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Bats and insect pest control: a review

Authors:
  • Museo di storia naturale - Università di Firenze Sezione di zoologia «La Specola»

Abstract

Bat conservation is important not only for biodiversity but also because these flying mammals provide ecological services essential for humans. In particular, bats are very useful for the control of insect populations and specifically pests to agriculture. Their diet very often includes Lepidoptera, a large order with several species very harmful to many plants of great economic interest. The diet of some European species of bats (e.g. Rhinolophus spp., Hypsugo savi, Nyctalus leisleri, N. noctula, Barbastella barbastellus, Plecotus spp., Myotis brandtii, M. bechsteinii, Eptesicus serotinus) includes high percentages of moths (Lepidoptera) and many of them are pests of economic importance. In the United States and Thailand some studies have economically quantified bats’ value as pest control expecially against moths; in Europe these studies are still scarce and need to be promoted giving even more support to the protection of this outstanding order of mammals.
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Vespertilio 17: 161–169, 2014
ISSN 1213-6123
Bats and insect pest control: a review
Marco riCCuCCi1 & Benedetto lanZa2
1 Gruppo Italiano Ricerca Chirotteri (GIRC), Pisa, Italy; marco.riccucci@gmail.com
2 Museo di Storia Naturale (Sezione Zoologica «La Specola») & Dipartimento di Biologia
Animale e Genetica, Università degli Studi di Firenze, Via Romana 17,
50125 Firenze, Italy; benedetto.lanza@libero.it
Abstract. Bats and insect pest control, an ecosystem service: a review. Bat conservation is important
not only for biodiversity but also because these ying mammals provide ecological services essential for
humans. In particular, bats are very useful for the control of insect populations and specically pests to
agriculture. Their diet very often includes Lepidoptera, a large order with several species very harmful
to many plants of great economic interest. The diet of some European species of bats (e.g. Rhinolo-
phus spp., Hypsugo savi, Nyctalus leisleri, N. noctula, Barbastella barbastellus, Plecotus spp., Myotis
brandtii, M. bechsteinii, Eptesicus serotinus) includes high percentages of moths (Lepidoptera) and
many of them are pests of economic importance. In the United States and Thailand some studies have
economically quantied bats’ value as pest control expecially against moths; in Europe these studies
are still scarce and need to be promoted giving even more support to the protection of this outstanding
order of mammals.
Agriculture, ecosystem services, Lepidoptera, moths, rice pests, Chilo suppressalis, olive fruit
y, Bactrocera oleae
Introduction
Only recently the protection of ecosystems and their conservation has been considered under
economic implications trying to understand how natural processes are important for the life and
survival of human beings. Those benets, measurable in economic terms, were called “nature’s
services” (Daily 1997, Daily et al. 2000); later and still today are referred to as “ecosystem ser-
vices” (Millennium Ecosystem Assessment 2005) and dened as benets to humankind derived
from resources and processes supplied by natural ecosystems.
The fundamental role of bats in maintaining ecosystems and their specic utility in the quality
of life were certainly underestimated until a few years ago. Bats are, with more than 1,300 species,
the second largest order of mammals (after rodents) and have colonized many different environ-
ments in all continents except Antarctica (Simmons 2005, Altringham 2011, Fenton & Simmons
2014). Over the past ten years, particular attention was paid to the economic value of bats in
agriculture and forestry, also the subject of several systematic reviews (Boyles et al. 2011, Kunz
et al., 2011, Ghanem & Voigt 2012, Boyles et al. 2013, Kasso & Balakrishnan 2013, Riccucci
& Lanza 2014) that highlight the still poor knowledge of the ecosystem services of insectivorous
bats in Europe. According to Boyles et al. (2011) in the United States the value of insectivorous
bats connected to the agricultural sector is about 22.9 billion USD a year (ranged from 3.7 to
53 billion USD per year). These estimates include the decreased costs of pesticide applications
reducing the development of pesticide resistance. Therefore there is an increasing interest of the
American farmers towards bats and how to attract them in their own land, even installing articial
roosts such as bat boxes (California Agriculture 1998, Kiser & Kiser 2002).
162
Most of the bat species (about 70%) are insectivorous, as the early Eocene bats (Habersetzer et
al. 1992, Simmons et al. 2008). In particular, some species from the fossil site of Messel (Germany)
used to prey on Lepidoptera (Richter 1993). Insect pests are a major problem in agriculture and
forestry (Hill 1983, 1987, 2008, Pollini 2013). Arthropods destroy between 18% and 26% of the
annual production of crops worldwide, for a value of over 470 billion USD (Culliney 2014). All
European species of Chiroptera are insectivorous (Dietz et al. 2009).
One of the most important ecosystem services of insectivorous bats is the control of herbivorous
arthropods including pest insects (Kunz et al. 2011, Ghanem & Voigt 2012). Among insects, moths
(order Lepidoptera) are major agricultural pests in many parts of the world (Zhang 1994, Hill
2008) and even in Europe, representing 91% of all lepidopterans (the other 9% are butteries).
Many of them are of great economic importance as pests of crops, horticultural plants or stored
products and woollens. Most moths are active at night or dusk, like bats.
Studies on the diets of European bats are here briey reviewed, mainly focusing on Lepidoptera
and on species of moths considered as agricultural pests (Hill 1983, 1987, 2008, Robinson et al.
2010, Pollini 2013). The aim is to highlight the economic benets of bats in insect pest control
and the urgent need to implement conservation actions as many species of bats are endangered
in several European countries (Temple & Terry 2007, Rondinini et al. 2013).
Moth-eating bats
Most of the studies on bats as biological pesticides refer to North America (Whitaker 1995, Cleve-
land et al. 2006, Federico et al. 2008, Boyles et al. 2011, Boyles et al. 2013). Foraging strategies
and diet of many species of European bats are relatively well-known (Beck 1995, Vaughan 1997,
Dietz et al. 2009, Lanza 2012).
The bat community in North America, as investigated by faecal analysis, consists of species
that eat mainly Lepidoptera (Ross 1967, Whitaker & Hamilton 1998). According to Ross (1967)
moths and beetles in North America, both representing very large groups, so numerous and
diverse in types and sizes that they are almost universally available as food for insectivorous
bats. Most African insectivorous bats also feed mainly on Lepidoptera and Coleoptera (Aldridge
& Rautenbach 1987).
A high number of insect species in the diets of bats have recently been identied using mole-
cular techniques on insect fragments in their faeces (Clare et al. 2009). Barnard (2011) provides
a useful appendix with extensive lists of prey species.
Signicant cases of pest control
It is of considerable interest the study carried out in Malta on the diet of Plecotus gaisleri. Borg
& Sammut (2002) mentioned this species as P. austriacus, but see Spitzenberger et al. (2006). The
examination of prey involved a bat present in a small room at the Museum of Natural History in
Mdina (Malta), where bat ate its preys. Bats use to eat the soft parts of their prey, the wings and the
hard ones are usually discarded. The discarded parts were collected and insect species identied
included several pest moths: Galleria mellonella – pest of apiculture; Autographa gamma – the
larvae feed on a wide variety of plants including pea (Pisum sativum), sugar beet (Beta vulgaris),
cabbage (Brassica oleracea); Chrysodeixis chalcites – prefers tomato, potato and pulses, but also
buds and fruits; Heliothis peltigera – prefers Solanaceae, Asteraceae and Fabaceae; Spodoptera
exigua – is a small black cutworm but voracious on different crops, such as sugar beet, corn,
163
Table 1. List of some Lepidoptera (moths) of agricultural interest found in the diet of European insectivorous
bats
bat species % of Lepidoptera family reference/s
lepidopteran species
Rhinolophus ferrumequinum 78% Jones 1990, Beck
Hepialus humuli Hepialidae 1995, Vaughan 1997,
Agrotis exclamationis Noctuidae Barnard 2011
Mesapamea secalis Noctuidae
Noctua comes Noctuidae
Noctua pronuba Noctuidae
Scoliopteryx libatrix Noctuidae
Rhinolophus hipposideros 19–89% Vaughan 1997, Beck
undetermined 1995, Lino et al. 2014
Rhinolophus euryale 69% Goiti et al. 2004, Goiti
undetermined et al. 2008
Rhinolophus mehelyi >90% Salsamendi et al.
undetermined 2008
Myotis bechsteinii 53–97% Vaughan 1997,
undetermined Noctuidae Barnard 2011
Myotis brandtii 91% Vaughan 1997,
undetermined Barnard 2011
Myotis nattereri 30% Beck 1995, Vaughan
undetermined 1997, Barnard 2011
Barbastella barbastellus 73–99% Jones 1990, Beck
undetermined 1995, Vaughan 1997
Eptesicus nillssonii 56% Beck 1995,
undetermined Vaughan 1997
Eptesicus serotinus 34%
undetermined Geometridae Beck 1995, Barnard
Noctuidae 2011
Pyralidae
Sphingidae
Tortricidae
Yponomeutidae
Zygaenidae
Odonestis pruni Lasiocampidae Mikula & Čmoková
Agrochola macilenta Noctuidae 2012: “more than
Agrotis ipsilon Noctuidae 80% of the consumed
Amphipoea oculea Noctuidae moths were important
Anarta myrtilli Noctuidae agricultural pests”
Autographa gamma Noctuidae
Brachionycha nubeculosa Noctuidae
Catocala electa Noctuidae
Catocala fulminea Noctuidae
Cucullia umbratica Noctuidae
Euplexia lucipara Noctuidae
Euxoa tritici Noctuidae
Lacanobia thalassina Noctuidae
Luperina nickerlii Noctuidae
Melanchra persicariae Noctuidae
Pachetra sagittigera Noctuidae
Tholera cespitis Noctuidae
Trachea atriplicis Noctuidae
164
Table 1. (continued)
bat species % of Lepidoptera family reference/s
lepidopteran species
Eptesicus serotinus Xestia castanea Noctuidae Mikula & Čmoková
(continued) Xestia c-nigrum Noctuidae 2012 (continued)
Mamestra brassicae Noctuidae
Noctua comes Noctuidae
Noctua fimbriata Noctuidae
Noctua pronuba Noctuidae
Stauropus fagi Notodontidae
Aglais urticae Nymphalidae
Vanessa cardui Nymphalidae
Pieris napi Pieridae
Coenonimpha arcania Satyridae
Cydia pomonella Tortricidae
Vespertilio murinus 49% Beck 1995, Barnard
undetermined 2011
Hypsugo savii 53%
undetermined Beck 1995
Nyctalus leisleri 67% Beck 1995, Vaughan
undetermined 1997, Barnard 2011
Nyctalus noctula 19–36% Noctuidae Beck 1995, Vaughan
undetermined Pyralidae 1997, Barnard 2011
Melanchra persicariae Noctuidae Poulton 1929
Mythimna pallens Noctuidae
Hepialus humuli Hepialidae
Triodia sylvina Hepialidae
Ourapteryx sambucaria Geometridae
Odontopera bidentata Geometridae
Ematurga atomaria Geometridae
Bupalus piniaria Geometridae
Biston betularia Geometridae
Pipistrellus kuhlii 38% Beck 1995
undetermined
Pipistrellus nathusii undetermined Beck 1995
Pipistrellus pipistrellus 33% Geometridae Beck 1995,
undetermined Noctuidae Barnard 2011
Pyralidae
Pipistrellus pygmaeus undetermined Barnard 2011,
Chilo suppressalis Pyralidae Flaquer 2011
Plecotus auritus 33% Arctiidae Beck 1985, Vaughan
undetermined Geometridae 1997, Barnard 2011
Hepialidae
Notodontidae
Nymphalidae
Pyralidae
Sphingidae
Thyatiridae
Abrostola triplasia Noctuidae Robinson 1990
Agrotis exclamationis Noctuidae
Amphipyra tragopoginis Noctuidae
Anitype chi Noctuidae
Apamea crenata Noctuidae
165
bat species % of Lepidoptera family reference/s
lepidopteran species
Plecotus auritus (continued) Apamea monoglypha Noctuidae Robinson 1990
Apamea sordens Noctuidae (continued)
Autographa gamma Noctuidae
Autographa jota Noctuidae
Autographa pulchrina Noctuidae
Caradrina morpheus Noctuidae
Cucullia umbratica Noctuidae
Diachrysia chrysitis Noctuidae
Lacanobia oleracea Noctuidae
Lacanobia thalassina Noctuidae
Mamestra brassicae Noctuidae
Mesapamea secalis Noctuidae
Mesoligia literosa Noctuidae
Mythimna impura Noctuidae
Naenia typica Noctuidae
Noctua comes Noctuidae
Noctua mbriata Noctuidae
Noctua janthina Noctuidae
Noctua pronuba Noctuidae
Oligia strigilis Noctuidae
Phlogophora meticulosa Noctuidae
Rhyacia simulans Noctuidae
Rusina ferruginea Noctuidae
Scoliopteryx libatrix Noctuidae
Xestia xanthographa Noctuidae
Deilephila elpenor Sphingidae
Hepialus humuli Hepialidae
Hepialus sylvina Hepialidae
Nola cucullatella Nolidae
Apamea monoglypha Noctuidae Buckhurst 1930
Noctua pronuba Noctuidae
Noctua comes Noctuidae
Mamestra brassicae Noctuidae
Mesapamea secalis Noctuidae
Agrotis nigricans Noctuidae
Agrotis exclamationis Noctuidae
Leucania conigera Noctuidae
Melanchra persicariae Noctuidae
Spilosoma lubricipeda Arctiida Poulton 1929
Noctua spp. Noctuidae
Plusia sp. Noctuidae
Autographa gamma Noctuidae
Triphosa dubitata Geometridae
Scoliopteryx libatrix Noctuidae
Orthosia sp. Noctuidae
Xylena exsoleta Noctuidae
Eumorpha satellitia Noctuidae
Plecotus austriacus 90% Arctiidae Beck 1995, Barnard
undetermined Drepanidae 2011
Endromidae
Geometridae
Lasiocampidae
Lymantriidae
Noctuidae
166
Table 1. (continued)
bat species % of Lepidoptera families reference/s
lepidopteran species
Plecotus austriacus Notodontidae Beck 1995, Barnard
(continued) Sphingidae 2011 (continued)
Tetheidae
Thiatiridae
Tortricidae
Plecotus gaisleri see text Borg & Sammut 2002
Tadarida teniotis 65–88% Whitaker et al. 1994,
undetermined Rydell & Arlettaz 1994
tomato, green bean, tobacco, grapes; Spodoptera littoralis – among host plants there are cotton,
horticultural crops (Solanaceae), corn; Noctua pronubacauses fatal damage to many plants:
carrots, strawberries, lettuce, tomato, potato, spinach; Agrotis ipsilon infested plants: Swiss
chard, corn, vegetable crops; A. puta, A.segetum – pests of various wild and cultivated plants.
The rice crops have a very important place in human nutrition; this graminaceous plant of Asian
origin is the staple food for about half of the world’s population (Kiple & Ornelas 2000, Timmer
2010) and it is cultivated in almost all countries (FAO 2014). The world rice crop is attacked by
more than 800 species of insects and at least 20 can cause serious economic damages (Heinrichs
1994). In Asia, where more than 90% of the world’s rice is produced, the average loss of yield
due to pests is around 20% (Pathak & Khan 1994). In Thailand bats act as efcient biological
control of rice pests (Leelapaibul et al. 2005, Wanger et al. 2014).
Conclusions
Bats play a relevant action in the protection of economically important crops against lepidopteran
pests. Insects considered as pests, often concentrate in large quantities in cultivated landscapes,
have been found in the diet of several species of bats. To install articial roosts (bat boxes) can
be a real important way to protect bats and to be very useful to agriculture as well. In the Ebro
Delta (Spain), where there are some of the largest European rice paddies, soprano pipistrelle,
Pipistrellus pygmaeus, acts as efcient biological controller of one of the most devastating pest,
the rice striped borer, Chilo suppressalis (Lepidoptera: Pyralidae). In this area several bat boxes
have been installed; they accommodate up to 4,500 bats and have greatly reduced the deleterious
impact of this pest on rice crops, minimizing the use of insecticides (Flaquer et al. 2011). In
France 24 samples were analyzed from droppings collected under articial lodgings (bat boxes)
on the edge of an olive orchard (sampling in September and October during the y ight period).
Four PCR tests were performed and the results show that six samples of bat droppings are po-
sitive showing an adult predation of the olive fruit y, Bactrocera oleae (Diptera: Tephritidae),
by Pipistrellus kuhlii (Ricard et al. 2008). The less pesticides used on crops the less we take in
when we eat. Bats are among the best friends to organic farmers. They play a role in pest control
and attracting bats to farms can make a signicant difference to farmers who want to use natural
biological insect control, rather than rely upon chemicals that may threaten our environmental
and personal health.
Table 1 shows Lepidoptera species (mostly moths) found in the diets of European bats. Only
species in the diet of a specic bat species are mentioned. About 80 species of moths are listed,
167
found in the diet of 22 species of bats. Lepidoptera make up a substantial part of the diet for Rhi-
nolophus spp., Myotis brandtii, M. bechsteinii, Nyctalus leisleri, N. noctula, Eptesicus serotinus,
Hypsugo savii, Barbastella barbastellus, and Plecotus spp. Among the eaten moths Agrotis excla-
mationis, A. ipsilon, A. segetum, Autographa gamma, Chilo suppressalis, Chrysodeixis chalcites,
Cydia pomonella, Galleria mellonella, Heliothis peltigera, Hepialus humuli, Mamestra brassicae,
Naenia typica, Noctua mbriata, N. pronuba, Odonestis pruni, Phlogophora meticulosa, Spodo-
ptera exigua, S. littoralis, Xestia c-nigrum are signicant agricultural pests. Whenever possible
Latin names were updated according to the current taxonomy.
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Bats are among the most economically important nondomesticated mammals in the world. They are well-known pollinators and seed dispersers, but crop pest suppression is probably the most valuable ecosystem service provided by bats. Scientific literature and popular media often include reports of crop pests in the diet of bats and anecdotal or extrapolated estimates of how many insects are eaten by bats. However, quantitative estimates of the ecosystem services provided by bats in agricultural systems are rare, and the few estimates that are available are limited to a single cotton-dominated system in Texas. Despite the tremendous value for conservation and economic security of such information, surprisingly few scientific efforts have been dedicated to quantifying the economic value of bats. Here, we outline the types of information needed to better quantify the value of bats in agricultural ecosystems. Because of the complexity of the ecosystems involved, creative experimental design and innovative new methods will help advance our knowledge in this area. Experiments involving bats in agricultural systems may be needed sooner than later, before population declines associated with white-nose syndrome and wind turbines potentially render them impossible. © 2013 Springer Science+Business Media New York. All rights are reserved.
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Order Chiroptera is the second most diverse and abundant order of mammals with great physiological and ecological diversity. They play important ecological roles as prey and predator, arthropod suppression, seed dispersal, pollination, material and nutrient distribution, and recycle. They have great advantage and disadvantage in economic terms. The economic benefits obtained from bats include biological pest control, plant pollination, seed dispersal, guano mining, bush meat and medicine, aesthetic and bat watching tourism, and education and research. Even though bats are among gentle animals providing many positive ecological and economic benefits, few species have negative effects. They cause damage on human, livestock, agricultural crops, building, and infrastructure. They also cause airplane strike, disease transmission, and contamination, and bite humans during self-defense. Bat populations appear to be declining presumably in response to human induced environmental stresses like habitat destruction and fragmentation, disturbance to caves, depletion of food resources, overhunting for bush meat and persecution, increased use of pesticides, infectious disease, and wind energy turbine. As bats are among the most overlooked in spite of their economical and ecological importance, their conservation is mandatory.