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\begin{document}

\title{Bat community response to insect abundance in relation to rice phenology
in Peninsular Malaysia}



\author[1]{NUR IZZATI ABDULLAH}%
\author[2]{Nurul-Ain Elias}%
\author[3]{Ohte Ohte}%
\author[4]{Christian Vincenot}%
\affil[1]{Kyoto University - Yoshida Campus}%
\affil[2]{Universiti Sains Malaysia}%
\affil[3]{Kyoto University}%
\affil[4]{University of Luxembourg}%


\vspace{-1em}



  
  \date{June 16, 2024}


\begingroup
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\selectlanguage{english}
\begin{abstract}
Bats provide us with important ecosystem services including insect
population controllers in agricultural areas. Studies on bats and insect
abundance in Malaysian rice fields are still lacking. Two harp traps and
two mist nets were used to trap bats at the Gunung Keriang while a light
trap was used to sample insects in the rice field area at three
identified sites. A total of 2499 bats from 27 species were captured and
for insect abundance a total of 161,539 individuals from 11 orders were
captured. Rhinolophus pusillus was recorded as the dominant bat species
in all seasons. In the dry season, the dominant insect pest was
\emph{Chilo polychrysus} (Stem borer) and in the wet season,
\emph{Nilaparvata lugens} (Brown planthopper) the dominant insect pest
species. Insects from the Order Coleoptera (the dominant insect Order in
dry season) may be eaten by bats that have a larger body size and that
have a strong bite force. Due to high food availability and insect
abundance, the peak time of bat foraging activity is the same as the
peak time of insect emergence. We found that there is a significant
relationship between bat activity with temperature and rainfall, but not
with insect abundance. This study further highlights the importance of
bats in regulating the insect pests population naturally in the rice
field area.%
\end{abstract}%



\sloppy


\textbf{Bat community response to insect abundance in relation to rice
phenology in Peninsular Malaysia}

Nur-Izzati Abdullah 1,2, Nurul-'Ain Elias 3, Nobuhito Ohte 1, Christian
E. Vincenot 2,4*

\begin{enumerate}
\tightlist
\item
  Department of Social Informatics, Graduate School of Informatics,
  Kyoto University, Yoshidahonmachi, Sakyo-ku, 606-8501 Kyoto, Japan
\item
  Island Bat Research Group, Kyoto, Japan
\item
  School of Biological Sciences, Universiti Sains Malaysia, 11800
  Gelugor, Penang, Malaysia
\item
  Faculty of Science, Technology and Medicine, University of Luxembourg,
  Esch-sur-Alzette, Luxembourg
\end{enumerate}

*Corresponding author: C.E. Vincenot, christian@vincenot.biz

\textbf{Abstract}

Bats provide us with important ecosystem services including insect
population controllers in agricultural areas. The study on bats and
insect abundance in Malaysian rice fields are still lacking. Two harp
traps and two mist nets were used to trap bats at the Gunung Keriang
while a light trap was used to sample insects in the rice field area at
three identified sites. A total of 2499 bats from 27 species were
captured and for insect abundance a total of 161,539 individuals from 11
orders were captured. \emph{Rhinolophus pusillus} was recorded as the
dominant bat species in all seasons. In the dry season, the dominant
insect pest was \emph{Chilo polychrysus} (Stem borer) and in the wet
season, \emph{Nilaparvata lugens} (Brown planthopper) the dominant
insect pest species. Insects from the Order Coleoptera (the dominant
insect Order in dry season) may be eaten by bats that have a larger body
size and that have a strong bite force. Due to high food availability
and insect abundance, the peak time of bat foraging activity is the same
as the peak time of insect emergence. We found that there is a
significant relationship between bat activity with temperature and
rainfall, but not with insect abundance. This study further highlights
the importance of bats in regulating the insect pests population
naturally in the rice field area.

\textbf{Keywords}

Rice fields, Limestone karst, Insect pest controller, Biological
control, Biodiversity conservation

\textbf{Introduction}

Bats provide us with important ecosystem services. Bats serve as
pollinators, seed dispersers and insect population controllers
(Kunz\emph{et al} ., 2011; Vincenot \emph{et al} ., 2017). Locusts,
planthoppers, leafhoppers, and rice stem borers are common insect pests
in rice fields (Khoo \emph{et al} ., 1991; Whitaker, 1993). Chemical,
physical, and biological controls are the main option for pest controls
in agricultural areas especially in rice fields. The usage of chemicals
such as herbicide, rodenticide and insecticide has been proven to have a
long-term effect towards the ecosystem (Chiaia-Hernandez \emph{et al} .,
2017).

Biological controls can also be a good option since it is more efficient
as all pests have their own natural enemies (Ooi, 2015). However, this
approach has long been neglected, probably due to either ignorance or to
farmers preferring immediate results. Barn owls (\emph{Tyto alba} ) have
been infrequently used to control rat populations in rice fields
(Hafidzi, 2003; Hafidzi \& Naim, 2003). Using insects that are natural
predators of insect pests is another example of biological control.
Ladybugs, ants, spiders, dragonflies and mirids (Way \& Heong, 1994;
Ooi, 2015) as well as some vertebrates like frogs, birds, and bats
(Leelapaibul \emph{et al.,} 2005) can control the insect pest population
naturally. Since rice fields have become the foraging areas for bats,
they can potentially be a biological control for insect pests (Lee \&
McCracken, 2005).

Insect-eating bats play a role as a natural predator in safeguarding the
surrounding protected areas as a biological control (Lee \& McCracken,
2005). About 70\% of bats are insectivorous (Simmons, 2005). Caves serve
as an essential roosting site for many bat species all around the world.
In caves, bats often roost in a large colony, which can result in the
large-scale depletion of insects, especially insect pests in the
surrounding agricultural area.

The contribution of bats towards controlling agricultural pests has been
mostly documented in the United States (McCracken \emph{et al.} , 2010;
Boyles \emph{et al.} , 2011), some parts of Canada (Clare \emph{et al.}
, 2009), Europe (Puig-Montserrat \emph{et al.} , 2015) and Madagascar
(Kemp\emph{et al.} , 2019). In Southeast Asia, Thailand (Leelapaibul
\emph{et al.} , 2003; Leelapaibul \emph{et al.} , 2005; Wanger \emph{et
al.} , 2014) has the highest reported studies of bats in rice field
areas. However, the situation remains unclear in Malaysia and other
Southeast Asian countries. Studies on bats in Malaysian rice field areas
are still lacking and more information is needed to determine their
contribution to the ecosystem.

The objective of this study is to document the insect abundance and
insect pest availability at different growing phases of paddies during
various growing seasons in rice fields nearby Gunung Keriang. Up to
date, there is still a lack of data regarding insect abundance
especially insect pests at different growing phase of paddy in rice
field area. This study aimed to test the importance of bats to
potentially help to control insect pest population naturally in the rice
field areas.

\textbf{Methods and materials}

Study area

Gunung Keriang is a small limestone hill rising out from a vast rice
field areas north of Alor Setar (northern Peninsular Malaysia). Sampling
was conducted in two different paddy growing seasons (based on MADA's
irrigation schedule):

Season 1 -- dry season (started in April 2021 end in September 2021)

Season 2 -- wet season (started in October 2021 end in February 2022)

Three identified sites were chosen around Gunung Keriang: MADA A (6\selectlanguage{ngerman}°10'
59.2'' N, 100°19' 22.4'' E), MADA B (6°11' 57.4'' N, 100°19' 50.0'' E),
and MADA C (6°11' 22.4'' N, 100°20' 30.2'' E) (Figure 1).

The trapping was conducted every month for three consecutive days in
MADA A, MADA B and MADA C starting from April 2021 until February 2022.
There are five main phases of paddy growing which are germination,
vegetative, reproductive, ripening and harvesting. For the dry season,
the reproductive phase was excluded due to restriction movement that was
implemented during that growing phase of paddy. For the wet season, we
recorded all the phases of paddy growth.

Insect Trapping

Insects were sampled using light traps that were placed at the three
identified sites before sunset. Each light trap used 60W 12V tungsten
bulbs and were set more than 1km distance from one another within a 2km
radius from Gunung Keriang where the harp traps are located. Insect
collections were conducted every hour starting at 19:00 until 07:00. The
trapped insects were killed by using ethyl acetate, following this they
were sorted and identified to Order or Family level based on Salleh
(1990) and Borror \emph{et al.} (1996). Selected insect pests were
identified to species and then stored in 97\% alcohol for future
molecular analysis.

Bat Trapping

Insectivorous bats were captured using two harp traps at different
elevations of Gunung Keriang (top, middle and low) and two high nets
were also used in the rice field area, for three consecutive nights per
sampling. High nets were set up at dusk (19:00), were checked every 10
to 15 minutes and were closed at 22:00. Harp traps were set up at
midnight (00:00), were checked every hour and were closed just after
dawn (07:00). Captured bats will be weighed, sexed and identified based
on their morphology (Kingston \emph{et al.} , 2006).

Local weather monitoring

The total monthly rainfall, plus the maximum and minimum monthly
temperature were provided by the Malaysian Meteorology Department for
Alor Setar, Kedah.

Data analysis

Peak time of insect emergence was analyzed based on the number of
insects collected per hour. It can be associated with bat foraging
activity in the following objective of the study. Insect presence was
used to estimate food availability for bats based on different stages of
paddy growth (germination, vegetative, reproductive, ripening and
harvesting). Insect data is recorded in two parameters: relative
abundance (number of insects of specific taxa/total number of insects)
and absolute abundance (number of insects of specific taxa). All the
statistical analyses were calculated in R version 4.2.2. The Pearson
parametric correlation test was used for the correlation analysis. The
variables were first centered and scaled before running for the
statistical test. For the multiple linear regression, the model used is
lm(bat activity \textasciitilde{} minimum temperature + rainfall,
data=mydata). We also run the regression model for these dominant bat
species: \emph{Rhinolophus pusillus} , \emph{Myotis ridleyi}
,\emph{Hipposideros larvatus} , \emph{Rhinolophus malayanus}
and\emph{Rhinolophus refulgens} . Multiple linear regression requires
some conditions of application for the model to be usable and the
results can be interpretable. The function check\_model() from the
\{performance\} package was used to test all of the conditions of the
model.

\textbf{Results}

A total 2499 individual bats from 6 Orders and 27 species were captured.
1608 individuals from 6 Orders and 21 species were recorded for the dry
season and 891 individuals from 5 Orders and 23 species were recorded
for the wet season (Table 1). \emph{Rhinolophus pusillus} was recorded
as the dominant bat species with the highest capture rate in the dry
season as well wet season. Throughout this study, a few single
individuals of rare bats were encountered and species that had never
been recorded previously at Gunung Keriang. These were\emph{Hipposideros
halophyllus} and \emph{Rhinolophus marshalli} .\emph{Miniopterus
magnater} and \emph{Scotophilus kuhlii} are a few open space bat species
that were captured in the dry season. In the wet season, single
individuals of \emph{Macroglossus minimus} and\emph{Cynopterus sphinx} ,
the frugivorous bats, were caught.

Based on the correlogram, the results show that the bat activity was
positively correlated with the average temperature and negatively
correlated with maximum temperature and rainfall (see diagnostic plot in
Suppl. Mat. Table 1). The insect activity was positively correlated with
minimum temperature and rainfall (Figure 2). The multiple linear
regression model met the conditions of validity (see diagnostic plot in
Suppl. Mat. Figure 1).

The coefficient of determination, R² is 0.35, therefore this indicates
that 35\% of the variance in bat activity can be explained by the
predictors based on the model (Figure 3). The coefficient value for
minimum temperature is significant with a p-value of 0.007 while
rainfall is significant with a p-value of 0.002. Regression analysis for
the five bat species separately did not return statistically significant
results and were therefore discarded.

For the dry season, 12 Orders of insects were recorded at the rice
fields (Figure 4) and the dominant insect Order was Coleoptera. The
germination phase of the paddy had the highest insect abundance compared
to the rest of the paddy phases. \emph{Chilo polychrysus} (Stem borer)
from the Order Lepidoptera is the insect pest species that was captured
for all phases of paddy growth in the dry season.

Meanwhile for the wet season, 13 Orders of insects were also recorded at
the rice fields (Figure 5). The dominant insect Order for this season is
Homoptera. The vegetative phase recorded the highest insect abundance
compared to the rest of the paddy phases. \emph{Nilaparvata
lugens}(Brown planthopper) from the Order Hemiptera is the insect pest
species that was captured for all phases of paddy growth in the wet
season.

Insects from the Orders Araneae and Odonata have also been captured in
the dry and wet season. These two insect Orders are known to be natural
enemies of insect pests in rice fields. From the Order
Araneae,\emph{Lycosa pseudoannulata} was the most common species
captured and for the Order Odonata, \emph{Agriocnemis} sp. was the most
common species captured. The most common natural enemies of insect pests
in rice field area are \emph{Ophionea} sp., \emph{Paederus fuscipes}
,\emph{Harmonia octomaculata} , \emph{Euborellia stali} ,
\emph{Limnogonous fossarum} and \emph{Riptortus linearis} .

Peak time of insect emergence with the highest individuals captured for
dry season was from 20:00 until 21:00 while for wet season, 19:00 until
20:00 (Figure 6). This time frame is expected to be the same as peak
time of the bat foraging activity. The time of bat emergence in the dry
season was from 19:00 until 21:00 while for wet season was from 20:00
until 21:00.

\textbf{Discussion}

Bats are known as opportunistic feeders which consume insects that fit
the best for their diet in terms of nutritional value and also depends
on their energy demand. Coleoptera is the most abundant insect Order
captured. Order Coleoptera possess a high number of insect species with
a wide range of size (Chown \& Gaston, 2010). Insects from the Order
Coleoptera also may be eaten by bats that have a larger body size, and
that have a strong bite force to feed on the hard-bodied prey. Bats with
bigger body sizes have more robust skulls and larger teeth, so these
bats are able to consume a wider size range and more hard-bodied prey
(Aguirre \emph{et al} ., 2003). However, it is still unsure that only
bigger bats only will consume insects from the Order Coleoptera. Bats
are known to regulate quite a number of insect pest Orders such as
Coleoptera, Lepidoptera, Diptera, Hemiptera and Isoptera (Kunz \emph{et
al.} , 2011).

The preliminary diet analysis study of \emph{Taphozous
melanopogon}(black-bearded Tomb bat) in rice field area in Gunung
Keriang found that they mainly consume insects from the Orders
Lepidoptera, Coleoptera and Diptera (Nur-Izzati \& Nurul-Ain, 2019).
\emph{Rhinolophus pusillus} was the most captured bat in the dry and wet
season with insects from the Order Coleoptera being the most captured
insect Order throughout the study. It is possible that \emph{R.
pusillus} may feed on insects from the Order Coleoptera since both of
them had the highest capture rate. In this study, \emph{R. pusillus} was
captured the most during dawn from 03:00 until 07:00. Insects from the
Order Coleoptera were sampled throughout the night, but their abundance
is the highest during dusk. Further study should be carried out to prove
that \emph{R. pusillus}feed on insects from the Order Coleoptera in the
near future.

The results from the regression in this study indicate that the
predictors are actually partially explaining the bat activity. Since
none of the contributions of the variables could not be statistically
established, there are definitely more important factors that play
valuable roles in influencing the results, such as the amount of light,
humidity or the result from the pooling of bats and insects. Since we
only take into account the temperature and rainfall in this study, other
variables may have been neglected. Moonlight and streetlight may affect
the insects that bats consume and also some bats may benefit from it
(Rowse \emph{et al} ., 2016). Slow-flying bats are highly affected by
the illuminance as this bat species forage insects in cluttered
vegetation and expose to predation rather than fast-flying bats such as
open space bat species which benefit by the large swarming of the flying
insects near streetlights (Azam \emph{et al} ., 2015; Azam \emph{et al}
., 2015).

Bat activity is often associated with local microclimates such as
temperature and rainfall while insect activity is proven to rely on
rainfall instead of temperature (Nurul-Ain \emph{et al} ., 2017). In
this study, we found that bat activity was influenced by temperature and
rainfall. Bats would avoid emerging from their roost site during rain to
avoid sensory constraint by rain drops on echolocation and emerge right
after the rain stops. Based on this observation, in the wet season,
there were only few or no bats before and after rain. But still a few
bat species would forage in rain when the resources offer a sufficient
energy gain (Voigt \emph{et al.} , 2010). Bats also tend to have a few
peak times on rainy nights. Bats emerge from their roosts starting at
dusk and actively forage for the first hour and just before dawn. A few
studies also reported that bat emergence and activity is associated with
the fluctuation in temperature (Wolbert \emph{et al} ., 2014;
Gorman\emph{et al} ., 2021). Due to high food availability and insect
abundance, the peak time of bat foraging activity is the same as the
peak time of insect emergence.

The insect abundance in each growing phase of paddy is diverse according
to different seasons. Different parts of the paddy plant such as leaf,
stem, seeds, and root were usually attacked by insect pests during the
development period of the plant (Maisarah \emph{et al} .,
2015).\emph{Chilo polychrysus} (Stem borer) was the dominant insect pest
captured in the dry season while \emph{Nilaparvata lugens} (Brown
planthopper) was the dominant insect pest captured in the wet season. In
this study, a conspicuous pattern was shown by the brown planthoppers as
they are the dominant insect pest captured in the wet season. The high
population of brown planthoppers is related to the heavy rainfall, high
temperature and high humidity (Win \emph{et al} ., 2011). Throughout
this study, insect activity was higher on warmer nights. The rainfall
may not affect the overall insect activity but impact certain insect
species. Further investigation should be made to find out more regarding
the relation of which insect Order or species is affected by the
temperature.

Brown planthoppers are highly attracted to light and were caught the
most when using light traps. Light traps are commonly used to sample
insect populations. By using light traps, it aids in monitoring the
actual pest population in the field. The light trap usage also is more
reliable and gains more accurate results in predicting the risk and
damage to the crops (Mohammad Aufa \emph{et al.} 2022). The early
detection of insect pest density, the population growth and the risk of
outbreak events can be successfully predicted for the late crop stage
(Badrulhadza \emph{et al} ., 2013). The Malaysia Agriculture Research
and Development Institute (MARDI) has created an early warning system
that would also help with a better insecticide application schedule plan
where there is a huge possibility of preventing excessive pesticide
usage and avoiding wasting operation costs (Mohammad Aufa \emph{et
al.}2022).

Insects from the Order Araneae and Odonata have also been captured along
with a few other insects that are known to be natural predators of
insect pests in rice fields (Ooi, 2015). \emph{Cyrthorhinus
lividipennis} and spiders are two important predator species that aid in
reducing the population of the planthopper (brown planthopper, \emph{N.
lugens} and whitebacked planthopper, \emph{Sogatella furcifera} )
(Ooi\emph{et al.} 1978; Ooi, 1980; Ooi, 1982). \emph{Agriocnemis} sp.
and\emph{Harmonia octomaculata} were commonly sighted throughout our
study in the rice field areas. The increase in the predator population
in the rice fields was correlated with the abrupt increase in the pest
population (Ooi \emph{et al.} 1978). An effort should be made to ensure
the predator population in the rice field area will remain continual to
prevent any recurrent outbreaks.

Based on the IUCN Red List of Threatened Species, \emph{Rhinolophus
convexus} was listed as data deficient (DD), \emph{Hipposideros
pomona}as endangered (EN), \emph{Hipposideros halophyllus} as vulnerable
(VU),\emph{Myotis ridleyi} and \emph{Hipposideros lekaguli} as near
threatened (NT) and the rest of the bat species captured in this study
were listed as least concern (LC) (IUCN, 2023). By capturing
more\emph{R. convexus} in the future, perhaps we can investigate and
learn more regarding this species' dietary habits and their potential
foraging ground. A high number of \emph{Myotis ridleyi} individuals were
captured suggesting that the decrease in this bat species population may
have a huge impact on the rice fields.

Our study further emphasizes on the role of bats in regulating insect
pests populations in agricultural areas such as rice fields. By
investigating their diet and microclimate factors, not only allows us to
gain a better insight on their environmental services, but also helps us
in understanding their behavior which is vital for mitigating
conservation plans. Even though the usage of insecticide is still widely
used by farmers, the combination of ecological-friendly methods for
controlling pests in agricultural areas help to ensure the sustainable
agriculture system. It helps to increase crop production and lower the
damages sustained by pests. Minimizing the chemical usage in rice fields
can slow down the process of pesticide resistance among insect pests.
The importance of understanding the need to conserve bats and their
roost site at Gunung Keriang is crucial as the bats aid in controlling
insect pest populations naturally in the rice fields.

\textbf{Acknowledgments}

We would like to thank Muda Agricultural Development Authority (MADA)
especially Mr. Mohd Ikhwanuddin Khairuddin for providing technical
support for this study. Our special thanks also to the field assistants:
Ummu Atiyyah Mohd. Talhah, Aqilah Hanani Mohd. Razani, Muhammad Amir
Shuib, Syafi'e Khazali, Mohammad Farhan Rashid, Mohd. Daniel Haiqal
Mohd. Zulfikar, Ng Xuanyi, Anis Suraya Kartika Azizan and Nur Azlin
Abdul Salim.

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