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Naturwissenschaften 86, 276–279 (1999)
Springer-Verlag 1999
Why Do Diurnal Moths Have Ears?
James H. Fullard
Department of Zoology, Erindale College, University of Toronto, 3359
Mississauga Rd., Mississauga, Ontario L5L 1C6, Canada
Jeff W. Dawson
Department of Biology, Queen’s University, Kingston, Ontario K7L 3N6,
Canada
Received: 14 September 1998 / Accepted in revised form: 11 December 1998
Introduction
Ears exist in moths primarily for the
purpose of detecting hunting bats at
night to avoid predation. The ears of
four species of day-flying Nearctic
moths are as sensitive as those of a
common, night-flying genus to the
frequencies emitted by sympatric bats
and show no evidence of being vestigial. We determined that all of the
day-flying moths spend 44–73% of
their 24-hour cycles active at night
when bats hunt. Two of the moths
tested are sound-emitting species and
may use their ears during intraspecific
communication. We conclude that the
functions of bat detection and social
communication are the only selective
forces acting on moth ears, and that
in their absence these sensory structures degenerate.
Most moths have simple ears on various parts of their bodies that they
use to detect the echolocation calls of
aerially hunting, insectivorous bats
[1]. Where bats are numerous and
diverse (e.g., the tropics), the ears of
sympatric moths are more sensitive to
a broader range of frequencies than
those that live in areas of lower bat
diversity (e.g., temperate regions) [2].
Certain habitats exist that are spatialCorrespondence to: J.H. Fullard
e-mail: jfullard@erin.utoronto.ca
Tel.: c1-905-828-5416
Fax: c1-905-828-3792
276
ly and/or temporally bat free (i.e.,
places and/or times that bats do not
exist), and some of the moths in these
habitats exhibit ears with varying levels of auditory degeneration (e.g.,
oceanic island moths [3], wintermoths
[4]). Other moths experience release
from bat predation and corresponding auditory degeneration by means
of extreme behavioral changes (e.g.,
flightlessness [5–8]). For temporal bat
release a pronounced example of auditory degeneration exists in certain
members of the Dioptinae, a group of
diurnal Neotropical moths [9]. If diurnal habits result in bat-free environments, we should expect auditory degeneration in day-flying moths, assuming that they do not use their ears
for other purposes (e.g., social communication). We examined the auditory, activity, and acoustic characteristics of four species of Nearctic dayflying moths to test this hypothesis.
Materials and Methods
From June until September 1998 we
collected the following noctuoid
moths from wild populations as they
flew during the day at the Queen’s
University Biology Station in eastern
Ontario, Canada: (Arctiidae) Cycnia
tenera, Ctenucha virginica; (Lymantriidae):Lymantria dispar (males only,
females do not fly); and (Noctuidae):
Caenurgina erechtea. We used standard techniques [9] to expose and re-
cord from the auditory nerve of
moths placed 20 cm from a Technics
loudspeaker (EAS-10TH400B). The
preparations were exposed to 10 ms
(1 ms rise/fall time) sound pulses at
frequencies of 5–100 kHz at 5-kHz increments generated by a WaveTek
function generator (model 23),
shaped by a Coulbourn S84-04 envelope shaper and amplified (National
Semiconductor LM1875 T). The presentation of the pulses was randomized by a MS-DOS program (written
by J.W.D.). The thresholds of the
most sensitive receptor cell (A1) were
recorded as the stimulus intensity (dB
SPL) required to elicit two action potentials to at least three stimulus
pulses in a row.
To determine the 24-h activity patterns of the moths we placed moths
(not the same as those used for the
auditory analyses) in 15.2-cm-tall
semicylindrical (6.5 cm diameter)
screened chambers that were supplied
with microcentrifuge tubes filled with
dilute sucrose and visually separated
from each other. The chambers were
placed in a 221!273!202 cm screen
enclosure in a partially open forest so
that they were exposed to ambient
temperatures and light levels and isolated from human disturbance. The
chambers were placed 60 cm before a
video camera capable of automatically switching from the use of ambient
light during the day to a built-in
source of near infra-red (wavelengthp980 nm) light during the night
(Sanyo VDC-9212). The camera’s
output was fed into a VCR in another
room, and the moths’ 24 h activities
were recorded using 10-h video tapes
(BASF T-200). Activity was scored as
the number of minutes of a 10-min
bin in which the moth expressed at
least one movement of a body length
or more that was accompanied by vigorous wing beats during the minute.
Sounds were recorded from the
moths using standard high-frequency
analogue recording techniques [10].
Moths were placed 5 cm in front of a
1/4 in. Brüel and Kjær (type 4135)
condenser microphone (coupled to a
Naturwissenschaften 86 (1999) Q Springer-Verlag 1999
Brüel and Kjær measuring amplifier,
type 2206) and tactually stimulated.
Sounds were recorded onto a RACAL Store 4D instrumentation tape
recorder and analyzed with a Windows-based fast Fourier transformation program (ScopeDSP, Version
3.5, Iowegian International Corp.,
~http://www.iowegian.com 1 ).
Results
Auditory Analyses
Figure 1 (left) compares the auditory
sensitivity curves (audiograms) of the
four day-fliers that we sampled to the
median audiogram of underwing
moths, Catocala spp., species that
were collected at ultraviolet lights
during the night [11]. All but one of
the day-fliers that we sampled have
audiograms resembling that of Catocala spp. and all appear similarly
tuned to the frequencies most commonly emitted by insectivorous bats
(heavy bar in the audiograms).
Activity Analyses
The actograms of Fig. 1 (right) illustrate that all of the moths spent a
large portion of their 24-h cycle flying
during nighttime. Using sunrise/sunset times of 0540 and 2030 hours, respectively (the average times for the
summer months at this site (Herzberg
Institute of Astrophysics, ~http:/
/www.hia.nrc.ca 1 ), the average percentage time spent nocturnally active
in all of the individuals were: Cycnia
tenera: 47.5%; Ctenucha virginica:
44.0%; Lymantria dispar: 53.9%; Caenurgina erechtea: 72.8%.
Fig. 1. Left, the audiograms of the day-flying moths sampled in our study (np5 for all species). Thin lines, individuals; thick lines, the median curves for each species. Included are the
median audiograms (broken line) of common, night-flying noctuids, Catocala spp. Thick bar,
bandwidth of predominant frequencies emitted by this area’s most common bats [22]. Right,
24-h actograms of the moths (np5 for all species, not the same as those used for the audiograms). Thin bars, ranges within each 10 min bin, thick bars are the mean values; shaded
boxes, night hours for the site used in this study
Acoustic Analyses
Figure 2 illustrates the time-amplitude and frequency analyses of these
sounds. The arctiids Cycnia tenera
and Ctenucha virginica emit sounds
when tactually stimulated, but Lymantria dispar and Caenurgina erechtea are silent. The sounds of the arctiids consist of trains of short clicks
with predominant frequencies of
68–75 kHz (C. tenera) and 34–37 kHz
(C. virginica), all within the best hearing range of their ears.
Discussion
The first explanation for ears in diurnal moths is that they are vestigial
and serve no present function. Since
there are only one (Notodontidae) to
two (e.g., Noctuidae) auditory receptors in the ears of noctuoid moths,
there would be little advantage for
these organs to quickly disappear following the relaxation of selection
pressure compared to more complex
Naturwissenschaften 86 (1999) Q Springer-Verlag 1999
organs such as eyes [12]. Symptoms of
auditory degeneration in bat-released
insects include insensitivity to high
( 1 50 kHz) frequencies and increased
threshold variability (e.g., oceanic island moths [3, 13, 14], flightless preying mantids [15], diurnal South American moths [9], wintermoths [4, 8]).
Only one of the moths in the present
study, Ctenucha virginica, exhibits
any evidence of high frequency insensitivity compared to the audiograms
277
Fig. 2. a) Oscillograms and frequency analyses (fast Fourier transformations) of the
sounds emitted by C. tenera and C. virginica.
The sounds consist of trains of short clicks
emitted as the sound-producing organ, the
tymbal, first experiences a musculated buckling producing the active modulation half-cycle (AMHC) followed by a passive series of
clicks emitted as the tymbal elastically returns to its original position producing the
passive modulation half-cycle (PMHC) [10].
The fast Fourier transformations are composites of each click in the AMHC
of the nocturnal Catocala spp. but C.
virginica appears to offset this with
high sensitivity at bat specific frequencies. The absence of overall insensitivity and high threshold variability in the day-flying moths of our
study leads us to conclude that their
ears are adaptively [16] functional.
The second explanation for ears in
diurnal moths is that the moths spend
278
at least part of their 24 h cycle flying
at night when it is necessary to detect
bats. The actograms suggest that all of
the moths that we studied spend a
considerable amount of time flying
when bats are active. Surveys made at
a local colony of 800–1000 Little
Brown bats (Myotis lucifugus) indicate that nightly foraging for this
common species begins between 2011
and 2132 hours, times that overlap
the 24-h activities of the moths we
tested. The day/night activities of
moths may also depend upon their
geographical distribution. Cycnia tenera, for example, ranges from central
Ontario south to Florida where it may
fly more during the relatively warmer
nights. Genetically linked northern
populations may favor more diurnal
(i.e., warmer) activity patterns while
retaining the auditory defenses of
their more nocturnal conspecifics.
The third reason for ears in diurnal
moths is that they use them to listen
for conspecific social sounds (e.g.,
mating calls [17]). The audiograms of
both C. tenera and C. virginica appear
tuned to the specific predominant frequencies of their clicks but are also
sensitive to sympatric bat frequencies.
The audiograms of C. virginica, the
most diurnal of the moths that we
tested, appear more narrowly tuned
than those of the other moths, suggesting that this moth’s ears listens
more for conspecific sounds than
bats, an explanation offered for the
sensitive ears of the diurnal Australian whistling moth, Hecatesia thyridion [18]. The sounds of C. tenera have
been implicated in both social [19]
and anti-bat [20] behaviors, but the
purposes of the sounds of C. virginica
are presently unknown.
In conclusion, diurnal moths have
physically evident ears for one or
more of the following reasons: (a) the
ears are vestigial, (b) the moths, although active during the day, still fly
at night and use them for bat detection, (c) the moths use their ears for
detecting social sounds. All of the
moths in our study have sensitive and
apparently functional ears, and probably use them as defense against bats
when flying at night while two species
(C. tenera and C. virginica) may additionally use them for detecting social
sounds. We reject the possibility that
day-flying moths have ears as a general auditory sense to detect unspecified predators other than bats for the
following reasons: (a) the majority of
exclusively diurnal, nonacoustic Lepidoptera (i.e., butterflies) are earless
(the reported ears of certain nymphalids [21] seem adapted for intraspecific communication), (b) in cases
in which exposure to bats has been
drastically reduced, there is severe
auditory degeneration (e.g., wingless/
earless moths [5]) and, (c) the behavior of diurnal predators is characterized by stealth rather than the emission of loud sounds as they approach
an intended prey. While eyes rather
than ears appear to be a diurnal insect’s greatest sensory defense, for
most insects that are active for during
even a small portion of a bat-inhabited night, the opposite seems true.
We thank Queen’s University for permission to use their facilities, Kathleen Pendlebury, Nadia Napoleone,
Alessandro Mori, and Tarah Harrison
for assistance in the field and Drs. W.
Conner, B. Fenton, and A. Surlykke
for comments on the manuscript. This
study was funded by a research grant
from the Natural Sciences and Engineering Research Council of Canada.
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Springer-Verlag 1999
Mitochondrial DNA Sequence Relationships of
the Newly Described Enigmatic Vietnamese
Bovid, Pseudonovibos spiralis
S.E. Hammer, F. Suchentrunk
Research Institute of Wildlife Ecology, Vienna Veterinary University,
Savoyenstrasse 1, A-1160 Vienna, Austria
R. Tiedemann, G.B. Hartl
Institut für Haustierkunde, University of Kiel, Olshausenstrasse 40–60,
D-24118 Kiel, Germany
A. Feiler
Staatliches Museum für Tierkunde, Dresden, Königsbrucker Landstrasse 159,
D-01109 Dresden, Germany
Received: 19 October 1998 / Accepted in revised form: 17 December 1998
Only recently several new ungulate
species from Southeast Asia have
been described [1–4]. From one of
these, the mysterious Vietnamese ungulate “Linh Duong” (Pseudonovibos
spiralis), living individuals have been
observed only by local hunters, but
horns have become available to the
Correspondence to: S. Hammer
(e-mail: hammer6zoo.univie.ac.at,
Tel.: 43-1-31336-1309,
Fax: c43-1-31336-778)
scientific community [3, 5]. Prior to
the description of this enigmatic new
species, such horns had already been
catalogued at the Kansas Museum of
Natural History in the United States,
but erroneously attributed to Bos
sauveli [5]. Consultations of old Chinese encyclopedias, compilations, and
textbooks from the Ming and early
Qing dynasties revealed a drawing of
a goatlike ungulate, roughly matching
the horn morphology of Pseudonovibos spiralis [6]. This illustration sug-
Naturwissenschaften 86 (1999) Q Springer-Verlag 1999
18. Surlykke A, Fullard JH (1989) Hearing
in the Australian whistling moth, Hecatesia
thyridion.
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76 : 132–134
19. Conner WE (1987) Ultrasound: its role in
the courtship of the arctiid moth, Cycnia
tenera. Experientia 43 : 1029–1031
20. Fullard JH, Simmons JA, Saillant PA
(1994) Jamming bat echolocation: the
dogbane tiger moth Cycnia tenera times
its clicks to the terminal attack calls of
the big brown bat Eptesicus fuscus. J Exp
Biol 194 : 285–298
21. Swihart SL (1967) Hearing in butterflies
(Nymphalidae: Heliconius, Ageronia). J
Insect Physiol 13 : 469–476
22. Fullard JH, Fenton MB, Furlonger CL
(1983) Sensory relationships of moths
and bats sampled from two Nearctic sites.
Can J Zool 61 : 1752–1757
gests morphological relationships of
this species with at least three genera
of Bovidae; the gazelles (Procapra),
the gorals (Nemorhaedus) and the
saigas (Saiga) [6].
Given the scanty information of reliable data on this species, we sequenced
a 415-bp fragment of the mitochondrial cytochrome b gene of P.
spiralis. DNA from horn fragments of
the paratypus B18480 [3] was extracted [10] and PCR amplified with
two oligonucleotide primers, L14724
and H15149 [11]. Both strands were
automatically sequenced on a LICOR 4000, and all steps, from DNA
extraction to sequencing, were independently repeated once, yielding an
unambiguous sequence.
A phylogenetic analysis was carried
out by including the following taxa
(Genebank accession numbers in parenthesis): Bison bonasus (Y15005),
Bos javanicus (D34636), Bos taurus
(V00654, J01394), Bubalus bubalis
(D34638),
Bubalus
mindorensis
(D82895),
Budorcas
taxicolor
(U17868), Capra falconeri (D84202),
Capra hircus (X56289), Capricornis
crispus (D32191), Gazella granti
(AF028820), Hemitragus jemlahicus
(U17866), Nemorhaedus caudatus
(U17861),
Ovibos
moschatus
(U17862), Ovis aries (X56284), Ovis
dalli
(U17860),
Saiga
tatarica
(U17864). The “maximum-likeli279