An ancient battle rages high above our heads in the night sky as bats, the consummate nocturnal predators hunt their insect prey using ultrasonic sonar. One of the most important factors in the successful adaptive radiation of bats is their effective echolocation system. Echolocating bats emit ultrasonic pulses and listen for the presence, delay, and harmonic structure of the echoes reflected from the objects in the environment (Jones and Teeling, 2006). The frequency of the echolocation calls varies from 8 to 215 kHz depending on the bat species. The pulse repetition rate of the calls can vary from roughly 3 to approximately 200 pulses s−1 (Simmons et al., 1979). The echolocation sequence of hunting insectivorous bats involves three main phases: search, approach, and terminal (buzz) (Griffin et al., 1960). Many, if not most, cases of insect hearing probably originated as a means for detecting and avoiding predators such as sensitivity to ultrasound appears to have coevolved with echolocation signaling by insectivorous bats (Greenfield, 2016). In moths bat-detection was the principal purpose of hearing, as evidenced by comparable hearing physiology with best sensitivity in the bat echolocation range, 20–60 kHz, across moths in spite of diverse ear morphology (Nakano et al., 2015). Tympanic organs (ears) of moths are sufficiently sensitive to detect the echolocation cries of most bats before the bats can register their echo (Greenfield, 2014 and Goerlitz et al., 2010). In addition to hearing ultrasound, many moths belonging to sub-family Arctiinae are also capable of producing ultrasound in the form of short, repetitive clicks in response to tactile stimulation and the ultrasonic signals of echolocating bats when they detect the sonar signals of attacking bats (Corcoran et al., 2010). Anti-bat sounds function in acoustic aposematism, startle, Batesian mimicry, Mullerian mimicry and sonar jamming. Beetles, mantids, lacewings, crickets, mole crickets, katydids, and locusts can detect the sonar emissions of bats and exhibit various forms of anti-bat behavior. Researchers are beginning to use sophisticated high-speed infrared videography and high-frequency microphone arrays to study bat-insect interactions under natural conditions that will yield a multitude of exciting predator-prey interactions in the future.

2. SEMINAR (ENT 591)
JAYANT YADAV (2017A39D)

3. OUT LINE OF THE SEMINAR
• Introduction
• Terminologies
• Bat Echolocation
• Moth Hearing
• Chemical Defenses
• Bat-Moth Story
• Diversity of Ears and Anti-Bat Strategies
• Summary
• Conclusion

4.  In the night sky high above our heads, an ancient battle rages i.e Bats vs Insects
 Bats, the nocturnal predators, hunt their insect prey using ultrasonic radar.
 Moths, beetles, mantids, lacewings, crickets, mole crickets, Katydids and locusts can
detect the sonar emissions of bats and exhibit various forms of anti-bat behavior.
 Insects counter with myriad behaviors including aerobic evasions, stealthy
adaptations and anti-bat sounds which function in acoustic aposematism, startle,
Batesian mimicry, Mullerian mimicry and sonar jamming.
 This presentation describes the insect preying mechanism of bats, how the insects
counter it and again what are the bat countermeasures to these defenses: The Arm Race

5. 1.Echolocation: Sonar uses small pulses of sound to locate the
position of objects in the vicinity of the source of the sound.
So how is this done?
The bat emits a pulse of sound and listens
carefully as the sound hits the objects in its
surroundings and is reflected back to the
bat’s ears.
Using the information the bat creates an
3-dimensional picture of its immediate
vicinity and this picture is updated each
time the bat receives an echo.
That is how the bats manage to avoid even
moving objects while they fly.

6. 2. Tymbal organ: The sound-producing structure in arctiine moths.
3. Duty cycle: The percentage of time occupied by sound.
4. Modulation cycle: Sound produced by one flexion and relaxation of a tymbal organ.
5. Acoustic aposematism: A prey strategy in which sound warns the predator of the
noxious characteristics of the prey.
6. Sonar jamming: A prey strategy in which the prey sounds render bat sonar less
effective.
7. Clutter zone: A zone near vegetation in which prey echoes blend in with the
echoes of the background and make prey detection more difficult.
8. Arm race: The evolutionary straggle between competing sets of coevolving genes
(Spp.) that develop adaptation against each other.
9. Batesian mimicry: A prey strategy in which a palatable individual, the mimic,
resembles an unpalatable and benefits from the resemblance predators.

7. •Where a harmless species mimics a harmful one (Hemeroplanes larva).
B
A
T
E
S
I
A
N
M
I
M
I
C
R
Y

8. 10. Mullerian mimicry: A prey strategy in which unpalatable or
otherwise noxious species resemble each other, gaining an advantage
by sharing the burden of educating predators.
• where two or more unpalatable species resemble each other.
Danaus chrysippus
(Mimic)
Danaus genetua
(Model)

9. Kingdom : Animalia
Phylum : Chordata
Class : Mammalia
Infraclass : Eutheria
Superorder : laurasiatheria
Order : Chiroptera
Group : Micro & Mega bat
About Bats……………!!
Scientific classification

10. Two traditionally recognized suborders of
bats are:
• Megachiroptera (Megabats).
• Microchiroptera
(Microbats/Echolocating bats).
• Bats represent about 20% of all classified
mammal species worldwide.
• About 70% of bats are insectivores &
some are frugivores.
• Pollinate flowers and disperse fruit seeds.
• Bats are important in reducing insect
pests, thus reducing the need for
pesticides.

11. What Do Bats Eat?
Insects - aerial hawkers Insects - ground feeders Nectar
Pollen
Fruit
Frog
fish
Rodents
Blood

12. Adaptations:
Flying Mammals.
They are often mistakenly called "flying rodents"
or "flying rats".
Use Echolocation to find their way in the dark
and locate food at night.
Chiroptera (“winged hands”) implies, the bones
in the wings of bats are elongated fingers.
Many species of bats have the ability to
Hibernate in adverse conditions.
Bats also escape adverse climatic conditions by
migrating altitudinally, moving up-slope to
cooler elevations.

14. • Most important factors in the successful adaptive radiation of bats is their effective
echolocation system.
• Old World fruit bats use echolocation as a means of spatial orientation in the dark, and a
large number actively pursue prey either partially or completely guided by sonar.
(Fenton, 1990)
• It emit ultrasonic pulses and listen for the presence, delay, and harmonic structure of the
echoes reflected from objects in the environment.
• Frequency of the echolocation calls varies from 8 to 215 kHz. Pulse repetition rate of the
calls can vary from roughly 3 to 200 pulses/sec. (Schnitzler and kalko, 2001)

15. The Echolocation sequence of hunting insectivorous bats
involves three main phases:
1. Search phase
2. Approach phase
3. Terminal phase
(Surlykke and Moss, 2000)

16. 1. Search phase:
Bat’s flight is relatively straight and the bat produces echolocation calls with a low
repetition rate (3–15Hz) and relatively long duration (5–30ms).
Fig. Echolocation sequences of a Myotis sp. bat successfully attacking a tethered noctuid moth
Time (MS)

17. 2. Approach phase:
Begins when a bat first responds to a
target by turning toward it and
increasing the pulse repetition rate.
Time (MS)
Fig. Echolocation sequences of a Myotis sp. bat successfully attacking a tethered noctuid moth

18. 3. Terminal phase:
Bat emits a group of short pulses (0.5–
1.0 ms) at a high rate (100–200 Hz) as it
closes on its airborne target.
Time (MS)
Fig. Echolocation sequences of a Myotis sp. bat successfully attacking a tethered noctuid moth

19. Fig : Successfully attacking a tethered sonar-jamming Bertholdia trigona.

20. Echolocating bats vary the Intensity, pulse repetition rate,
frequency-time structure, directionality and harmonic components
of their echolocating calls according to the situation.
(Ghose and Moss, 2003)
This plasticity allows them to avoid obstacles and locate objects in
different habitats.
Bats typically have wing morphologies and echolocation repertoires
specialized for the habitat in which they forage and they impose a
strong selective pressure for defensive counter adaptations by
insects.
(Fullard, 1998)

21. • Tympanic organs (ears) sensitive to ultrasound have evolved multiple times in
nocturnal Lepidoptera and exist in nearly half of extant species.
(Ratcliffe, 2010)
• High-frequency ears arose from vibration-sensitive proprioreceptors in:
i. Thorax (eg., Noctuoidea),
ii. Abdomen (e.g., Pyralidae and Geometridae)
iii. Mouthparts (e.g., some Sphingidae)
These sensors preadapted moths for the detection of airborne sound and the
echolocation emissions of bats . (Fullard and Yack, 1993)
•In the noctuid subfamily Arctiinae, tiger moths, the tympanic membranes are
located on the thorax and are typically most sensitive to frequencies between 30 and
50 kHz. (Fullard, 1988)

23. Hoy and Robert, 1996
Table 1. Occurrence of tympanal organs in seven orders of insects
ORDER SUPER
FAMILY/FAMILY
SPECIES EAR LOCATION
Neuroptera Chrysopidae Chrysoperla carnea Wing base
Lepidoptera Geometridae Larentia tristata Abdomen
Notonectidae Phalera bucephala Metathorax
Arctiidae Cycnia tenera Metathorax
Nymphalidae Heliconius erato Base of the fore or hind wing
Hedyloidea/hedylidae Hyacinthine
Coleoptera Cicindelidae Cicindela marutha Abdomen
scarabaeidae Euetheola humilis Cervical membranes
Dictyoptera Mantodea Mantis religiosa Ventral metathorax
Blattoidea Peripleneta americana Metathorasic leg
Orthoptera Acrididae Locusta migratoria First abdominal segment
Gryllidae Gryllus bimaculatus Prothorasic legs
Hemiptera Cicadidae Cystosoma saundersii abdomen
Corixidae Corixa puncatata Mesothorax
Diptera Tachinidae Ormia ochracea Ventral prosternum
Sarcophagidae Colcondomyia audotrix Ventral prosternum

24. • Moth ears are simple in neurophysiological design, with from one to four
sound-sensitive cells, yet they provide their bearers with critical
information about their acoustic surroundings.
(Miller and Surlykke, 2001)
• They are sufficiently sensitive to detect the echolocation cries of most bats
before the bats can register their echo.
(Goerlitz et al., 2010)
• Moth species capable of detecting bats have a clear survival advantage (up
to 40%) over species that lack ears.
(Barber and Conner, 2006)

25. Prey defenses into two categories:
• Primary defenses : Prevent detection by the predator.
• Secondary defenses : Enhance survival after detection.
(Ratcliffe, 2010)
Moth ears can mediate both types of defenses:
- If the moth hears the bat first and turns away, avoiding
detection, the response would be considered a primary defense.
- If the moth responds after detection by the bat with more
complex sound production, the responses would be secondary defenses.

26. • In addition to hearing ultrasound, many arctiines are also capable of producing
ultrasound in the form of short, repetitive clicks in response to tactile
stimulation and the ultrasonic signals of echolocating bats.
(Corcoran et al., 2010)
• The sound producing organs of arctiines are tymbals and modified cuticular
plates on either sides of the third segment of the thorax.
• During flexion and relaxation cycle in the tymbal due to modified steering
muscles, clicks are produced.
• The resulting sounds register their peak intensity in the ultrasonic frequencies
ranging from 30 to 75 kHz and have sound pressure levels as high as 119 dB
measured at 2 cm.
(Sanderford and Conner, 1990)

27. Fig. Tiger moth acoustic defense strategies: Column 1: Species name, image, and defensive strategy.
Column 2: Scanning electron micrographs of the tymbal organs of each species. Column 3:
Spectrogram of tymbal sounds. Column 4: Palatability of species compared to noctuid controls.
Barber and Conner, 2006

28. Fig 6. Classification of anti-bat moth sounds plotted in acoustic space along maximum duty
cycle and modulation cycle complexity axes. Each number represents a species. The sonar-
jammers cluster contains Bertholdia trigona (B) and the aposematic/ mimetic cluster contains
Cycnia tenera (C) and Euchaetes egle (E).
(Corcoran et al., 2010)

29. • Tiger moths are well known for the defensive chemicals that they produce or
sequester from their host plants . (Nishida, 2002)
• Their chemical repertoire (known) includes biogenic amines, lichen phenolics,
azoxyglycosides, and iridoid glycosides. (Bowers, 2009)
• Pyrrolizidine alkaloids (PAs) and Cardiac glycosides (CGs) are prominent.
(Hartmann, 2009)
• PAs have a variety of effects on vertebrates, ranging from bitter taste in low
concentrations to tissue damage and death in high concentrations.
(Hartmann and Witte,1995)
• Defensive properties of PAs is their bitter taste.
• PAs are also effective feeding deterrents for invertebrate and vertebrate predators
such as spiders, sucking bugs, birds, and bats. (Hristov and Conner, 2005)

30. Table 2: Examples of plant allelochemicals sequestered by Lepidoptera (butterflies/moths)

31. Arctiids acquire and sequester PAs in two ways:
- As larvae while feeding on their PA-laden host plants
- As adults imbibing PAs from the surface of withered PA-containing plants
(Conner and Jordan, 2009)
• The pharmacological effects of cardenolides (cardiac glycosides) arise from
their inhibition of the Na+/K+ ATPases and the activation of emesis.
(Brower, 1984)
• Arctiid larvae obtain CGs from their food plants (usually Asclepiadaceae or
Apocynaceae), sequester them in body tissues, and then transfer them to the
adult stage through metamorphosis. (Wink, 1990)
• The toxins can be stored in the integument and hemolymph of larvae and adults
and are sometimes exuded secretions from the adults’ cervical glands.
• Both PAs and CGs are effective in deterring bat predation.
(Hristov and Conner, 2005)

32. Hypotheses:
1. Startle hypothesis: Suggest that the sounds elicit the mammalian startle
reflex.
(Miller,1991)
2. Jamming hypothesis: Maintains that the sounds confuse the bat by
interfering with its echolocation system.
(Ratcliffe and Fullard, 2005)
3. Aposematism hypothesis : Claims that the sounds warn the bat of the
moth’s distastefulness.
(Acharya and Fenton, 1999)

33. SONAR JAMMING
 Bertboldia trigona produces acoustic signals in response to bat cries. They have
very high duty cycle, a high degree of frequency modulation and larger number of
clicks/cycle .
 These are produced during the final moments of a bat’s attack to be most
effective.
 There are 3 mechanisms of sonar jamming:-
i. Phantom echo hypothesis: It suggested that the clicks and echolocation calls
have similar spectral properties. Thus bat could mistake clicks as echoes
returning from other objects and become confused. (Fullard et al., 1979)
ii. Masking hypothesis: It suggested that moth clicks mask the presence of
echoes rendering the moth invisible. (Mohl and Surlykke, 1989)
iii. Ranging hypothesis: It suggested that the clicks disrupt the neural mechanism
which encodes time of arrival of moth’s echo . Thus bat can not predict the real
distance or range of the moth. (Tougaard et al., 2004)

34. Fig: Unsuccessfully attacking a tethered sonar-jamming Bertholdia trigona.

35. Barber and Conner, 2007

36. ACOUSTIC APOSEMATISM
• Dunning (1968) - First to find evidence for acoustic aposematism.
Two groups of moths to caged bats:
- Live unpalatable arctiids capable of producing sound.
-Control group composed of silent palatable non-arctiid species.
“Bats avoided clicking arctiids more often than non-clicking species”
• Eckrich and Boppre (1990) found evidence for the importance of moth
defensive chemistry on the efficacy of sound.
• Dunning et al., 1992 later presented arctiids with their tymbals destroyed to
free-foraging bats :
• They observed that, on average, bats captured more muted arctiids than
sound producing arctiids.
• But after capture, the bats rejected a large proportion of the muted arctiids
relative to control non-toxic and non-acoustic moths.
• This proves that jamming or startle do not alone accounted for the
interaction and it also depends upon defensive chemistry of the moths.

37. Barber and Conner, 2007
Fig: Aposematism experiment having control and experimental moths

38. Case study:
•Multi-species experiments
•Single-species experiments
2005
N. I. Hristov · W. E. Conner
Department of Biology, Wake Forest University,
Winston-Salem, NC 27109, USA
e-mail: conner@wfu.edu

39. C+S+: Unpalatable moth that produces Sound
C+S−: Unpalatable moth that does not produce Sound
C−S+: Palatable moth that produces Sound
C−S−: Palatable moth that does not produce Sound
Fig. 1 A. Arctiid species and their representative categories used in the multispecies
approach. B. Approach and capture sequence of a big brown bat (Eptesicus fuscus) with a
control wax moth (Galleria mellonella) as prey

40. Fig. Multispecies predictions and results for the interactions of big brown
bats with control and experimental moths under the acoustic aposematism
hypothesis
A. Aposematism hypothesis:

41. Fig. Multispecies predictions and results for the interactions of big brown
bats with control and experimental moths under the acoustic jamming
hypothesis
B. Jamming hypothesis:

42. Fig. Multispecies predictions and results for the interactions of big brown
bats with control and experimental moths under the acoustic startle
hypothesis
C. Startle hypothesis:

43. ACOUSTIC MIMICRY
 Some palatable species should
produce sounds but not back them
up with defensive chemistry
(Batesian mimicry).
some unpalatable species should
benefit from bearing an acoustic
resemblance to other more common
unpalatable species (Mullerian
mimicry).

44. Barber and Conner, 2007
Fig : Batesian mimicry experiment. Red bats (Lasiuris borealis) and big brown
bats (Eptesicus fuscus) learned to avoid C. tenera but then avoid subsequently
presented E. egle due to Batesian mimicry.

45. • Eared moths have an optimal frequency range between 20 kHz and 50 kHz, which
coincides with the peak frequency used by most insectivorous bats.
(Nakano et al., 2015)
• The primary function of the moth ear is to detect and avoid the hunting of bats. Eared
moths show a series of defensive behaviors, when they are exposed to the cries emitted
by insectivorous bats. (Yuping et al., 2009)
• Moths are not the only insects to evolve bat detectors. (Miller and Surlykke, 2001)
• Insect ears have evolved in at least 7 of 29 insect orders . (Hoy,1998)
• The proprioreceptor precursors are found throughout the bodies of insects and so too
are ears. (Yack and Fullard,1990)

46. Beetles: Tiger beetle :Cicindela marutha
Largest order of insects is heavily
preyed on by some bats.
Possess ultrasound-sensitive ears on
first abdominal segment that are
sensitive to sound between 30 kHz and
60 kHz.
Their ears are tucked neatly away
under the fore of their elytra.
Thus only hear when they are in flight.
Beetles respond to bat sonar with head
roles, elytra swings, and changes in
wing beat frequency.
(Miller and Surlykke, 2001)

47. Night-flying dynastine scarab
beetles (Scarabaeidae) also have
ultrasound-sensitive ears.
They are located on the cervical
membranes and represent an
independent evolution of auditory
organs in the Coleoptera.
In response to simulated bat cries
(20–80 kHz) beetles executed a
head role characteristic of in-flight
turning and dropped to the
ground, classic antibat maneuvers.
(Fenton and Roeder, 1974)
Scarab Beetles

48.  Median cyclopean ear in praying
mantids (Mantodea).
 It functions as a single unit, hence
the term cyclopean.
 Sixty-five percent of mantids have
them and they are generally
sensitive to sounds between 25
and 50 kHz.
 In Parasphendale agrionina
(Mantidae), the ears mediate a
suite of defensive behaviors.
 The behaviors result in clear
evasive maneuvers—dives, turns,
and spirals—that thwart capture
by echolocating bats.
Praying mantids
Yager and Hoy, 1986

49. Green Lacewings:
One of the most interesting insect bat
detectors is the ear found on the wings of
green lacewings (Chrysopidae).
The ear is a swelling located on the radial
vein of the forewings.
When a green lacewing detects the sonar
signals of a bat, it folds its wings and
drops rapidly.
To render its trajectory less predictable, it
extends its wings, i.e., puts on its air
breaks, at random intervals.
Interestingly, bats may counter dropping
strategies by approaching targets from
underneath

50. Crickets:
 Female true crickets (Gryllidae) including
Australian oceanic field crickets, Teleogryllus
oceanicus, use their ears to localize the low-
frequency calling song of potential mates.
 A second high frequency peak in the sensitivity
of their hearing allows them to detect and steer
away from bats while searching for mates
 Similar responses have been noted in members
of the genus Gryllus .
 Cricket ears are located just below the “knee”
(tibia-femur joint) on the forelegs in the
location of the proprioreceptive subgenal
organ in other insects.

51. Katydids:
Recent studies indicate that some
katydids (Tettigoniidae) can detect the
bat sonar signal of gleaning bats
In response to the echolocation calls
of sympatric bats, they shut down
their own acoustic courtship displays
to avoid passive detection by gleaners.
Flying Neoconocephalus ensiger shows
classic bat avoidance in the presence
of bat-like ultrasound. Within 50 ms
of receiving a sound pulse, they close
all four wings and begin a free fall.

52. Locusts:
Adult migratory locusts (Locusta migratoria:
Acrididae) speed up their flight and turn away
from ultrasonic pulses that mimic bat
echolocation calls.
This response is mediated by paired abdominal
tympana and is considered an early warning
system for bats.
Interestingly, African tribes take advantage of
the high-frequency hearing of locusts by
rapping a metallic pot to deflect medium sized
swarms of locusts from their property.

53. Earless Insects:
Insects without ears are not totally at the mercy of
echolocating predators.
Nocturnal moths that lack bat-detecting ears
should fly particularly fast or fly erratically .
(Lewis et al., 1993)
To fly close to vegetation in what bioacousticians
refer to as the clutter zone.
Lekking ghost moths (Hepialus humuli ) appear to
use this strategy.
They carry out their sexual flight displays within
0.5 m of the surrounding vegetation and gain
protection by exploiting the clutter zone.
(Rydell, 1998)
Lekking ghost moths (Hepialus humuli )

54. Bat Strategies To Counter Insect Defense: The Arm Race
There is an evolutionary struggle in bats and insects with sequential adaptations and
counter adaptations. The frequency sensitivity of moth ears is clearly the result of
selection pressure of bats.(100)
 The bat’s counter adaptation is broadly termed as Stealth Echolocation and it
works as follows:
i. Some bats lowers the frequency (10 to 100 times) of their sonar, rendering it
difficult for moths to detect, due to decrease in action distance.
ii. Some bats counters insect defense by moving to ultrahigh frequencies much
above the sensitivity range of moths.
iii. Red bats approaches to their prey from below and thus anticipate the dropping
behavior of insects.

55. Economic Importance of Bats in Agriculture
• Bats are voracious predators of nocturnal insects, including many crop and forest pests.
• Loss of bats in North America could lead to agricultural losses estimated at more than
$3.7 billion/year. (Justin et al., 2011)
• Single colony of 150 Big brown bats (Eptesicus fuscus) in Indiana has been estimated to
eat nearly1.3 million insects pests every year, possibly contributing to the disruption of
population cycles of agricultural pests. (Whitaker., 1995)
• Single little brown bat can consume 4 to 8 g of insects each night during the active
season. (Kurta et al., 1989)
• One million bats estimated to have died from WNS (White Nose Syndrome). Thus
between 660 and 1320 metric tons of insects are no longer being consumed each year in
WNS affected areas. (Boyles and Willis., 2010)

56. CONCLUSION
1. Echolocating bats have been a major selective force on nocturnal insects,
resulting in an escalating arms race of bat sonar adaptations and insect anti-bat
counter adaptations.
2. Some insects produce anti-bat sounds when they detect the sonar signals of
attacking bats.
3. Anti-bat sounds function in acoustic aposematism, startle, Batesian mimicry,
Mullerian mimicry and sonar jamming.
4. Sonar jamming appears to function by interfering with the target-ranging
program of bats.
5. Moths, beetles, mantids, lacewings, crickets, mole crickets, katydids, and
locusts can detect the sonar emissions of bats and exhibit various forms of anti-
bat behavior.