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The Monumental Mistake of Evicting Bats from Archaeological Sites-A Reflection from New Delhi

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We highlight the importance of an integrated management policy for archaeological monuments and the insect-eating bats that roost inside them. We refer to India, but the issue is general and of worldwide significance. There is increasing evidence that the ecosystem services provided by insect-eating bats in agricultural fields are of vital economic importance, which is likely to increase as chemical pest-control methods become inefficient due to evolving multi-resistance in insects. We visited five archaeological sites in the city of New Delhi. We found bats at all five locations, and three of them harbored large colonies (many thousands) of mouse-tailed bats and tomb bats. These bats likely disperse over extensive areas to feed, including agricultural fields in the vicinity and beyond. All insect-eating bats should be protected and properly managed as a valuable resource at the archaeological sites where they occur. We firmly believe that "fear" of bats can be turned into curiosity by means of education and that their presence should instead enhance the value of the sites. We suggest some means to protect the bats roosting inside the buildings, while mitigating potential conflicts with archaeological and touristic interests.
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Heritage 2019, 2, 553–567; doi:10.3390/heritage2010036 www.mdpi.com/journal/heritage
Communication
The Monumental Mistake of Evicting Bats from
Archaeological Sites—A Reflection from New Delhi
Ravi Umadi 1, Sumit Dookia 2 and Jens Rydell 3,*
1 Independent Researcher, Basavanagar Road, Kagwad, Karnataka 591223, India; ravisumadi@gmail.com
2 University School of Environment Management, Guru Gobind Singh Indraprastha University, Sector 16 C,
Dwarka, Delhi 110078, India; sumitdookia@gmail.com
3 Biology Department, Lund University, 223 62 Lund, Sweden
* Correspondence: jens.rydell@telia.com; Tel.:+46-705181431
Received: 14 January 2019; Accepted: 03 February 2019; Published: 8 February 2019
Abstract: We highlight the importance of an integrated management policy for
archaeological monuments and the insect-eating bats that roost inside them. We
refer to India, but the issue is general and of worldwide significance. There is
increasing evidence that the ecosystem services provided by insect-eating bats in
agricultural fields are of vital economic importance, which is likely to increase as
chemical pest-control methods become inefficient due to evolving multi-resistance
in insects. We visited five archaeological sites in the city of New Delhi. We found
bats at all five locations, and three of them harbored large colonies (many
thousands) of mouse-tailed bats and tomb bats. These bats likely disperse over
extensive areas to feed, including agricultural fields in the vicinity and beyond. All
insect-eating bats should be protected and properly managed as a valuable
resource at the archaeological sites where they occur. We firmly believe that “fear”
of bats can be turned into curiosity by means of education and that their presence
should instead enhance the value of the sites. We suggest some means to protect
the bats roosting inside the buildings, while mitigating potential conflicts with
archaeological and touristic interests.
Keywords: agroecology; archaeological conservation; biological control; heritage;
ecosystem service; pest control
1. Introduction
Effective solutions to environmental issues often require constructive
interactions between experts from different scientific disciplines. Indeed,
cooperation across subject boundaries may give rise to new ideas, and it is in the
interface between subjects that new fields of research may sprout. In this article, we
aim to stimulate such interdisciplinary interactions, specifically involving
archaeologists, conservation biologists, and perhaps also agricultural scientists. The
root of the issue is the potential conflict arising because of the dualism inherent in
the human perception of bats; unappreciated, feared, or even hated on one side, but
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high-profile conservation targets of economic significance on the other. In this note,
we call for an integrated management policy for ancient monuments and the bats
that live inside them.
There are several thousand historical temples and monuments in India, mostly
administrated by the Archaeological Survey of India [1]. Many of them are currently
being restored, and more are likely to undergo restoration efforts, partly to facilitate
the development of tourism—a rapidly growing sector in India [2]. The restoration
and preservation projects require the consideration of threats from different angles,
such as the chemical and biological degradation of the buildings [3], safety issues,
the presence of drug abuse, litter, and, last but not least, deliberate destruction and
vandalism [4–6]. In this note, we concentrate on the relationship between buildings
and bats.
Archaeological sites are essential parts of the cultural heritage of India and the
world, but we must not ignore the fact that they also harbor wild animals, notably
bats, which are valuable parts of the natural heritage. Buildings and the resident bats
should be managed wisely and sustainably for the benefit of both, and bats should
not be evicted or eradicated from archaeological sites without earnest consideration.
As we shall see, there is increasing evidence that bats are of considerable economic
value, because they increase agricultural yields by feeding on pest insects [7,8].
In 1962, bats were reported to be “extremely common” in India, particularly in
natural or artificial ”caves”, including dark corners of old monuments and temples
[9–11]. However, things may have changed since 1962, and there is now an urgent
need of a comprehensive update of the bat populations in India. Nevertheless, the
temples and monuments probably still house many bats, which may remove tons of
insects each night over adjacent and distant agricultural fields. Bats are incredibly
efficient consumers of flying insects [12,13] and can control and suppress
populations of pests [14,15]. To find food, some bats, including those considered in
this paper, hunt socially [16] and communicate over long distances [17–19], thereby
rapidly congregating at rich feeding sites [20,21], for example, where migrations or
outbreaks of pest insects occur [22,23].
Little research on this topic has been conducted in India, and indeed, bats remain
severely understudied and undervalued in this country. Also, they remain
essentially unprotected in India, which is a cause of grave concern in itself. By this
note, we attempt to highlight the central role of ancient monuments for the bat
populations therein, the pest control function maintained by bats in agriculture, and
ultimately, the sustainability of food production in India. We emphasize that the
ideas outlined here are based on evidence from other countries. They are speculative
with respect to India, only because relevant studies have not been carried out.
2. The Sites
During a week in October 2018, we visited five archaeological sites in central
New Delhi that still have bat colonies (Table 1). The visits were made in the daytime,
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with the principal purpose of watching and photographing the resident bats in their
natural habitat.
Table 1. The archaeological sites visited in October 2018 and some basic information about them.
Site Type of
Building Location Time of
Construction
Comments on
Renovation, Lighting,
etc.
References
Agrasen ki
Baoli Stepwell
Connaught
Place, New
Delhi
14th century None [24,25]
Feroz Shah
Kotla
Mughal fort,
mosque,
stepwell
Vikram Nagar,
New Delhi 14th century
Extensive outdoor
lighting, many visitors,
mosque still used
[26,27]
Qutb Minar
Complex
Mughal fort,
minar,
mosque
Mehrauli, New
Delhi
1192–1316 and
later
Extensive renovation,
many outdoor lights,
intensive tourism
[26,28,29]
Zafar
Mahal Mughal fort Mehrauli, New
Delhi
18th and 19th
centuries None [26,30]
Khirki
Mosque
Mughal fort,
mosque
Malviya Nagar,
New Delhi 14th century Renovation ongoing [25,31,32]
One of our sites was the Agrasen ki Baoli, a stepwell, constructed in the 14th
century to store rainwater [24]. The other four sites were mosques or forts,
constructed under Mughal power during either the Delhi Sultanate (1206–1526) or
the subsequent Mughal Empire (1565–1857) [25,26].
The Feroz Shah Kotla fortress mostly consists of ruins but includes Jami Masjid,
an old mosque which is still in use [27]. Many vaults and chambers inside the
mosque are intact and are frequented by religious people on a large scale on
Thursdays for the performance of rituals. [27]. There were several thousand
Thursday visitors at the mosque at the time of our first visit, and hundreds of
worshippers shared the space inside the vaults and chambers with thousands of
bats.
The Qutb Minar complex is also a famous tourist spot and, in fact, the most
visited archaeological site in India [28]. It is also a designated UNESCO World
Heritage site [29]. The 74-m-high Qutb Minar and the associated archaeological
complex include the beautiful Alai Darwaza Gate, the Tomb of Iltutmish, and the
Quwwatul Islam, which is the oldest mosque in India, then constructed with reused
material from several Brahman temples [29]. The entire complex has recently been
thoroughly renovated and extensively fitted with outdoor lights for esthetic and
safety purposes. Thereby, it has become quite unfriendly to bats, but some tomb bats
still roost in the unlit chambers (Figure 1).
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Figure 1. A small group of naked-backed tomb bats (Taphozous nudiventris) in a chamber in Qutb
Minar area in New Delhi. Photo by J. Rydell 2018.
The remaining two sites are also open to tourists, but the number of visitors is
much lower. The Zafar Mahal monument was built during the 18th and 19th
centuries, toward the end of the Mughal Empire [30]. This monument has become
entirely enveloped by the surrounding city concrete and traffic over the years.
However, there is still room for many bats in several dark chambers and vaults
remaining inside (Figure 2). The site is so far untouched by recent renovation
attempts, and there are no esthetic lights installed in the premises. However, urban
lighting is prevalent in the surroundings.
Figure 2. A group of lesser mouse-tailed bats (Rhinopoma hardwickii) in Zafar Mahal in New Delhi.
Photo by J. Rydell 2018.
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Finally, the Khirki Mosque, one of the most important Mughal monuments
[31,32], has also become encroached by the growing city, but, fortunately, there are
no lights installed in the fort. It harbors many bats of at least four different species,
most of them roosting in the dark chambers at ground level, which can be accessed
from the outside (Figure 3). Renovation work is ongoing, and it seems likely that it
will affect the colony of fruit bats that reside in the main part of the mosque, but
hopefully, the chambers at the ground level, where most of the insectivorous bats
live, will escape this fate.
Figure 3. A greater mouse-tailed bat (Rhinopoma microphyllum) in a dark chamber in the Khirki
Mosque, New Delhi. Photo by J. Rydell 2018.
A common factor which made these forts attractive to bats is the presence of
several dark and undisturbed vaults or chambers. Smaller groups of bats are usually
less selective and were also found in more exposed sites. Darkness is an essential
habitat feature for bats, particularly at the roost, because it is their principal
protection against predation [33]. Proximity to good feeding sites is another
important feature of a good bat roost. Although the forts are all located in urban
settings, this has not always been the case, and the distances to the nearest
agricultural fields, where the bats may feed, are no more than 2–5 km, a distance
that they cover each night easily.
The mouse-tailed bats roosting in the vaults of Feroz Shah Kotla mosque showed
a surprising tolerance to visitors even at close range, at least as long as they were
ignored by the crowd. This suggests that the bats are seldom harassed in this place.
Indeed, it was quite clear that they were tolerated by the crowd and considered as a
natural feature of the place. In contrast, the bats reacted defensively to our torches
and cameras, a situation they were not accustomed to (Figure 4).
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Figure 4. Part of a colony of greater mouse-tailed bats (R. microphyllum) in the Feroz Shah Kotla
mosque in New Delhi. The tight clustering is a defensive behavior in response to our disturbance with
torch and camera. Interestingly, the bats never responded in this way to the crowd of worshippers
just a meter or two away. Photo by J. Rydell 2018.
3. The Bats
Bats were found in all the visited sites, although their numbers varied,
depending on the availability of undisturbed dark spaces for roosting. At each site,
we did a quick survey to record the species present and obtain a rough idea of their
numbers (Table 2).
Table 2. The sites visited and the bat species observed during a one-week field trip to some New Delhi
monuments in October 2018.
Site Estimated no. of
Bats Species Roosting Location
Agrasen Ki Baoli 10,000+ Fruit bats Rousettus leschenaulti High in the ceiling
Zafar Mahul 1000+
100+
Mouse-tailed bats
Tomb bats
Rhinopoma spp.
T. nudiventris
In dark vaults
Small groups in vaults
Feroz Shah Kotla
Mosque
10,000+
100+
Mouse-tailed bats
Tomb bats
Rhinopoma spp.
T. nudiventris
In dark vaults
Small groups in vaults
Khirki Mosque
1000+
10,000+
10+
Fruit bats
Mouse-tailed bats
Tomb bats
R. leschenaulti
Rhinopoma spp.
T. nudiventris
In the ceiling
In dark vaults
Small groups in vaults
Qutb Minar Complex 100+ Tomb bats T. nudiventris Small groups in vaults, a bigger
group in the tower
Although there were many individual bats at the sites, they belonged to no more
than four species (Table 2), which is just a tiny fraction of the over 100 bat species
known from the Indian subcontinent [34]. The sample represents species that are
relatively tolerant to the presence of people and perhaps other forms of disturbance.
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The mouse-tailed bats, of which we found two species, the greater Rhinopoma
microphyllum and the lesser Rhinopoma hardwickii, live either in small groups in
relatively exposed corners or in big groups (several thousand individuals) in dark
vaults outside the main tourist areas. These bats were by far the most numerous. The
larger naked-backed tomb bats (Taphozous nudiventris) typically roosted in small
groups in cracks and relatively exposed positions on the walls and ceilings in vaults
and rooms. There was also a relatively big colony of what we think was this species,
emerging from a high position (ca. 40–50 m) on the Qutb Minar in the evening.
In Table 2 we provide rough estimates of the number of individuals of each
species that we observed. The three insectivorous species are all specialized for a
nocturnal life in the free aerospace, where they are seldom seen from the ground.
The mouse-tailed bats have somewhat short and blunt wings and are weak but
persistent fliers [9]. They usually feed at high altitude and 10 km or more from the
roost [16]. In contrast, the tomb bats have longer and narrower wings, which
facilitate faster and straighter flight, and they probably fly much further [35].
Although they find their insect food using echolocation, just as most other bats, they
use vision to navigate over long distances [36].
Two of the sites that we visited also harbored big colonies of fruit bats, Rousettus
leschenaulti, (Table 2). Fruit bats are important as seed dispersers and pollinators of
fruiting trees and offer a host of ecological services [37] but they sometimes raise
concern in tourist sites because of their noisy presence and odorous excretions.
However, in this paper, we will not discuss the fruit bats any further. It is the insect-
eating bats that are the focus of this note.
4. Insect Pests of Rice
Rice (Oryza sativa) is by far the most important crop in Asia and the world, and
we will use it as an illustrative example. However, the pest situation is comparable
for all major crops in India, including wheat (Triticum aestivum), cotton (Gossypium
hirsutum), soybean (Glycine max), potatoes (Solanum tuberosum), sugarcane
(Zaccharum officinarum), and maize (Zea mays) [38].
Pest outbreaks are a significant constraint on rice production in India and
elsewhere [39,40]. The industrial pesticide production and application on cash crops
in India is poorly regulated [41], and, at the same time, the use of chemical pesticides
in agriculture has dramatically increased over the last decades [42]. The adverse
effects of pesticide usage in food crops have been well documented [43], and it is
evident that such methods of pest control are unsustainable [44]. In place of chemical
pest control agents, other, mostly biological, means are currently being developed,
such as mating disruption by use of pheromones or sterile males [45,46]. However,
such biological agents represent only a minor proportion of the options available on
the market at present [47]. In light of this, the viability of natural pest control agents,
such as bats [48,49], will become more and more critical as multi-resistant pests
evolve, and chemical control becomes increasingly inefficient.
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The economic value of the ecosystem service rendered by bats by feeding on
pest insects has never been estimated with respect to India. However, there is
growing evidence from other parts of the world, including southern USA [50–52],
Southeast Asia [53], the Mediterranean [54], China [55], and Madagascar [56], that
bats are major consumers of pest insects with a potential or proven capacity to
reduce or control their populations. The sustainability aspect of rice cultivation and
food security directly attributable to the conservation of bats is already evident in
Southeast Asia [57]. It is noteworthy that such studies make financial projections that
closely follow the current economic trends and, hence, should serve as a basis for
the economics of conservation policies.
There are about 20 species of insects regarded as major pests of rice in India
(Table 3). The adult stages of most of them are active at night or dusk and dawn, and
this is usually also the time when their migratory flights take place [58]. This means
that the pests are potential food for bats, which are active and search for food at the
same time of the day. Indeed, some of the pests, including the most problematic of
them all, the brown planthopper (Nilaparvata lugens) and the white-backed
planthopper (Sogatella furcifer) are the most important food sources for insectivorous
bats feeding over paddy fields in Thailand [59,60] and presumably elsewhere as
well.
Table 3. Some of the most important pests of rice in India and notes on the life habits of the adult
stage. The species list is partly adopted from reference [61]. Species marked * are known to be
consumed extensively by bats in Thailand (wrinkle-lipped free-tailed bat, Chaerephon plicatus
[53,60]).
Major Insect Pests of Rice in India Migratory Outbreak
Species Flies at Night Reference
Hemiptera Brown planthopper (Nilaparvata lugens) Yes* Yes [62,59]
White-backed planthopper (Sogatella
furcifer) Yes* Yes [63]
Green leafhopper (Nephotettix virescens) Yes [64]
Green leafhopper (Nephotettix nigropictus) Yes [63]
Zigzag leafhopper (Recilia dorsalis) Yes [65]
Mealy bug (Brevennia rehi) No No(?) [65]
Orthoptera Rice grasshopper (Hieroglyphus banian) Yes No [66]
Mole cricket (Gryllus orientalis) No Yes [65]
Diptera Rice gall midge (Orseolia oryzae) Yes [67]
Lepidoptera Yellow stem borer (Scirpophaga incertulas) Yes [68]
Dark-headed stem borer (Chilo polychrysus) Yes [69]
Striped stem borer (Chilo suppressalis) Yes [63]
Pink stem borer (Sesamia inferens) Yes [66]
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Rice leaf folder (Cnaphalocrocis medinalis) Yes Yes [70]
Armyworm (Spodoptera mauritia) Yes Yes [71]
Rice caseworm (Nymphula depunctalis) Yes [66]
Coleoptera Rice hispa (Dicladispa armigera) Yes Yes [65]
4. Discussion
Will it be practically possible to conserve and manage the tourists and the old
buildings as well as the bats therein in a sustainable and non-destructive way? We
certainly think so and, indeed, we believe that the bats themselves may even
enhance the touristic quality and excitement [72,73]. For example, an evening exodus
of thousands of bats from an old monument is a spectacular sight, which probably
would be appreciated by many visitors [74], particularly if the show is combined
with high-quality information about the ecological importance of the building and
the bats. And what could be a better setting for an evening lecture or a public bat-
watch excursion than an Indian 14th century Mughal monument?
The presence of many bats residing in old buildings sometimes raises concern
because of known or suspected weathering effects on the buildings. Degradation
and staining of monuments due to bat excretions certainly occur, but serious
weathering effects are unusual and depend critically on the chemical composition of
the building material and the excretions [75,76]. Decaying bat guano is usually acidic
[77] and therefore affects some limestones and sandstones [75]. However, Indian
monuments and temples are constructed from many different materials, depending
on the local geology and, although most rocks may be stained, they are not degraded
by bat guano or urine [76]. It is essential that the eviction of bats be restricted to cases
where it is considered absolutely necessary to prevent irreversible damage, on the
basis of authentic scientific information [78].
Large accumulations of bat guano and urine from bats sometimes have a strong
smell, and this could indeed repel visitors from compartments used by bats. More
seriously, however, dry accumulations of feces can lead to allergic reactions [79] or
histoplasmosis [80] infections in humans, particularly if the infected air is inhaled
frequently. Hence, it may be wise to remove accumulated bat feces (while using a
breathing mask) now and then from spots frequented by tourists, to minimize the
smell and the health risk. For the protection of tourists and bats, visitors should be
discouraged from entering poorly ventilated compartments with large bat colonies
(thousands of bats) and accumulations of feces. If necessary, such compartments can
be gated to give bats free passage in and out, while stopping humans from entering.
How such bat gates should be designed and constructed is critically important and
is described in [81]. Gating could be a suitable measure at some of the ground level
compartments of the Khirki mosque, for example (Figure 3).
There is a rich folklore about bats in India, just as in Europe and elsewhere [82],
generally depicting bats in a bad light, and this often results in a “fear” of bats [83].
However, in contrast to Europe, there is usually no religious mandate to persecute
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bats in India, where particularly the Hindu philosophy rather emphasizes the value
of life in harmony with nature [84]. In the Feroz Shah Kotla, we observed what
seemed to be a tight but peaceful coexistence of bats and humans, mainly Muslims
in this case, which must have persisted for a very long time, perhaps for centuries.
We do not believe that the average tourist, whether Indian or European, is afraid of
bats in the strict sense, but it is very important that this sensitive issue is handled
with due respect [83]. European bats, including those in churches and houses, are
now seen in a much more positive light than they were just a decade or two ago,
thanks to education and enlightenment activities in combination with legal
protection. In the case of bats, “fear” is partly an expression of curiosity and
fascination, which can be turned into excitement by means of education, perhaps
through cooperation with bat scientists. In our view, graffiti and other signs of
vandalism [4,5], in combination with an accumulation of plastic bags and other
garbage [6] in and around the buildings, almost certainly affect the appeal of the
place. Signaling neglect and poor management, the piles of rubbish probably have a
much stronger repelling effect on tourists than the presence of bats.
There are very few studies where the fates of bat colonies have been monitored
at archaeological sites, following renovations and light installations. However, a
recently published long-term (30 years) study of bat colonies (brown long-eared
bats, Plecotus auritus) in 115 historical churches in Sweden [85] shows that major
renovation work may cause the disappearance of bats, but more likely they will be
back when conditions return to normal after the renovation. More importantly, the
installation of esthetic and/or safety lights, usually done simultaneously with the
renovations, is a more serious problem, particularly if the bats´ roost and emergence
sites become illuminated. In such cases, the bats usually disappear slowly but
permanently, most likely because of starvation [86]. Hence, while renovation work
is not necessarily harmful to resident bats in the long run if done with care, the
installation of lights often has a catastrophic effect on the bat population.
Reported cases of declining populations of wrinkle-lipped free-tailed bats
(Chaerephon plicatus) roosting in Buddhist temple caves in Cambodia are quite
alarming, although the reason behind the decline remains unknown [87]. One
possible explanation is that the use of pesticides in rice fields, where the bats feed,
has affected their reproduction and survival over a long time. Bats eat a lot and often
live for decades and, if the prey on insects containing pesticides, they may
accumulate dangerous concentrations of such chemicals [88]. The scenario predicted
by this hypothesis is worrying indeed, as it probably means a severe decline in the
ecosystem service now provided by bats.
5. Conclusion
There is a long line of reasoning between the management of old monuments in
Delhi for the facilitation of tourism, the welfare of the roosting bats therein, and their
presumed pest control service over the surrounding agricultural fields. Bats are
living components of old monuments, where they may have roosted for centuries,
Heritage 2019, 2, 36 563
and should be treated as such whenever possible. The ecosystem service they
provide by feeding on agricultural pests is considerable (worth 3.7 billion dollars
annually in the USA [7]; no figure exists for India). In comparison, the budget for the
Archaeological Survey of India for 2018 was 140 million dollars [1,2], which is only
a small fraction of the presumed value of the bats. Darkness is the bats´ principal
protection against predators [89]. We emphasize that lights must be used
restrictively and with great care [90]. Clearly, the pivotal role of old monuments
harboring bats in tourism, sustainable farming, food safety, and the economic well-
being of the society cannot be ignored considering the evidence at hand.
Author Contributions: Conceptualization and field observations: All authors; first draft: J.R.; reviewing,
editing, and approval: All authors.
Funding: We had no external funding for this project. However, we acknowledge the Ekman Foundations for
general support of studies on the environmental effects of light pollution (to J.R.).
Acknowledgments: We appreciate the help of Rajlakshmi Jha for the information about roosting sites of bats
in Delhi monuments and of Johan Eklöf for advice and comments on the manuscript. R.U. extends his
gratitude to Subhas and Geeta Umadi for tolerance and support, and to Kiko for moral support during the
preparation of this manuscript.
Conflicts of Interest: The authors declare no conflict of interest.
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Insect migrations represent large movements of resources across a landscape, which are attractive to predators capable of detecting and catching them. Brazilian free-tailed bats (Tadarida brasiliensis (I. Geoffroy, 1824)) consume migratory noctuid moths, which concentrate in favourable winds resulting in aggregations of prey that attract bats hundreds of metres above ground. Although T. brasiliensis are known to feed on these aggregations of migratory moths, changes in their foraging behaviours have not been linked to moth migration events. We investigated possible shifts in the bats’ foraging behaviours when moths are migrating with respect to altitude and moth abundance. We recorded 1104 echolocation call passes of T. brasiliensis at ground level and at altitudes of ∼100 and ∼200 m above ground level. We found proportionally more bat activity at higher altitudes when migratory moth abundance was high. We also found that bats decreased call frequency and bandwidth and increased call duration at higher altitudes and behaved similarly with increasing moth abundance even at ground level. Our results support predictions that bats change foraging behaviour in response to seasonal availability of migratory moths and document alterations in echolocation call parameters that are consistent with optimizing prey detection.
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Chaerephon plicatus consumes large amounts of planthoppers, which are the most serious pest in Asian rice fields. Brown planthoppers (Nilaparvata lugens) are known to migrate at high altitude and can cause severe damage and economic loss over a large area. However, we lack evidence whether this bat species also forage at high altitudes. This study investigated the stratification in foraging activity of C. plicatus at approximately 0, 100, and 200 m above ground level by using a helium-filled balloon-kite. The activity of C. plicatus aloft (100 m and 200 m) on average was six to twelve times higher than that close to the ground. Peak activity corresponded with the top of the nocturnal stable boundary layer, which is also the layer of maximum temperature and wind speed. Nilaparvata lugens has been found flying at the altitude where peak bat foraging activity occurs, which suggests that C. plicatus actively follows these migratory insects in the air. Thus, C. plicatus bats potentially play an important role in insect pest suppression in the areas they inhabit as well as at the landscape scale. However, the height of peak activity also corresponds with the height of wind turbine blades, thus, such turbines may pose a serious threat to the species.
Article
Observations of animals feeding in aggregations are often interpreted as events of social foraging, but it can be difficult to determine whether the animals arrived at the foraging sites after collective search [1–4] or whether they found the sites by following a leader [5, 6] or even independently, aggregating as an artifact of food availability [7, 8]. Distinguishing between these explanations is important, because functionally, they might have very different consequences. In the first case, the animals could benefit from the presence of conspecifics, whereas in the second and third, they often suffer from increased competition [3, 9–13]. Using novel miniature sensors, we recorded GPS tracks and audio of five species of bats, monitoring their movement and interactions with conspecifics, which could be inferred from the audio recordings. We examined the hypothesis that food distribution plays a key role in determining social foraging patterns [14–16]. Specifically, this hypothesis predicts that searching for an ephemeral resource (whose distribution in time or space is hard to predict) is more likely to favor social foraging [10, 13–15] than searching for a predictable resource. The movement and social interactions differed between bats foraging on ephemeral versus predictable resources. Ephemeral species changed foraging sites and showed large temporal variation nightly. They aggregated with conspecifics as was supported by playback experiments and computer simulations. In contrast, predictable species were never observed near conspecifics and showed high spatial fidelity to the same foraging sites over multiple nights. Our results suggest that resource (un)predictability influences the costs and benefits of social foraging.
Article
The conversion of natural habitats to agriculture is one of the main drivers of biotic change. Madagascar is no exception and land-use change, mostly driven by slash-and-burn agriculture, is impacting the island's exceptional biodiversity. Although most species are negatively affected by agricultural expansion, some, such as sy-nanthropic bats, are capable of exploring newly available resources and benefit from man-made agricultural ecosystems. As bats are known predators of agricultural pests it seems possible that Malagasy bats may be preferentially foraging within agricultural areas and therefore provide important pest suppression services. To investigate the potential role of bats as pest suppressors, we conducted acoustic surveys of insectivorous bats in and around Ranomafana National Park, Madagascar, during November and December 2015. We surveyed five landcover types: irrigated rice, hillside rice, secondary vegetation, forest fragment and continuous forest. 9569 bat passes from a regional assemblage of 19 species were recorded. In parallel, we collected faeces from the six most common bat species to detect insect pest species in their diet using DNA metabarcoding. Total bat activity was higher over rice fields when compared to forest and bats belonging to the open space and edge space sonotypes were the most benefited by the conversion of forest to hillside and irrigated rice. Two economically important rice pests were detected in the faecal samples collected-the paddy swarming armyworm Spodoptera mauritia was detected in Mops leucogaster samples while the grass webworm Herpetogramma licarsisalis was detected from Mormopterus jugularis and Miniopterus majori samples. Other crops pests detected included the su-garcane cicada Yanga guttulata, the macadamia nut-borer Thaumatotibia batrachopa and the sober tabby Ericeia inangulata (a pest of citrus fruits). Samples from all bat species also contained reads from important insect disease vectors. In light of our results we argue that Malagasy insectivorous bats have the potential to suppress agricultural pests. It is important to retain and maximise Malagasy bat populations as they may contribute to higher agricultural yields and promote sustainable livelihoods.
Article
The brown planthopper (Nilaparvata lugens) is one of the major insect pests of rice fields in Southeast Asia. They have been widely acknowledged for causing significant rice yield losses. However, the wrinkle-lipped free-tailed bat (Chaerephon plicatus Buchannan, 1800) is a known agent of pest suppression for white-backed planthoppers (Sogatella furcifera), and may also suppress brown planthopper populations. Hence, it is important to investigate the diet of C. plicatus in areas where brown planthoppers are common to determine whether these bats feed on these insects. To accomplish this objective, we analyzed the diet of C. plicatus from two caves that differed in the percentage of surrounding land area occupied by rice fields (70% versus 22%). Bat fecal pellets were collected monthly for a year. A total of 720 fecal pellets were analyzed, and the results revealed that C. plicatus feeds on at least eight insect orders, including Coleoptera, Homoptera, Hemiptera, Diptera, Lepidoptera, Odonata, Hymenoptera and Orthoptera. Specifically, homopterans comprised the greatest diet volume in the rice growing season, whereas coleopterans were most abundant in the diet when rice fields were fallow. Moreover, most homopterans were identified as brown planthoppers. To estimate the relative numbers of brown planthoppers consumed during each month, the number of genitalia of male brown planthoppers was counted. We recorded the greatest numbers of genitalia during the rice planting period, with an average of four genitalia per fecal pellet. Examining both the percent volume and percent frequency of each insect order in the diet of C. plicatus revealed that the two study caves were no significantly different, even though the proportion of surrounding active rice fields was different. Our results suggest that tens of millions of brown planthoppers are consumed by this bat species each night. The similar diets of the two study colonies may be due to their high altitude foraging and preference for migratory insects. Our results indicate that the wrinkle-lipped freetailed bat is an important biological suppression agent of brown planthoppers in rice fields.