Ramirez-Franceletal2021Bats and Their Vital Ecosystem Services - A Global Review

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Bats and their vital ecosystem services: A global review
Article in Integrative Zoology · May 2021

DOI: 10.1111/1749-4877.12552
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Integrative Zoology 2021; 0: 1–22 doi: 10.1111/1749-4877.12552
REVIEW
Bats and their vital ecosystem services: a global review
Leidy Azucena RAMÍREZ-FRÁNCEL,1,2 Leidy Viviana GARCÍA-HERRERA,1,2

Sergio LOSADA-PRADO,3 Gladys REINOSO-FLÓREZ,3 Alfonso SÁNCHEZ-HERNÁNDEZ,4
Sergio ESTRADA-VILLEGAS,2,5,6 Burton K. LIM7 and Giovany GUEVARA3
1
Programa de Doctorado en Ciencias Biológicas & Grupo de Investigación en Zoología (GIZ), Facultad de Ciencias, Universidad del
Tolima, Ibagué, Colombia, 2 Programa para la Conservación de los Murciélagos de Colombia, Bogotá D.C., Colombia,
3
Departamento de Biología & Grupo de Investigación en Zoología (GIZ), Facultad de Ciencias, Universidad del Tolima, Ibagué,
Colombia, 4 Departamento de Matemáticas y Estadística, Facultad de Ciencias, Universidad del Tolima, Ibagué, Colombia, 5 Yale
School of the Environment, Yale University, New Haven, Connecticut, USA, 6 Smithsonian Tropical Research Institute, Balboa,
Republic of Panama and 7 Department of Natural History, Royal Ontario Museum, Toronto, Ontario, Canada
Abstract
Bats play crucial ecosystem services as seed dispersers, pollinators, controllers of insects, and nutrient recyclers.
However, there has not been a thorough global review evaluating these roles in bats across all biogeographical
regions of the world. We reviewed the literature published during the last two decades and identified 283 relevant
studies: 78 dealt with the control of potential insect pests by bats, 80 related to the suppression of other arthro-
pods, 60 on the dispersal of native or endemic seeds, 11 dealt with the dispersal of seeds of introduced plants,
29 on the pollination of native or endemic plants, 1 study on pollination of introduced plants, and 24 on the use
of guano as fertilizer. Our literature search showed that queries combining the terms “seed dispersal,” “insectiv-
orous bats,” “nectarivorous bats,” “use of guano,” and “ecosystem services” returned 577 studies, but half were
experimental in nature. We found that the evaluation of ecosystem services by bats has been mostly conducted in
the Neotropical and Palearctic regions. To detect differences across relevant studies, and to explain trends in the
study of ecosystem services provided by bats, we performed generalized linear mixed models (GLMM) fitted with
a Poisson distribution to analyze potential differences among sampling methods. We identified 409 bat species that
provide ecosystem services, 752 insect species consumed by bats and 549 plant species either dispersed or polli-
nated by bats. Our review summarizes the importance of conserving bat populations and the ecological services
they provide, which is especially important during the current pandemic.
Key words: chiroptera, ecosystem services, frugivory, guano, insectivory, nectarivory, pest control, pollination,
seed dispersal
INTRODUCTION
Correspondence: Leidy Azucena Ramírez-Fráncel, Programa Bats contribute to the maintenance of environmental
de Doctorado en Ciencias Biológicas & Grupo de Investigación stability through ecosystem provisioning and regulating
en Zoología (GIZ), Facultad de Ciencias, Universidad del services such as insect pest control, pollination, seed dis-
Tolima, Altos de Santa Elena, Ibagué, Colombia.
persal, and production of guano as plant fertilizer (Mil-
lennium Ecosystem Assessment 2005; Kunz et al. 2011).
Email: [email protected]
© 2021 International Society of Zoological Sciences, Institute of Zoology/ 1

Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd.
L. A. Ramírez-Fráncel et al.
Even though bats are fundamental to the functioning of graphic ranges (Toyama et al. 2012), we need more re-
natural and modified landscapes, there are misconcep- search to quantify the pollen loads carried by bats, the
tions that have led to the underestimation of the ecolog- effectiveness of pollen transfer, and the monetary value
ical roles that bats play (Cleveland et al. 2006; Kalka of such service (Sheherazade 2018).
et al. 2008; Boyles et al. 2011; De Carvalho-Ricardo et al. Bats play an important ecological role in soil fertility
2014; Medellin et al. 2017; Kemp et al. 2019). There- and nutrient distribution. Bats facilitate nutrient transfer
fore, it is paramount to adequately quantify and highlight through their guano because they are highly mobile and
the benefits humans receive from bats in order to promote can use different shelters and habitats for feeding and rest-
their conservation. ing. For example, a colony of a million bats of T. brasilien-
Recent studies have shown that the regulating services sis in Texas can produce 22 kg of nitrogen in the form
bats provide are crucial to food production (Williams- of guano (Kasso & Balakrishnan 2013). In Thailand and
Guillén et al. 2016; Whitby et al. 2020). Bats are efficient Cambodia, the collection of guano in refuges of Mops
top-down regulators of at least 12 orders of insects, some plicatus and Scotophilus kuhlii contributes to the local
of which are agricultural pests, including Coleoptera, economy (Leelapaibul et al. 2005; CBNRM 2009; Chhay
Diptera, Hemiptera, Isoptera, and Lepidoptera (Kunz 2012), and its use increases the growth of plants compared
et al. 2011). Bats that eat insects reduce costs of artificial to other types of fertilizers (Sothearen et al. 2014).
controlling measures (Williams-Guillén et al. 2008). For Although bats provide essential ecosystem services,
example, Tadarida brasiliensis benefits farmers in south- more than a third of all bat species assessed by the In-
ern Texas, USA, by avoiding costs of insecticide use and ternational Union for Conservation of Nature (IUCN) are
loss of cotton production that amount to US$ 741 000 considered threatened or data poor, and more than half
a year (Cleveland et al. 2006). Likewise, Mops plicatus have unknown population trends. In the last Red List is-
(= Tadarida plicata in all studies we reviewed), prevents sued by IUCN, 77 species are endangered (Fenton et al.
the loss of thousands of tons of rice in Thailand due to in- 2020). Additionally, at least 988 of the approximately
sect infestations that cause serious damage to these crops 1400 known bat species need urgent conservation ac-
(Wanger et al. 2014). Although the importance of bats in tions and further research (Frick et al. 2020). The main
controlling insect pests is known in North America and threats faced by bats are habitat loss, damage to roosts,
Europe, there is still an information gap in developing and hunting (IUCN Species Survival Commission 2001;
countries where food production is usually at small spatial Red Latinoamericana y del Caribe para la Conservación
scales and embedded in heterogeneous matrices of land de los Murciélagos RELCOM 2010). Another less ob-
cover types (Carle et al. 2002; Ghanem & Voigt 2012). vious threat is our incapacity to adequately assess the
The functional role that bats play in seed dispersal ecosystem services bats provide, mostly because of their
is also an ecosystem service of paramount importance. nocturnal and cryptic lifestyles. Moreover, bats are er-
The Neotropical leaf-nosed bats (Phyllostomidae) facili- roneously stigmatized in many areas of the word, and
tate forest succession by dispersing seeds in open areas, the current acute respiratory syndrome COVID-19 has
speeding up forest regeneration (Mesquita et al. 2001). generated fear, to the point of harming bat populations
In the Paleotropics, the environmental services provided (Bonilla-Aldana et al. 2020; Gutiérrez et al. 2020; Rocha
by flying foxes (Pteropodidae) contribute to the mainte- et al. 2020; Tiwari et al. 2020). For instance, there was
nance of a significant number of plants. For example, fly- a surge of reported events to evict bats from dwellings
ing foxes disperse up to 34% of plants that have economic and structures, some of which led to direct bat deaths (Lu
importance in Africa (Muscarella & Fleming 2007). et al. 2021), reducing the ecosystem services these bat
Pollination is another essential ecosystem service, with populations provide. Therefore, it is urgent to prioritize
bats pollinating more than 500 species of angiosperms long-term projects where scientists and local communi-
worldwide with socioeconomic value, including crops ties work in unison to protect bats (Voigt & Kingston
such as durian, bitter beans, jackfruit, and cacti (Fleming 2016) and appreciate the ecosystem services we receive
et al. 1994; Franceschinelli & Bawa 2000; Herrera et al. from bats.
2001; Campbell et al. 2002; Dutech et al. 2002; Lim et al. One way to underscore the importance of bats to
2018b). Bats have been found to be the main pollinator humans is to adequately quantify the impacts of the
of Durio zibethinus in Indonesia, a service that is valued ecosystem services bats provide. Given that previous
at ≈$ 117/ha during the fruiting season (Sheherazade & quantifications have not been exhaustive, here we make
Tsang 2019). Although bats are known to be important the most thorough evaluation of the ecological processes
pollinators of native species, some with restricted geo- related to each service, identify gaps in our knowledge,
2 © 2021 International Society of Zoological Sciences, Institute of Zoology/

Bats and ecosystem services
and define priorities for future research on the economic We tested for differences in the assessment of the
benefits of bats. The objectives of our study were to 4 ecosystem services using a generalized linear mixed
investigate the impact of bats as insect controllers, seed model (GLMM; Stasinopoulos & Rigby 2007). This
dispersers, flower pollinators and producers of fertilizer method allowed us to compare the number of studies per
based on research output during the past 2 decades across ecosystem service among biogeographic regions, habi-
different biogeographical regions of the world. tats, and methods employed. We used 2 sets of GLMM,
one to determine which cofactors were fixed or random,
and the other to determine the contribution of each fixed
MATERIAL AND METHODS effect on the response variable. These 2 GLMMs allowed
us to (1) identify the main cofactors used to assess ecosys-
Literature related to ecosystem services provided tem services by bats, (2) assess nonlinear impacts of the
by bats cofactors, (3) detect thresholds statistically, and (4) test
across a broad set of statistical families to ensure the
We searched the scientific literature published between best fit for the data. We employed a zero-inflated Poisson
January 2000 and July 2020 in Google Scholar, Google distribution because many combinations of cofactors and
Books, Scopus, ScienceDirect, and the Web of Knowl- levels were zero. Finally, we ranked all the models from
edge databases. Studies were searched in English, Span- the second GLMM based on !AIC values, and selected
ish, and Portuguese using the key terms: insectiv∗ or a final model with the lowest AIC (Jørgensen 2004). We
frugivor∗ or nectarivor∗ or pollinat∗ or guano in com- used R 3.3.3 software (R Core Team 2017) for all statisti-
bination with bat∗ or Chiroptera. We also searched for cal analyses. GLMMs were run using the gamlss and lme4
papers with the following combinations of terms: “forag- R-package (Table 1; Table S4, Supporting Information).
ing ecology + bat∗,” “insectivorous bats + feeding in-
sectivorous bat or diet∗ + bat insect pest + bat control
insect,” “frugivorous bats + seed dispersal + feeding fru-
givorous bats,” “nectarivorous bats + pollination by bats RESULTS
+ feeding nectarivorous bats,” “bat∗ prey,” and “use of We found 577 studies that investigated bat insect con-
guano + bat guano”. These keywords and combinations trol, seed dispersal, pollination and use of guano. We ex-
were selected to cover the maximum number of published cluded 200 studies because they were reviews, editorials,
studies, which often use a variety of terms to describe or conference summaries. Of the remaining, we excluded
the ecosystem services bats provide. Additionally, we in- 94 because they did not have a clear research question or
cluded studies from the references of the papers found did not postulate a hypothesis about the functional role of
by the search, as well as opportunistic additions from bats. The remaining 283 studies were reviewed for 2 cri-
personal bibliographies. The search was limited to pa- teria: (1) effectiveness of bats in insect control, dispersal
pers from experimental results with clearly stated research of seeds, pollination of either native or introduced plants,
questions or hypotheses (Table S1, Supporting Informa- and use of guano; and (2) information on the methodolo-
tion). Technical reports, reviews, conference summaries, gies used, such as fecal analysis, exclusion experiments,
and project reports were excluded. We updated taxonomic captive experiments, insect traps, germination tests, and
information from the literature searches to Simmons and whether studies were conducted in connected or isolated
Cirranello (2020); a taxonomic and geographic database landscapes (Fig. 2).
for bats (https://batnames.org/). The 283 studies were conducted in 53 countries, in 6
of the 7 biogeographic regions of the world (Morrone
2015), and in 2 transition zones (Chinese and Saharo-
Analyses and model selection
Arabian). The majority of the studies were conducted in
We first grouped all the studies by the type of en- the Neotropical region (38.87%), followed by the Palearc-
vironmental service (e.g. insect controllers), and then tic region (19.08%). The least represented regions were
discriminated studies by the following cofactors: world the Chinese and Saharo-Arabian transition zones (0.35%)
region, insect type, seed type, pollen type, guano use, (Fig. 3). Within the Neotropical region, most studies
habitat, and methods. We considered several levels within (15.55%) assessed ecosystem services related to the dis-
each cofactor according to different aspects of bat ecology persal of native or endemic seeds, followed by studies re-
(Fig. 1). The response variable was the number of studies lated to the consumption of arthropods (7.42%). In the
per ecosystem service. Palearctic region, most studies evaluated the control of

Figure 1 Factors and levels used for a global review of the ecosystem services provided by bats across the world. We employed a
complete factorial design among all factors by using an interaction term.
arthropods (8.13%), potential pest insects (7.77%), and studies on pollination, of which 29 addressed native or
the use of guano (3.18%, Fig. 4). endemic plants, and only one on introduced plants. We
The results presented herein are related to the ecosys- found 32 bat species that pollinate plants, which repre-
tem services provided by 18 of the 21 families of bats, sents 3% of all species from the 3 families that provide
excluding Cistugidae, Craseonycteridae, and Rhinonyc- this service (Pteropodidae, Phyllostomidae, and Vesper-
teridae, which account for only 13 species according to tilionidae). Finally, 24 studies assessed the use of guano
Simmons and Cirranello (2020). Of the 283 studies, 158 as fertilizer (Fig. 5). Twenty bat species have been used
focused on insect control, 78 on control of potential pest for their guano production, which only represents 2% all
insects, and 80 on control of other arthropods. We found species from 9 families (Fig. 6).
286 bat species from 17 familes that consume insects, We identified 3 insect orders, 26 families, and 238
which represents approximately 20% of all the bat species species of potential pests of agricultural crops. We also
(1413). There were 71 studies focused on seed dispersal; identified 13 insect orders, 112 families, and 510 species
60 on dispersal of native or endemic seeds, and 11 on of other arthropods consumed by insectivorous bats from
dispersal of introduced seeds. We found 111 bat species 17 families. The number of bat species per family re-
that disperse seed, which represents approximately 26% ported as insect controllers in relation to the total number
of all species from the 2 families that provide this ser- of species per family were: Emballonuridae 32.7%, Fu-
vice (Pteropodidae and Phyllostomidae). There were 30 ripteridae 50%, Hipposideridae 4.4%, Megadermatidae

Table 1 Results of the 3 GLM models applied to all the Table 1 (Continued)
analyzed datasets and their correspondent significance
Random-effects models
Linear of fixed-effects model
!AIC 1.669 Degrees of freedom for the fit: 36
X77 −0.381 0.448 −0.849 0.396
Factors Estimate SE t value P (>|t|) X78 −0.117 0.456 −0.256 0.798
X79 −2.098 0.813 −2.581 0.009∗∗
Intercep 1.18 0.521 2.267 0.023∗
X710 −2.893 1.072 −2.699 0.006∗∗
X1 0.208 0.045 4.586 <0.005∗∗∗
X711 0.632 0.338 1.868 0.061
X2 −0.399 0.167 −2.391 <0.005∗
X712 −1.305 0.498 −2.62 0.009∗∗
X3 −0.633 0.252 −2.515 <0.005∗
X713 0.569 0.424 1.343 0.179
X4 −1.537 0.281 −5.464 <0.005∗∗∗
X714 −1.29 0.528 −2.442 0.016∗
X5 −1.966 0.449 −4.376 <0.005∗∗∗
X715 −0.975 0.516 −1.887 0.059
X6 −0.2 0.078 −2.556 <0.005∗
X716 −2.2 0.801 −2.747 0.006∗∗
X7 −0.046 0.014 −3.172 <0.005∗∗
X717 −0.819 0.484 −0.169 0.091
Random-effects models X718 0.682 0.613 −1.112 0.266
Generalized linear mixed model

Intercept −2.494 6232 −3.804 <0.005 !AIC 1.424 Degrees of freedom for the fit: 6
X12 −2.494 0.398 1.318 0.187
(Intercept) −4.987 1.214 −4.108 <0.005∗∗∗
X13 0.525 0.398 1.318 0.187
X12 −2.485 1.035 −2.401 0.016∗
X14 0.853 0.37 2.304 0.0212∗
X13 0.693 0.352 1.97 0.049∗
X15 1.948 0.35 5.567 <0.005∗∗∗
X14 1.228 0.326 3.765 <0.005∗∗∗
X16 0.992 0.375 2.643 0.008∗∗
X15 2.215 0.302 7.329 <0.005∗∗∗
X17 1.492 0.363 4.111 <0.005∗∗∗
X16 1.178 0.328 3.59 <0.005∗∗∗
X18 −2.488 1.066 −2.334 0.019∗
X17 1.522 0.317 4.081 <0.005∗∗∗
X21 0.598 0.415 1.44 0.15
X18 −2.486 1.035 −2.401 0.016∗
X22 0.462 0.408 1.131 0.258
X62 −2.485 0.732 −3.395 <0.005∗∗∗
X31 0.518 0.413 1.253 0.21
X63 1.969 0.217 9.09 <0.005∗∗∗
X32 −0.933 0.497 −1.88 0.06
X64 0.714 0.248 2.881 0.004∗∗
X41 −0.224 0.438 −0.512 0.608
X65 0.405 0.262 1.547 0.122
X42 −3.559 1.078 −3.302 <0.005∗∗∗
X72 0.058 0.336 0.172 0.863
X62 −2.821 0.767 −3.679 <0.005∗∗∗
X73 1.278 0.273 4.686 <0.005∗∗∗
X63 1.267 0.304 4.171 <0.005∗∗∗
X74 0.778 0.291 2.671 0.007∗∗
X64 0.214 0.321 0.667 0.505
X75 −1.446 0.553 −2.617 0.009∗∗
X65 0.166 0.338 0.493 0.622
X76 −2.833 1.024 −2.768 0.004∗∗
X72 −0.348 0.397 −0.877 0.38
X77 −0.348 0.375 −0.927 0.354
X73 0.811 0.324 2.504 0.012∗
X78 −0.268 0.366 −0.731 0.465
X74 0.297 0.349 0.851 0.395
X79 −2.139 0.743 −2.878 0.006∗∗
X75 −1.589 0.613 −2.594 0.009∗∗
X710 −2.833 1.023 −2.768 0.006∗∗
X76 −2.89 1.067 −2.71 0.006∗∗
X711 1.245 0.274 4.547 <0.005∗∗∗
(Continued)
(Continued)

Table 1 (Continued) 9.4%, Thyropteridae 20%, and Vespertilionidae 30.6%.

For seed dispersal, we identified 32 plant orders, 70
Generalized linear mixed model
families, and 471 species of native or endemic seeds,
and 3 plant orders, 5 families and 26 species of seeds of
!AIC 1.424 Degrees of freedom for the fit: 6 introduced or exotic plants. The number of bat species
per family reported as seed dispersers in relation to the
X712 −0.887 0.447 −1.985 <0.005∗∗∗
total number of species in each family were Phyllosto-
X713 0.212 0.324 0.653 0.514 midae 37.2% and Pteropodidae 13.9%. We identified 7
X714 −1.041 0.472 −2.204 0.028∗ plant orders, 20 families, and 78 species of native or
X715 −0.887 0.447 −1.985 0.047∗ endemic species pollinated by bats, and 1 plant order,
X716 −2.139 0.743 −2.878 0.006∗∗ 1 family, and 6 species of introduced or exotic plants
X717 −0.635 0.41 −1.55 0.121
pollinated by 3 families of bats. The number of bat
species per family reported as pollinators in relation
X718 −1.041 0.472 −2.204 0.028∗
to the total number of species per family were: Phyl-
∗∗∗
, P < 0.0001; ∗∗ , P < 0.001; ∗ , P < 0.05. lostomidae 9%, Pteropodidae 5.5%, and Vespertilionidae
0.2% (Tables 2 and 3 and Tables S3–S5, Supporting
Information).
33.3%, Miniopteridae 22.9%, Molossidae 41.5%, Mor- Our initial GLMM included the 7 cofactors and 38 lev-
moopidae 55.6%, Mystacinidae 50%, Myzopodidae 50%, els, producing 5040 combinations, all used as fixed ef-
Natalidae 9.1%, Noctilionidae 100% Nycteridae 12.5%, fects Y = X1 + X2 + X3 + X4 + X5 + X6 + X7 + ε,
Phyllostomidae 6.3%, Pteropodidae 0.5%, Rhinolophidae where: Y is the number of studies; X1 (region), X2 (type
Figure 2 Flowchart for article selection and number of studies selected to conduct a global review of the ecosystem services provided
by bats.

Figure 3 Geographic distribution of studies assessing ecosystem services provided by bats across the world (N = 277). Biogeo-
graphical regions were modified from Morrone (2015). Pie charts indicate the proportion of studies per ecosystem servicefor each
biogeographical region. The countries with representative studies are highlighted and the asterisk (∗) corresponds to the location in
the Chinese region north of the city of Guangzhou, Guangdong Province.
of insect), X3 (type of seed), X4 (type of pollen), X5 (use The final statistical model was:
of guano), X6 (habitat), X7 (methods), and ε (statistical Yi = −4.98(intercept) + X14 (1.22) + X15 (2.21) +
error). We found that all the cofactors were highly signifi- X16 (1.17) + X17 (1.52) − X62 (2.48) + X63 (1.96) +
cant (P < 0.005). Therefore, we used the following mixed X73 (1.27) + X711 (1.24), where Yi represents the num-
effect model Y ∼ X1 + X6 + X7 (1 | X2) + (1 | X3) + (1 | ber of studies; −4.98 is the intercept; X1, X6, and X7 cor-
X4) + (1 | X5) + ε, and we generated 16 significant com- respond to the cofactors of region, habitat, and methods,
binations. This second set of models revealed that cofac- respectively. Sub-indices represent levels, which indi-
tors X2, X3, X4, and X5 were random (P < 0.005; Table cate their respective interaction; X14 (Nearctic-region) +
1). This type of analysis allowed us to identify the most X15 (Neotropical-region) + X16 (Oriental-region) +
commonly used cofactors when studying ecosystem ser- X17 (Palearctic-region) − X62 (habitat-desert) + X63
vices by bats. The cofactor regions (Neotropical, Palearc- (habitat-forest) + X73 (methods-fecal samples) + X711
tic, Oriental, and Nearctic; P < 0.0001), habitat (desert (methods-mist nets and acoustic monitoring). The vari-
and forest; P < 0.0001), and methods (stool samples, mist ance of cofactors (1 | X2), (1 | X3), (1 | X4), and (1 | X5)
nets and acoustic monitoring; P = 0.001) were highly sig- were: σ 2 X2 = 19.71, σ 2 X3 = 18. 79, σ 2 X4 = 5.65, and
nificant. This model showed the greatest importance with σ 2 X5 = 7.46, respectively. The total variance was σ 2 =
the lowest AIC (1669.7; Table 1). 51.61.

Figure 4 Distribution of the relative number of studies that have experimentally assessed ecosystem services provided by bats with
respect to biogeographical regions across the world.
DISCUSSION
Our comprehensive literature review found 283 exper-
imental studies that quantified the importance of bats to
the provision of 4 key ecosystem services: (1) control of
potential pest insects and other arthropods, (2) dispersal
of native-endemic and introduced seeds, (3) pollination
of native-endemic and introduced plants, and (4) use of
guano as fertilizer. In general, we found that studies eval-
uating pest control were conducted in all biogeographical
regions, but most were done in the Palearctic. The ma-
jority of studies investigating seed dispersal and plant
pollination were conducted in the Neotropical region and
focused on native species. There is a knowledge gap in
documenting the ecosystem services provided by bats in
the Australian, Chinese, Ethiopian, and Saharo-Arabian
regions or transition zones. The difference in the assess-
ment of ecosystem services by bats may partly reflect a
bias in research among regions. Moreover, the Australian,
Chinese, Ethiopian, and Saharo-Arabian regions are a
priority for bat research and conservation because most
species with insufficient data in the IUCN Red List (Frick
Figure 5 Relative proportion of studies with respect to insect,
et al. 2020) are found in these 4 regions. Therefore,
seed, pollen type and use of guano as fertilizer that have exper-
researchers, government agencies, and local stakeholders
imentally been assessed for the ecosystem services provided by
bats throughout the world. need to share knowledge, develop capacities, and prior-
itize research conservation efforts to ensure long-term
stability of bat populations, especially in these regions

Figure 6 Relative proportion of studies with respect to use of guano as fertilizer that have experimentally assessed the ecosystem
services provided by bats across the world.
Table 2 Identified taxa known to be pest, potential pest insects, and other arthropods in studies on the importance of bats as insect
controllers
Potentially Other New genera reported in this

Order Families Genera Species pest insects arthropods Families Genera review (after Kunz et al. 2011)
Arachnida 1 3 4 4
Araneae 10 30 44 1 43
Trombidiformes 2 3 3 3
Blattodea 1 1 1 1
Coleoptera 1 29 35 9 26 4 2 1
Diptera 26 79 137 26 111 1 1 1
Ephemeroptera 7 13 18 6 12
Hemiptera 13 20 21 5 15 3 5 2
Isoptera 1 3 3 3
Hymenoptera 3 6 6 2 4
Lepidoptera 40 294 448 180 269 5 6
Megaloptera 1 1 1 1
Neuroptera 2 4 5 1 4
Orthoptera 1 2 2 1 1
Plecoptera 4 4 4 1 3
Trichoptera 8 14 19 5 14
Total 121 506 751 237 514 13 14
Additional information on the listed studies is provided in Tables S3 and S3a, Supporting Information.

Table 3 Known plants that are dispersed (D) or pollinated (P) or both (D-P) by bats
Fleming et al. 2009 New Kunz et al. 2011 New

report report
in this in this
Order Families Genera Species Service Families Genera Species Family Genus Species
review review
Alismatales 1 1 1 D 1 3
Apiales 1 1 2 D 1 1 1 1
Aquifoliales 1 1 1 D 1
Arecales 1 13 16 D 1 3 3 1 13 5 8
Asterales 1 5 6 D-P 1 3 3 2 2
Asparagales 1 2 3 D-P 1 3 17 1 1 1
Brassicales 3 3 4 D 1 3 8 1 1 1
Canellales 1 2 2 D 2
Caryophyllales 3 6 7 D-P 1 24 43 1 1 2
Celastrales 2 2 3 D 1
Chloranthales 1 1 1 D 1
Cucurbitales 3 7 8 D 1 4 5 6
Crossosomatales 1 1 1 D 1
Ericales 6 17 28 D-P 2 4 18 1 3 7 6 8
Fabales 2 12 19 D-P 1 22 59 3 1 3 4 4
Fagales 1 1 1 P
Gentianales 4 19 26 D 2 7 11 1 1 1 18
Gnetales 1 1 1 P 1
Icacinales 1 1 1 D 1
Laurales 3 7 8 D 1 7
Lamiales 6 11 11 D-P 4 14 31 8
Magnoliales 2 9 11 D 1 1 1 9
Malpighiales 10 28 47 D-P 4 7 12 4 6 2 21
Malvales 2 15 25 D-P 3 1 1 2
Myrtales 4 17 38 D-P 2 3 3 1 2 3 3 11
Oxalidales 2 2 3 D 2
Pandanales 2 5 5 D 1 1 1 4
Pinales 1 1 1 P
Piperales 1 2 45 D 1 1 1
Poales 2 4 8 D-P 2 9 41 2
Proteales 1 2 2 D 1 1 1 2
Rosales 6 20 124 D-P 3 5 3 12
Santalales 2 2 5 D 1 1 1 2
Sapindales 6 22 27 D-P 1 1 1 3 3 6 5 15
Saxifragales 1 1 1 D 1
Scrophulariales 1 1 1 D 1
Solanales 1 11 51 D 1 7 13 1 1 9
(Continued)

Table 3 (Continued)
Fleming et al. 2009 New Kunz et al. 2011 New

report report
in this in this
Order Families Genera Species Service Families Genera Species Family Genus Species
review review
Vitales 1 1 1 D 1 1 1 1
Violales 1 2 4 D 1 1 1
Zingiberales 2 2 5 D-P 1 1 1
Total 92 261 554 27 116 270 18 29 54 32 168
Additional information on the listed studies is provided in Tables S4 and S4a, Supporting Information.
of the world (Luo et al. 2013; Feijó et al. 2019; Sasse & sis can also deplete local populations of these pests in
Gramza 2021). one growing season (Federico et al. 2008). Economically,
Our analyses show that the assessment of ecosystem Maine and Boyles (2015) estimated that the suppression
services provided by bats in transformed landscapes of herbivores by bats is worth more than 1 billion USD in
and agricultural crop areas remains largely unexplored corn production, and bats may further benefit farmers by
(Toffoli & Rughetti 2017; Maas et al. 2018). Our re- indirectly suppressing pest-associated fungal growth and
sults also indicate that recent molecular techniques have mycotoxin in corn.
not been widely used to assess the services that bats The Oriental region accounts for 87% of rice (Oryza
provide. For example, stable isotopes, metabarcoding, sativa) production worldwide, and provides this staple
and high-throughput sequencing (HTS) can characterize to more than half of the world’s population (FAO 2017).
bat trophic ecology with greater resolution to unravel Therefore, it is surprising that only 6 studies have as-
overlooked dietary diversity, but these methods are not sessed the impacts of bats on rice production. One notable
commonly employed. example is from Wanger et al. (2014), who found that
the effect of a single bat species (Mops plicatus) prevents
rice loss of almost 2900 tons per year in Thailand. Such
Insectivorous bats contribute to food production
prevention translates into approximately 1.2 million USD
Insectivorous bats are key insect suppressors in agri- annually, or rice meals for almost 26 200 people annually.
cultural systems (Maine & Boyles 2015; Russo et al. Rice is also a key crop in Central and South America, but
2018; Kemp et al. 2019; Castillo-Figueroa 2020). We little is known about the role of bats in the control of rice
found 158 studies documenting that bats consume pests pests in the Americas. A recent study from Venezuela
in large quantities and benefit crop production. How- has shown that bats actively forage above rice fields, es-
ever, the distribution of research is not homogenous pecially during the dry season when insect abundance is
across regions. We found 22 studies from the Palearc- low in nearby forest fragments (Azofeifa et al. 2019). The
tic, 16 from the Neotropical and Nearctic, 11 from the most common bat species in these fields was Molossus
Ethiopian, and 6 from the Oriental and Australian re- molossus, which feeds copiously throughout the whole
gions (Table 2 and Table S2, Supporting Information). life cycle of the crop. In contrast, Myotis nigricans is
Half (49.37%) of the studies reported that bats suppress more active during the vegetative and reproductive phase
agricultural pests (e.g. Chironomus aprilinus, Cricoto- of the crop, and feeds more often during the wet season
pus bicinctus, Helicoverpa zea, Spodoptera frugiperda, (Azofeifa et al. 2019). The role of bats in the control of
S. littoralis, Tetramorium caespitum, and Xyleborus fer- pest insects on rice is just starting to be evaluated, and
rugineus) that affect the production of apples, avocado, more studies are needed to quantify the benefits of bats
barley, cotton, coffee, corn, pine, rice, sorghum, tobacco, in the Oriental and Neotropical regions.
yam, and wheat (McCracken et al. 2012; Long et al. 2013; Overall, insectivorous bats provide pest regulation ser-
Aizpurua et al. 2018). For example, T. brasiliensis con- vices for key crops, but we still do not know the extent of
sumes large amounts of H. zea and S. frugiperda, whose the relationship between bat diversity and abundance or
larvae damage cotton and corn crops in North America richness of prey. Moreover, we have largely ignored the
(Lee & McCracken 2002; Krauel et al. 2018). T. brasilien- study of insect species that damage globally important

crops (e.g. rice, cotton, sorghum) that are consumed by However, Sánchez and Giannini (2018) reported that
bats. Furthermore, studies in the Australian and Oriental germination success is greatly affected if 2 bat species
regions are necessary to determine the range and abun- consumed the same species of fruit. The state of ripeness
dance of prey items consumed by bats to evaluate their of the fruit has also been recognized as a determining fac-
effectiveness as pest regulators, and to calculate the total tor in the germination process (Schupp et al. 2010). For
economic benefit that bats provide. example, Traveset and Verdú (2002) found that germina-
tion probability was heavily influenced by seed texture,
temperature, and humidity, but also by gut passage.
Seed dispersal
Additionally, the type of plant influences germination
Bats are crucial for reforestation because they disperse success because after passing through the bat’s gut, tree
seeds of many plant species (Lobova et al. 2009) away seeds had higher probability of germination than seeds of
from the parental tree, thus increasing the probability that herbs and shrubs (Corlett 2017). Despite different seed
seeds colonize new forest patches (Tsoar et al. 2010). We germination experiments, Saldaña-Vázquez et al. (2018)
found that 51 of 71 experimental studies that assessed concluded that the primary service that bats provide is to
ecosystem services by frugivorous bats were conducted transport seeds away from parent plants, and bats may not
in the Neotropical region, 11 in the Oriental region, 8 in significantly improve seed germination. Fruit bats play
the Ethiopian region, and 1 in the Nearctic region. Even an important role in seed dispersal, but it is necessary
though other studies have assessed some aspects of the to compare the relative importance of seed transport
ecology and evolution of seed dispersal by bats (Castillo- versus seed germination to conclude which aspect is
Figueroa 2020), our review highlights the disparity of more important as an ecosystem service.
studies across biogeographic regions. Bats are also important for commercial fruits in the
Neotropical fruit bats (Phyllostomidae) are important Paleotropics (Kasso & Balakrishnan 2013). A recent
seed dispersers of a large number of plants with high study in Malaysia has shown that a common urban bat
ecological and economic value (Scanlon et al. 2014). (Cynopterus brachyotis) disperses seeds of both native
Currently, 549 plant species in 191 genera and 62 plant and exotic species that assist forest regeneration in de-
families are dispersed by bats in the Neotropics (Table graded landscapes (Lim et al. 2018a). Likewise, in the
S3, Supporting Information). In many cases, bats are the Western Ghats of India, it was found that the benefits
primary dispersal agents for numerous plants (Ghanem of fruit bats are greater than the damage they generate.
& Voigt 2012). Old-world fruit bats (Pteropodidae) dis- Aggregation of seeds of commercial fruit crops (cashews
perse about 300 species of plants (Table 3 and Table S3, and areca) by fruit bats reduces labor costs in plantations
Supporting Information), and commercial crops (Kasso (Deshpande & Kelkar 2015). Nevertheless, more research
& Balakrishnan 2013). Our review identified 130 plant is needed to help validate the perceived economic benefits
genera dispersed by fruit bats that were not reported in and costs derived from fruit bats in different agroforestry
the review by Kunz et al. (2011). This new contribution systems. For example, we could quantify the cost of scat-
allows us to highlight bat’s increased potential for forest tering seeds manually into degraded areas as a restoration
restoration. strategy, and compare such costs to the service provided
The diet of bats is influenced by the distribution and by bats.
availability of food, which varies spatially and temporally,
and also shows high interspecific variability (Barclay &
Pollination
Jacobs 2011). A high number of studies report only
food lists or just new dietary items. Less information is Bat pollination is key for food production and for-
published on broader bat feeding ecology, or their contri- est ecology (Macgregor & Scott-Brown 2020). Most
bution to environmental function. Therefore, we are still (70%) of the studies that evaluated this ecosystem service
unable to fully understand how bats impact ecosystems were conducted in the Neotropical region. The Neotrop-
at different spatial scales, and how changes in land use ical subfamilies Glossophaginae and Lonchophyllinae
affect seed dispersal by bats (Wood et al. 2012). are specialized in nectar consumption (Datzmann et al.
Despite that many plant species are consumed by bats, 2010), and pollinate approximately 549 plant species in
the beneficial effects of seed dispersal by bats is not well 191 genera and 62 families. Pteropodid bats pollinate ap-
understood. A recent meta-analysis by Saldaña-Vázquez proximately 168 plant species in 100 genera and 41 fam-
et al. (2018) showed that bat seed dispersal does not ilies (Kunz et al. 2011). Our review identified 18 orders
necessarily increase the probability of seed germination. of plants that were not reported by Fleming et al. (2009)

and Kunz et al. (2011) (Table S3, Supporting Informa- is considered one of the best natural fertilizers (Tuttle &
tion). Many of these plants are the most important species Moreno 2005). In Mexico, prices can vary from $1.25
in their habitats, at least in terms of biomass. For exam- to $12.00 per 0.5 kg, depending on packaging size and
ple, bat-pollinated columnar cacti and agaves are domi- ingredient concentration (Kunz et al. 2011). Guano ex-
nant vegetation elements in Neotropical arid and semiarid tracted from Bracken Cave in Texas ranged between $2.86
habitats (Kunz et al. 2011; Tremlett et al. 2020). Addi- and $12.10 per kg in the early 2000s (Tuttle & Moreno
tionally, the emblematic baobabs of the Ethiopian region 2005).
are pollinated by bats (Acharya et al. 2015; Nor Zalipah Bat guano is an essential supply of nutrients and or-
et al. 2016; Aziz et al. 2017). ganic material that improves plant growth compared to
Although bat pollination is an important ecosystem other fertilizers. In Cambodia, Sothearen et al. (2014)
service, it remains poorly understood. The importance of found that bat guano had a greater and significant ef-
bats as pollinators of tropical crops has been well estab- fect on plant growth on 6 economically important species
lished for species such as durian, bitter beans, and jack- compared to chemical fertilizers. In India, Shetty et al.
fruit (Lim et al. 2018b), but most studies are usually re- (2013b) found that only small amounts of bat guano are
stricted to 1 pair of species at a single site. Moreover, few needed to improve plant growth. Thus, using guano as a
reports have quantified the market value of bat pollination natural fertilizer is being used extensively in developing
(Klatt et al. 2014). Additionally, previous studies have not countries, and demand is increasing among organic farm-
been able to isolate the impact of bat pollination on crop ers in developed countries. Bat guano, like other organic
performance from other vertebrate and invertebrate pol- fertilizers, not only provides essential nutrients, but also
linators (Ratto et al. 2018). This oversight hampers our increases soil fertility and can be easily integrated into
ability to assess the full range of benefits of bat polli- conventional fertilization practices (Saleque et al. 2004;
nation on crop production (Melathopoulos et al. 2015). Mottaghian et al. 2008). The use of bat guano can help
Nevertheless, a recent study in Mexico has shown that reduce the use of chemical fertilizers, which come from
Leptonycteris yerbabuenae is the most effective pollina- a highly polluting industry that uses huge amounts of en-
tor of the cactus Stenocereus queretaroensis compared to ergy. Moreover, bacteria extracted from bat guano can im-
diurnal pollinators. Flowers pollinated by bats were 35% prove detergents, help to detoxify industrial wastes, and
more likely to become mature fruits compared to flowers can be a source of potassium nitrate (Tuttle & Moreno
pollinated by diurnal animals (Tremlett et al. 2020). A re- 2005).
duction in the service provided by this bat species would We only found 24 studies related to the potential of
result in a decrease in the size and quality of the harvest. guano as fertilizer. Given the high rates of soil erosion
Despite the economic value of some bat-pollinated crops, worldwide, the use of guano can improve soil fertility
the importance of bats as pollinators is often overlooked (Doughty et al. 2016). Therefore, it is important to con-
(Ratto et al. 2018), especially because most studies have tinue studying the benefits of guano, and the dynamics
omitted small-scale crops, which account for 83% of the within caves in relation to the distribution of nutrients and
global agricultural production (Potts et al. 2016). the impacts of guano harvesting on bat populations.
It is necessary to undertake new investigations to eval-
uate whether bat pollination translates into increased fruit
production, especially for commercial trees and tropical Methods used to assess ecosystem services
crops. Given that nectar consumption does not guaran-
provided by bats
tee pollination success, it is necessary to further inquire
whether frequency of visits and pollen deposition capac- Several methods have been used to assess the ecosys-
ity translates into pollination effectiveness and fruit pro- tem services that bats provide (Kunz & Parsons 2009). For
duction. insect predation, the most common methods used were
mist nets, acoustic monitoring, fecal sampling, molecular
analysis, insect traps, and exclusion experiments. Fecal
Use of bat guano
sample analysis and the use of insect traps have been
Bats play an important ecological role in soil fertil- crucial non-invasive methods to assess bat diets (Trites
ity. Bat guano extracted from caves is used as fertilizer & Joy 2005), and both methods provide reliable dietary
in agriculture because it is rich in nitrogen and phospho- estimates with high statistical power (Hope et al. 2014).
rus (Shetty & Streepada 2013a; Ware et al. 2020). Guano However, these methodologies have several drawbacks.
has been widely traded in some parts of the world and For example, species-level identification can be highly

uncertain (Gosselin et al. 2017) because digested soft studies using these methods can be especially useful to
items become unsuitable for identification (Nilsen quantify the significance of bat guano in agroecosystems.
et al. 2012), and presence of other prey items may be
underestimated (Gosselin et al. 2017). To overcome
these limitations, advances in molecular methods allow Challenges when assessing ecosystem services
the identification of cryptic dietary items, and reveal One of the main challenges to assess ecosystem ser-
predator–prey interactions with greater taxonomic reso- vices provided by bats is to adequately ascertain how
lution (Pompanon et al. 2012). Metabarcoding and envi- bat mobility affects provisioning and regulating services.
ronmental DNA have been used to examine the impact Bats are highly mobile (Lumsden et al. 2002; Lentini
of bats as control agents of potential pest insects (Burgar et al. 2012), so bats foraging in a particular area are not
et al. 2014; Brown et al. 2015) and to monitor fluctuations necessarily considered local residents. Therefore, bats can
in insect pests in bat-scat assays (Maslo et al. 2017). The provide services from where bats roost to where they for-
use of artificial shelters and exclusion experiments also age (Law & Chidel 2006; van Toor et al. 2019). The study
provide reliable information to predict yield optimization of insect predation, seed dispersal, plant pollination, and
of insect consumption by bats (Maas et al. 2015). use of guano also requires a broader scope of knowl-
For provisioning services through seed dispersal, we edge beyond the traditional tools that bat ecologists use.
found that most studies used fecal samples, germina- Researchers should incorporate other techniques (remote
tion tests, radio-telemetry, and feeding experiments in sensing, metabarcoding, and econometric analyses) into
captivity. These methods allow the quantification of the their toolbox to better monetize ecological processes.
night-to-night consumption of fruits, but are limited Another challenge is to determine the spatial scale at
because they are unable to determine the quantity and the which bats provide ecosystem services. Frequently, plot-
type of seeds that are dispersed (Saldaña-Vázquez et al. scale studies are insufficient to explain landscape hetero-
2018). Moreover, the aforementioned methods cannot geneity, especially in agricultural mosaics where land use
determine whether the dispersal event was effective from varies at small spatial scales (Boyles et al. 2011; Kemp
the point-of-view of plant regeneration (Cubiña & Aide et al. 2019). Therefore, plot-based studies do not nec-
2001; Ingle 2003). Other methods should be used, such as essarily provide adequate empirical data in a replicated
exclusion experiments coupled with direct observations fashion to properly assess service provisioning. For ex-
to provide a reliable estimation of the dispersal services. ample, research on partial prioritizations for the protec-
These methodologies should evaluate effectiveness of tion of ecosystem services is biased towards services that
dispersed seeds in natural conditions and germination only provide benefits at local scales (Luck et al. 2012).
potential, as well as usefulness in the regeneration of Finally, there is a mismatch between species-oriented
degraded landscapes. ecological research that addresses the mechanisms under-
For pollination services, many of the conventional lying the provision of services, and conservation-oriented
techniques are still used, such as assessment of flower research that identifies critical aspects related to particu-
availability, fecal content analysis, direct observations, lar services. Harmonization between these 2 approaches
and chemical analysis (Voigt et al. 2009). While these is critical to improve our understanding of the provision
techniques provide valuable insights into the dietary of ecosystem services in human-altered landscapes. This
habits of flower-visiting bats, new techniques have been methodology also needs to overcome the economic costs
developed in recent years. For example, the use of stable of evaluating the ecosystem services that bats provide
isotopes or remote sensing allows a more detailed evalu- at an adequate spatial scale. Such costs usually exceed
ation of the source of the pollen, the movement of pollen the limits of research budgets in developing countries
by bats across the landscape, and the effectiveness of pol- (Schägner et al. 2013; López-Hoffman et al. 2014).
lination.
The methods most commonly employed to assess the
use of bat guano were collection of droppings from the Proposal to stimulate research on the ecosystem
roosts and vermicompost. Both methods allow mineral-
services provided by bats
ization of guano to produce fertilizer (Shetty & Streepada
2013a; Ware et al. 2020). Likewise, the addition of Despite the economic benefits we receive from bats
bat guano to other organic fertilizers from vermicom- (Kunz et al. 2011; Kasso & Balakrishnan 2013; Russo
post stimulates plant growth significantly (Ievinsh 2011; et al. 2018), many species continue to be threatened
Grantina-Ievina et al. 2013; Karlsons et al. 2015). More by multiple factors (habitat loss and fragmentation,

Figure 7 Tripartite aspects and actions to increase our understanding of ecosystem services provided by bats and our capacity to
preserve them. Each set indicates key necessities in education, ecological services provided by bats, and conservation initiatives.
Intersections indicate key actions that will stimulate research and improve bat conservation.
destruction and vandalism of roosts, and human–bat con- and AICOM for their acronyms in Spanish) by the Red
flicts). Many of these threats are related to unawareness Latinoamericana y del Caribe para la Conservación de los
and stigmatization (MacFarlane & Rocha 2020; Rocha Murciélagos (RELCOM) (Aguirre et al. 2014).
et al. 2020). To overcome these obstacles, we need more Even though the main goal of the present review is
environmental education and transdisciplinary research, to highlight the primary ecosystem services that bats
and integration of stakeholders in bat conservation (Frick provide, it is key to recognize as many other benefits
et al. 2020). We propose 3 strategic aspects and actions as possible. For example, bats are excellent subjects for
(Fig. 7): (1) ongoing environmental education based on studies on healthy aging, cancer prevention, and disease
updated scientific research, (2) more research on ecosys- defense (Zhang et al. 2013; Irving et al. 2021). Addi-
tem services provided by bats while making technical lit- tionally, bats are used in biomimetic engineering, radar
erature amenable to the general public, and (3) increase engineering, and robotics (Kasso & Balakrishnan 2013;
the size of conservation areas and the raise the protection Steckel & Peremans 2013; Teeling et al. 2018; Zhao
level of sites vital for bats. A notable example is the recog- 2020). Communicating the economic and supplementary
nition and protection of key sites and areas for bat conser- benefits provided by bats will help raise awareness among
vation across Latin American and the Caribbean (SICOM the public and policy makers of the importance of bat

conservation (Williams-Guillén et al. 2016; Tremlett with devastating repercussions for conservation efforts
et al. 2021). More positive press is especially important (López-Baucells et al. 2018). The brutal and unfounded
now, as the COVID-19 pandemic from SARS-CoV-2 backlash against bats in many countries around the world
continues (Sasse & Gramza 2021). Recent publications (Durán 2020; Goyal 2020; Lentini et al. 2020; Tsang
(MacFarlane & Rocha 2020; Rocha et al. 2020) define 2020) constitutes a renewed threat. Therefore, conser-
guidelines for communicating key issues about bat con- vationists and health officials face the challenge of in-
servation and zoonotic diseases. Here, we summarize the forming the public about the health risks associated with
current knowledge on the ecosystem services provided land use change that threatens the integrity of ecosystems
by bats, and highlight crucial aspects that will stimulate and wildlife, while underscoring the importance of bats
more research and effective bat conservation (Fig. 7). worldwide. Such complex issues require an integrated and
transdisciplinary research agenda to support the design
and execution of action plans to minimize zoonotic health
CONCLUSIONS AND risks, while supporting bats and their associated ecosys-
RECOMMENDATIONS FOR FURTHER tem services (Kunz et al. 2011; Russo et al. 2018; Frick
et al. 2020; MacFarlane & Rocha 2020; Rocha et al. 2020;
RESEARCH Sasse & Gramza 2021). The quantification of the known
We provide a comprehensive review of the experimen- and potential ecosystem services provided by bats, includ-
tal studies that have addressed ecological services pro- ing those related to human health and well-being (Teeling
vided by bats around the world. In total, we found 158 et al. 2018), constitute a fundamental pillar to guarantee
studies that have assessed insect predation, 71 studies that long-term conservation of bats and their habitats.
have assessed seed dispersal, 30 studies that have assessed
plant pollination, and 24 studies that have assessed the use
of guano as fertilizer. Our results show that most studies ACKNOWLEDGMENTS
on ecosystem services by bats have been conducted in the The authors wish to thank the staff of the Research
Neotropical and Palearctic regions, usually in forests and Group in Zoology (GIZ), Universidad del Tolima (Ibagué,
deserts, and have most often used fecal samples, mist nets, Colombia). L.A.R.-F. and L.V.G.-H. thank the Convocato-
and acoustic monitoring as research methods. ria No. 755, 2016 para la Formación de Capital Humano
For insect pest control, we found that experimental de Alto Nivel para el Departamento del Tolima, Colfu-
methodologies (e.g. enclosures) in agricultural systems turo (Minciencias) and Departamento del Tolima for sup-
can provide valuable information. However, results from port (doctoral scholarships) during the development of
experimental approaches are limited by their cost, dura- this review. We thank the Editor-in-Chief and 3 review-
tion, and can vary greatly between landscapes and crops ers for suggestions to improve the final version of our
(Maas et al. 2018). Therefore, generalizations from such manuscript.
approaches can be restrictive. For seed dispersal and
plant pollination services, experimental en/exclosures,
and construction of roosts in agricultural systems can CONFLICT OF INTEREST
provide valuable insights. Nevertheless, such studies The authors declare no conflict of interest.
need to carefully consider potential pitfalls related to
design, materials, duration, and they need to account for
co-variation in other conditions around the landscape
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els testing for impact differences of bats as insect con-
SUPPLEMENTARY MATERIALS
trollers, seed dispersers, flower pollinators and fertilizer
Additional supporting information may be found on- producers as determined by research during the past two
line in the Supporting Information section at the end of decades in the different biogeographical regions of the
the article. world
Table S1 List of selected papers. Study on bats as Figure S5b Graphs of results from generalized linear
insect pest controllers, Study on bats as insect other mixed models in R
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Bats and their vital ecosystem services: A global review

Article in Integrative Zoology · May 2021

Leidy AZUCENA Ramirez Francel Leidy Viviana García-Herrera

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Sergio Losada-Prado Sergio Estrada-Villegas

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Bats and their vital ecosystem services: a global review

Leidy Azucena RAMÍREZ-FRÁNCEL,1,2 Leidy Viviana GARCÍA-HERRERA,1,2

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Generalized linear mixed model

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Table 1 (Continued) 9.4%, Thyropteridae 20%, and Vespertilionidae 30.6%.

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Potentially Other New genera reported in this

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Fleming et al. 2009 New Kunz et al. 2011 New

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Fleming et al. 2009 New Kunz et al. 2011 New

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