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Eukaryon, Vol. 12, March 2016, Lake Forest College
Detecting the danger: How do moths and
butterflies manage to escape their predators?
Joshua Spreng
Department of Biology
Lake Forest College
Lake Forest, Illinois 60045
Introduction
Hearing organs are essential sensory systems for intraspecific
communication as well as for detection and avoidance of predators. Using
technological as well as molecular methods, studies provide knowledge
and a better understanding of the structure as well as of the evolutionary
development process of acoustic sensory organs in animals, especially
in insects. The ability to detect acoustic signals generated by prey, predator, competitors (rivals) and applicable mates is crucial for survival and
reproduction (Hoy, 1996; Yager, 1999). The bat – moth model is a significant representative of coevolution and leads to a better understanding of
prey – predator relationships and how organisms respond and adapt – behaviorally as well as morphologically – to their environment and increased
predator pressure. Some nocturnal flying insects developed ears that are
sensitive to ultrasound as a response to the echolocation predation strategies of various bats and can therefore be seen as a product of evolutionary
adaptation (Windmill, 2006). Studies have also shown that nocturnal insects not only perform escape maneuvers after the detection of predators
but also actively send back signals in order to startle and irritate the predators (Fournier, 2013; Miller, 2001; Corcoran, 2011; Nakano, 2015). Furthermore, studies have revealed that bats themselves have responded to the
evolved detection and interference strategies of moth as well by changing
the frequency and / or amplitude of signals during echolocation and by
listening to the sound produced during the prey’s escape movements (Miller, 2001; Conner, 2011). Researching such species interactions not only
increases the knowledge of how different organisms influence each other,
but also informs us about evolution on a larger scale.
Anatomy of the acoustic sensory organ in insects: The tympanate ear
The sensory part of the auditory system of animals consists of
the tympanate ear, which acts as a pressure detector and is found in a
variety of organisms, from invertebrates to vertebrates (Yager, 1999). However, compared to vertebrates, the auditory sensory organs of insects are
present in a wide variety and are not located near the center of the nervous
system (cranial), but are found on various locations on their bodies (Hoy,
1996; Kamikouchi, 2013). The locations are different among various insect species and may even vary within a particular species: In crickets, for
example, the tympanate ears are located on the forelegs (Geurten, 2013;
Poltnick, 2012), in grasshoppers, on the first abdominal segment (Plotnick,
2012), in butterflies, near the wings (Lucas, 2014), in moths, on the first
abdominal segment, at the base of the forewings or at the anterior or posterior region of the second abdominal segment (Pfuhl, 2015). The tympanate ears consist of three anatomical parts: the tympanum, the tracheal
sac, and the tympanal organ. The tympanum is a thin skin layer that will
vibrate if there is any change in pressure detected. The tracheal sac is an
air filled sac inside of the tympanum, which increases the frequency of the
vibration, but is not responsible for tuning or directionality (Yager, 1999).
The tympanum is responsible for converting the changes in pressure to
motions of the membrane. The tympanal organ is in charge of transcribing
or changing the produced mechanical signal into a neural signal (Yager,
1999). Scientists have determined two main causes that are responsible
for the development and evolution of tympanate ears. The first is intra
species communication through sound recognition and localization. The
second is the detection of predators, particularly bats, by being sensitive
to ultrasound (Hoy & Robert, 1996; Stumpner & Helversen, 2001; Senter,
2008).
Detection of predators and escape maneuvers
Butterflies and moths are related insects in terms of evolution.
They are both members of the order Lepidoptera . By generating a molecular dataset, using a phylogenomic analysis, scientists were able to establish a close relationship between moths and butterflies, which contradicted
the historical placement of butterflies - data of nucleotides and amino acid
Review Article
yielding nearly identical and transcriptome-based trees are well supported
(Kawahara, 2014). Moths and butterflies do not only share similar characteristics such as wings that are covered with scales, but both own hearing
organs that are specially adapted to detect the sounds that are generated
by their predators (Fournier, 2013). Since most of the butterflies are day active, their ears are sensitive to day active predators. Nymphalid butterflies
(Morpho peleides) and crepuscular owl butterflies (Caligo Eurilochus) for
example have a frequency sensitivity of 1kHz and 1 - 4 kHz, respectively,
and are therefore able to detect the approach of eastern phoebe (Sayornis
phoebe) and the chickadee (Poecile atricapillus) whose frequency of wing
flapping is 18.5 +/- 0.19 kHz and 20.7 +/- 2.5 kHz, respectively (Fournier,
2013; Lucas, 2014). Playbacks of recorded flight sounds of an attacking
bird lead in a signal transportation across auditory nerve cells of both noctuid moths and nymphalid butterflies, resulting in escaping maneuvers of
the organisms (Fournier, 2013).
As a response to the increasing predation pressure by insectivorous bats, nocturnal insects evolved sensitivity to the ultrasonic echolocation calls of bats (Nakano, 2015). Most moths have evolved sensitivity to
ultrasonic sound between 20-60 kHz at its best and nocturnal butterflies of
Hedyloidea have shown sensitivity between 40 kHz and 80 kHz (Nakano,
2015: Lucas, 2014). Other insects such as crickets, katydids, beetles,
and lacewings are able to detect the sonar radiation of bats and perform
various behavior forms in response to it (Conner, 2011). Since species of
moths differ greatly in size, there is a correlation between body size and
sensitivity, i.e. best heard frequency: The ears of larger sized moths are
tuned to be more sensitive (Nakano, 2015; Miller, 2001). Although large
moths reflect an intense echo due to their body size and are therefore
detectable by bats on a distance of up to 10 m, those moths are capable
of detecting bats over a distance of 100 m due to their adapted sensitivity
(Miller, 2001). Exposed to imitating sounds of bat calls, moths have shown
a variety of escaping movements consisting of turning and flying away, zigzag and looped-shaped flights, and abrupt and powerful dives or passive
falls (Miller 2001; Conner 2012).
Strategies to avoid predators’ attacks: Consternation, warning and masking
Besides the escape movements after detecting predators, studies have shown that nocturnal insects such as moths have other strategies
that prevent them from being eaten and therefore contribute to their survival. Some moth species developed sound producing organs, tymbals, which
are not only used in order to communicate with other individuals in the species (i.e. through courtship calls in order to reproduce), but are also being
used to agitate and / or irritate attacking bats (Nakano, 2015). In order to
confuse bats, male as well as female moths respond to the echolocation
calls of bats by emitting a single or a series of click calls in the ultrasonic range (Nakano, 2015). Those click calls have three hypothesized main
purposes: 1.) Causing the bats to interpret moth clicks as echoes (known
as phantom echo hypothesis), 2.) Decreasing the bats’ precision during the
distance evaluation process (known as ranging interference hypothesis),
and 3.) Fully masking the echo of the moths, making them temporarily
“invisible” for bats (known as the masking hypothesis) (Corcoran, 2011).
Analysis of the bats response in terms of echolocation and flight movement support the ranging hypothesis (Corcoran, 2011). Moths, such as
tiger moths, not only seem to borrow the bats’ strategy of distance and
location strategy by evaluating the repetition rate of the bat calls to the
clicking signals, but also interfere and interrupt the bat’s precise echolocation technique by sending long series of high density clicks that overlap
with the bats’ own echo (Nakano, 2015). Furthermore, studies have shown
that some moths also use sounds as acoustic warnings. Arctiid moths, for
example, are toxic and use single click calls in order to extend their supplemental visual warning, which consist of bright colors (Nakano, 2015).
The fact that moths do not represent the main part of the diet of bats may
explain the effectiveness of the escape and defense strategies of moths
(Miller, 2001).
Countering strategies and adaptations: Predators respond
Scientists stated possible explanations of adaptations and
counter strategies which would allow bats to avoid the defense mechanisms of moths. One possible counter tactic is changing the frequency
during echolocation, i.e. moving the sonar frequency out of the range of
the sensitivity of tympanate ears of insects by using higher or lower frequencies (Miller, 2001; Conner 2011). There is evidence that some bats
are emitting echolocation signals with an increased frequency that have
the effect of overcoming insect detection abilities (Miller, 2001; Goerlitz,
Eukaryon, Vol. 12, March 2016, Lake Forest College
Review Article
2010; Conner 2011). However, since an increase in frequency and / or
amplitude also results in an increase of the resolution of the echolocation
process, it is not yet clear whether this behavior represents an adaptation
as a response to the moth hearing or a general improvement of the sonar
technique (Miller, 2001; Goerlitz, 2010; Conner 2011). Studies have shown
that aerial-hawking bats, for example, emit echolocation signals of a high
– amplitude nature in order to expand their detection range, which may
result in an increase of the bats’ ability to detect and catch their prey (Goerlitz, 2010). Through bat flight-path and moth neurophysiology analyses,
scientists were able to show that bats of Barbastella barbastellus perform
a counter strategy, known as stealth echolocation, by emitting signals with
amplitudes that are 10 to 100 times lower than the ones of aerial-hawking
bats and which are undetectable by moths, resulting in significant capturing
success (Goerlitz, 2010; Conner, 2011). This technique gives Barbastella
an advantage over other ariel-hawking bats, but it also comes with a cost:
it reduces the detection distance (Goerlitz, 2010). A second strategy could
be the changing of the intensity of the signals during echolocation: Since
intensity of sound is proportional to the pressure of the sound, bats will be
less detectable to the tympanate ear of the insect (Miller, 2001). Listening
to the sound produced by the prey while moving around or by moving their
wings can be seen as a third strategy (Miller, 2001). However, this strategy
has its limits and does not work for organisms that stay motionless: Sedentary moths, for example, have been found to stay motionless or freeze
upon hearing of echolocation signals (Miller, 2001). To decide if the behavior of bats turning off echolocation can be seen as a counter strategy is
difficult. Miller (2001), for example, states that it is possible that bats stop
the echolocation process since they do not require further updates on the
estimated position of the resting prey. Furthermore, scientists were able to
show that some predators made modifications on their wings, in order to be
acoustically undetectable by prey. Barn owls (Tyto alba), for example, feed
on moths and have developed specific feather arrangements that significantly reduce noise that is produced while hunting (Sarradj, 2011; Fournier
2013).
Note: Eukaryon is published by students at Lake Forest College, who are
solely responsible for its content. The views expressed in Eukaryon do not
necessarily reflect those of the College. Articles published within Eukaryon
should not be cited in bibliographies. Material contained herein should be
treated as personal communication and should be cited as such only with
the consent of the author.
Conclusion and Future Studies
The research performed by various scientists show that the ability of insects, such as moths and butterflies, to detect acoustic signals that
are generated by other organisms is not only crucial in terms of intra-species communication and reproduction but also in terms of surviving. The
development of hearing systems and their adaptations, the evolvement
of strategies to prevent a predator’s attack, and the counter strategies of
predators are all evolutionary processes. The moth – bat relationship is
a prime example of this. In order to detect and escape predators, moths
and butterflies have evolved and adapted hearing organs and are capable
of performing a variety of escape maneuvers. Furthermore, some moths
developed strategies to either confuse or warn bats or to make themselves
temporally “invisible”. Bats, on the other hand, have evolved behavioral
counter strategies to possibly avoid the defense mechanisms of moths.
Some of them can increase the bats’ ability to detect and catch moths while
others are only effective to a certain degree (i.e. some moths stay motionless if they detect a predator and are therefore difficult to be distinguished
by the predator itself). Future research is required to decide whether the
behavior of turning off echolocation can be seen as a counter strategy and
if predators have adapted morphologically, i.e. by modifying their feathers
in terms of sound reduction and their attacking behaviors (Miller, 2001;
Sarradj, 2011; Fournier, 2013).
The scientists’ findings not only contribute to a better understanding of how ears in insects, such as moths and butterflies, evolved and
are used to detect predators in order to maintain survival, but also of how
and to what degree organisms put evolutionary pressure on each other.
This may lead to an increase in knowledge about predator/prey relationships, how organisms adapt and respond to their environment (including
other organisms) in order to survive, and why organisms behave the way
they do. On an even larger scale, these results may provide a better understanding of the concept of evolution.
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