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ISRAEL JOURNAL OF ECOLOGY & EVOLUTION, Vol. 53, 2007, pp. 173–177
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A field assessment of the defensive responses of moths to
an auditory stimulus
Justin R. St. Juliana,a,†,* Brock M. Fenton,b Carmi Korine,a Berry Pinshow,a
Michal Wojciechowski,a and Vasiliy Kravchenkoc
a
Mitrani Department of Desert Ecology, Jacob Blaustein Institute for Desert Research,
Ben-Gurion University of the Negev, Sede Boqer Campus 84990, Israel
b
Department of Biology, The University of Western Ontario, London,
Ontario N6A 5B7 Canada
c
Department of Zoology, Tel Aviv University, P.O. Box 39040, 69978 Tel Aviv, Israel
Abstract
We examined the responses of moths to an auditory stimulus in the field
with respect to moth size, moth activity state (at rest or flying), whether it
responded, and response type. Moths most commonly responded by changing flight direction. Flying moths responded significantly more often to the
auditory stimulus than did resting moths; small- and medium-sized moths responded significantly more often than larger ones. We found no differences in
use of response types between size classes. We suggest that these behavioral
responses to the auditory stimulus are likely due to evolved induced responses
to detection of predatory bats.
Keywords: activity state, anti-predator behavior, bat, moth, predation, prey size
Introduction
The ability of some moth species to hear the echolocation calls of hunting bats allows
them to avoid approaching danger (Waters, 2003). Flying moths that can hear and respond to specific echolocation calls evade attacking bats more than moths that cannot
hear bat calls (Acharya and Fenton, 1999). To bats that hunt flying prey, sedentary moths
are less noticeable than flying ones because of their lack of motion and the masking effect of background (Arlettaz et al., 2001). Thus moths at rest should tend to respond less
to an auditory stimulus because a response would tend to decrease, rather than increase,
safety.
Surlykke et al. (1999) demonstrated that larger moths are more easily detected by bats
than smaller ones, but larger moths also tend to be better at detecting bat echolocation
calls. Thus, larger moths may have a greater tendency to respond to an auditory stimulus
in the field.
*Author to whom correspondence should be addressed. E-mail: [email protected]
†
Current address: Department of Ecology and Organismal Biology, Indiana State University, Science Building, Room 281, 600 Chestnut St., Terre Haute, Indiana 47809, USA.
Accepted November 2007.
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Diversity in traits such as morphology and escape behavior can be anti-predator adaptations. Larger insectivorous bats tend to eat larger prey, and smaller ones eat smaller
prey (Aldridge and Rautenbach, 1987). Medium-sized moths could be under predation
pressure from both larger and smaller bats. If so, medium-sized moths should tend to
respond to an auditory stimulus with a greater diversity of responses.
Methods
The research was conducted at Ben-Gurion University of the Negev, Sede Boqer Campus, Israel (30º51¢N, 34º47¢E, 475 m asl). Observations were made from 21:00 to 02:00
h on 16 nights, between 2 July and 10 August 2003. We tested moths 1 to 5 meters from
street lights. Each moth we tested was visually classified as small, medium, or large. We
collected 50 voucher specimens to record the species composition in each size class,
and used length (tip of the head to end of the wings) as an index of size. Small, medium,
and large moths were 6 to <14 mm, 14 to 18 mm, and 19 to 23 mm long, respectively.
Large moths included Arctiidae (1 Utethesia pulchella), Noctuidae (1 Agrotis segetum, 5
Helicoverpa armigera, 1 Heliothis nubigera, 1 Heliothis peltigera, 1 Mythimna sicula, 2
Spodoptera exigua), and Pyralidae (1 Lamoria species). The noctuid Spodoptera exigua
(n = 15) was the only medium-sized moth captured. Small moths included Noctuidae (9
Spodoptera exigua), Pyralidae: (1 Lamoria species), Tineidae, and 12 Microlepidoptera
of several different species.
We followed the responses of moths to an auditory stimulus in four settings: (1) at
rest on a light, a light pole, or on other objects; (2) flying around lights; (3) flying in a
constant direction; and (4) flying after being shaken from vegetation or a light. Moths
shaken from vegetation or a light were given 5–10 seconds to adopt a behavior (flying
in a constant direction or around the light) before we stimulated them.
We tested the responses of moths to an electronic dog whistle (Dazer II, K-II Enterprises, Camillus, NY, USA). The observer stood ~1 to 3 meters from the moth, triggered
the Dazer for ~ 0.5 to 2 seconds, and recorded the moth’s response.
For resting moths, we recorded two broad categories of response: (a) no response,
i.e., the moth remained sedentary (some shuddered or moved their wings; this was not
counted as a response), or (b) response (moved to a new location). For flying moths, we
observed two general responses: (a) no response (the moth continued to fly around the
light or did not discernibly change course), or (b) response. We categorized four specific
responses: (1) dive—the moth flew (or “fell”) straight toward the ground; (2) change—
the moth changed its flight direction, or flew away from the light; (3) spiral—the moth
spiraled downwards; (4) erratic—the moth rapidly changed flight direction several times
immediately after the stimulus. For moths flying around lights, an erratic response was
more frequent changes in flight direction, coupled with increased flight speed.
We performed this experiment with the expectation that the response of moths to the
Dazer would yield insights into moth responses to bat vocalizations, with the following caveats. The Dazer produces multiharmonic sounds dominated by 24.1 kHz. The
Vol. 53, 2007defensive responses of moths to an auditory stimulus
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Dazer’s sound pressure is ~105 dB SPL at 1 m. This sound pressure is similar to that
used by some bats (Waters and Jones, 1995) at near-attack distances. Many aerial-feeding bats use echolocation calls with energy in the frequency range of the Dazer (Fenton
et al., 1998). Dazer sounds are audible to moths with ears and elicit defensive behaviors
(Rydell et al., 1997; Reddy and Fenton, 2003; Svensson et al., 2003). Four aerial insectivorous bat species ranging from 6 to 35 g are common at the foraging site (Korine and
Pinshow, 2004). These include: Pipistrellus kuhlii (frequency range (FR): ~36–47 kHz,
peak frequency (PF) ~ 42 kHz), Eptesicus bottae (FR: ~30–42, PF: ~32), Tadarida
teniotis (FR: ~9–30, PF ~ 13 kHz), and Taphozous perforatus (FR 25–33, PF ~29 kHz).
No bats in the study area vocalize exactly at the frequency of the Dazer; therefore, we
are unable to categorize the Dazer sound as an “artifical bat call” because our results may
be an artifact of the Dazer’s specific properties. Nonetheless, it is reasonable that if the
moths at our study site can detect and respond to bat vocalizations, they can do likewise
for frequencies within the spread of bat vocalizations in the study area. Therefore, we
believe that responses of moths to the Dazer should yield insights into the responses of
moths to real bats.
Results and Discussion
Moth activity state (flying vs. resting) and propensity to respond
We obtained data from 843 individual moths (215 large , 410 medium, 216 small).
Flying moths responded significantly more often (n = 732, 83.2% responded) to Dazer
signals than resting moths (n = 109, 12.1% responded) (N = 841, df = 1, Pearson’s Χ2 =
273.4, p < 0.0001). The tendency of a resting moth to respond was not affected by its
size (N = 109, DF = 2, Pearson’s Χ2 = 0.563, p = 0.7546).
Not moving in response to an intense call may be adaptive (because it does not break
acoustic crypsis), but the opposite could be true in response to a less intense call (= more
distant bat). The tendency of a resting moth to respond to a bat call should follow a
hump-shaped curve where moths respond at intermediate intensities, but not at greater
intensities, where a response would break crypsis, and not at weak intensities where risk
is low and responding is maladaptive.
A flying moth’s propensity to respond and moth size
To determine if larger flying moths responded more frequently than small- or medium-sized moths, we used a Χ2 analysis comparing response (yes or no) and moth size
(small, medium, or large). There was a significant result where large moths responded
less than expected (N = 732, df = 2, Pearson’s Χ2 = 25.8, p < 0.0001; Large: N = 156,
71.2% responded, Medium: N = 382, 89.0% responded, Small: N = 194, 81.4% responded). This could be because larger moths use other defenses to avoid bat predation.
The medium-sized moths responded the most and this could imply that they are under
greater predation pressure.
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A flying moth’s use of response types and moth size
In our study the most common response was change in direction, followed by dive,
then erratic, and finally spiral. The confidence intervals (CI) for probability of responses
did not overlap between any of the responses (Change, N = 283, prob. = .391, lower CI =
0.353, upper CI = 0.430; Dive: N = 188, prob. = 0.309, lower CI = 0.273, upper CI =
0.346; Erratic: N = 134, prob. = 0.220, lower CI = 0.189, upper CI = 0.255; Spiral: N =
49, prob. = 0.081, lower CI = 0.061, upper CI = 0.105).
To determine if the use of response type differed across size classes, we used a Χ2
analysis that included moth size (small, medium, or large) and response type (change,
dive, erratic, or spiral) and found that the use of the four categories of evasive behavior
did not differ significantly across size classes (N = 609, df = 6, Pearson’s Χ2 = 5.3, p =
0.5024; Large: change = 36.0%, dive = 28.8%, erratic = 27.0%, spiral = 8.1%; Medium:
change = 38.5%, dive = 32.7%, erratic = 19.7%, spiral = 9.1%; Small: change = 42.4%,
dive = 28.5%, erratic = 23.4%, spiral = 8.1%).
Although the use of response types was independent of moth size, we found that
moths use several different evasive maneuvers. This suggests that variability of response
may be important in avoiding bat predation.
Conclusion
We suggest that a moth’s behavioral response to the Dazer’s auditory stimulus is likely
due to evolved induced responses for detection of predatory bats. A moth responding to
a bat call in flight, or not responding while at rest, is an important distinction with consequences for fitness. We found that sympatric moths of various species and sizes exhibited several different behavioral responses to the auditory stimulus. While the propensity
to respond was a function of moth size, the use of each response type was independent of
moth size. The use of a given response is more likely dependent on the environment, the
moth’s activity state, and the intensity of the bat call than on the size of the moth. While
the neurological processes and behavioral responses of moth responses to bat ultrasound
are well documented (see Waters, 2003), moth behavior in nature may be more complex
in the field than in the laboratory. Future studies in natural settings that incorporate more
realistic acoustic stimuli, and considerations for environmental context, will be necessary to tease out the details of moth hearing-based defenses directed at bats.
Acknowledgments
This project was initiated during the 2003 Bat Predator-Prey Interaction Workshop held
at the Mitrani Department of Desert Ecology (MDDE). The workshop was supported by
the Blaustein Center for Scientific Cooperation and the Office of Donor and Associates
Affairs, Ben-Gurion University; The Department Evolution, Systematics and Ecology,
The Hebrew University of Jerusalem; and The Israel Society of Zoologists. We thank
B.P. Kotler, N. Kronfeld-Schor, and several reviewers for comments on this manuscript.
This is paper number 594 of the MDDE.
Vol. 53, 2007defensive responses of moths to an auditory stimulus
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