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Ecosystem services are the benefits obtained from the environment that increase human well-being. Economic valuation is conducted by measuring the human welfare gains or losses that result from changes in the provision of ecosystem services. Bats have long been postulated to play important roles in arthropod suppression, seed dispersal, and pollination; however, only recently have these ecosystem services begun to be thoroughly evaluated. Here, we review the available literature on the ecological and economic impact of ecosystem services provided by bats. We describe dietary preferences, foraging behaviors, adaptations, and phylogenetic histories of insectivorous, frugivorous, and nectarivorous bats worldwide in the context of their respective ecosystem services. For each trophic ensemble, we discuss the consequences of these ecological interactions on both natural and agricultural systems. Throughout this review, we highlight the research needed to fully determine the ecosystem services in question. Finally, we provide a comprehensive overview of economic valuation of ecosystem services. Unfortunately, few studies estimating the economic value of ecosystem services provided by bats have been conducted to date; however, we outline a framework that could be used in future studies to more fully address this question. Consumptive goods provided by bats, such as food and guano, are often exchanged in markets where the market price indicates an economic value. Nonmarket valuation methods can be used to estimate the economic value of nonconsumptive services, including inputs to agricultural production and recreational activities. Information on the ecological and economic value of ecosystem services provided by bats can be used to inform decisions regarding where and when to protect or restore bat populations and associated habitats, as well as to improve public perception of bats.
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Ann. N.Y. Acad. Sci. ISSN 0077-8923
ANNALS OF THE NEW YORK ACADEMY OF SCIENCES
Issue: The Year in Ecology and Conservation Biology
Ecosystem services provided by bats
Thomas H. Kunz,1Elizabeth Braun de Torrez,1Dana Bauer,2Tatyana Lobova,3
and Theodore H. Fleming4
1Center for Ecology and Conservation Biology, Department of Biology, Boston University, Boston, Massachusetts.
2Department of Geography, Boston University, Boston, Massachusetts. 3Department of Biology, Old Dominion University,
Norfolk, Virginia. 4Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona
Address for correspondence: Thomas H. Kunz, Ph.D., Center for Ecology and Conservation Biology, Department of Biology,
Boston University, Boston, MA 02215. kunz@bu.edu
Ecosystem services are the benefits obtained from the environment that increase human well-being. Economic
valuation is conducted by measuring the human welfare gains or losses that result from changes in the provision
of ecosystem services. Bats have long been postulated to play important roles in arthropod suppression, seed
dispersal, and pollination; however, only recently have these ecosystem services begun to be thoroughly evaluated.
Here, we review the available literature on the ecological and economic impact of ecosystem services provided by
bats. We describe dietary preferences, foraging behaviors, adaptations, and phylogenetic histories of insectivorous,
frugivorous, and nectarivorous bats worldwide in the context of their respective ecosystem services. For each trophic
ensemble, we discuss the consequences of these ecological interactions on both natural and agricultural systems.
Throughout this review, we highlight the research needed to fully determine the ecosystem services in question.
Finally, we provide a comprehensive overview of economic valuation of ecosystem services. Unfortunately, few
studies estimating the economic value of ecosystem services provided by bats have been conducted to date; however,
we outline a framework that could be used in future studies to more fully address this question. Consumptive goods
provided by bats, such as food and guano, are often exchanged in markets where the market price indicates an
economic value. Nonmarket valuation methods can be used to estimate the economic value of nonconsumptive
services, including inputs to agricultural production and recreational activities. Information on the ecological and
economic value of ecosystem services provided by bats can be used to inform decisions regarding where and when to
protect or restore bat populations and associated habitats, as well as to improve public perception of bats.
Keywords: arthropod suppression; biological pest control; ecosystem valuation; insectivory; pesticide reduction;
pollination; seed dispersal; sustainable agriculture
Introduction
Ecosystems consist of living organisms and their
interactions with the abiotic environment (both
physical and chemical). Terrestrial ecosystems in-
clude forests, grasslands, deserts, wetlands, and
caves. Aquatic ecosystems include rivers, streams,
lakes, ponds, estuaries, and oceans. For thousands
of years, both terrestrial and aquatic ecosystems have
been subject to human alterations, including con-
version of natural ecosystems to agricultural ecosys-
tems that were needed to sustain increasing human
population growth. Natural ecosystems throughout
the world have become increasingly threatened by
human-generated or anthropogenic factors such as
urbanization, mining, deforestation, chemical and
light pollution, and invasive species. Healthy ecosys-
tems are especially important in providing various
regulatory processes (e.g., insect suppression, pol-
lination, seed dispersal, purification of water and
air, stabilization of soils, decomposition of wastes,
binding of toxic substances, mitigation of diseases,
mitigation of floods, and regulation of climate, etc.);
products or provisions (e.g., food, fuel, fiber, and
medicines); supporting processes (e.g., nutrient cy-
cling, soil formation, and primary production); and
doi: 10.1111/j.1749-6632.2011.06004.x
Ann. N.Y. Acad. Sci. 1223 (2011) 1–38 c
2011 New York Academy of Sciences. 1
Ecosystem services provided by bats Kunz et al.
cultural benefits (e.g., aesthetic, spiritual, educa-
tional, and recreational) that improve human well-
being.1Theseprocessesandproductsarecommonly
referred to as ecosystem services2,3and have been
duly recognized by the United Nations Millennium
Ecosystem Assessment.4,5Ecosystem services vary
depending on the ecosystems and the organisms
that they constitute. In this paper, we consider the
role of bats in providing ecosystem services, focusing
primarily on those that both regulate and provide
services needed to sustain humankind, with brief
references to supporting and cultural services. One
of the grand challenges that society faces is how best
to identify, protect, and conserve services that are
critical for human and ecosystem health.1,6
In their present form, bats have been on Earth
forover52millionyears
7and during this period
have diversified into at least 1,232 extant species.8,9
Bats have evolved an incredibly rich diversity of be-
havioral, roosting, and feeding habits.10,11 By day,
many species occupy caves and cave-like structures,
such as tombs and mines;12 others roost in tree cavi-
ties and foliage,13 sometimes modifying foliage into
unique tent-like structures.14–16 By night, bats fill
the skies to forage on a diversity of food items rang-
ing from insects, nectar, and fruit, to seeds, frogs,
fish, small mammals, and even blood.
Unfortunately, many threats face bats today. Bats
in western cultures have long been subjects of dis-
dain and persecution and have often been depicted
in the popular media as rampant vectors of dis-
ease, blood-sucking demons, ingredients of witches
brew, and, at times, associated with the dark side
of some religious practices.17 Common myths in-
clude that bats are attracted to and become caught
in women’s hair, are associated with the devil, and
that extracts from the skin of bats can cure bald-
ness.18,19 As with many myths and folklore, there
may be some elements of truth, yet the vast majority
of real or imagined images of bats often portrayed in
art, poetry, books, movies, television, and the press
convey them as having little redeeming value ex-
cept to frighten for the sake of corporate or personal
profit. By contrast, in many eastern cultures, espe-
cially those that prevailed during the middle and late
Qing Dynasty (1644–1911) in China, bats were con-
sidered to be symbols of good fortune, such as long
life, health, wealth, virtue, and serenity of mind.18,19
Today, these cultural symbols persist, but appear to
be less important to modern Chinese society.20
Since their evolutionary origin, some species of
bats have become locally extirpated or regionally
extinct, mostly for unknown reasons.21 In recent
years, increased evidence of anthropogenic activi-
ties such as depletion or destruction of forests and
other terrestrial ecosystems, disturbances to caves,
depletion of food resources, overhunting for bush
meat,22 increased use of pesticides,11,23 and the pro-
liferation and operation of utility-scale wind energy
facilities20,24–26 have contributed to unintended and,
in some cases, unprecedented mortality of bats. Bats
that roost in caves, for example, are often disturbed
by unsuspecting visitors either during maternity pe-
riods or hibernation, which can lead to death or
abandonment. Bats known to roost in buildings are
sometimes excluded or even exterminated for per-
ceived or real threats to human health, and some-
times simply from unfounded fear stirred by the
media.
Increased human populations and associated
habitat degradation have been linked to the decline
of many fruit-eating and nectar-feeding species, es-
pecially of endemic taxa and certain tropical species
that evolved on remote islands.27 Increased human
pressures by indigenous cultures in Asia, Africa, and
the Pacific Islands for bush meat have also led to the
local or regional extirpation of some species. The
recent decline of the little brown myotis, Myotis lu-
cifugus, one of the most common and widespread
species in North America, has been attributed to
white-nose syndrome,28 an emerging disease asso-
ciated with the putative fungal pathogen, Geomyces
destructans,29,30 which may have been introduced
from Europe.31,32
Bat biologists are often asked, “Why should we
care about bats?” The simple answer is that scientists
care about the fate of animals and as a consequence
have invested their careers in studying and, perhaps
more importantly, protecting these marvelous flying
mammals. Benefits that humans inadvertently and
unsuspectingly derive from bats will be forever lost
or severely diminished, causing both known and
unknown consequences to the ecosystems in which
they have evolved.
The rich diversity of dietary habits of bats, rang-
ing from species that feed on insects and other
arthropods to those that feed on fruit, nectar, and
flowers,10,11 provide valuable ecosystem services
and, thus, are the subjects of this paper, although
other species that feed on seeds, frogs, fish, small
2Ann. N.Y. Acad. Sci. 1223 (2011) 1–38 c
2011 New York Academy of Sciences.
Kunz et al.Ecosystem services provided by bats
mammals, and even blood also assume important
roles in ecosystems as predators or prey in sustain-
able ecosystems. Bats provide value to ecosystems
as primary, secondary, and tertiary consumers that
support and sustain both natural and human dom-
inated ecosystems ranging from the simple to the
complex. In this review, we describe the ecosystem
services provided by bats that feed on insects and
other arthropods, on nectar and pollen, and on fruit.
Insectivorous species, largely feeding on airborne in-
sects and other arthropods, suppress both naturally
occurring and anthropogenically-generated insect
populations (such as agricultural pest species and
insects that annoy or transmit specific pathogens
to humans and other mammals) and contribute
to the maintenance of ecosystem stability. Frugiv-
orous bats help maintain the diversity of forests by
dispersing seeds across different ecosystems, often
introducing novel plant species into previously dis-
turbed landscapes33 and to oceanic islands.34 Sim-
ilarly, nectarivorous bats that visit flowers provide
valued ecosystem services by pollinating plants, dis-
persing pollen, and, thus, helping to maintain ge-
netic diversity of flowering plants. In addition to
suppressing insect populations, pollinating flowers,
and dispersing seeds, insectivorous, nectarivorous,
and frugivorous species may redistribute nutrients
and energy through their guano to sustain terres-
trial, aquatic, and cave ecosystems. Lastly, where
data are available, we consider the economic value
of bats to terrestrial ecosystems. While data on the
economic value of bats to ecosystems are limited, we
present a framework that is needed to make such as-
sessments and to examine why the diverse forms of
this group of mammals deserve respect, protection,
and conservation.
The role of bats in arthropod suppression
Among the estimated 1,232 extant bat species,8over
two thirds are either obligate or facultative insecti-
vores (Table 1). They include species that glean in-
sects from vegetation and water in cluttered forests
to those that feed in open space above forests, grass-
lands, and agricultural landscapes (Fig. 1). Although
popular literature commonly recognizes bats for
their voracious appetites for nocturnal and crepus-
cular insects,35 the degree to which they play a role in
herbivorous arthropod suppression is not well doc-
umented. In this section, we review the available lit-
erature on the predator–prey interactions between
Figure 1. Brazilian free-tailed bat (Tadarida brasiliensis)fly-
ing with a moth in its mouth (photo by Merlin D. Tuttle, Bat
Conservation International, www.batcon.org).
bats and arthropod pests—including the magnitude
of arthropod consumption by bats, the responses
of prey to threats of predation, and the quantitative
impacts of bats on arthropod populations—and dis-
cuss the various methods used to obtain these data.
This type of information could ultimately be used to
estimate the ecological and economic value of bats
in both natural and agricultural systems, a topic
that we discuss in detail in the section on economic
valuation of ecosystem services.
Dietary considerations: what’s on the menu?
Foraging modes. Insectivorous bats use various
methods for capturing and consuming insect prey
(Table 1). Aerial hawking bats hunt prey on the fly,
often scooping insects from the air with their wing
or tail membrane and transferring them to their
mouths.36–38 Gleaning bats, those that take prey
from surfaces, generally forage in cluttered envi-
ronments (e.g., dense foliage) where background
echoes can mask echoes from insects.38,39 Some
gleaners are able to finely discriminate targets us-
ing low-intensity,broadband echolocation calls,40,41
whereas others passively listen for prey-generated
sounds or use vision and/or olfaction.38 Trawling
bats glean insects off the surface of water using their
long feet and/or tail membrane. Fly-catching and
perch-hunting bats hang from perches and wait for
aerial and ground-dwelling prey, respectively. These
foraging modes, however, are not mutually exclu-
sive, and it is often difficult to categorize a given
species.
General insect consumption. Studies of dietary
habits of insectivorous bats date back many
Ann. N.Y. Acad. Sci. 1223 (2011) 1–38 c
2011 New York Academy of Sciences. 3
Ecosystem services provided by bats Kunz et al.
Tab l e 1. An ecological classification of bats, Order Chiroptera. Taxonomy follows Wilson and Reeder.241
Number
of genera,
Family (common name) species Distribution Diet and foraging modes
Pteropodidae (Old World
fruit bats)
42, 186 Old World tropics
and subtropics
Plant visitors that feed nearly
exclusively on nectar and fruit;
most species feed in forest
canopies, but a few feed in forest
understories
Rhinolophidae (horseshoe
bats)
1, 77 Old World tropics
and subtropics
Insectivorous: use aerial hawking,
gleaning, fly catching, perch
hunting; many forage very close
to the ground, hover in place, and
pluck prey from spider webs
Hipposideridae (Old World
leaf-nosed bats)
9, 81 Old World tropics
and subtropics
Insectivorous: use aerial hawking,
gleaning, fly catching, perch
hunting; fly close to the ground
Megadermatidae (false
vampire and
yellow-winged bats)
4, 5 Old World tropics Both insectivorous and carnivorous:
primarily use perch hunting;
consume arthropods and small
vertebrates (e.g., fish, frogs,
lizards, birds, mice, or other bats)
Rhinopomatidae
(mouse-tailed or
long-tailed bats)
1, 4 Old World tropics Insectivorous: little information on
foraging behavior; fly at least
6–9 m above ground; slit-like
nostrils that can exclude sand and
dust
Craseonycteridae (Kitti’s
hog-nosed bat)
1, 1 Thailand Insectivorous: use aerial hawking,
gleaning; glean insects and spiders
from tree-top foliage and can
hover
Emballonuridae (sac-winged,
sheath-tailed, and ghost
bats)
13, 51 Pantropical Insectivorous: use primarily aerial
hawking; have long narrow wings
for swift flight; occasionally eat
fruit
Nycteridae (slit-faced or
hollow-faced bats)
1, 16 Old World tropics Primarily insectivorous: consume
insects, spiders, small scorpions;
one species specializes on
vertebrates (e.g., frogs, small
birds); forage close to surfaces
Myzopodidae (Old World
sucker-footed bat)
1, 1 Madagascar Insectivorous: little is known about
its foraging behavior
Mystacinidae (New Zealand
short-tailed bats)
1, 2 New Zealand Primarily insectivorous: use aerial
hawking but well adapted to
hunting arthropods on the
ground; also pollinate certain
terrestrial flowers and eat fruit
Continued
4Ann. N.Y. Acad. Sci. 1223 (2011) 1–38 c
2011 New York Academy of Sciences.
Kunz et al.Ecosystem services provided by bats
Tab l e 1. Continued
Number
of genera,
Family (common name) species Distribution Diet and foraging modes
Phyllostomidae (New World
leaf-nosed bats)
55, 160 Neotropics Diverse foraging and feeding habits,
including gleaning and aerial
insectivores, carnivores,
blood-feeders, nectar-feeders, and
fruit-eaters. Plant-visiting species
forage in forest understory and
canopy
Mormoopidae (ghost-faced
bats, moustached bats, and
naked-backed bats)
2, 10 Neotropics Insectivorous: primarily feed on insects
closetooronsurfacesofwater
Noctilionidae (bull dog bats) 1, 2 Neotropics Both species capture insects in or from
the surface of water; Noctilio
leporinus eatsfish,frogs,and
crustaceans by trawling its long feet
and claws through the water
Furipteridae (smoky bats and
thumbless bats)
2, 2 Neotropics Insectivorous: may specialize on moths
and butterflies
Thyropteridae (disc-winged
bats)
1, 3 Neotropics Insectivorous: characterized by fluttery,
moth-like flight; consume small
insects
Natalidae (funnel-eared bats) 3, 8 Neotropics Insectivorous: characterized by fluttery,
moth-like flight; consume small
insects
Molossidae (free-tailed bats) 16, 100 Cosmopolitan
in tropics and
subtropics
Insectivores: use aerial hawking; most
species forage in open areas and are
swift, straight fliers
Vespertilionidae (evening and
vesper bats)
48, 407 Cosmopolitan Primarily insectivorous: diverse
foraging modes including aerial
hawking (often using their tail
membrane as a scoop), gleaning,
trawling; a few species eat scorpions,
fish, and small birds
years,42–49 but few have assessed the potential im-
pacts of prey consumption on human health or
natural and agricultural systems. Although it is be-
yond the scope of this review, there has been con-
siderable debate as to the degree of prey selection
by bats.38,50 While some studies have shown indi-
viduals to actively select among available prey,51–54
others have concluded that insectivorous bats are
generalist predators, feeding on a wide diversity of
taxonomic groups and opportunistically consum-
ing appropriately sized prey according to its avail-
ability within a preferred habitat.48,50,55 Insectiv-
orous bat activity and diversity are strongly cor-
related with arthropod abundance,56–58 suggesting
that bats seek out areas of concentrated prey sources.
Although there is considerable variation in the rel-
ative proportions consumed by different species,
most insectivorous bats eat large quantities of lepi-
dopterans (moths), coleopterans (beetles), dipter-
ans (flies), homopterans (cicadas, leaf hoppers),
and hemipterans (true bugs).44,47,59–63 Some species
also eat unusual prey items such as scorpions and
Ann. N.Y. Acad. Sci. 1223 (2011) 1–38 c
2011 New York Academy of Sciences. 5
Ecosystem services provided by bats Kunz et al.
spiders.64 Prey size can vary from as small as 1 mm
(midges and mosquitoes) to as large as 50 mm long
(beetles and large moths), depending on the species
of bat.52,59,60,65–68 Bats often forage throughout the
night, returning to their roosts to nurse young and
to rest during periods of low insect activity.59,69,70
The magnitude of arthropod consumption by
a bat varies considerably by species, season, and
reproductive cycle. On average, insectivorous bats
maintained in captivity have been estimated to con-
sume up to 25% of their body mass in insects each
night (Myotis lucifugus and Eptesicus fuscus,46 M.
lucifugus and M. thysanodes,71 Lasiurus cinereus,72
Lasionycteris noctivagans73 ). Under natural condi-
tions, these estimates increase, most likely due to
higher energy demands. Using field metabolic rates
based on turnover of doubly labeled water, Kurta
et al.74 estimated that at the peak night of lacta-
tion, a 7.9 g little brown bat (M. lucifugus) needs
to consume 9.9 g of insects (over 100% of its body
mass) to account for the marked increase in energy
expenditures due to this costly stage of the repro-
ductive cycle.75 At peak lactation, a female Brazilian
free-tailed bat (Tadarida brasiliensis) can consume
up to 70% of her body mass in insects each night;
furthermore, she frequently culls her prey, consum-
ing only the nutrient-rich abdomen of moths while
discarding the wings, head, and appendages, which
greatly increases feeding efficiency and hence the
quantity of insects consumed.61 To put this in per-
spective, an average maternity colony of one million
Brazilian free-tailed bats weighing 12 g each could
consume up to 8.4 metric tons of insects in a single
night. These studies hint at the immense capability
of nightly insect consumption and at the potential
role of bats in top-down suppression of arthropod
populations.
Agricultural pests and pesticide use. Herbivo-
rous arthropods destroy approximately 25–50%
of crops worldwide.76,77 The response to these
threats by modern agriculture has been predom-
inantly through the application of synthetic pes-
ticides, a practice that has led to many unin-
tended consequences including human health risks,
degradation of ecosystem function, evolved toxicity
resistance by pests, and severe alterations of the
dynamics of agribusiness.76,78–80 The World Re-
sources Institute estimates that over 400 pest species
have evolved resistance to one or more pesticides,
and that despite an increase in pesticide use, the
proportion of crops destroyed by insect pests in
the United States has doubled (to 13%) since the
1940s.81 By eliminating beneficial invertebrate and
vertebrate predators through indiscriminate use of
broad-spectrum insecticides, insect species that are
not normally considered pests are often elevated to
pest status.80,82 Efforts to curb the widespread and
indiscriminate use of chemical pesticides include the
promotion of biological controls.83 An estimated
99% of potential crop pests are limited by natural
ecosystems,80,84 of which some fraction can be at-
tributed to predation by bats. Naylor and Ehrlich80
estimated that the value of the global pest control
ecosystem service ranges between $54 billion and $1
trillion, an estimate that includes reductions in both
crop losses due to pests and direct/indirect costs of
pesticide use. Pimentel et al.77 concluded that a 50%
reduction in pesticide use could be achieved with
only a 0.6% increase in the cost of purchased food,
provided that biological, cultural, and environmen-
tal pest control technologies are used.
Consumption of specific agricultural pests by
bats. Various species of prominent agricultural in-
sect pests have been found in the diets of bats
based on identification of insect fragments in
fecal samples and stomach contents. These in-
sects include, but are not limited to, June bee-
tles (Scarabidae), click beetles (Elateridae), leafhop-
pers (Cicadelidae), planthoppers (Delphacidae),
the spotted cucumber beetle, (Diabrotica undecim-
punctata, Chrysomelidae), the Asiatic oak weevil
(Cyrtepistomus castaneus, Curculionidae), and the
green stinkbug (Acrosternum hilare , Pentatomidae)
(Table 2 and Appendix A).
Based on the dietary composition, minimum
number of total insects per guano pellet, number
of specific agricultural pest species in each pellet,
and the number of active foraging days per year,
Whitaker85 calculated that a colony of 150 big brown
bats (Eptesicus fuscus) in the midwestern United
States annually consumes approximately 600,000
cucumber beetles, 194,000 June beetles, 158,000
leafhoppers, and 335,000 stinkbugs. Subsequently,
assuming that each female cucumber beetle lays 110
eggs,86 this average-sized bat colony could prevent
the production of 33,000,000 cucumber beetle lar-
vae (corn rootworms), which are severe crop pests
(Appendix A). While these calculations include a
6Ann. N.Y. Acad. Sci. 1223 (2011) 1–38 c
2011 New York Academy of Sciences.
Kunz et al.Ecosystem services provided by bats
large number of assumptions and ignore various
sources of natural variation, this study took the extra
step of translating ecological data into a form more
readily appreciated by the public. With the addition
of data on corn rootworm damage to crops in the
study area, an economic value for this colony could
be estimated.
A common challenge in these investigations is
the overwhelming lack of basic ecological informa-
tion regarding foraging behavior and diet for many
species of bats. For example, traditional dietary
analyses through fecal or stomach contents have
historically only identified arthropod fragments
to the ordinal or familial level, rather than to
species,46,60,69,87 and in cases where species identi-
fication is possible, it has typically been restricted
to hard-bodied insects, such as beetles, that re-
main partially undigested. Recently, novel molecu-
lar techniques have allowed detection and species
identification of both hard- and soft-bodied in-
sects, such as lepidopterans, within guano collected
from bats.88–93 Whitaker et al.90 described the de-
velopment of quantitative polymerase chain reac-
tion (qPCR), coupled with controlled feedings of
known insects to captive bats, as an approach to
estimate the number or percent volume of specific
insects consumed by wild bats. qPCR has been used
to document consumption of the corn earworm
moth (Helicoverpa zea) and the beet armyworm
(Spodoptera exigua),both major pests of corn, cot-
ton, and other crops throughout the United States,
by Brazilian free-tailed bats, Tadarida brasiliensis, in
south-central Texas.88,90,92 Brown91 used qPCR to
identify the pecan nut casebearer moth (Acrobasis
nuxvorella),the hickory shuckworm moth (Cydia
caryana), and H. zea moths in the diet of Brazil-
ian free-tailed bats from guano collected beneath
bat houses located in organic pecan orchards. This
author also identified the southern green stink bug
(Nezara viridula) by sequencing insect fragments
found in the guano (see Appendix A).
To da t e, C l a r e et al.89 conducted the most com-
prehensive dietary analysis of an insectivorous bat.
These authors extracted DNA from insect fragments
found in fecal samples and used a polymerase chain
reaction (PCR) coupled with a sequence-based tech-
nique to assess the diet of the eastern red bat, Lasiu-
rus borealis, in Canada. Through comparison of fecal
DNA sequences to a reference database, they were
able to identify 127 prey species (5 orders, 16 families
of lepidopterans), some of which were notable agri-
cultural, forest, and orchard/garden pests including
gypsy moths (Lymantria dispar ), tent caterpillars
(Malacosoma sp.), coneworms (Dioryctria sp.), cut-
worms (Noctua pronuba), snout moths (Acrobasis
sp.), and tortrix moths (Cydia sp.) (see Table 2 and
Appendix A). All bats were captured in a provin-
cial park that was adjacent to agricultural land. Al-
though this study provides unprecedented detail re-
garding the diversity of insects consumed by the
eastern red bat, the techniques used did not allow
for quantification of pest consumption, and the au-
thors did not have sufficient data to estimate the
ecological or economic value of these bats to any
particular ecosystem.
Direct and indirect impacts of insectivorous
bats
Understanding complexities of predator–prey in-
teractions. The studies reviewed in the previous
sections document the consumption of herbivorous
arthropods by bats; however, few studies have mea-
sured their actual impacts on natural or agroecosys-
tems. Top- and midlevel predators can have direct
effects on herbivore communities and indirect ef-
fects on plant communities through both density-
mediated (consumption) and trait-mediated
(behavioral) interactions.94 The following sections
address the research that has begun to document
these interactions between insectivorous bats and
their prey.
A pioneering study by Buckner dating back to the
1960s, which examined the role of vertebrate preda-
tors in the biological control of forest insects,95 il-
lustrates the complexities involved with assigning
avaluetonaturalpredatorsandmayserveasa
template for the assessment of the ecosystem ser-
vices provided by bats. Buckner asserted that three
basic measurements must be made to understand
a predator–prey system: density of the prey, den-
sity of the predators, and the extent of destruction
of prey by the predators. Few studies have thor-
oughly evaluated these seemingly simple questions.
Equally fundamental, but perhaps more ecologically
complex, is the evaluation of an individual predator
species in relation to its local ecological community.
What is the predator’s capacity for consumption
of the prey? What are the effects of the density of prey
or the presence of alternative prey on the predator’s
density and/or rate of consumption? What defense
Ann. N.Y. Acad. Sci. 1223 (2011) 1–38 c
2011 New York Academy of Sciences. 7
Ecosystem services provided by bats Kunz et al.
Tab l e 2 . Examples of studies found in the literature documenting the consumption of agricultural insect pests by
different species of bats, analytical methods used for dietary analysis, and estimated quantity of consumptiona
Estimate of
Pest species Species of bat predator Analysis consumption (%)
Coleoptera
June beetles (Scarabidae) Cave myotis, Myotis velifer59 Stomach content 15.9 of Coleoptera
Brazilian free-tailed bat,
Tadarida brasiliensis66
Fecal dissection 19.7 of Coleoptera
Eastern red bat, Lasiurus
borealis242
Fecal dissection 11.2
Northern long-eared myotis,
M. septentrionalis242
Fecal dissection 5.5
Big brown bat, Eptesicus
fuscus45,85,242243
Fecal dissection 29.6
Click beetles or wire worm
(Elateridae)
Big brown bat, E. fuscus243 Fecal dissection 31.2
Spotted cucumber beetle,
Diabrotica
undecimpunctata
(Chrysomelidae)
Big brown bat, E.
fuscus45,85242
Fecal dissection 28.2
Brazilian free-tailed bat, T.
brasiliensis66
Fecal dissection Unreported
Evening bat, Nycticeius
humeralis244
Fecal dissection 23.5
Indiana myotis, Myotis
sodalis245
Fecal dissection 1.1 (3.9 by frequency)
Little brown myotis, Myotis
lucifugus242
Fecal dissection 5.3
Asiatic oak weevil,
Cyrtepistomus castaneus,
(Curculionidae)
Indiana myotis, Myotis
sodalis245242
Fecal dissection 7.7 (23.2 by frequency)
Eastern red bat, Lasiurus
borealis242
Fecal dissection 29
Big brown bat, Eptesicus
fuscus242
Fecal dissection 13.9
Homoptera
Leaf hoppers (Homoptera:
Cicadelidae)
Cave myotis, M. velifer59 Stomach content 17.4 of Homoptera
Big brown bat, E. fuscus45,85 Fecal dissection 8.2
Brazilian free-tailed bat, T.
brasiliensis66
Fecal dissection 37.3 of Homoptera
Big free-tailed bat, Nyctinomops
macrotis246
Fecal dissection 26.7 (58.9 by frequency)
Eastern pipistrelle, Perimyotis
subflavus242
Fecal dissection 14.5
Indiana myotis, M. sodalis242 Fecal dissection 1.8 (17.9 by frequency)
White-backed planthopper,
Sogatella sp. (Delphacidae)
Wrinkled-lipped bats, Tadarida
plicata63
Fecal dissection 25.3 by frequency∗∗
Continued
8Ann. N.Y. Acad. Sci. 1223 (2011) 1–38 c
2011 New York Academy of Sciences.
Kunz et al.Ecosystem services provided by bats
Tab l e 2. Continued
Estimate of
Pest species Species of bat predator Analysis consumption (%)
Hemiptera
Stink bugs (Pentatomidae) Brazilian free-tailed bat, T.
brasiliensis66
Fecal dissection 26.8
Green stink bug, Acrosternum
hilare
Indiana myotis, Myotis
sodalis245
Fecal dissection 0.1 (1.4 by frequency)
Hoary bat, Lasiurus cinereus242 Fecal dissection 43.8
Eastern red bat, Lasiurus
borealis242
Fecal dissection 2.1
Big brown bat, E.
fuscus45,85,242,243
Fecal dissection 18.3
Brown stink bug, Euschistus
servus
Big brown bat, E. fuscus242 Fecal dissection 2.5
Northern long eared myotis, M.
septentrionalis242
Fecal dissection 1.0
Lepidoptera
Corn earworm moth,
Helicoverpa zea
(Noctuidae)
Brazilian free-tailed bat, T.
brasiliensis88,92
Molecular: qPCR N/A
Gypsy moths, Lymantria
dispar (Lymantriidae)
Eastern red bat, Lasiurus
borealis89
Molecular:
sequence based
N/A
Cutworms, Noctua pronuba
(Noctuidae)
Coneworms, Dioryctria spp.
(Pyralidae)
Tent caterpillars, Malacosoma
spp. (Lasiocampidae)
Tortrix moths, Cydia sp.
(Tortricidae)
Diptera
Mosquitos (Culicidae) Indiana myotis, M. sodalis245 Fecal dissection 1.0 (4.3 by frequency)
Hessian fly, Mayetoila
destructor
Indiana myotis, M. sodalis245 Fecal dissection <0.1 (0.4 by frequency)
aEstimates of consumption are in percent volume of the total diet unless otherwise specified. See Appendix A for
descriptions of pest species.
The study from which estimates of consumption are taken if more than one.
∗∗Estimate refers to Homoptera: “most” were Sogatella sp.
mechanism does the prey have and use against the
predator? Buckner argued that until these aspects are
studied thoroughly, the understanding of predation
as a biological control factor will be incomplete.
Researchers investigating invertebrate and aquatic
systems have begun to do this (reviewed in Refs. 96
and97),butfewifanystudiesofvertebratepredators
have fully addressed these important questions.
Ecosystem services of the Brazilian free-tailed
bat: a case study. Of the approximately 900 insec-
tivorous bat species, the Brazilian free-tailed bat,
Tadarida brasiliensis, provides one of the most im-
pressive examples of continental-scale natural pest
suppression in the world.98 Severalstudieshaveat-
tempted to document the nightly foraging behav-
ior and prey consumption patterns in this species
Ann. N.Y. Acad. Sci. 1223 (2011) 1–38 c
2011 New York Academy of Sciences. 9
Ecosystem services provided by bats Kunz et al.
Figure 2. Brazilian free-tailed bats (Tadarida brasiliensis) dis-
persing over agricultural landscapes from a maternity roost in
south-central Texas (photo by Merlin D. Tuttle, Bat Conserva-
tion International, www.batcon.org).
to better understand its ecosystem service.62,66,99,100
Millions of Brazilian free-tailed bats migrate north-
ward each year in the spring from Mexico to form
enormous maternity colonies in limestone caves
and bridges throughout the southwestern United
States.43,101 Each evening, large numbers of bats
emerge from these roosts (Fig. 2) and disperse across
natural and agricultural landscapes in high enough
densities to be detected by NEXRAD WSR-88D
Doppler weather radars.99 As recently as the 1950s
and early 1960s, midsummer colonies of Brazil-
ian free-tailed bats in 17 caves in the southwest-
ern United States were estimated to total about 150
million individuals.102 However, recent estimates,
based on improved census methods using thermal
infrared imaging and computer detection and track-
ing algorithms, conclude that these same caves now
house closer to nine million bats, indicating either
a marked population decline or an overestimation
in past observations.103 The likelihood of historic
overestimatesissupportedbyfurtherquantitative
assessments of colony dynamics and emergence be-
havior of Brazilian free-tailed bats that roost in
Carlsbad Caverns, New Mexico.104
Although Brazilian free-tails are known to con-
sume a wide variety of prey items (12 orders, 35 fam-
ilies), numerous studies indicate that moths (Lep-
idoptera) are their primary food source,61,62,66,105
including devastating agricultural pests such as the
corn earworm or cotton bollworm moth (Helicov-
erpa zea) and the tobacco budworm moth (Heliothis
virescens).88,98 Studies have found that the propor-
tion of moths consumed by Brazilian free-tailed bats
increases markedly during their early morning for-
aging bouts in comparison to evening foraging bouts
fromMaytotheendofJune,
66,105 a time period that
coincides with the immigration of swarms of corn
earworm moths and fall armyworms, Spodoptera ex-
igua, into Texas from northern Mexico on prevailing
winds.106,107 In a study on the foraging activity of
these bats at high altitudes, McCracken et al.100 doc-
umented that echolocation search calls and feeding
buzzes were most abundant at ground level and at
400–500 m above ground level, the latter of which
corresponds with the low-elevation southerly wind
jet, a major aeroecological corridor for the nocturnal
dispersal of corn earworm moths, fall armyworms,
and other insects. Des Marais et al.108 used stable
isotope ratios of carbon from bat guano to esti-
mate that more than one-half of all insects eaten by
Brazilian free-tailed bats that roost in Carlsbad Cav-
erns fed on crops, based on landscape data showing
that 90% of the crops surrounding the cave were C3
plants while the majority of the native plants were
C4. Similarly, Mizutani et al.109 estimated that two-
thirds of the guano sampled from a cave housing
several million Brazilian free-tailed bats in Arizona
included insects or other arthropods that fed on C3
crops (cotton and alfalfa) in an area dominated by
native C4 vegetation.
These studies strongly suggest that Brazilian free-
tailed bats opportunistically forage over agricultural
fields that both produce and attract large insect pop-
ulations. Research suggests that after initial arrival
into Texas from northern Mexico, corn earworm
and tobacco budworm moths and their progeny
undergo an annual migration northward through
the southern and central croplands of the United
States.106,107 Thus, the benefits conferred to agricul-
ture by consumption of these moths by bats may
not be limited to their local foraging areas (e.g., in
Texas and New Mexico) but may extend to agri-
cultural landscapes hundreds of kilometers away.
Several recent studies have estimated the economic
value of the pest suppression service provided by
Brazilian free-tailed bats98,103,110,111 and are further
discussed in the section on valuation of ecosystem
services.
Density-mediated direct and indirect effects: con-
sumption. Research evaluating ecosystem services
of other insectivorous bat species fall far behind that
of the Brazilian free-tailed bat; however, several re-
cent studies have provided compelling evidence that
10 Ann. N.Y. Acad. Sci. 1223 (2011) 1–38 c
2011 New York Academy of Sciences.
Kunz et al.Ecosystem services provided by bats
bats can limit insect populations in both agricultural
and natural systems.
For example, Williams-Guill´
en et al.112 and Kalka
et al.113 separated the effects of insectivorous birds
and bats on pest suppression by conducting preda-
tor exclosure experiments in a coffee plantation in
Mexico and a lowland tropical forest in Panama, re-
spectively. Both studies placed agricultural netting
around individual plants to exclude bats at night and
birds during the day. Previous studies using preda-
tor exclosures attributed any results of arthropod
suppression to bird predation,114,115 ignoring bats
as potential contributors. Williams-Guill´
en et al.112
found that, by excluding bats, total arthropod den-
sities increased by 84% per coffee plant in the wet
season but were not affected in the dry season. They
attributed the seasonal difference to the increased
abundance, reproductive activity, and hence energy
demands of bats during the wet season. In both sea-
sons, bats and birds together had the highest impact
on arthropod densities, suggesting an additive effect.
Although there was a clear direct effect of bats and
birds on herbivorous arthropods, the authors did
not find a significant indirect effect on leaf damage
for any of the treatments. By contrast, Kalka et al.113
demonstrated that the exclusion of bats from five
common tropical understory plants significantly in-
creased both arthropod densities (by 65%) and leaf
damage (by 68%) relative to control treatments.
They also found that bats consistently had a higher
impact on insect populations than birds. These au-
thors emphasize that their estimates of direct and
indirect impacts of both groups are likely conserva-
tive due to predation by aerial insectivores outside
of the exclosures, the exclusion of large arthropods
along with bats and birds, the presence of predatory
arthropods in the exclosures, and their focus on
understory plants rather than the more-productive
forest canopy. For both of these studies, a list of in-
sect orders that were suppressed is available in their
supporting online material; however, neither study
identified pests to the species level, nor did they at-
tempt to estimate the economic value of bats in these
systems.
Reiskind and Wund67 provided compelling evi-
dence that northern long-eared bats (Myotis septen-
trionalis) suppress mosquito (Culex spp.)popula-
tions through direct predation. Although bats are
commonly credited for their role in mosquito con-
trol, this is the first study documenting a quanti-
tative impact on mosquito populations. Predator
enclosures were erected in the field that contained
artificial oviposition sites and allowed passage of
naturally occurring mosquitoes. These researchers
released wild-captured northern long-eared bats
into the enclosures to forage for a total of nine nights.
They found that nightly oviposition by mosquitoes
was reduced by 32% in enclosures that contained
bats when compared to control enclosures with no
bats. Based on their finding of no difference between
control enclosures and unenclosed artificial oviposi-
tion sites adjacent to bat enclosures, they concluded
that these effects were due to predation rather than
the alteration of mosquito behavior.
Exclosure and enclosure studies, such as those de-
scribed above, have the potential toprovide valuable
information on the direct and indirect effects of bats
as arthropod predators; however, results should be
interpreted with caution. Exclosures effectively ex-
clude bats that glean insects directly from vegeta-
tion but most likely have a limited effect on aerial
insectivores that capture insects on the fly often far
from the plant of interest. Enclosures, on the other
hand, may inflate estimates of prey suppression due
to unnatural conditions such as an elevated density
of bats or limited availability of other suitable prey
items within the enclosures.
Trait-mediated indirect interactions: ecology of
fear. Predator–prey interactions are central fea-
tures in all ecological communities, yet traditional
models of predator–prey dynamics treat individ-
uals as unresponsive units and do not consider
the prey’s physical or behavioral response to the
presence of a predator.116 In a fear-driven system,
prey enact an inducible defense in response to the
presence or threat of a predator in order to re-
duce the risk of consumption by altering such be-
haviors as predator vigilance, foraging decisions,
and mate attraction.97,116 This behavioral plastic-
ity may have significant impacts on species in-
teractions, community structure, and ecosystem
function.97,117
The threat of predation by bats has led to the
evolution of both physical and behavioral defense
mechanisms in many species of moths, including
aposematic signaling,118,119 the production of ul-
trasonic jamming clicks,120 and evasive flight ma-
neuvers121 to avoid consumption. In an agricultural
setting, the presence of bats may alter the behavior
Ann. N.Y. Acad. Sci. 1223 (2011) 1–38 c
2011 New York Academy of Sciences. 11
Ecosystem services provided by bats Kunz et al.
and/or population dynamics of moth pests within
that system. Belton and Kempster122 found that the
infestation rate of sweet corn (maize) by the Eu-
ropean corn borer, Ostrinia nubilalis (Lepidoptera:
Pyralidae),was reduced by over 50% in test plots
that were exposed to ultrasound broadcast at fre-
quencies, amplitudes, and pulse rates characteristic
of bat calls. This result provides an excellent ex-
ample of the ecology of fear; however, the sample
size of the study was very small (only two replicates
over one season), the broadcasts may not have rep-
resented natural levels of bat activity, and possible
changes in predation due to bat responses to the
broadcast were not accounted for. In a laboratory
study, the true armyworm, Pseudaletia umpuncta
(Lepidoptera: Noctuidae), and the European corn
borer, altered their mating behavior in response to
high levels of simulated predation risk (ultrasonic
bat calls) by reducing their mate-seeking behavior,
pheromone production, and mating calls.123 Huang
et al.124,125 documented that when exposed to ultra-
sound in the laboratory, female Indian meal moths,
Plodia interpunctella (H ¨
ubner) (Lepidoptera: Pyral-
idae) received fewer spermatophores from males,
produced fewer and smaller larvae, reduced mate
calling, and reduced the length of mating time when
compared to female moths not exposed to ultra-
sound. These studies suggest that the mere presence
of bats, whether foraging due to high prey avail-
ability or being attracted to roosting opportunities,
may aid in reducing damaging activities or disrupt-
ing population dynamics of insect pests in a given
agricultural landscape.
Conclusions, future directions, and
management of arthropod suppression
services
The studies reviewed in this section hint at the im-
mense potential for bats to provide pest suppression
services in both natural and agroecosystems; how-
ever, more research is needed to adequately doc-
ument the extent to which bats interact with and
limit insect pest populations across the geograph-
ical landscape and over time. Some of the authors
have attempted to address one or all of the three ba-
sic measurements outlined in Buckner:95 density of
predator,densit y of prey, and capacit y of destruction
of prey; however, uncertainties lie in each of these
parameters. Determining the degree of spatial and
temporal overlap between predator and prey, how
the densities of the predator and prey are affected by
third party effects, such as alternative prey sources or
competition, and how crop production affects these
relationships are all examples of sources of varia-
tion and uncertainty. This information is essential
in models predicting the ecological and economic
value of a predator.
Unfortunately, small-scale temporal and spatial
variation in the diet is often difficult to detect
through traditional methods and requires extensive
fieldwork. The findings by Whitaker et al.105 and
Lee and McCracken,66 that dietary composition is
markedly different between the evening and morn-
ing foraging bouts of female Brazilian free-tailed
bats living in caves near major agricultural regions,
illustrate the importance of taking into consider-
ation temporal variation when characterizing the
diet of a species as well as assessing any potential
ecosystem service. Other studies have shown tem-
poral variation in the diet of bats by season,126,127
year,60,128 and age class.129,130 Dietary variation also
exists between co-occurring species and geograph-
icallywithinagivenspecies.
48,60,131–133 Addition-
ally, many frugivorous and nectarivorous bat species
(e.g., Glossophaga soricina;134,135 Phyllostomus dis-
color and Phylloderma stenops136 ) include insects in
their diets as a supplement to their dominant food
sources. For example, among the 39 species of bats
captured in an agricultural mosaic in Mexico, 22
were classified as omnivorous (i.e., consuming in-
sects in addition to fruit, nectar, or meat).137 These
species are not typically considered when evaluat-
ing potential pest suppression yet undoubtedly con-
tribute to the overall service. Findings from these
studies highlight the importance of encouraging
high bat diversity (not only species richness, but
also reproductive class and functional diversity) in
a given area to maintain ecosystem function.
A detailed resolution of dietary composition
across bat species, in which identification of prey
items is to species rather than only to the fa-
milial or ordinal level, is needed to track pat-
terns of consumption of agricultural pests spatially,
seasonally, and relative to other benign insects.
Molecular techniques used by McCracken et al.88,92
and Clare et al.89 have the potential to yield this
scale of resolution and offer exciting new avenues
for research in mapping food webs and trophic cas-
cades; however, studies on quantifiable effects of bats
on crop yields and damage should be coupled with
12 Ann. N.Y. Acad. Sci. 1223 (2011) 1–38 c
2011 New York Academy of Sciences.
Kunz et al.Ecosystem services provided by bats
these dietary analyses to avoid making assumptions
of impact based purely on evidence of consump-
tion. Similarly, studies investigating the biology of
bat populations within specific agroecosystems—
roosting dynamics, habitat selection, and estimates
of density—are critical for a complete evaluation
of the role of bats in pest suppression, leading ulti-
mately to an estimate of the economic value of this
service.
Beyond the studies reviewed here, there have
been many other studies investigating habitat use
by insectivorous bats in agricultural systems that
have not specifically addressed the effects of bats on
pest suppression (e.g., organic farms in the United
Kingdom,56,57 shade cacao plantations in Brazil,138
olive orchards in Greece,139 Midwestern agricultural
land,140 cereal crops in England,141 arboreal crops
in Mexico,137 and agricultural riparian areas142).
These, and other agroecosystems where high bat ac-
tivity has been documented, are ideal candidates for
further research investigating the potential ecosys-
tem service provided by insectivorous bats.
Incorporating the results of ecosystem service
studies into integrated pest management (IPM) pro-
grams designed to restore the natural predator–pest
balance83 has the potential to lead to beneficial re-
sults for both farmers and bats. Natural predators
may not control 100% of forest and agricultural
pests, but a combination of factors can keep pop-
ulations, and therefore crop losses, in check. With
white-nose syndrome causing massive declines of
up to 90% and expected regional extinctions of in-
sectivorous bat populations in the eastern and mid-
western United States,28 the loss of this important
regulating service may severely impact agricultural
production in affected areas.143 Identification and
measurement of the magnitude and value of this
naturalpestcontrolservicecanbeaneffectivetool
in influencing public support, policy, and private
land management toward conservation of natural
ecosystems; however, due to the complexities and
large scale at which natural pest control acts, cross-
disciplinary approaches, collaboration, and creativ-
ity are essential.
Pollination and seed dispersal
In addition to insect suppression through predation,
some bat species also play important roles as pollina-
tors and seed dispersers in tropical and subtropical
habitats throughout the world. These ecosystem ser-
vices are provided primarily by bats in two families,
Pteropodidae in the Old World and Phyllostomi-
dae in the New World (Table 1). These two fami-
lies are distantly related and differ in evolutionary
age. Current information suggests that Pteropodi-
dae evolved in Asia about 56 mya (million years
ago), whereas Phyllostomidae evolved in the north-
ern Neotropics about 35 mya.144 Because feeding
on nectar and pollen requires relatively specialized
morphology (e.g., elongated snouts and tongues),
relatively few members of these families are obligate
(or nearly so) pollinators. Only 15 species in six gen-
era are morphologically specialized nectar-feeders
in the Pteropodidae; other members of this family
are primarily fruit-eaters, although species in gen-
era such as Cynopterus ,Epomophorous,andPtero-
pus also visit flowers opportunistically (Fig. 3). The
Phyllostomidae contains a diverse array of feeding
adaptations (Table 1), but over one half of its species
are plant-visitors. About 38 species in 16 genera are
specialized nectar-feeders; 90 species in 22 genera
are primarily frugivorous, although a number of
these in genera such as Artibeus,Carollia,andPhyl-
lostomus also visit flowers (Fig. 4).
Unlike predation, which is an antagonistic pop-
ulation interaction, pollination and seed dispersal
are mutualistic population interactions in which
plants provide a nutritional reward (nectar, pollen,
and fruit pulp) for a beneficial service: pollen and
seed dispersal. Bats, along with many other flower-
visiting and fruit-eating animals, provide important
mobility for plant gametes and propagules. As a re-
sult, there has been extensive coevolution between
plants and their pollinators and seed dispersers.
Figure 3. Wahlberg’s epauletted fruit bat (Epomophorus
wahlbergi) approaching a baobab flower of which it pollinates
(photo by Merlin D. Tuttle, Bat Conservation International,
www.batcon.org).
Ann. N.Y. Acad. Sci. 1223 (2011) 1–38 c
2011 New York Academy of Sciences. 13
Ecosystem services provided by bats Kunz et al.
Figure 4. (A) Lesser long-nosed bat (Leptonycteris curasoae)
approaching a Saguaro cactus flower of which it pollinates
(photo by Merlin D. Tuttle, Bat Conservation International,
www.batcon.org). (B) Jamaican fruit bat (Artibe us jamaicen-
sis) removing a ripe tropical almond fruit (Terminalia catappa)
before taking off in flight (photo by Merlin D. Tuttle, Bat Con-
servation International, www.batcon.org).
Bat pollination occurs in about 528 species in
67 families and 28 orders of angiosperms world-
wide (Fig. 4). Pteropodid bats are known to pol-
linate flowers of about 168 species in 100 genera
and 41 families; phyllostomid bats pollinate flowers
of about 360 species in 159 genera and 44 fami-
lies.145 Most of the plants pollinated by pteropodid
bats, which are substantially larger than phyllosto-
mids, are canopy trees or shrubs, whereas those pol-
linated by the smaller phyllostomids are epiphytes
andlianasaswellastreesandshrubs.
146 The fruit
diets of phyllostomids are much better known than
those of pteropodids. A total of at least 549 species in
191 genera and 62 families are dispersed by bats in
the Neotropics.147 Pteropodid bats are known to eat
fruit from at least 139 genera in 58 families.148 As in
the case of flowers, most fruits eaten by pteropodid
bats are produced by trees or shrubs, whereas those
eaten by phyllostomids include fruits produced by
epiphytes and vines as well as trees and shrubs.
Major plant families (in terms of number of gen-
era) containing species either pollinated or dis-
persed by the two families of bats are listed in
Table 3. Reflecting the independent evolution of
bat–plant interactions in Old and New World plant
lineages, only a few families are common in the di-
ets of both bat families. For flowers, these include
Fabaceae, Malvaceae (especially subfamily Bom-
bacoideae, formerly known as Bombacaceae), and
Bignoniaceae (in which bat flowers occur in differ-
ent clades in the Old and New Worlds). For fruits,
these include Arecaceae (palms) and Sapotaceae.
Although only represented by a few genera in the di-
ets of bats, a few additional families are notable for
containing many species of bat-pollinated flowers
or bat-dispersed fruit. In the New World, these in-
cludeflowers(CampanulaceaeandMarcgraviaceae)
and fruit (Araceae, Cecropiaceae, Clusiaceae, Piper-
aceae, and Solanaceae). In the Old World, these in-
clude fruit (Moraceae). Figs (Moraceae) are very
important in the diets of both pteropodid and phyl-
lostomid bats worldwide (Fig. 5).
The evolution and ecology of bat–plant interac-
tions are discussed in detail in Fleming,149 Fleming
Tab l e 3. Examples of the most important angiosperm families (in terms of number of plant genera, in parentheses)
whose flowers are pollinated and/or seeds dispersed by pteropodid and phyllostomid batsa
Bat family Pollination Seed dispersal
Pteropodidae Bignoniaceae (10), Fabaceae (11), Malvaceae (7),
Myrtaceae (8), Sapotaceae (7)
Anacardiaceae (8), Arecaceae (7), Meliaceae (8),
Rubiaceae (7), Sapotaceae (10)
Phyllostomidae Cactaceae (26), Fabaceae (23), Malvaceae (18),
Solanaceae (7), Bignoniaceae, Bromeliaceae,
Gesneriaceae (6)
Arecaceae (15), Cactaceae (11), Moraceae (10),
Myrtaceae (10), Sapotaceae (6)
aSources of data: work by Fleming et al.;145 Lobova et al.;147 and Mickleburgh et al.148
14 Ann. N.Y. Acad. Sci. 1223 (2011) 1–38 c
2011 New York Academy of Sciences.
Kunz et al.Ecosystem services provided by bats
Figure 5. Gambian epauletted fruit bat (Epomophorus gam-
bianus) taking flight after plucking a fig infructescence
(photo by Merlin D. Tuttle, Bat Conservation International,
www.batcon.org).
and Kress,150 Fleming and Muchhala,146 Fleming
et al.,145 Lobova et al.,147 and Muscarella and Flem-
ing.151 Here, we discuss these interactions in terms
of the ecosystem services that provide direct and
indirect benefits to humans.
Services providing direct benefits to humans
Although bat pollination is relatively uncom-
mon compared with bird or insect pollination in
angiosperms, it involves an impressive number of
economically and/or ecologically important plants
(Table 4). In arid habitats in the New World, two
families, Agavaceae and Cactaceae, have enormous
economic and ecological value. Many species of pan-
iculate Agave rely heavily on phyllostomid bats for
pollination, and many of these same bats are also
major pollinators and seed dispersers of columnar
cacti.152 Three species of Leptonycteris bats are espe-
cially important in this regard in the southwestern
United States, Mexico, and northern South Amer-
ica (Fig. 4). The bat-pollinated A. tequilana is the
source of commercial tequila, a multimillion dol-
lar industry in Mexico; other species of Agave are
used locally to produce similar alcoholic beverages
such as pulque, mescal, and bacanora. Agaves are
also important sources of sisal fiber in many trop-
ical localities. Although bats are not the exclusive
pollinators of most species of Agave, they are crit-
ically important pollinators in tropical latitudes in
the New World.153 This is also true of bats polli-
nating columnar cacti. For example, bats are mi-
nor pollinators of the two northernmost columnar
cacti, Carnegiea gigantea and Stenocereus thurbei,in
the Sonoran Desert, but they are the nearly exclu-
sive pollinators of columnar cacti in south-central
Mexico and northern Venezuela.152
Large-scale cash crops produced by plants ei-
ther (originally) pollinated or dispersed by bats in-
clude nonnative bananas and mangos in the New
World and native bananas, breadfruits, durians,
mangos, and petai (Parkia speciosa) in the Old World
(Table 4). Of these, only durians and petai currently
rely on bats (among other animals) for pollination.
ThesameistruefortreessuchasCeiba pentan-
dra, the kapok tree, and Ochroma lagopus, the balsa
tree. Other bat-fruits that are harvested and sold lo-
cally include sapodilla and organ pipe cactus (Steno-
cereus) in the New World and the shea butter tree
(Vitellaria (Butyrospermum) parkii)inAfrica.
154–156
Many other species are listed in Table 4. Placing
a dollar value on the economic services of plant-
visiting bats is important but is beyond the scope
of this paper for at least two reasons: lack of read-
ily accessible information about the economic value
of many crops, especially ones that are sold locally,
and, more importantly, lack of detailed knowledge
about the actual contribution of bats to the pollina-
tion and/or seed dispersal of many of these plants.
In the case of cultivated plants, bats are no longer
needed to pollinate their flowers or disperse their
seeds. But the ecological services these bats provide
for their wild relatives are important for preserving
genetic diversity in these plants.
In India, the Mahwa tree (Madhuca indica), also
called the honey tree, sugar tree, or Indian butter
tree, is pollinated by Pteropus giganteus, Rousettus
leschenaulti,andCynopterus sphinx.157 These polli-
nation services highlight one of the highly valued
ecosystem services provided by plant-visiting bats
both culturally and economically. The timber of this
tree is used for making wagon wheels in India. The
flowers, also called honey flowers, are used as food
and for preparing a distilled spirit (matkom duhli).
Sun-dried fruits are directly consumed by humans,
and the oil extracted from flowers and seeds, known
locally as mahwa,mowrah butter,oryallah, is incor-
porated into soaps, candles, cosmetics (e.g., lipstick,
lotions), and lubricants, and used medicinally as an
emetic, an antirheumatic, and in the treatment of
leprosy. Extracts from the fruits are also thought to
prevent wrinkles and restore skin flexibility.158,159
Seedcakes made from M. indica are used as food
for cattle and goats160–163 and are known to increase
their milk production.164
Ann. N.Y. Acad. Sci. 1223 (2011) 1–38 c
2011 New York Academy of Sciences. 15
Ecosystem services provided by bats Kunz et al.
Tab l e 4. Examples of economically and ecologically important plants that are either pollinated (P) or dispersed (D)
by batsa
Plant family and
subfamily Taxon Service Comments
Economically important plants
Anacardiaceae Anacardium occidentale D Cashew, yields three major global and local
economic products: cashew (seed), cashew
apple (hypocarp), and cashew nutshell
liquid (mesocarp resin)262,263
Mangifera indica D Mango,commercialcropgloballyand
locally147
Spondias DS.cytherea,S.mombin,and S. purpurea fruits
are important locally in tropical America
and consumed fresh or preserved147
Annonaceae Annona DA. muricata (soursop), A. reticulata (custard
apple), A. squamosa (sweetsop) with edible
syncarps are locally important in tropical
America147
Araceae Anthurium, Philodendron D Commonly cultivated as ornamental plants147
Araliaceae Dendropanax arboreus D Cultivated ornamental and timber plant in
tropical America135,264,265
Arecaceae Acrocomia, Astrocaryum, Bactris,
Euterpe, Prestoea, Roystonea,
Sabal, Socratea
D Used as source of “palm-hearts,” especially
Euterpe edulis and E. oleraceae147
Euterpe edulis D Source of popular ac¸a´
ı fruits266
Phoenix dactylifera D Date palm, commercial crop and staple food
for Arabia and North Africa; leaves for
matting and thatch135,267,268
Roystonea regia D Royal palm, commonly cultivated267,269
Sabal palmetto D Leaves are commercially important source of
fibers and thatch; stems used for furniture
and wharf-piles267
Socratea exorrhiza D Wood used for construction135,147,262,270272
Agavaceae Agave, subgenus Agave P Paniculate agaves such as A. tequilana are used
to make tequila, mescal, bacanora, etc., with
high economic value; leaf fiber is used as
sisal153,273
Boraginaceae Cordia dodecandra D Cultivated for edible fruits and fine timber in
tropical America135
Cactaceae Many genera in tribe
Pachycereeae, subfamily
Cactoideae
P, D Native populations in the southwestern U.S.
and Latin America harvest fruits of
bat-pollinated cactus species in genera such
as Carnegiea,Pachycere us ,andStenocereus.
Some species of Stenocereus are grown
commercially for their fruits152,156
Continued
16 Ann. N.Y. Acad. Sci. 1223 (2011) 1–38 c
2011 New York Academy of Sciences.
Kunz et al.Ecosystem services provided by bats
Tab l e 4. Continued
Plant family and
subfamily Taxon Service Comments
Caricaceae Carica papaya D Papaya, widely cultivated in tropics for fruits
and as a source of papain used in culinary
and medical products147
Caryocaraceae Caryocar P, D Many species have seeds that are oil source in
tropical America; C. glabrum (soapwood)
inner bark used for washing135,274,275
Cecropiaceae Cecropia peltata D Wood used for pulp, also cultivated as
ornamental in tropical America147
Chrysobalanaceae Chrysobalanus icaco D Grown for edible fruits; seed oil used for
candles in West Africa147
Clusiaceae Clusia, Symphonia, Vismia D Resins are locally medicinal in South
America147
Combretaceae Terminalia catappa D Tropical almond, source of valuable timber,
edible seeds, tannins for dye, bark extract
for medicine in Indomalaya147
Cyclanthaceae Carludovica palmata D Panama hat palm, grown for hat manufacture,
important export plant for Ecuador, also
used for mats and baskets in tropical
America135,136,149,276
Ebenaceae Diospyros digyna, D. kaki D Grown for edible fruits (black sapote, Japanese
persimmon) in Central America and
Asia147
Fabaceae
Faboideae
Dipteryx odorata D Fragrant seeds used for scenting tobacco and
snuff147
Andira inermis D Valuable timber, bark used for medicine,
planted for shelter belts in West Indies
(cabbage-tree)147
Fabaceae,
Mimosoideae
Inga vera D Guaba, widely grown in South America for
edible fruit pulp, timber, shade, medicine,
and alcoholic beverage cachiri277,278
Parkia speciosa P Commercially important fruit species in
Southeast Asia154
Lecythidaceae Lecythis pisonis D Paradise nuts, cultivated in South America for
edible seeds147,279
Malpighiaceae Malpighia glabra D Barbados cherry, edible fruits high in vitamin
C, also ornamental in tropical
America135,262,280
Malvaceae,
Bombacoideae
Ceiba P Fibers from fruits of C. pentandra and other
species of Ceiba are used to make
kapok154
Malvaceae Ochroma P Balsa, world’s lightest commercial timber135
Continued
Ann. N.Y. Acad. Sci. 1223 (2011) 1–38 c
2011 New York Academy of Sciences. 17
Ecosystem services provided by bats Kunz et al.
Tab l e 4. Continued
Plant family and
subfamily Taxon Service Comments
Malvaceae,
Helicteroideae
Durio PD. zibethinus (durian) and several other
species of Durio are cultivated widely for
edible fruits and seeds in Southeast Asia and
elsewhere in the tropics135,154
Moraceae Artocarpus DA. altilis (breadfruit) and other species are
cultivated and sold commercially
throughout tropical Asia and Australasia as
a source of starch-rich infructescences147
Brosimum alicastrum D Breadnut, seeds are edible and valuable source
of fiber, vitamins, and microelements; leaves
used for fodder; latex and wood are also
utilized147
Ficus D Numerous species of fig used for rubber, fibers,
paper, timber, medicine, and as ornamentals
throughout the world tropics147
Muntingiaceae Muntingia calabura D Firewood crop in tropical America147
Musa ceae Musa P, D Bananas, pteropodid bats both pollinate
flowers and disperse seeds of wild bananas.
Cultivated bananas have very high
economic value147
Myrtaceae Anamomis umbellulifera D Edible fruits in West Indies135,262,280
Psidium guajava D Guava, cultivated for edible fruits, commercial
crop in tropical America147
Syzygium cumini, S. jambos, S.
malaccensis
D Rose apple, cultivated for edible fruits in Old
World tropics147
Passifloraceae Passiflora D Passionfruit, important edible tropical fruits147
Piperaceae Piper aduncum D Fruits edible in Puerto Rico147
Poly gonacea e Coccoloba uvifera D Seaside grape, cultivated for edible fruits in
tropical America147
Rhamnaceae Hovenia dulcis D Japanese raisin tree, swollen, fleshy pedicels are
sweet and edible; also used in medicine and
fortimberinAsia
281
Rosaceae Eriobotrya japonica D Loquat, native to Asia but widely cultivated
throughout world tropics for edible fruits147
Rubiaceae Coffea arabica D Coffee, native to Old World but cultivated for
seeds as source of coffee throughout the
world267
Rutaceae Casimiroa edulis D White sapote, cultivated for edible fruits in
Central America135
Salicaceae Flacourtia indica D Fruits edible and medicinal in Old World
tropics135,262,280
Sapindaceae Melicoccus bijugatus D Mamoncillo, edible fruits in tropical
America147
Continued
18 Ann. N.Y. Acad. Sci. 1223 (2011) 1–38 c
2011 New York Academy of Sciences.
Kunz et al.Ecosystem services provided by bats
Tab l e 4. Continued
Plant family and
subfamily Taxon Service Comments
Sapindus saponaria D Soapberry, fruits used as soap substitutes in
tropical America135,149,280
Sapotaceae Chrysophyllum cainito D Star-apple, cultivated for edible fruits in
tropical America147
Manilkara DSpeciesofManilkara, including M. zapota
(sapodilla), produce commercially valuable
fruits147
Mimusops elengi D Cultivated for fragrant flowers throughout
tropics135,262,280
Pouteria DP. sap o t a (sapote) is important Carribean fruit;
P. campechiana is also a source of edible
fruits in Central America147
Sterculiaceae Guazuma ulmifolia D Light timber for boats, barrels, and fuelwood
in tropical America263,267
Ulmaceae Trema micrantha D Used for pre-Hispanic barkcloth in tropical
America; soft timber for matches and chests;
also used in shade coffee
plantations265,282,283
Vitaceae Vitus vinifera D Grape vine, source of edible fruits and
alcoholic beverages, native probably to Asia,
broadly cultivated throughout the
world135,280,284
Ecologically important plants
Agavaceae Agave P Many species of paniculate agaves are
conspicuous members of arid upland
habitats in the Neotropics153,273
Arecaceae Many New and Old World genera D Palms are common elements of many tropical
forests, especially in the Neotropics147,148
Cactaceae,
Cactoideae
Many columnar cacti in several
tribes of this subfamily
P, D Columnar cacti are keystone species in many
arid Neotropical habitats152,156
Cecropiaceae Cecropia DSpeciesofCecropia are important pioneer trees
throughout the Neotropics151,285
Clusiaceae Vismia DVismia shrubs are important pioneer species
in the Neotropics151
Malvaceae,
Bombacoideae
Adansonia,Bombax,Ceiba,
Pachira,Pseudobombax,etc.
P Trees of this subfamily are often dominant (in
terms of basal area) members of tropical
forests worldwide135,286,287
Moraceae Ficus D Fig trees are often keystone members of
tropical forests worldwide169
Piperaceae Piper DPiper shrubs are pioneer plants and common
members of Neotropical forest
understories288
Continued
Ann. N.Y. Acad. Sci. 1223 (2011) 1–38 c
2011 New York Academy of Sciences. 19
Ecosystem services provided by bats Kunz et al.
Tab l e 4. Continued
Plant family and
subfamily Taxon Service Comments
Solanaceae Solanum DSolanum shrubs are pioneer plants and
common members of Neotropical forest
understories, particularly at
mid-elevations289
Ulmaceae Trema micrantha D Fast-growing pioneer tree265,282,283
aSource of commercial uses of these plants comes from work by Mabberley,155 unless noted. In cases when there are
more than three references of a particular bat–plant interaction, a reference to the appendices of the review, by Lobova
et al.,147 is given. Please note that for most of these plants, the precise quantitative role that bats play as pollinators and
dispersers is unknown.
Throughout much of India, there appears to be a
social taboo against cutting M. indica,probablydue
to its recognized value in tribal regions. However, in
the North Karanpura Valley, this is one of the most
threatened species, where it is being destroyed by the
thousands in coal mining regions.165 The economic
importance of pollination by fruit bats and the prod-
ucts derived from species such as the Mahwa tree
extend well beyond the borders of India. Increased
efforts are needed to educate government agencies,
industries, international corporations, and the gen-
eral public about the ecological and economic value
of plant-visiting bats to this species and other native
flowering and fruit-bearing trees.166
The tropical almond tree, Terminalia catappa
(Combretaceae) of Indomalaya, is an example of a
bat-dispersed tree with many human uses. This tree
is dispersed by Cynopterus bats throughout Asia. In
India, it is important in coastal communities where
it provides shade, fuel-wood, and edible nuts.164 The
timber derived from almond trees makes a decora-
tive general-purpose hardwood and is well suited for
making furniture and for interior building timbers.
Tannin is extracted from the bark, leaves, roots, and
the fruit shell. The large leaves are also used as wrap-
ping material and have many medicinal uses, includ-
ing diaphoretic, antiindigestion, and antidysentery.
Young leaves are used to cure headaches and colic.
A black dye is obtained from the bark, fruit, and fo-
liage. Its leaves and bark have a wide range of other
medicinal uses. Children sometimes consume the
outer flesh of agreeable fruit types. In the Philip-
pines, a wine is made by fermentation of mature
fruits.Thenutsmaybeconsumedfreshafterex-
tracted from the shell or preserved by drying or
smoking and consumed up to a year later. Sun-dried
kernels yield 38–54% of bland, yellow oil that is ed-
ible. The bark is used as an astringent for dysentery
and thrush.167,168
Services providing indirect benefits to humans
Over and above the economic value of their pollina-
tion and seed dispersal services, plant-visiting bats
provide important ecological services by facilitating
the reproductive success of their food plants, includ-
ing seed set and the recruitment of new seedlings
and saplings. Many of these plants are among the
most important species in terms of biomass in their
habitats (Table 4). In the New World, bat-pollinated
columnar cacti and agaves are dominant vegeta-
tion elements in arid and semiarid habitats as are
various species of Bombacoideae in dry and wet
tropical forests throughout the world. Bat-dispersed
palms and figs are also common in many tropical
forests worldwide. Because they are also eaten by
many birds and mammals, figs often act as keystone
species (i.e., species whose ecological impact often
exceeds their biomass) in tropical forests.169 Figs are
important bat-fruits throughout the tropics. Bat-
dispersed, soft-fruited species of Cecropia,Piper,
Solanum,andVismia are critically important early
pioneer species that are among the most abundant
plants during early primary and secondary succes-
sion in the Neotropics.151 Fruit-eating phyllostomid
bats thus play an extremely important role in forest
regeneration in the New World. This is not nec-
essarily true in the Paleotropics, where most early
successional plants are bird dispersed. Pteropodid
20 Ann. N.Y. Acad. Sci. 1223 (2011) 1–38 c
2011 New York Academy of Sciences.
Kunz et al.Ecosystem services provided by bats
bats play a more important role in the dispersal
of later successional trees than in the dispersal of
pioneer species.151 Some of these plants, such as
species of Pouteria and Plaquium (both Sapotaceae)
in Asia and Milicia (Chlorophora)excelsa and
Antiaris africana (both Moraceae) in Africa, are
important timber trees.170 An exception to this is the
dispersal of seeds of pioneer species of Ficus in the
Old World. During the recolonization of Krakatau,
for example, bird- and bat-dispersed figs were early
colonists and attracted frugivores that brought in
seeds of other plant taxa.171 Thus, bat-dispersed figs
likely “jump-started” forest regeneration on these
islands.
One of the most important ecological services
that bats provide for their food plants is long-
distance dispersal of pollen and seeds. This is es-
pecially true in arid New World habitats where Lep-
tonycteris species visiting the flowers of columnar
cactihavealargeforagingarea.
172 Flower-visiting
phyllostomid and pteropodid bats forage in both
continuous forest and forest fragments and, thus,
help to maintain genetic connections among frag-
mented plant populations. For example, phyllosto-
mid bats pollinating Hymenaea courbaril trees in
tropical dry forest fragments in Puerto Rico often
move pollen 600–800 m between individuals.226 In
Brazil, Phyllostomus species are known to move the
pollen of Hymenaea courbaril trees 18 km between
individuals in riverine forest.173 Glossophagine bats
regularly move pollen between individuals of the
canopy tree Ceiba pentandra within continuous for-
est and between forest trees and isolated pasture
trees in western Mexico.174 The Australian pteropo-
did Syconycteris australis usually moves pollen <
200 m between Syzygium cormiflorum trees but also
moves pollen up to about six km between individu-
als in different habitat patches.175
Most seed dispersal systems, including those in-
volving vertebrates, produce leptokurtic dispersal
distributions. That is, most seeds are dispersed close
to parent plants with only a few being dispersed
100s to 1,000s of meters away. Seeds dispersed by
frugivorous bats undoubtedly conform to this pat-
tern, but bats can also provide relatively long seed-
dispersal distances for their food plants. For ex-
ample, in central Panama the Jamaican fruit bat
Artibeus jamaicensis carries single fig fruits 100–
250 m away from fruiting plants before beginning
to feed in a night roost; it often feeds at several
trees located a kilometer or more apart in a sin-
gle night.176 Similarly, Cynopterus sphinx, the Asian
pteropodid ecological analogue of the Neotropical
A. jamaicensis, is known to forage on more than one
island in the Krakatau group in a single night.171 Al-
though it is generally a short-distance seed disperser,
the phyllostomid Carollia perspicillata is known to
move 1–2 km between foraging areas and frequently
moves seeds between habitats.149,177 In contrast to
forest-dwelling frugivorous birds, phyllostomid and
pteropodid bats readily fly over open areas and defe-
cate seeds in flight. As a result, phyllostomid bats
eating the small seeds of pioneer plant species pro-
vide substantial mobility for their seeds and help
them to quickly colonize forest treefall gaps and dis-
turbedareassuchasabandonedpasturesandlogged
forests.151
We close this section with a brief discussion of
an important conservation concern associated with
plant-visiting bats. Many species of nectar- or fruit-
eating bats annually migrate between a series of
landscapes, and these movements are driven by sea-
sonal fluctuations in the availability of flower or
fruit resources. In western Mexico, for example,
many individuals of the lesser long-nosed bat, L.
yerbabuenae, spend the fall and winter in tropical
dry forest where they mate. Here, they feed on the
flowers and fruit of dry tropical forest trees and
shrubs. In the spring, many females migrate up to
1,000 km north to form maternity colonies in the
Sonoran Desert where they feed on flowers and fruit
of columnar cacti. In late summer and early fall,
females and their offspring move into upland ar-
eas of southern Arizona and Sonora, Mexico, where
they feed at flowers of paniculate agaves before mi-
grating south again.178 Seasonal movements among
landscapes by flower-visiting bats are also known to
occur in northeastern Costa Rica, lowland Malaysia,
and in the eucalypt forests of eastern and northern
Australia.179–181 Similarly, some frugivorous phyl-
lostomid and pteropodid bats undergo altitudinal
or latitudinal movements.182,183 For example, pop-
ulations of the African pteropodid Eidolon helvum
migrate over 1,000 km annually from the Demo-
cratic Republic of Congo to central Zambia.184 Most
of the foraging areas along the migration route are
not protected by conservation legislation.
Because they often move across international bor-
ders, as well as among habitats that often do not
have state or federal protection, migratory species
Ann. N.Y. Acad. Sci. 1223 (2011) 1–38 c
2011 New York Academy of Sciences. 21
Ecosystem services provided by bats Kunz et al.
are of special conservation concern.183 This is es-
pecially true of vertebrate pollinators and seed dis-
persers whose movements and survivorship are of
critical importance for the reproductive success of
their food plants. Protection of migratory pathways
and critical feeding areas of migrants must be major
conservation goals worldwide.
Finally, some of the greatest conservation con-
cerns in bats involve island-dwelling species, in-
cluding nectar- and fruit-eaters.185,186 Because of
their remoteness, oceanic islands usually have re-
duced biodiversity and disharmonic (unbalanced)
faunas in which bats play an especially important
role in the pollination and dispersal biology of trees,
vines, and shrubs.187 As a result of overhunting,
persecution, and habitat destruction, many island
bats are critically endangered, and their conserva-
tion is of substantial concern to bat biologists and
ecologists.183,188,189
Provisioning and cultural services
Bats provide additional provisioning and cultural
ecosystem services beyond the regulatory services
(i.e., arthropod suppression, pollination, and seed
dispersal) that we have emphasized throughout this
paper. In this section, we briefly discuss these un-
derappreciated benefits to humans provided by bats
and then revisit them in the section on valuation of
ecosystem services.
Redistribution of nutrients from guano
Guano from bats has long been mined from caves
for use as fertilizer on agricultural crops due to
the high concentrations of nitrogen and phospho-
rous, the primary limiting nutrients of most plant
life.190,191 Although the benefits of nitrogen to plants
are well known, most of the evidence supporting
bat guano as fertilizer is anecdotal, and few studies
have explicitly measured its effects on plant growth
parameters.192 Because bats regularly or occasion-
ally roost in caves, they are thought to provide the
primary organic input to cave ecosystems, which
are inherently devoid of primary productivity.193–196
Cave-dwelling salamander and fish populations and
invertebrate communities, for example, are highly
dependent upon the nutrients from bat guano.197,198
Several researchers have begun to investigate the
potential ecological role of guano in nutrient redis-
tribution over the landscape via the “pepper-shaker
effect.”191,192,199,200 Because insectivorous bats con-
sume energy rich prey, experience rapid digestion
during flight, and forage significant distances over
heterogenous habitat types, it is expected that guano
is sprinkled over the landscape throughout the
night.201 Thus, bats contribute to nutrient redis-
tribution from nutrient-rich sources (e.g., lakes and
rivers) to nutrient-poor regions (e.g., arid or upland
landscapes). However, to date, no studies have ex-
plicitly tested this prediction. Reichard192 estimated
that a colony of one million Brazilian free-tailed
bats, Tadarida brasiliensis,inTexascouldcontribute
3,600,000 kJ/day of energy and 22,000 g of nitro-
gen in the form of guano. He also demonstrated
that moderate applications of guano in a controlled
greenhouse experiment promoted growth in a grass
species native to Texas (Indian grass, Sorghastrum
nutans), but reduced root/stem ratio and had a neu-
tral effect on two other native species: little bluestem,
Schizachyrium scoparium,andprairieconeowers,
Ratibida columnifera, respectively. He further spec-
ulated that guano deposition may have species-
specific effects on plant communities and thus em-
phasize the need for more in-depth experimental
and field studies. Other trophic ensembles (e.g., nec-
tarivorous, frugivorous, carnivorous bats) may sim-
ilarly contribute to nutrient cycling through guano
redistribution; however, we were not able to find any
studies investigating this potential service.
Bats in medicine and culture
As described in the introduction, bats have long been
feared in a diversity of human cultures. Although it
is beyond the scope of this paper to provide a full
treatment of this topic, it is important to also note
the value of bats to ancient and contemporary reli-
gions and cultures worldwide. Bat symbols appear
in priceless artifacts, such as wall paintings in Egyp-
tian tombs from 2000 B.C., Chinese bowls carved
of white jade, Japanese prints, and ancient temple
paintings of the Mayan bat god.18 In fact, the Mayan
“Zotzil,” the bat people, continue to live in south-
ern Mexico and Guatemala in cities with the same
name: “Tzinacantlan,” or the Bat City. These and
other cultural heirlooms are not only symbolically
cherished for their historical significance but also
generate direct revenue for the countries and muse-
ums that display them to curious tourists.
Bats have also long been used for food and
medicine.18,22 Witches and sorcerers used bats in
ancient magic to induce desire and drive away sleep.
22 Ann. N.Y. Acad. Sci. 1223 (2011) 1–38 c
2011 New York Academy of Sciences.
Kunz et al.Ecosystem services provided by bats
Shamans and physicians used bats to treat ailments
of patients ranging from baldness to paralysis.18,202
Some of these traditions continue today, though
bats are now consumed primarily as meat.22 One
exception is the anticoagulant compound that is
found in the saliva of the common vampire bat,
Desmodus rotundus. This compound, Desmodus ro-
tundus salivary plasminogen activator (DSPA), has
drawn considerable attention from the medical
community as a potential treatment for strokes be-
cause, unlike the alternatives, it can be administered
much later after a stroke has occurred and still be
effective.203
Today, bats provide aesthetic value through cave
visits, nocturnal tours in national parks, and edu-
cational nature programs. These activities provide
adventure and life memories for the public and
revenue for the communities and companies in-
volved.204 Bats also commonly appear as symbols
or logos in popular movies (e.g., Batman), products
(e.g., Bacardi rum), and holidays (e.g., Halloween),
all major revenue-generating endeavors.205 Finally,
the study of bat echolocation and locomotion has
provided inspiration for novel technological ad-
vances in such fields as sonar systems, biomedical
ultrasound, sensors for autonomous systems, wire-
less communication, and BATMAVs (bat-like mo-
torized aerial vehicles).206,207 Although extremely
difficult to quantify, it is important to recognize the
extraordinary value of bats to ancient and contem-
porary traditions and science.
Valuation of ecosystem services provided
by bats
As described in the preceding sections, bats provide
a variety of ecosystem services that improve human
well-being. To date, few studies have attempted to
place an economic value on these ecosystem ser-
vices. This section describes various methods that
could be used to value ecosystem services provided
by bats and then reviews the available studies that
have attempted to do so. Although some of these ser-
vices provide direct benefits to humans (e.g., food,
fuel, fiber, and fertilizer), most ecosystem services
offer indirect benefits (e.g., pest suppression, seed
dispersal, and pollination). Often times, little atten-
tion is paid to the “free” (i.e., nonmarketed) services
provided by ecosystems either because the benefits
of the services are not fully understood by decision
makers or because the benefits accrue to nonowners
of the ecosystem providing the service. Moreover,
little consideration has been given to the role of bats
in supporting entire cave ecosystems by providing
essential organic input that supports assemblages of
endemic cave flora and fauna. Information on non-
market values of ecosystem services can be used to
inform decisions regarding whether to protect ex-
isting ecosystem services, improve the current pro-
vision of ecosystem services, or restore previously
lost ecosystem services.4,208
The economic approach to valuation
Traditionally, economic valuation is the process of
measuring the human welfare gains or losses that
result from changes in the provision of ecosys-
tem services. The purpose of economic valuation
is to provide a common metric with which to com-
pare the impacts of alternative management or pol-
icy decisions among ecosystem services and other
market-based goods and services.4Consumer sur-
plus and producer surplus are the welfare measures
commonly used in economic valuation.208,209 Con-
sumer surplus is the amount that consumers would
be willing to pay for a good or service above the
amount that they actually pay, while producer sur-
plus is the amount that producers receive for a good
or service less what it costs them to produce it. Con-
sumer and producer surplus can be measured for
market-based goods (e.g., food) by direct estima-
tion of demand and supply functions. For nonmar-
keted goods and services, including most ecosystem
services, alternative valuation methods have been
developed.208,209 These methods fall into two broad
categories. Revealed preference approaches value of
ecosystem services through observing consumer or
producer behavior for related goods and services.210
For example, crop production often uses a variety of
ecosystem services as inputs.211 However, it is not
always possible to directly observe consumption or
production of ecosystem services. In addition, some
ecosystemserviceshavenonuseorexistencevalues.
In these cases, stated preference methods of valua-
tion, whereby individuals state their individual will-
ingness to pay for ecosystem services, can be used.212
While a complete assessment of valuation methods
is beyond the scope of this paper, Appendix B pro-
vides brief descriptions for the various methods that
could be used to value the ecosystem services pro-
vided by bats.
Ann. N.Y. Acad. Sci. 1223 (2011) 1–38 c
2011 New York Academy of Sciences. 23
Ecosystem services provided by bats Kunz et al.
Applying economic valuation to ecosystem
services provided by bats
Few studies have attempted to value the ecosystem
services provided by bats. In this section, we high-
light those that have been published. We also discuss
a small number of nonbat studies that describe an
interesting approach or present results that might
be similar to those used to value bats.
Regulating services. As described earlier, bats
provide a number of regulating services including
pest suppression, seed dispersal, and pollination
within both agricultural and natural ecosystems.
Determining the economic value of regulating ser-
vices provided by bats to natural ecosystems is ex-
tremely challenging and no studies were found.
Thus, we focus here on studies where the ecosys-
tem service is provided directly to the production of
goods and services consumed by humans.
One early study describing the economic impor-
tance of bats is that of Fujita and Tuttle,154 in which
the authors identify 289 Old World tropical plant
species that rely on the pollination and seed dis-
persal services of bats for their propagation (see
also Table 4). These plants, in turn, contribute to
the production of 448 bat-dependent products in
a variety of categories, including timber and other
wood products (23%); food, drinks, and fresh fruit
(19%); medicines (15%); dyes, fiber, animal fodder,
fuel wood, ornamental plants, and others. Fujita
and Tuttle154 describe the economic value of some
of these products; for example, fiber produced from
kapok trees is reported to be worth $4.5 million.
However, because bat-provided services represent
one input within a multi-input production process,
only a portion of the total value of the end product
can be attributed to bats. The primary contribution
of this study is in highlighting the expansive role that
bats play in the production of goods that contribute
to human well-being.
More recently, three studies assess the economic
importance of pollination services provided to
world agr iculture.213–215 In each study, the contribu-
tion of animal pollinators, including bats, to global
primary crop production is assessed. In an exten-
sive literature review, Klein et al.213 evaluate the de-
pendence on animal pollinators of primary agricul-
tural crops. Dependence categories are based on the
percentage of crop production that would be lost
without animal-mediated pollination, a damage
function type of analysis but without an economic
component. Their results show that while 87 pri-
mary crop species depend to some degree on ani-
mal pollination, these crops account for only 35% of
global production. Of the crops directly consumed
by humans, pollinators were found to be essential
for 13, highly dependent for 30, moderately depen-
dent for 27, slightly dependent for 21, unimportant
for 7, and of unknown significance for 9. The ma-
jority of these crops are pollinated by bees; however,
birds, bats, and other insects also contribute to the
pollination of the world’s leading crops.216 In partic-
ular, bats are important pollinators of durian (Durio
zibethinus), star apple (Chrysophyllum cainito), and
velvet bean (Mucuna pruriens). Production data for
these bat-dependent crops are not reported sepa-
rately but rather appear in aggregated crop group-
ings, so there is no way to extract the specific
value of bat pollination services from this study
or other studies that use Klein et al.’s dependence
values.
Gallai et al.214 combine pollination dependence
ratios with regional measures of crop production
and prices in an economic valuation of the pollina-
tion services provided to 100 world food crops. Of
these, 46 crops depend to some degree on animal
pollinators (6 essentially dependent, 13 highly de-
pendent, 13 moderately dependent, and 14 slightly
dependent), accounting for 39% of world produc-
tion value. The economic value of the portion of
crop production due to animal-dependent polli-
nation is calculated by multiplying the total pro-
duction value of each crop by its pollinator de-
pendence ratio, a damage function approach to
valuation. Summing over all crops, the total eco-
nomic value of global pollination services is es-
timated to be 153 billion ($200 billion), rep-
resenting 9.5% of the value of world food crop
production in 2005. A small portion of this total
is due to bat pollination services. Using rough ap-
proximations for demand functions, Gallai et al.
also estimate consumer surplus values for pollina-
tion services to be between 191 and 310 billion
($250 and $405 billion), indicating that the dam-
age function approach may underestimate the true
economic value for pollination services.
Bauer and Sue Wing215 develop a multiregion,
multisector model of global agricultural production
and trade that incorporates Klein et al.’s213 pollina-
tor dependence ratios as exogenous neutral shocks
24 Ann. N.Y. Acad. Sci. 1223 (2011) 1–38 c
2011 New York Academy of Sciences.
Kunz et al.Ecosystem services provided by bats
to four broad crop sectors. Pollinator loss scenar-
ios are implemented as catastrophic shocks to each
regional economy, with the services of animal pol-
linators being completely lost and the productiv-
ity of pollinator-dependent crops declining by the
corresponding dependence ratio. This general equi-
librium analysis estimates the crop sector losses to
be $10.5 billion globally, but total economy-wide
losses that account for price effects on downstream
sectors (e.g., processed foods) and households to be
$334.1 billion, an order of magnitude greater. Once
again, a small portion of this amount is due to bat
pollination services.
We found no studies that estimated the economic
value of seed dispersal services provided by bats.
However, multiple studies describe the ecological
relationship between bat-mediated seed dispersal
and timber volume for economically important tree
species.151,217 To estimate the economic value of the
seed dispersal service due to bats, the quantitative
relationship between the seed dispersal contribu-
tion of bats and the volume of marketable timber by
species, similar to Klein et al.’s213 pollinator depen-
dence ratio, would first need to be established. This
information could then be fed into economic analy-
ses similar to those described earlier for pollination
services.
One study estimating the economic value of seed
dispersal services provided by the Eurasian jay to
regeneration of giant oak in a Stockholm National
UrbanParkinSweden
218 mentions that bats do re-
side in the park, but it is unlikely that insectivorous
bats (the only bat feeding ensemble present in Swe-
den) would contribute to seed dispersal. Notwith-
standing, the study uses a replacement cost approach
that could be used to estimate the economic value of
seed dispersing bats. By first quantifying the number
of oaks that are due to jays, the authors then esti-
mate the costs associated with two different types
of manual replacement, seeding acorns, or plant-
ing saplings. The value of seed dispersal services per
pair of jays was estimated at SEK 35,000 ($4,935)
for seeding acorns and SEK 160,000 ($22,560) for
planting saplings, which aggregates up to between
SEK 1.5 million and SEK 6.7 million ($212,000 and
$945,000). The authors acknowledge Shabman and
Batie’s219 three conditions for use of the replace-
ment cost approach and argue that the first two
conditions are met by their study but concedeuncer-
tainty whether the third condition is met, although
they contend that public support for preservation
of giant oak is great.
Three related studies approximate the economic
value of pest suppression services provided by
Brazilian free-tailed bats to the production of cot-
toninTexas.
98,103,110 In the first study, Cleveland
et al.98 employed both damage function and re-
placement cost approaches in approximating the
economic value of bats’ pest control service across
a 4,000 Ha region. The damage function approach
required a detailed assessment of the ecological rela-
tionships between Brazilian free-tailed bats, cotton
bollworm adults, cotton bollworm larvae, and cot-
ton crops detailing how these relationships vary over
the course of the growing season. The value of the
avoided damage to cotton is approximately $0.02
per bat per night in mid-June (dropping to zero by
August) for a total annual value of $638,000. The re-
placementcostapproachwasbasedonanestimated
reduction of at least one pesticide application early
in the growing season due to high bat predation rates
keeping the number of cotton bollworm larvae be-
low the economic threshold for pesticide use. The
value of pesticides not used (i.e., replaced by the bat
service) is approximately $100,000 per year across
the region. Betke et al.103 used data collected with
thermal imaging technology to update the estimate
of bat population across this same cotton-producing
region. Feeding this information into the pesticide
allocation model used by Cleveland et al.,98 Betke
et al. present an updated measure for the pesticide
replacement cost of $500,000 annually.
The Cleveland et al.98 study, using values from
Pimentel et al.,77 also estimates the reduction in
external environmental costs resulting from lower
pesticide use at $3,000 per year. These external
costs are those nonprivate costs incurred by so-
ciety including loss of natural enemies, loss of
wild pollinators, groundwater and stream contam-
ination, and the impact on local bird and fish
populations.
Federico et al.110 develop a more detailed dy-
namic model of the bat–bollworm–cotton agroe-
cosystem, which includes multiple life stages for
both bats and bollworm and compares conven-
tional and transgenic cotton crops. Once again, the
pest control services provided by bats are approx-
imated through estimates of crop damage avoided
and number of pesticide applications reduced. Four
different crop-pesticide scenarios were assessed,
Ann. N.Y. Acad. Sci. 1223 (2011) 1–38 c
2011 New York Academy of Sciences. 25
Ecosystem services provided by bats Kunz et al.
resulting in a range of per-hectare values for bat
pest suppression services: (i) $86 for conventional-
spray, (ii) $757 for conventional-no spray, (iii) $46
for transgenic-spray, and (iv) $214 for transgenic-no
spray. By combining two valuation methods, both
Cleveland et al.98 and Federico et al.110 go beyond
the basic damage function approach by allowing
producers to vary a second production input (pes-
ticide applications) in their simulations. This use of
the replacement cost method seems appropriate as
it is based on the economic pest threshold concept
that cotton producers use in their decision-making
process for pesticide applications.
In an unrelated study, G´
andara Fierro et al.111 es-
timate the economic value of a population of Brazil-
ian free-tailed bats in Nuevo Le ´
on, Mexico to range
from 6.5 to 16.5 million Mexican pesos ($479,000–
1.2 million) with an average value of 260 pesos ($19)
per hectare. The authors use a simple replacement
cost method, basing their estimate on the identifica-
tion of potential insect pests in the guano of a large
colony of bats, surveys of 101 local farmers attesting
to the cost and use of pesticides and the presence or
absence of bats in different crops, and estimates by
Federico et al.220,221 that bats reduce crop damage
by 25–50%.
Rather than valuing the direct contribution of
regulating services to agricultural production, some
studies value the indirect contribution that natural
landscapes make by providing forage and nesting
habitat for pollinators, seed dispersers, and natu-
ral enemies.222,223 In this case, crop production is a
function of the quantity of nearby natural habitat.
While these studies have predominantly focused on
coffee production, which is bee-pollinated, the same
methods could be applied to bat-serviced crops re-
sulting in values for conservation of natural habitat
used by bats.
Provisioning services. Bats provide a direct
source of food in many countries.22 Although no
studies were found estimating market demand or
supply of bat bushmeat, several studies reported
anecdotal pricing information for local consump-
tion of bats ($2.50–3.50 per bat in Malaysia and $10
per bat in Jakarta for Pteropus vampyrus and P. h y -
pomelanus);154 (65 Naira [$0.43] per kg for Eidolon
helvum);224 ($0.50–1.25 for P. vampyrus natunae;225
[$0.50–1.50 for P. r u f u s ]226). In an analysis of
several types of bushmeat for vitamin and mineral
composition, bats were found to have the highest
value (i.e., lowest cost per kilogram) of protein.224
Several studies have reported on the overhunting
of bat bushmeat, indicating a need for further con-
servation efforts including recommendations for
the establishment of protected areas.186,225,227,228
However,anoteofcautionmaybeinorder,asFa
et al.229 reported a negative relationship between the
quantity of bushmeat harvested and the distance
between settlements and national parks for many
species, although bats were a very small percentage
of the total bushmeat harvested in their study area.
Bats also provide another marketable product,
bat guano, which is used as a natural fertilizer. Once
again, we were not able to find any formal stud-
ies estimating market demand and supply of guano.
However, an Internet search (keywords: bat guano
price) conducted in September of 2010 revealed
more than 950 bat guano products, clearly indicat-
ing a market for the product. Prices for bat guano
organic fertilizer varied between $1.25 and $12.00
per pound, depending on the size of the package
(larger packages have lower per-unit prices) and the
mix of ingredients.
Culturalservices. Although per haps not as widely
practiced as bird watching or whale watching, bat
watching is a growing recreational activity. The ma-
jority of bat viewing takes place at cave entrances
where nightly emergences can be viewed. Many sites
charge small fees ranging from $5 to $12 per visitor,
which can be interpreted as an individual’s mini-
mum willingness to pay to view bats.230 The 5th
Annual Austin Bat Fest reportedly drew over 40,000
participants to the area surrounding the Congress
Avenue Bridge, a roosting site for an estimated 1.5
million Brazilian free-tailed bats.231 Tickets to the
day-long event cost $7.00 and included a number
of band performances, crafts exhibits, and educa-
tional displays. The bridge is home to one of the
largest urban bat colonies in the United States, and
bat viewing at the bridge is typically free. A fiscal im-
pact study of bat-watching visitors estimated tourist
bat-related expenditures of $3 million per year, with
one third of the visitors coming from outside of
Tex a s . 232 Ecotourism clearly is one way to support
bat conservation.233
In terms of general conservation or existence val-
ues for bats, one recent contingent valuation study
included one species of bat (Myotis emarginata)in
26 Ann. N.Y. Acad. Sci. 1223 (2011) 1–38 c
2011 New York Academy of Sciences.
Kunz et al.Ecosystem services provided by bats
its assessment of willingness to pay for biodiver-
sity conservation in a national park in Spain.234
Through a photo questionnaire, bats (along with
snakes and spiders) were valued five times less than
other species (lynx and eagle) due in part to a lack
of understanding regarding their ecological role as
well as a potential aversion factor. This study high-
lights the need for further public education on the
ecosystem services provided by bats.
Challenges associated with valuation of
ecosystem services
It is not possible within this paper to fully de-
scribe the process involved in economic valuation of
ecosystem services. The National Research Council
(NRC)208 provides a book-length treatment of the
subject, and Appendix C offers a five-step summary
of guidelines. Here, we describe the major challenges
one might encounter when conducting a valuation
study.
The fundamental challenge of valuing ecosystem
services lies in providing an explicit description
and adequate assessment of the links between
the structures and functions of natural systems,
the benefits (i.e., goods and services) derived by
humanity, and their subsequent values. (NRC
2005, p. 2)208
As can be seen in the studies by Klein et al.,213
Cleveland et al.,98 and others, development of de-
tailed descriptions of ecological production func-
tions that quantitatively articulate relationships be-
tween bats and the marketed output requires much
effort at great cost. But these details are necessary in
order to estimate the economic value of the polli-
nation, seed dispersal, and pest suppression services
provided by bats to agricultural and natural systems.
It is tempting to try to use values from previous stud-
ies in new applications, a practice known as benefits
transfer. However, great care should be taken when
applying benefits transfer or when conducting orig-
inal studies that might be used in later studies.235,236
Similar care should be taken when scaling up re-
sults from field- or farm-level analyses to regional
or global analyses, as it is possible that stakeholder
values will vary at different spatial scales.237 It is
also important to clearly define the change (increase
or decrease) in the ecosystem service that is being
valued.238
As noted above, direct estimation of supply or
cost functions is difficult due to lack of data that in-
cludes measurements of the ecological entities (e.g.,
bats and bollworms). Efforts should be made to
collect these types of data, at least for important
crop systems. This includes getting information on
other inputs into the production process and assess-
ing producer decision making when various inputs
change.Itislikelythatmanyagriculturalproducers
are unaware of the services that bats provide because
much of this activity occurs at night. Producer sur-
veys could be used to provide education as well as
elicit information on producer decision making.
The majority of valuation studies of ecosystem
services focus on a single service. Additional chal-
lenges exist when attempting to measure values
for multiple ecosystem services because double-
counting of services is possible and tradeoffs be-
tween services may exist.238–240
Summary and conservation considerations
Ecosystem services are the benefits that humans ob-
tain from ecosystems that enhance their well-being.
As reviewed here, bats provide many ecosystem ser-
vices. Humans derive direct benefits from bats as
food, guano for fertilizer, and through contributions
to medicine and culture. Perhaps more significantly,
yet much more difficult to quantify, humans derive
indirect benefits from bats through arthropod sup-
pression, forest regeneration, and maintenance via
seed dispersal and pollination of a wide variety of
ecologically and economically important plants. In
turn, the contribution of these services by bats to
healthy, functioning ecosystems provides additional
benefits to humans by supporting vital regulatory
processes such as climate regulation, nutrient cy-
cling, water filtration, and erosion control. Unfor-
tunately, many misconceptions about bats persist,
especially in the neotropics, where humans regularly
have negative interactions with vampire bats;205
thus, conservation efforts often fall short. Assigning
values to the different ecosystem services provided
by bats is one way of positively influencing the
public’s perception of these beneficial mammals;
however, economic valuation of these services re-
mains in its nascency. Here, we have reviewed most
of the existing literature on the three primary ecosys-
tem services provided by bats and highlighted areas
of research that deserve further attention. We have
also outlined both market and nonmarket valua-
tion methods that either have been or could be used
to estimate the economic value of these ecosystem
Ann. N.Y. Acad. Sci. 1223 (2011) 1–38 c
2011 New York Academy of Sciences. 27
Ecosystem services provided by bats Kunz et al.
services. As was noted by the few published stud-
ies, these values can be quite substantial. However,
a distinct challenge exists in that most of these ef-
forts require detailed descriptions of ecological pro-
duction functions (e.g., Klein et al.’s213 pollinator
dependence ratios) or consumer surveys of house-
holds in developing countries that require substan-
tial time and monetary investments. Nevertheless,
at a time when critical threats face bat populations
(e.g., white-nose syndrome) and biodiversity as a
whole is rapidly declining worldwide, the develop-
ment of alternative conservation strategies—such
as the valuation of ecosystem services—should be-
come a priority.
Acknowledgments
We wish to thank Merlin D. Tuttle and Bat Con-
servation International for allowing us to use the
images of bats included in this paper, and Meera
Banta for assistance. We also wish to thank Justin
Boyles and two anonymous reviewers for making
valuable suggestions on an earlier version of this pa-
per. Lastly, we wish to thank Rick Ostfeld and Bill
Schlesinger, Cary Institute for Ecosystem Studies,
for inviting us to prepare this chapter, and Douglas
Braaten, director and executive editor of Annals of
the New York Academy of Sciences, for his patience.
Appendix A:
Examples of economic and ecological
damage caused by insect pests consumed
by bats
June beetles. Adults are herbivorous and have the
potential to defoliate trees in large numbers; their
larvae, white grubworms, attack the roots of grasses
and various crops such as corn, wheat, oats, barley,
sugarbeets, soybeans, and potatoes.247,248
Wireworms/Click beetles. Wireworms, click
beetle larvae, cause several million dollars worth
of damage annually, and no crop is known to be
entirely immune.249
Leafhoppers and planthoppers. Thesetruebugs
are vectors of plant pathogens such as the rice dwarf
and the maize mosaic viruses, as well as phytoplas-
mas and bacteria.250 The brown planthopper has
resulted in cumulative losses of rice estimated in the
hundreds of millions of dollars, and other species
act as serious agricultural pests to potatoes, grapes,
almonds, citrus, and row crops.251
Spotted cucumber beetles (Diabrotica undecim-
punctata). Serious pests of corn, spinach, and var-
ious cucurbit vines.86 In their larval stages, Diabrot-
ica spp. (referredtoascornrootworms)decimate
corn crops, costing farmers in the United States an
estimated $1 billion annually in crop yields and costs
of pesticide applications. The United States Depart-
ment of Agriculture (www.usda.gov) reports that
more hectares of cropland are treated with insecti-
cide to control corn rootworm than any other pest
in the United States.
Stinkbugs. Serious pests of various crops in-
cluding apples, pecans, soybeans, cotton, field
corn, grain sorghum, peaches, and vegetables.252
Stinkbugs pierce plant tissues with their mandibular
and maxillary stylets to extract plant fluids, which
results in staining of the seed, deformation and abor-
tion of the seed and fruiting structures, delayed plant
maturation, and the predisposition to colonization
by pathogenic organisms.
Gypsy moths. Serious pests of several hundred
species of trees, bushes, and shrubs, both hardwood
and conifer, and can lead to the complete defolia-
tion when in high enough densities.253 Introduced
into North America in the late 1800s, their range
has continually expanded westward and now threat-
ens temperate forested ecosystems throughout the
northeast.254
Tent caterpillars. Have irruptive population dy-
namics, generally advancing to pest status every
year in some regions of the United States and caus-
ing considerable defoliation of trees over extensive
areas.255
Coneworms. Larvae feed within cones on cone
scales and seeds of various species of firs and west-
ern pines,256 and can cause significant damage to
fertilized conifer plantations and loblolly pine seed
orchards.257,258
Cutworms. Destructive garden pests, causing fa-
tal damage to nearly any type of vegetable, fruit, or
flower.259
Tortrix moths. Many moths of the genus Cydia are
economically important due to the damage they in-
flict on fruit and nut crops, and include notable pests
such as the coddling moth, pear moth, alfalfa moth,
and hickory shuckworm moth.
Snout moths. Members of the genus Acrobasis
feed on a wide variety of shoots, nuts, and fruits
28 Ann. N.Y. Acad. Sci. 1223 (2011) 1–38 c
2011 New York Academy of Sciences.
Kunz et al.Ecosystem services provided by bats
including alders, birches, hickories, pecans, and
cranberries.
Corn earworm and tobacco budworm moths.
Rank among the top pests in the United States in
damage caused to crops and number of insecticides
applied to crops to control them.260 In Texas, corn
earworms are present in an estimated 98% of corn-
fields. Each female corn earworm moth potentially
lays over 1,000 eggs in her lifetime,261 which then
develop into larvae that infest corn, cotton, or other
crops.
Appendix B:
Methods for the valuation of ecosystem
services
Revealed preference methods of valuation
Ecosystemservicessuchaspestsuppression,seed
dispersal, and pollination are often inputs into the
production of agricultural crops.211 Aproduction
function approach to valuation can be used to com-
pare the levels of agricultural production with and
without the ecosystem service or with a reduction
in the service.290 In these situations, the ecosystem
service input appears as an argument in the supply
or cost function along with other inputs to produc-
tion such as labor, capital, and materials (e.g., fer-
tilizers). Estimation of consumer and producer sur-
plus welfare measures using a production function
approach often requires substantial time-series or
cross-sectional panel data that include, among other
things, measurements of the ecosystem service input
(e.g., the number of bats feeding in each farm across
several farms across multiple growing seasons). Be-
cause there is often a lack of sufficient data, a damage
function approach to valuation is sometimes used.290
This approximation is based on the idea that arthro-
pod predators, seed dispersers, and pollinators re-
duce the loss of agricultural crops that would other-
wise result without the associated ecosystem service.
It is an approximation rather than a true estimate,
because it assumes that use of all other inputs to the
production process remain constant, and that the
price of the agricultural output does not change.
Although fewer data are required with the dam-
age function approach, challenges with establishing
clear ecological relationships between the ecosystem
service and agricultural output remain.
A related valuation method is the replacement cost
method in which the value of the ecosystem service
is estimated by what it would cost to replace the ser-
vice using an alternative approach. Forexample, pest
suppression services may be estimated by the cost
of the chemical pesticides that would be required to
provide the same level of production output. How-
ever, caution must be exercised when using replace-
ment costs as they do not reflect actual consumer
or producer behavior and, thus, are not true wel-
fare measures.208 For example, farmers might not
be willing to pay the full amount for equivalent pest
control. Shabman and Batie219 describe three con-
ditions that should be met when using replacement
costs in valuations of ecosystem services: the alter-
native must provide the same level of service, the
alternative must be the least-cost alternative, and
there should be substantial evidence that individ-
uals would be willing to pay for the alternative if
the ecosystem service were eliminated. It is this last
criterion that is typically difficult to ascertain.
Another revealed preference method for valu-
ation of ecosystem services is the hedonic pricing
method in which property values reflect a number
of characteristics of a parcel of land including any
ecosystem services provided from within the par-
cel itself or from neighboring parcels. The price of
a parcel can be broken down into a set of implicit
prices for each of the characteristics. This method is
commonly used for valuing air and water quality or
open space amenities, but could potentially be used
to value ecosystem services provided by bats.
A fifth revealed preference valuation technique is
the travel cost method, which estimates the recre-
ation values associated with ecosystem services. Us-
ing the opportunity cost of time and actual costs
incurred with traveling to a particular recreation
site, the demand for recreation can be estimated.
Expanding the analysis to multiple sites with vary-
ing levels of ecosystems services can elicit values for
particular services. Travel cost studies are often used
to assess ecotourism or sport hunting values.210
Food, fuel, and other goods are often harvested
directly from the ecosystem rather than being pur-
chased through markets. For example, bats are
hunted for local consumption in many develop-
ing countries.22 In these situations, time allocation
models can be used to estimate the time invested
in hunting and gathering versus other household
activities. These studies are typically conducted
through household surveys although a researcher
may directly observe the behavior.
Ann. N.Y. Acad. Sci. 1223 (2011) 1–38 c
2011 New York Academy of Sciences. 29
Ecosystem services provided by bats Kunz et al.
Stated preference methods of valuation
Stated preference methods of valuation such as con-
tingent valuation and conjoint analysis involve sur-
veys that contain hypothetical scenarios of ecosys-
tem services and elicit individual willingness to pay
for well-defined changes to one or more ecosystem
service.212 Despite some early concern over the use
of stated preference surveys, the techniques have im-
proved considerably over the past two decades and
are commonly accepted methods for eliciting non-
market values.4,208 Stated preference surveys are the
only economic valuation method available for as-
sessing existence values.
Appendix C:
Steps used in the valuation of ecosystem
services
There is no one-size-fits-all process for valuing
ecosystem services. Each valuation study has its own
policy context, within which is an associated set of
ecosystem services. The following five steps, adapted
from work by Hein et al.,237 NRC,208 and MEA,4are
offered as valuation guidelines. For each step, a set
of qualifying questions is provided.
Step 1. Identify the policy or decision context for the
valuation exercise:
What is the purpose and how will the results be
used?
Which ecosystem services will be included?
What is the appropriate geographic scale?
How is the valuation question framed?
Step 2. Assess the underlying ecology (structure,
functions, processes):
How well understood is the ecosystem of inter-
est?
Are important dynamics understood?
Are important nonlinearities and thresholds
understood?
Are the complexities of the system under-
stood?
Are the linkages between policy alternatives and
ecological responses understood?
Step 3. Translate ecological functions to ecosystem
services:
Can the outputs from the ecological models be
used as inputs to the economic models?
Are all direct and indirect linkages between eco-
logical functions and ecosystem services under-
stood?
Step 4. Translate ecosystem services to values:
What valuation methods are appropriate?
What data are available?
How will aggregation of values across individ-
uals, services, and time be handled?
How will double-counting be avoided?
Step 5. Assess the level of uncertainty:
What are the primary sources of uncertainty?
What methods will be used to address uncer-
tainty?
Are there important gaps in our knowledge?
Are there important potential irreversibilities?
Conflicts of interest
The authors declare no conflicts of interest.
References
1. Chivian, E. & A. Bernstein Ed. 2008. Sustaining Life. How
Human Health Depends on Biodiversity.OxfordUniversity
Press. New York.
2. Daily, G.C. 1997. Nature’s Services. Societal Dependence on
Natural Ecosystems. Island Press. Washington, DC.
3. Daily, G.C., T. S¨
oderqvist, S. Aniyar, et al. 2000. The value
of nature and the nature of value. Science 289: 395–396.
4. Millennium Ecosystem Assessment. 2003. Ecosystems and
Human Well-Being: A Framework for Assessment .Island
Press. Washington, DC.
5. Millennium Ecosystem Assessment. 2005. Ecosystems and
Human Well-Being: Synthesis. Island Press. Washington,
DC.
6. Kremen, C. 2005. Managing ecosystem services: what do
we need to know about their ecology? Ecol. Lett. 8: 468–
479.
7. Simmons, N.B., K.L. Seymour, J. Habersetzer & G.F. Gun-
nell. 2008. Primitive Early Eocene bat from Wyoming and
the evolution of flight and echolocation. Natu re 451:U818–
U816.
8. Schipper, J., J.S. Chanson, F. Chiozza, et al. 2008. The status
of the world’s land and marine mammals: diversity, threat,
and knowledge. Science 322: 225–230.
9. Simmons, N.B. 2010. Personal Communication.American
Museum of Natural Histor y. Ne w York.
10. Patterson, B.D., M.R. Willig & R.D. Stevens. 2003. Trophic
strategies, niche partitioning, and patterns of ecolog-
ical organization. In Bat Ecology. T.H Kunz & M.B.
Fenton, Eds.: 536–579. University of Chicago Press.
Chicago.
11. Simmons, N.B. & M. Conway. 2003. Evolution and ecolog-
ical diversity of bats. In Bat Ecology. T.H. Kunz & M.B. Fen-
ton, Eds.: 493–535. University of Chicago Press. Chicago.
30 Ann. N.Y. Acad. Sci. 1223 (2011) 1–38 c
2011 New York Academy of Sciences.
Kunz et al.Ecosystem services provided by bats
12. Kunz, T.H. 1982. Ecology of Bats. Plenum Press. New York.
13. Kunz, T.H. & L.F. Lumsden. 2003. Ecology of cavity and
foliage roosting bats. In Bat Ecology. T.H. Kunz & M.B.
Fenton, Eds.: 3–89. University of Chicago Press. Chicago.
14. Kunz, T.H., M.S. Fujita, A.P. Brooke & G.F. McCracken.
1994. Convergencein tent architecture and tent-making be-
havior among neotropical and paleotropical bats. J. Mamm.
Evol. 2: 57–78.
15. Rodr´
ıguez-Herrera, B., R.A. Medell´
ın & R.M. Timm.
2007. Murcielagos Neotropicales Que Acampan enHhojas.
Neotropical Tent-Roosting Bats.InstitutoNacionaldeBio-
diversidad. Santo Domingo de Heredia, Costa Rica.
16. Chaverri, G. & T.H. Kunz. 2010. Ecological determinants of
social systems: perspectives on the role of roosting ecology
in the social behavior of tent-roosting bats. In Behavioral
EcologyofTropicalAnimals,AdvancesintheStudyofBehav-
ior. R. Macedo, ed.:Vol. 42, 275–318. Elsevier. New York.
17. Lewis, J.R. & E.D. Oliver. 1996. Angels A to Z. Visible Ink.
Detroit, Michigan.
18. Allen, G.M. 1962. Bats:Biology,Behavior,andFolklore.Har-
vard University Press. Cambridge, MA.
19. Tupinier, D. 1989. La Chauve-souris et L’homme.
L’Harmattan. Paris.
20. Nabhan, M.L., J.R. Aliperti, J. Feng & T.H. Kunz. 2010.
Bats and Wind Energy Development in China: An Emerging
Threat to Cultural and Ecological Harbingers of Good For-
tune. Unpublished manuscript. Boston University, Boston,
MA.
21. Eiting, T.P. & G.F. Gunnell. 2009. Global completeness of
the bat fossil record.