-A, Forestry Suppliers, Inc., Jackson, USA) to take the average of four points, one
in each cardinal direction; (4) average DBH of all surrounding trees; (5) average distance
to closest trees in which the plot was divided into four quadrants and the distances to the
closest tree in each quadrant were averaged to obtain the value; (6) understory coverage
from the ground to a height of one meter, and (7) understory coverage between 1 and 2
meters above the ground. To measure the understory coverage a set of 2 meter tall
aluminum poles, marked every 2 cm was placed vertically at the base of the plant (Fig. 1
and Fig. 2), an observer than walked 10m north, south, east and west and counted the
number of marks that were visible on the pole from the ground to 1 meter and 1 meter to
2 meters. The average from the four observations was taken as the value (Rodriguez­
Herrera et aI., 2008). Non-normal data was transformed prior to analyses using arcsin and
log transformations.
17
MANOVA was used to test for overall differences in plot habitat among plants
with tents and without tents for each species and to compare both species habitat
preferences. Subsequent t-tests were used to discern which variables were driving any
differences. Additionally, Principal Components Analyses was used to ordinate and
visualize site differences. Separate PCAs were run on the Asterogyne spp., P. turbinata,
and all vegetation plots of either species containing tents datasets. Axes with eigen
values> 1 were retained for interpretation. Post hoc two sample t-tests were used to test
for differences in habitat use ordinated on resulting PCA axes. Habitat loading values of
0.30 or higher were used to interpret and describe PCA axes (McCune and Grace 2002).
RESULTS
A total of 14 A. martiana. plots with tents and 32 without as well as 19 P.
turbinata plots with tents and 54 without tents were measured.
Asterogyne martiana.
MANOVA indicated that A. martiana. plots with tents and without tents were
different (Wilks A=0.59068; P=0.003). Asterogyne spp. plots containing tents tended to
contain fewer surrounding trees (two sample t-test; P=0.013) and had available roost sites
higher off the ground (two sample t-test; P=0.024).
PCA representing the Asterogyne spp. vegetation plots with and without tents
resulted in 3 significant axes that explained 59% of the total variation. PC 1 (Table 1)
differentiated positive loading sites consistent with higher number of trees and roost
height from negative loading sites with fewer but greater sized trees that lacked
understory growth. PC2 (Table 1) revealed positive loadings associated with larger dbh
18
of surrounding trees, higher roost sites, and greater understory growth from negative
loading sites with greater distances to the surrounding trees. PC3 (Table 1) differentiated
positive loading sites coherent with greater canopy cover and more trees with larger dbh
from negative lading sites. Post hoc two sample t tests did not indicate differences
among along PC1 or PC2 axes, however, PC3 distinguished that the number of
surrounding trees, the average DBH of surrounding trees and canopy cover was greater in
plots with tents than those without tents (P=0.049; Fig. 3; Table 1).
Potalia turbinata
MANOVA indicated that P. turbinata. plots with tents and without tents were
different (Wilks)...= 0.75106 ; P=0.014). Potalia turbinata plots containing tents tended
to have the roost site located further away from surrounding trees (two sample t-test;
P=0.010) and had available roost sites higher off the ground (two sample t-test; P=0.023).
PCA representing the Potalia turbinata vegetation plots with and without tents
were compared and resulted in 3 significant axes that explained 61 % of the total
variation. PC 1 (Table 1) differentiated positive loading sites consistent with greater
understory growth from negative loading sites with greater canopy cover. PC2 (Table 1)
revealed positive loadings associated with a greater number of surrounding trees, from
negative loading sites consistent with greater roost height, greater distance from
surrounding trees and larger average dbh of surrounding trees. PC3 (Table 1)
differentiated positive loading sites coherent with a greater roost height, further distance
from surrounding trees and more surrounding trees in the vegetation plot from negative
lading sites with a smaller average dbh of surrounding trees. Post hoc two sample t tests
19
did not indicate differences among along PC 1 axis, however, the PC2 and PC3 axes
distinguished that the number of surrounding trees, the average DBH of surrounding
trees, the distance to the nearest tree and height of the roost site was greater in plots with
tents than those without tents (P=0.014 and P=0.048, respectively; Fig. 4; Table 1).
Combined
When comparing both data sets combined, there was a difference between all
A. matiana and P. turbinata, vegetation plots there was a difference (P< 0.001) however
there was no difference detected between plant without tents (P= 0.145) and no difference
between all vegetation plots containing tents (P= 0.574).
023).
PCA representing the combined vegetation plots with and without tents were
compared and resulted in 2 significant axes that explained 600/0 of the total variation.
PC 1 (Table 1) differentiated positive loading sites consistent with higher roost sites, a
greater number of surrounding trees and greater understory growth from negative loading
sites with larger average dbh of surrounding trees. PC2 (Table 1) revealed positive
loadings associated with greater canopy cover from negative loading sites consistent with
greater roost height and a greater distance from surrounding trees. Post hoc two sample t­
tests did not indicate differences among along PCl or PC2 axes (Fig. 5; Table 1).
DISCUSSION
20
The process of selecting a site occurs at various scales; as different species of tentroosting bats are present in various areas of the forest. These two particular species are
present in the understory, leading the study to examine the micro-habitat at this level.
This study provides evidence that tent-making bats do have preferences in habitats that
they construct their tents in. It seems that at least these two tent-making bat species are
selecting for taller plants, in more open areas, with greater canopy cover.
We propose that these preferences could relate to multiple origins including predator
avoidance and microclimate regulation. The open areas around the roost may also allow
for easy entrance and exit by a flying bat, which could permit a faster entrance or escape
allowing predator avoidance to likely be a major factor. Predators of tent-making bats
include double-toothed kites (Harpagus bidentatus), red-backed squirrel monkeys
(Saimiri oerstedii), common squirrel monkeys (Saimiri sciureus), and white-faced
capuchin monkeys (Cebus capucinus; Boinski and Timm 1985). These predators sneak
up on the roosts of resting bats during the daytime. In the taller plants that occur in open
areas it may be more difficult for predators to arrlbush the bats as individuals would have
more time to escape and evade the predator if it was detected or caused a disturbance
while climbing in the tree. If the plants are in an open area, it may also force the predator
to approach from the ground giving the roosting bats a greater opportunity to spot the
predator and flee the site.
The preference for a greater amount of canopy cover could be linked to
microclimate regulation and protection from the elements. In the tropical climate, it is hot
and humid so bats may seek out a roost that is not in direct sunlight in an effort to stay
21
cooler during the day. Heavy rains are also common in this area and a greater canopy
cover would allow for more protection during heavy rainfall causing less mechanical
damage to tent roosts (Jordan and Heuveldop, 1981; Nadkami and Sumera, 2004; Tobon­
Marin, 1999).
It is also important to note that the plants without tents measured in this study
may not necessarily be unfavorable habitat, but that tent-making bats just have not yet
utilized them. This helps to explain the wide range of variation in vegetation plots not
containing any tents.
This study verifies that tent-making bats do indeed display a preference within
their habitat when selecting their roosts. We hypothesize that the remaining species of
tent-making bats in Central and South America would have similar preferences because
of similar environmental challenges. However, further studies are needed to see if our
results are applicable on a wider scale to all Neotropical tent-making bats.
Information collected from this study could lead to improving management and
conservation plans for private reserves, which actively manage for wildlife. Because it
requires time, equipment, and trained personnel to capture bats, reserves with limited
monies available for conservation could instead work on indirectly monitoring bats
species by examining properties for tents. A vegetation-focused study could even be
incorporated into ecotourism programs for educational purposes providing feedback on
the status of bat species in the area (Meyer et aI., 2010; Rodriguez-Herrera et aI., 2007).
This may influence the types of plants that are allowed to thrive and which ones can be
cut down to make trails and other recreational luxuries. Because predator pressures seem
to have a large influence on disrupting the normal activity of tent-making bats, large
22
numbers of people hiking would most likely negatively impact the bat populations in the
area. Therefore, it may be important to avoid areas where tents may occur. Trails and
activities that occur on the biological reserves should take place in restricted areas that
avoid areas that have high densities of tent-making bats.
It has also been suggested that bat diversity and abundance serves as a good
indicator for disturbance levels in the Neotropics (Medellin et aI., 2000). Tent-making
bats in this area are mostly in the family Phyllostomidae, which is a group that is not well
represented in areas with high levels of disturbance. If biological reserves want to
maintain a low level of impact to the surrounding environment, bats could be used as an
indicator to measure the levels of activity that occur on their property. Because high
numbers of bats would likely occur in undisturbed areas, the number of bat tents present
on the property could be correlated to a value of reserve efforts to regulate environmental
impacts.
ACKNOWLEDGEMENTS
I would like to thank Mark Pyron, Stephen Jacquemin, and Emmanuel Pequefio
for all of their support and assistance. I would also like to thank Tirimbina Biological
Reserve and Ball State University for access and opportunity to work on this project.
LITERATURE CITED
ALTRINGHAM, 1. D. 1996. Bats Biology and Behavior. Oxford University Press Inc. New
York, New York, USA.
BAT CONSERVATION INTERNATIONAL. 2012 All about bats.
<www.batcon.orgJindex.php/all-about-bats.html>.
BOINSKI, S. AND R. M. TIMM. 1985. Predation by squirrel monkeys and double toothed
23
kites on tent-making bats. American Journal of Primato logy, 9:121-127.
CHAPMAN, F. M. 1932. A home making bat. Natural History (New York), 32:555.
CHAVERRI, G. AND T. H. KUNZ. 2006. Roosting ecology of the tent-making bat Artibeus
watsoni (Chiroptera: Phyllostomidae) in Southwestern Costa Rica. Biotropica,
38: 77-84.
JORDAN, C. F., AND 1. HEUVELDOP. 1981. The water budget of an Amazonian rain forest.
Acta anlazonica, 11: 87-92.
KUNZ, T. H. AND L. F. LUMSDEN. 2003. Roosting Ecology in Bat Ecology. Pp 3-89. The
University of Chicago Press. Chicago, Illinois, USA.
KUNZ, T. H., AND G. F. MCCRACKEN. 1994. Tents and harems: alteration of leaves by
foliage roosting bats. Living World, 1993-1994:32-37.
LAVAL, R. K., AND B. RODRIGUEZ-HERRERA. 2002.
Murci<~lagos
de Costa Rica. Instituto
Nacional de Biodiversidad, Santo Domingo de Heredia, Costa Rica.
LEWIS, S. E. 1995. Roost fidelity of bats: a review. Journal of Mammalogy, 76: 481-496.
MEDELliN, R. A., M. EQUIHUA, AND M. A. AMIN. 2000. Bat diversity and abundance
as indicators of disturbance in neotropical rainforests. Conservation Biology,
14: 1666-1675.
MEYER,C.F.J.,L. M.S. AGUIAR, L. F. AGUIRRE,J.BAUMGARTEN, F. M. CLARKE,
J.COSSON, S. E. VILLEGAS, J. FAHR, D. FARIA, N. FUREY, M. HENRY,R.
HODGKISON,R. K.B. JENKINS, K. G. JUNG, T. KINGSTON, T. H. KUNZ,M. C.
MACSWINEYGONZALEZ,1. MOYA, J. PONS, P. A. RACEY, K. REX,E.M.
SAMPAIO, K. E. STONER, C. C. VOIGT, D. VON STADEN, C. D. WEISE, E.
K.V. KALKO. 2010. Long-term monitoring of tropical bats for anthropogenic
24
impact and gauging the statistical power to detect population change. Biological
Conservation 143:2797-2807.
NADKARNI, N. M., AND M. M. SUMERA. 2004. Old-growth forest canopy structure and its
relationship to throughfall interception. Forest Science, 50: 290-298.
NOWAK, R. M. 1994. Walker's Bats of the World. The Johns Hopkins University Press,
Baltimore, Maryland, USA.
RODRIGUEZ-HERRERA B., R. A. MEDELLIN, AND M. GAMBA-RIDS. 2008. Roosting
requirements of white tent-making bat Ectophylla alba (Chiroptera:
Phyllostomidae). Acta Chiropterologica, 10: 89-95.
RODRIGUEZ-HERRERA B., R. A. MEDELLIN, AND R. M. TIMM. 2007.
Murch~lagos
neotropicales que acampan en hojas. Instituto Nacional de Biodiversidad,
Santo Domingo de Heredia, Costa Rica.
STONER, K. E. 2000. Leaf selection by the tent-making bat Artibeus watsoni in
Asterogune martiana paln1s in south-western Costa Rica. Journal of Tropical
Ecology, 16: 151-157.
TOBON-MARIN, C. 1999. Monitoring and modeling hydrological fluxes in support of
nutrient cycling studies in Amazonian rain forest ecosystems. Tropenbos,
Wageningen, Series 17, 162 pp.
25
Figure 1. Potalia turbinata plant with an umbrella tent. The majority of the leaves are
bitten at the base and fold down forming a closed umbrella-like structure.
26
Figure 2. Asterogyne martiana plant containing two bifid tents. Pink arrows show the
leaves involved in tent construction.
27
~
U)
cu
cu cu >
2-,
M
u
CL
J
0
•
0
o·
0
•
0
aD
0
o
0
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o
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0
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•
•
0
0
0
0
0
•
•
0
•
•
o •
0
·0
0
0
•
•
0
-1
Avg DBH of Trees
Dist to Cosest Tree
Low Cover
-2
PC 1
1
~nner
Height
of Trees
2
-3~1--------------~--------------~--------------~--------------~----~
-2
-11
°1
0
0
0
28
Figure 3. Scatterplot of the two significant axes of the principal component analysis examining Asterogyne spp. plants with and
without bat tents measured throughout Tirimbina Biological Reserve in the Heredia province of Costa Rica in the months of January,
February, March and April of2011. Closed markers signify plants containing at least one tent created by bats, open markers denote
plants not currently containing a tent.
cC
~i~ 11
g'i
oo~
~~8
U)
V)
...
...,
Q.
>
...
<
>
~
c
~
::c
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...
cu
cu
t­
V)
ua..
(V')
0
I
-31
-21
-11
o~
1
2
3­
-2
0
0
.
[]
o.
0
0
-1
0
A vg DBH of Trees
Dist to Closest Tree
Height
0
00
•
0
•
0
•0
00
0
0
0
0
[]
0
0
0
o.
00
0
0
0
•
•
[]
PC 2
0
So
0
o •
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0
0
[]
101
00
1
0
~
0
0
00
0
0
0
0
0
0
0
2
3
rtJmber of Trees
0
29
Figure 4. Scatterplot of the two significant axes and primary loadings of the principal component analysis examining Potalia
turbinata plants with and without bat tents measured throughout Tirimbina Biological Reserve in the Heredia province of Costa Rica
in the months of January, February, March and April of2011. Closed markers signify plants containing at least one tent created by
bats, open markers denote plants not currently containing a tent.
C
.Wl
Z~
V)
!
8 .52'
Rfc
u a
V) "'"
CU
0
...,t-
~ ~
cucu~.c
cu
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C
0
-1•
0
-3
1
o
o
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•
o
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o
o
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•• 0
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0 0
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o
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-
o
o
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•
o
-
o
-
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4
Number of Trees
Low Cover
Mid Cover
Height
•
0
R.~ 00
~~
§ 00 Cj
Figure 5. Scatterplot of the first two principal components examining all plant groups measured throughout Tirimbina Biological
Reserve in the Heredia province of Costa Rica in the months of January, February, March and April of 2011. Circles represent
Asterogyne spp. and squares represent Potalia turbinata. Closed markers signify plants containing at least one tent created by bats,
open markers denote plants not currently containing a tent.
DBH of Trees
-4
is -3----r
(I)
....
....0
U -2-
0
~
~
~
I-
0-
1-
2­
a 3-
ua..
N
a..
cu
>
0
u 4­
>
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30
PC2
1.376
PC3*
1.104
Number of Trees
0.438 -0.173
0.413
Average DBH
-0.411
0.357
0.484
Dist. to Closest Tree -0.413 -0.380
0.121
0-lm Cover
-0.502
0.424
0.001
1-2 m Cover
0.149
0.568 -0.201
Canopy Cover
0.262
0.215
0.696
Roost Height
0.355
0.387 -0.236
*Denotes axis with significant habitat separation
among plots containing tents and those without
tents based upon a post hoc two sample t-test.
_~r.?p~t!i~~ ________ .9:.2~~ __ ~~12? __ Q.} ~~
Eigen value
PC1
1.647
Asterogyne spp.
months of January, February, March and April 2011.
PC1
1.899
0.271
0.177
0.010
-0.167
0.642
0.609
0.391
0.070
PC2*
1.217
0.174
0.386
-0.665
-0.453
-0.066
-0.148
0.064
-0.416
PC2
0.989
0.141
-0.020
-0.081
-0.822
-0.042
-0.007
0.561
-0.037
Between Tent
Types
PC3*
PC1
3.224
1.152
0.165 I 0.461
0.494
0.432
-0.307 -0.349
0.492 -0.177
-0.102
0.476
-0.157
0.509
0.312 -0.229
0.535
0.350
Potalia turbinata
around plants with and without bat tents located on the Tirimbina Biological Reserve in the Heredia province of Costa Rica in the
31
Table 1. Eigen values, proportions, and loadings for principal component analyses of each set of habitat data. All data was collected
Plants of th e target genus ASlerogy ne and Potalia
rbinata, whh and without tents, were located by visual
observation in Tirimbina Biological Reserve in Heredia
Province of Costa Rica. Plants without tents were used as
th e control. Once located a 10 m radius plot was measured
and all vegetation in the plot was evaluated for th e
followin g variables: ( I) height of target plant, (2) density of
target plant, (3) density of trees, (4) canopy cover, (5)
average DBH of all surrounding trees, (6) average distance
to closest trees, (7) understory coverage at a height below
one meter, and (8) understory coverage between 1 and 2
meters.
The most important factors for tent selection were then
determined using a principal component analysis of the
vegetation variables and two sample T-tests.
Methods
U NIVERS ITY .
BALL ST ATE Special thanks to: Emmanuel Pequeno Bernal Rodriguez Herrera Mark Pyron
~ Acknowledgements
fI (1 tr1sb S ILIlli R M T rm m 19H S. PrcJu ti on by ~qu.i flc l "' onk.-~ a nd doublc-\Ill)\hed
kites on tcnt-nmkmg bat~ A rncrim" Jauntal qll 'nf//alology 9 121-1 27
Bmukc. A P. 1'il87. Tent constructIOn a nd sO ~ J lll org<lQlafti un 111 V" lIIpr~~sflIlYll1ph""u
(Chiroptera Phy llostomidae) in Costa Ri ca. .JmJrnal ,!/liupil;{l i h '%gy 3 171­
175 .
C havcrri, G. a nd T H. KunL 2006. RoostIng ('cology of the lent-making bat Arlib~us
walsolli tC!lIfoptcra : Ph, Ilostomidae) 10 suuthwestern Costa Rica. H iolrup,.·a 38 '
77-84
r ]WI;, J,e and R M. Timm. 1985 Roostll1l.' SIte s~lec\l un by A rli bclI.\ l"'IS(",i
Chiroptcra : PhylJostomidac) on Anlh fm um rave"ii (Araccaej in Co,la Rica
Journal un ropicall..·olugy I : 241-247
Kunz T H. and G.F McCracken . 1996 Tents and harems apparent deft'nce of fo liage
roosts by tent-making bats . JO llmul ~1lroplcal 1,'cology 12 : 121 - 13 7
Rodrig uez-Herrera. B . R A Medellin, amI M Gamba-Rius . 200 R, Roosting
requirements of whit~ tent-making bat h'clup"y"" ulb" (Chiroptera :
PhylJostomldae A,,/(l Chiroplelvlogi,'a 10: 89·95
')toner. K.E ZO llO J . ~~lr selection by the tcnt-maklllg bat r4 rtib':I/ ,\ " ·,,I.wlII In l~ sl"lOgJl/Ie
/IIarliall" palms in suuthwestern Costa RIca JUI/,.,.al u( 7ivpio',,/ l ,,,olugy 16: 151­
157
References
Vampyressa nymphaea showed a selective preference
for taller Folalia plants and ones that were in an open area
further away from other trees (p=O.004). Suggested
explanations for these factors relate back to predator
avoidance. The main predators of tent making bats include
various species of snakes, monkeys, and birds of prey. The
taller plants located in open areas make it difficult for
predators to ambush the bats while in their roosts. Open
areas around the roost also allow for easy entrance and exit
by a fl ying bat.
/Jrlibeus lIIals oni di splayed a preference for taller
s/cJ"ogyne plants and towards areas with greater canopy
coverage (p=O.O 13). The difference of canopy cover here is
most likely for mi croclimate regulati on and protection from
the elements. In the tropical climate it is already hot and
humid so the bats may seek out a roost that is not in direct
slIn light in an effort to stay cool. Greater canopy cover also
allows· fo r more protection during heavy rains that are quite
common.
Th is study provides evidence that tent-making bats do
indeed display a preference when selecting their roosts. I
hypothesize that the remaining species of tent-making bats
in Central and South America would have similar
preferences, however more information about tropical bat
and plant species is needed. Information collected from
studies such as this could be used in making management
and conservation plans for private reserves such as
Tirimbina, which actively manage for wildlife.
Currently 22 species of bats are known to roost in tents
constructed of modified leaves. Knowledge of roosting
ecology in many of these bats is inadequate but it is
suspected that bats are highly selective. The benetits of a
ent are thought to include protections from elem ents of
wind and rai n, regulation of microclimate, and predator
avoidance. It has also been suggested that tents may al so
he lp reduces paras ites, since roosts can be changed often.
The understand ing of habitat preferences is crucial in
implementi ng proper management and conservation em.)rt's.
The obj ective of this study was lo eX~\'lTl i ne habitat
v ~' jal-lp5 ~urro und!l1g tent roosts
::lnd to determine any
preference that Arlib(!us (Derm anura) 'walsoni ([homas'
fruit-L:ating bat) and Vamp) ressa rf)'mp haea (striped yellow­
eared bat) have in selecting their roosts in ,-/slerogyne
0, ig.1) n.nd Pu/alia 11frbin afa (Fig.2). res p ectiv~ly .
.F igure 2. Pala lia lur binala
pl an t WIth an umbrella tent.
Results and Discussion
Introduction
5/24/2012 Investigation of Surrounding Habitat of Roosts Used by Dermanura watsoni and Vampyressa nymphaea in Costa Rica -Predator avoidance
Snakes, monkeys,
birds of prey
Julia Nawrocki Ball State University Muncie,lN • Lowland and mid-elevation humid forests
Diet consists mainly offruit
Supplemented with insects and
pollen
Tent construction
.
~~I:;:=~
' Protection from rain and sun exposure
-Knowledge of preference and related behaviors
are stilt poorly understood
• ] -2 meters tall
- Blade length ranging from 0.7 to 1.0 meters
--
~
Microhabitat regulation
~.
~4"' ..;;".,: ~.'"
..t·.... .,-....."
Five species in Central and South America are common ly used by Demanura watsoni Bifid Tent five different styles
Chaverri and Kunz (2006) suggested th at males are the
primary constructors
Uses 4 I species of plants
• Distributed from southeastern Nicaragua to
western Columbia
Diet consists of mainly fruit
Brooke (1987)* found that
V nymphae a uses a harem mating
system
,~."
• Found only in Costa Rica
and Panama
• Umbrella tent
'eN~l"_&$j~l or"""'i(._ I'
,
••
1111
......~~ItWIIN\.8IHI(~.'· t'fI~~ .. lD:.tJo
,
'
1
5/24/2012 • To examine possible characteristics that
influence the bat to choose specific plants to
use for roosts
• Each species was examined separately
• Vegetation in surrounding LO m circle
was measured for the follow ing
variables:
I Height of plant
Density of target plant
Density of trees
Canopy cover
- Average DBH of all surrounding trees /l Average distance to the closest trees
~ Understory coverage at a height below 1
meter
Understory coverage at a height b tween
I and 2 meters
• The b ig yellow eared bat showed the most
selecti ve preference for the height of the plant
and the distance to the closest tree (p=0.004).
• Thomas' fruit-eating bat displayed a preferen ce
towards height of the plant and canopy cover
(p=0.013).
• Plants were located by visual observation in
Tirimbina Biological Reserve in Heredia
Province of Costa Rica
• With tents and without tents (controls)
• Determined the most important factors for tent
site selection by using
Principal Component Analysis of vegetation
variables
Two Sample T-test for comparison of roost habitat
variables
Preferences might be explained by predatory
avoidan e and temperature regulation.
• Tent-maki ng bats display a preference within
the ir habitat for roost selection
.
.
. ,.
• Habitat loss is a major threat
More information about tropical
bat & plant species
-",­
"
I
-,. '
I
2
5/24/2012 ,
BALL STATE
Special thanks to
UNIVER..I TY.
Emmanuel Pequeno
Bernal Rodriguez Herrera
Timothy Carter
Mark Pyron
3