Download Sex-based predation on moths by insectivorous bats, Acharya, 1995

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BC/UIV.. 1995. 49, 1461-1468
Sex-biased predation on moths by insectivorous bats
Department
of Biology,
LALITA
ACHARYA
York University, 4700 Keele Street, North
(Received
jnal
York, Ontario
A43J IP3, Canada
20 January
1994: initiul acceptance
I9 April 1994;
ucceptance
I4 June 1994; MS. number:
~6905)
Two species of insectivorous bats, Lasiurus cinereus and L. borealis, ate significantly more
male than female moths in the wild. The observed bias was likely to be a consequence of sexual
dimorphism
in moth flight activity associated with sexual differences in mate acquiring mechanisms.
Female moths flew less than males and their activity peaks occurred at different times. The peak of male
activity coincided with a peak in bat activity in the middle of the night, while female activity peaked
earlier in the night when bat activity was relatively low. The results of this study are interpreted in a
sexual selection framework, and the conclusions about predation risk from bats that hunt airborne prey
are applicable to all nocturnally
flying insects that exhibit sexual dimorphism
in flight activity.
Abstract.
Inter-sexual differences in parental investment bias
the ratio of sexually receptive females to males and
generate competition
among members of the sex
investing less time and energy in offspring for
members of the sex investing more in offspring
(Trivers 1972). The sex that provides relatively
little parental investment (usually males), has a
much greater potential rate of reproduction
than
the other sex (Clutton-Brock
& Vincent 1991).
Because of this high reproductive potential, selection favours a tendency in males to exhibit traits
(for locating, attracting or competing for females)
that increase the probability of mating successfully
(Krebs & Davies 1993): these traits, however, may
also place males at a higher risk of predation than
females (Magnhagen
1991). It is often difficult to
observe predation in the wild, therefore relatively
few studies have directly demonstrated
higher
male mortality due to predation or parasitism (e.g.
Cade 1975; Burk 1982; Gwynne 1987; Sakaluk
1990; Rehfeldt 1992).
Moths use a pheromone-based
system for longdistance communication
between the sexes. In
most moth species, males follow pheromone
plumes emitted by a stationary female (Greenfield
1981). Females of most moth species can fly, but
flight is usually used for finding oviposition sites,
escaping from predators and, in some cases, for
finding food. Flight in females is sluggish and, in
many species, females do not fly until they have
mated and deposited some of their egg mass. In
some moth species, females are flightless (Sattler
1991).
0003-3472/95/061461+08
$08,00/O
Sexual dimorphism
in moth flight activity
should put males at a higher risk of predation
than the more sedentary females. Moths make up
a large proportion
of the diets of many species of
insectivorous bats (Whitaker 1988), and for some
bat species foraging in particular areas, moths are
the main food items (e.g. Acharya & Fenton
1992). For many adult moths, it is likely that
insectivorous
bats are their major nocturnal
predators. The importance of bats as predators
of moths is apparent in that many species of
moths possess echolocation
(bat) detecting ‘ears’
(Fullard 1987). In this paper, I present evidence
for male-biased predation on moths by insectivorous bats in the field that supports the hypothesis that searching for mates is a risky behaviour.
METHODS
The study was conducted at Pinery Provincial
Park
near Grand
Bend, Ontario,
Canada
(81.83”W, 43.25”N) in June, July and August of
1992 and 1993. The park is situated on the shore
of Lake Huron. The vegetation
is composed
mostly of oak (Quercus spp.) and plantation pine
(Pinus resinosa and P. strobus). At this site, bats
feed around street lights that illuminate
three
campground
entrances and the park’s main
entrance. These lights are the foci of bat and insect
activity (Hickey & Fenton 1990). Lusiurus cinereus
and L. borealis (Vespertilionidae)
are the two
most common bat species at these lights, although
c 1995 The Association
1461
for the Study
of Animal
Behaviour
.
1462
6”
Animal
Behaviour.
0
Figure 1. Schematic representation of sexual dimorphism
in wing coupling structures found in species of moths
examined in this study; f: frenulum, r: retinaculum.
Eptesicus fuscus and Myotis luc~jiigus also occasionally feed on insects at the lights. Lusiurus
cinereus and L. borealis attack moths that fly
around
the lights (Hickey & Fenton 1990;
Acharya & Fenton 1992) and the outcome of
their attacks is clearly visible with the aid of a
hand-held spotlight.
To determine the sex ratio of the moths eaten
by the bats (to test the null hypothesis that the
ratio did not deviate from unity), I examined
wings culled and dropped by foraging bats. Culled
wings fluttered towards the ground following a
successful attack, and were caught with a hand
net. I collected only wings that I could unambiguously assign to a single attack. In 1992 and 1993,
culled wings were examined from 33 nights (146 h)
and 19 nights (136.8 h) of observation, respectively. In 1992, wings were collected for only part
of the night (85 ~~~250.9 f 80.2 min from
sunset). In 1993, wings were collected from dusk
to dawn, weather permitting (T+ so=432.1 f
94.7min from sunset). The wings were identified
to family after Cove11 (1984) and the sex
recorded. In many moth families, specialized
structures hold the wings together in flight, and in
most species there is sexual dimorphism in these
structures (Eaton 1988; Scoble 1992). In males,
a spine, or frenulum, arising from the base of the
hind wing attaches to a hook or flap, the retinaculum, on the underside of the forewing (Fig. 1). In
females, the frenulum is usually composed of two
or more spines that arise from the hind wing base.
The retinaculum in females is a patch of stiff hairs
or scaleson the underside of the forewing (Fig. 1).
I included moths from the families Noctuidae,
Notodontidae, Arctiidae and Geometridae in the
49, 6
analysis because they were the most numerous
medium-sized moths flying around the lights.
Microlepidopterans were excluded because their
culled wings were often damaged, and could not
be accurately identified to sex. Culled wings from
the gypsy moth, Lymantria &spar (Lymantriidae),
were not included in the analysis because females
of this speciesare flightless.
To determine the overall sex ratio of the community of moths flying around the lights, I set a
light trap at a site a few hundred metres from
where the bats were foraging. The trap was set
once a week for 12 weeks (early June to late
August) in 1992 and 1993. In 1993, to examine
moth activity patterns across the night, I divided
the nightly trapping period into three intervals:
early, middle and late. The early period began at
the end of Civil Twilight (sun’s disk 12” below the
horizon) and ended 2 h later. The late period
included the 2 h before the beginning of Civil
Twilight. The middle period included the period
between the end of the early period and beginning
of the late period, and varied according to time of
season (range= 190-405 min). In 1992, traps were
set only for the early and middle parts of the
night. Moths caught in the trap were later identified to family and to sex. I calculated the ratio of
male to female moths caught by the trap over the
whole summer and determined whether the ratio
differed from 1:1. Similarly, I compared the trap
sex ratio with the sex ratio obtained from culled
wings. Additionally, I calculated the mean density
of moths per h for each sex during each period of
the night, and compared patterns of activity over
the night between the two sexes.
Concurrent with the insect sampling in 1993,
I measured activity of bats across the night (for
12 nights). Activity was monitored with two
bat detectors (Ultrasound Advice, London). One
detector was tuned to 20 kHz (the frequency
containing the most energy for L. cinereus) and
the second detector was tuned to 40 kHz (the
frequency containing the most energy for
L. borealis). Echolocation calls of the two species
are clearly distinguishable because of these frequency differences and differences in call length
(Fenton & Bell 1981). Echolocation calls were
monitored for one lo-min period at the beginning
of each hour. One listener counted passes(a train
of echolocation calls produced by an individual
bat) and feeding buzzes (a series of echolocation
calls produced at a rapid rate as a bat attacks a
Achurya:
Sex-biased predation
flying insect; Griffin 1958) for L. cinereus, and the
second listener did the same thing for L. borealis.
The same listener was always responsible for
monitoring the same species.I compared the mean
number of passesand buzzes per 10-min sampling
interval among periods of the night and between
species,and I compared patterns of activity (for
passesand buzzes) over the night between the two
species.
Sex ratios were compared using chi-squared
analyses on raw data. 1 used analysis of variance
(ANOVA) to compare mean moth density
between periods, and bat activity between periods.
Where the standard deviations were proportional
to the means, ANOVA was performed on logtransformed (log s+O.Ol) data to correct for
heteroscedasticity. Untransformed means are
reported. A rejection level of 0.05 was used in all
tests, and all tests were two-tailed. Statistical
Analysis Systems software (SAS 1985) was used
to perform the ANOVA.
loot
80
I
1463
1
(a)
149
60
40
2
5
‘t
z
20
0 i
-2
1 (b)
60
40
RESULTS
In 1992 and 1993, bats caught significantly more
male than female moths (1992: 4.7: 1, x2=75.63,
&‘=I. l-0.001;
1993: 5.8:1, x*=66.85, df= 1,
P<O.OOl; Fig. 2) and there was no significant
difference between the 2 years (x2=0.57, df=l,
DO.1). The data from the light trap showed a
similar significant bias towards the capture of
males (1992: 3.01:1, xZ= 133.75, df=l, ZQO.001;
1993: 3.04:1, x2=195.02, df=l, P<O.OOl;Fig. 2),
also with no significant difference between years
(x’=O.O148, df= 1, D-0.9). In 1992 and 1993, the
sex ratio was significantly more male-biased in the
culled wing data than in the trap data (1992:
x2=4.02, df=l, P<O.O5; 1993: x2=6.76, df=l,
BO.01; Fig. 2).
The sex ratio (calculated from trap data) was
significantly male-biased (PcO.005) on each night
in 1992 and 1993 (except for one night in 1992
when the sex ratio was not significantly different
from unity). There was significant heterogeneity in
the sex ratio between nights (1992: x*=42.71,
df= 11; 1993: x2=38.97, df= 11). In 1992 and 1993,
the ratio of males to females within each moth
family was significantly male-biased (P<O.O05for
all families; Fig. 3). The sex ratio of moths
trapped varied with moth family (1992: x2= 11.04,
df=3, P<O.OOl; 1993: x*=43.92, df=3, PcO.001).
20
0
Wings
Figure 2. Number
of male (0) and female (M) moths
(expressed
as percentage
of total moths)
caught
by
a light trap and by foraging
bats (15. cinereus
and
L. borealis)
in (a) 1992 and (b) 1993. Numbers
above
bars indicate sample sizes of moths or wings captured.
The small sample sizes for the wing data precluded analysing those data by family or night.
Bat activity, as measured by both passes and
buzzes, was significantly different across time
periods (passes: F,, , 9,,= 10.42, P<O.OOOl;buzzes:
F 2.,9,,=8.04, P<O.O005;Fig. 4), with significantly
higher activity (passesand buzzes) in the middle
period of the night than in the early and late
periods (Student-Neuman-Keuls test: PcO.05).
The early and late periods were not significantly
different. There were significant differences in
activity levels between the two bat species for
both passes (F,,,,,=964,
P<O.O02; L. borealis>
L. cinereus) and buzzes (F,,,,,=6.94,
P<O.Ol;
L. cinereus>L. borealis). There was no significant
interaction between bat speciesand period of the
night for either passes or buzzes suggesting that
1464
Animal
.
1001
80
Behaviour.
49, 6
(a)
-
II
57
98
60
-
42
60
1
Noctuidae
Geometridae
Arctiidae
Notodontidae
Moth family
Figure 3. Number of male (Cl) and female (W) moths
(expressed as percentage of total moths) from the
families Noctuidae, Geometridae, Arctiidae and Notodontidae caught by a light trap in (a) 1992 and (b) 1993.
Numbers above bars indicate sample sizes of moths
captured.
patterns of activity over the night were similar for
both L. cinereus and L. borealis.
In 1993, the ratio of males to females caught
in the trap within each time period was significantly male-biased (early: 1.6: 1, x2= 10.14, df= 1,
P<O.OOl;
middle:
4.03:1, x2= 170.88, df= 1,
WO.001; late: 3.06:1, x2=30.51, df=l, P<O.OOl).
A comparison of mean moth density (number of
moths/h) between periods of the night revealed a
significant interaction
between sex and period
(F,,,,=3.73, NO.03) suggesting that moth density
over the night differed between males and females.
An examination
of moth activity for each sex
separately revealed that male activity was signifi-
Early
Middle
Late
Time of night
Figure 4. Mean ( +SE) number of L. cinereus (Cl) and
L. bore& (W) passes (a) and buzzes (b) per IO-min
interval for early, middle and late periods of the night in
1993. Total number of IO-min sampling periods for each
species was 48 in the early and late periods and 100 in
the middle period. Activity was sampled 1 night a week
for 12 weeks from early June to late August 1993.
cantly higher in the middle of the night than in the
early and late periods
(F2.,,=4.19,
PcO.03;
Student-Neuman-Keuls
test: PcO.05; Fig. 5).
Female activity decreased over the night but there
were significant differences only between the early
and late periods (F,.,,=3.31,
PcO.01; StudentNeurnan-Keuls
test: PcO.05; Fig. 5). Similar
patterns were observed in 1992, although activity
was measured only in the early and middle periods
that year; males were significantly
more active
in the middle of the night than early in the
night (t=2.89, df=22, P<O.Ol), while females were
significantly more active early in the night than in
Acharya:
Sex-biased predation
10 ,
1
8t
Early
Middle
Time
Late
of night
Figure 5. Mean (+SE) number
of male (Cl) and female
(W) moths caught
per h by a light trap in the early,
middle and late periods
of the night in 1993. Trap was
set once a week for I2 weeks from early June to late
August
1993.
the middle of the night (t= - 1.94, df=22,
PCO.04).
Becausefemale Lymantria dispar (gypsy moths)
do not fly, this species was not included in the
above analyses. In 1992 and 1993, all of the
L. dispar caught in the light trap were male (N=58
and N=208, respectively). Similarly, all of the
L. dispar wings dropped by the bats in 1992 and
1993 were from male moths (N=7 and N=l9,
respectively).
DISCUSSION
Overall, bat captures of four families of macrolepidopteran moths were significantly malebiased, a pattern also observed in moths collected
in light traps. The sex ratio of each family of
moths caught in the trap was significantly male
biased, but there were significant differences
between families in the ratio of males to females.
Captures in light traps indicated significant differences in the times of peak activity between male
and female moths, with male activity peaking in
the middle of the night and female activity peaking earlier in the night. Bat activity was significantly higher in the middle part of the night than
in the early and late periods of the night.
Sexual dimorphism in the flight activity of
moths is the most likely explanation for the
1465
male-biased predation I documented. Females
may have been at a lower risk of bat predation
because they flew lessthan males and did most of
their flying at different times than males. Bat
activity appeared to coincide with overall moth
activity (which was dominated by male moth
activity). The peak in male moth flight activity
corresponded with the peak in bat activity in the
middle of the night. By not elevating their activity
during this time period, female moths reduced
their risk of predation. Bat activity around the
lights reflects the overall activity patterns of
L. cinereus and L. borealis in my study area.
Radio-tagged L. cinereus and L. borealis at Pinery
arrive at the lights within 30 min of becoming
active, and spend most of their nightly foraging
time within 500 m of the lights (Hickey & Fenton
1990; Hickey 1993). The greater male-bias seen in
the culled wing data than in the light trap data
could be another indication of sexual dimorphism
in moth flight activity; females attracted to street
lights may eventually stop flying and land close to
the lights, whereas males (because of their tendency to fly more) would continue to fly and have
a higher risk of being eaten by foraging bats.
Light trap data would not reflect this behaviour
because moths attracted to the light usually fall
into the trap and cannot escape.
Some species of moth may avoid foraging
bats by flying when bats are less active as has
been suggested for Malacosoma
americanum
(Lasiocampidae; Lewis et al. 1993). Bat activity
levels may also have influenced the phenology of
sound-producing arctiid moths (Fullard 1977).
Sexual dimorphism in moth flight times is supported by a laboratory study of daily flight times
of male and female moths (Edwards 1962);
females were most active between sunset and
midnight, males between midnight and sunrise.
Similar patterns have been witnessed in the field
(Williams 1935, 1939). Peaks in male activity
probably represent an active search for females
(Edwards 1962), while female activity peaks early
in the night may reflect females actively searching
for ‘calling’ sites.
The heterogeneity among moth families in the
sex ratio of moths captured in the trap could
indicate taxonomic variation in the relative
amounts of flying done by males and females.
Alternatively, the differences could reflect temporal variation (between nights) in the emergence
of males and females within a species. In many
1466
Animal
Behaviour,
.
insects (including Lepidoptera) males emerge
before females, a phenomenon termed protandry
(Wiklund & Fagerstrom 1977). The extremely
male-biased sex ratios seen in the trapped
Notodontidae and Arctiidae could have resulted
from the initial emergence (dominated by males)
of a single specieson one night.
It is unlikely that protandry could explain the
overall sex-biased predation I observed because
the culled wing data were collected on many
nights spread across the summers of 2 years.
Biased sex ratios following eclosion of both sexes
are unusual among Lepidoptera (Wagner &
Powell 1988), thus it is doubtful that the malebiased predation I witnessed was a reflection of
a male-biased sex ratio in the entire moth community at this site. Although there are cases in
which the population sex ratio of some moth
speciesis skewed, either towards males or females
(e.g. Wagner & Powell 1988) most studies show a
sex ratio close to unity (e.g. Dahlsten et al. 1992)
following eclosion of both sexes.
An alternative explanation for the sex-biased
predation on moths in my study is that relative to
female moths, males are more attracted to lights
as light traps sometimes catch relatively more
males than do other methods (e.g. Hamilton &
Steiner 1939; Weissling & Knight 1994). Hsiao
(1973) indicated that there is no difference
between the flight behaviour and paths of male
and female moths flying to lights. However, he did
not discuss whether there are inter-sexual differences in the likelihood of initiating phototactic
flight. A plausible explanation for the discrepancy
between trapping methods is that light traps exaggerate a naturally occurring sex-bias in flying
moths. Because of their attractive power over
relatively long distances (relative to passive traps),
light traps may be more likely to catch the already
volant and stronger flying individuals (i.e. males).
Even if lights do exaggerate a naturally occurring
sex-bias, this phenomenon is interesting because
street lights are a common feature of the urban
and rural landscape. Some bat speciesin all parts
of the world exploit the predictable insect concentrations around lights (e.g. Fullard 1989; Acharya
& Fenton 1992; Rydell 1992).
The preferential light attraction hypothesis,
however, does not explain male-biased predation on cockchafers, Melolontha
melolontha
(Coleoptera), by aerially hunting Rhinolophus
ferrumiquinum
(Chiroptera: Rhinolophidae; Jones
49, 6
1990). Like moths, cockchafers use pheromones
for intra-sexual communication. The males’
search for females appeared to place the male
cockchafers at a higher risk of bat predation than
the more sedentary females. The bats observed by
Jones (1990) foraged over dairy pasture and
woodland, areas relatively free of light pollution.
The most parsimonious explanation for the sexbiased predation observed is that it was a consequence of sexual dimorphism in flight activity.
Although female moths apparently have a
lower risk of predation than males do from
aerially hunting insectivorous bats, the females’
sedentary behaviour should make them more
vulnerable to bats that glean prey from surfaces.
Most gleaning bats use prey-generated cues to
locate their prey (e.g. Tuttle & Ryan 1981;
Marimuthu & Neuweiler 1987; Anderson & Racey
1993). One would predict that the sex ratio of
moths eaten by gleaning bats would be near unity,
or perhaps even female-biased if female moths are
more sedentary than males. There are no data
available on the sex ratio of moths eaten by
gleaning bats.
The flight dimorphism hypothesis predicts that
bats hunting airborne prey will take only males in
moth specieswhere females are flightless. My data
on Lymantria dispar, gypsy moths, support this
prediction. Females of this species possessfully
developed wings, but are practically flightless
(Sattler 1991). I did not observe female L. dispar
flying at Pinery, and the bats and light traps
caught only males. Furthermore, in 15. dispar there
is sexual dimorphism in hearing (Cardone &
Fullard 1988). Female L. dispar have significantly
less sensitive ears in the 20-50 kHz range (sympatric bats echolocate at these frequencies) than
do males. The females’ best frequencies are in the
‘non-bat’ range of IO-20 kHz.
Apart from L. dispar, I found no data on sexual
dimorphism in hearing in other speciesof moths.
In mantids (Dictyoptera), however, auditory
sexual dimorphism (females have reduced ultrasonic hearing) is common and closely tied to
dimorphism in wing length (Yager 1990).
Mantises with long (functional) wings have sensitive ultrasonic hearing while those with short
(non-functional) wings do not. Predator avoidance has been suggested as a major function of
hearing in many mantis species (Yager et al.
1990). If this hypothesis is true, then non-volant
mantises would not need bat-detecting ears.
Ackarya:
Sex-biased
For night-flying insects in general, I predict that
if there is sexual dimorphism
in flight activity,
then there will also be sexual dimorphism
in
predation
risk from aerially hunting bats, and
sexual dimorphism
in auditory
capability
(for
insects that hear ultrasound). Data from L. dispar
support all of these predictions; however, in this
species females do not fly. For species of moths
where females fly (but less than males), data on
possible sexual dimorphism in hearing are lacking.
For mantids, there are data on sexual dimorphism
in hearing, but none on predation
risk from
hunting bats. The results of this study provide
field evidence of sex-biased predation on moths,
and support the hypothesis that searching for
mates is a risky behaviour.
predation
V., Jr. 1984. A Field Guide to the Moths of
North
America.
Boston, Massachusetts:
Houghton Mifflin.
Dahlsten, D. L.. Rowney, D. L., Copper, W. A.
& Wenz, J. M. 1992. Comparison of artificial pupation shelters and other monitoring methods for
endemic populations of Douglas-fir tussock moth,
Grgyia
pseudorsugara
(McDunnough) (Lepidoptera:
Lymantriidae). Can. Enromol., 124, 359-369.
Eaton, J. L. 1988. Lepidopteran
Anatomy.
New York:
John Wiley.
Edwards, D. K. 1962. Laboratory determinations of the
daily flight times of separate sexes of some moths in
naturally changing light. Can. J. Zool., 40, 51 I-530.
Fenton, M. B. & Bell, G. P. 1981. Recognition of species
of insectivorous bats by their echolocation cells. J.
Cove&
C.
Eastern
Mammal.,
I thank Lella Dal Ferro, Sue Gallo and Shannon
Pennington
for help in the field, and the Ontario
Ministry of Natural Resources for permission to
conduct my research in Pinery Provincial Park. I
appreciate the assistance of Terry Crabe and the
rest of the park’s naturalists during my work at
Pinery. Thanks to Ted Burk, Brock Fenton, Brian
Hickey, Kim Hughes,
David Pearl and an
anonymous
referee for valuable comments on
early versions of the manuscript.
This research
was supported by a Natural Sciences and Engineering Research Council of Canada (NSERC)
research grant to M. B. Fenton and an NSERC
postgraduate scholarship to L.A.
REFERENCES
Acharya, L. & Fenton, M. B. 1992. Echolocation behaviour of vespertilionid (Lasiurus cinereus and Lasiurus
borealis)
attacking airborne targets including arctiid
moths. Cua. J. Zoo/., 70, 1292-1298.
Anderson, M. E. & Racey. P. A. 1993. Discrimination
between fluttering and non-fluttering moths by brown
long-eared bats, Plecorus auritus. Anim. Behav., 42,
489493.
Burk, T. 1982. Evolutionary significance of predation on
sexually signalling males. Fla Entomol., 65, 9%104.
Cade, W. H. 1975. Acoustically orienting parasitoids: fly
phonotaxis to cricket song. Science, 190, 13 12-l 3 13.
Cardone, B. & Fullard, J. H. 1988. Auditory characteristics and sexual dimorphism in the gypsy moth.
Ph)siol.
Emomol..
13, 9-14.
Clutton-Brock, T. H. & Vincent, A. C. J. 1991. Sexual
selection and the potential reproductive rates of males
and females. Nurure. Land, 351, 58-60.
62, 233-243.
Fullard, J. H. 1977. Phenology of sound-producing
arctiid moths and the activity of insectivorous bats.
Nature,
ACKNOWLEDGMENTS
1467
Lond.,
267, 4243.
Fullard, J. H. 1987. Sensory ecology and neuroethology
of moths and bats: interactions in a global perspective. In: Recent Advances in the Study of Bats (Ed. by
M. B. Fenton, P. Racey & J. M.-V.- Rayner), pp.
244-272. Cambridne: Cambridge Universitv Press.
Fullard, J. H. 1989.Echolocatioi
survey of-the distribution of the Hawaiian hoary bat (Lasiurus
cinereus
semorus) on the island of Kaua’i. J. Mammal.,
70,
424-426.
Greenfield, M. D. 1981. Moth sex pheromones: an
evolutionary perspective. Fla Entomol., 64,4-17.
Griffin, D. R. 1958. Listening in the Dark. New Haven:
Yale University Press.
Gwynne, D. T. 1987. Sex-biased predation and the risky
mate-locating behaviour of male tick-tack cicadas
(Homoptera: Cicadidae). Anim. Behav., 35, 571-576.
Hamilton, D. W. 8~ Steiner, L. F. 1939. Light traps and
codline. moth control. J. econ. Entomol.. 32. 867-872.
Hickey, M. B. C. 1993. The foraging and thkrmoregulatory behaviour of female hoary bats, Lasiurus
cinereus. Ph.D. thesis, Toronto, York University.
Hickey, M. B. C. & Fenton, M. B. 1990. Foraging by red
bats Lasiurus
borealis:
intraspecific chases do not
mean territoriality. Can. J. Zool., 68, 2477-2482.
Hsiao, H. S. 1973. Flight paths of night-flying moths to
lights. J. Insect Physiol., 19, 1971-1976.
Jones, G. 1990. Prey selection by the greater horseshoe
bat (Rhinolophus ferrumiquinum):
optimal foraging by
echolocation? J. Anim. Ecol., 59, 587-602.
Krebs, J. R. & Davies, N. B. 1993. An Introduction
IO Behavioural
Ecology.
3rd edn. Oxford: Blackwell
Scientific Publications.
Lewis, F. P., Fullard, J. H. & Merrill, S. B. 1993.
Auditory influences on the flight behaviour of moths
in a Nearctic site. II. Flight times, heights, and
erraticism. Can. J. Zool., 71, 1562-1568.
Magnhagen, C. 1991. Predation risk as a cost of reproduction. Trends Ecol. Evol., 6, 183-185.
Marimuthu, G. & Neuweiler, G. 1987. The use of
acoustical cues for prey detection by the Indian false
vampire bat, Meguderma
lyra J. camp. Physiol.,
160,
509-515.
1468
Animal
Behaviour,
Rehfeldt,
G. 1992. Impact
of predation
by spiders on
a territorial
damselfly
(Odonata:
Calopterygidae).
Oecologia
(Bert.),
89, 55C556.
Rydell,
J. 1992. Exploitation
of insects around
street
lamps by bats in Sweden. Funcr. Ecol., 6, 744-750.
Sakaluk,
S. K. 1990. Sexual selection
and predation:
balancing
reproductive
and survival
needs. In: Insect
Defenses
(Ed. by D. L. Evans & J. 0. Schmidt),
;;esp-90.
Albany:
State University
of New York
SAS. 1985. SAS User’s Guide: Statistics.
Version
5 edn.
Cary. North
Carolina:
SAS Institute.
Sattler,
K. 1991. A review
of wing
reduction
in
Lepidoptera.
Bull. Br. Mus. nat. Hisi. (Enromol.),
60,
243-288.
Scoble, M. J. 1992. The Lepidoptera.
New York: Oxford
University
Press.
Trivers,
R. 1972. Parental
investment
and sexual selection. In: Sesuul Selection
and the Descent
of Man:
1871-1971
(Ed.
by B. Campbell),
pp.
136179.
Chicago:
Aldine.
Tuttle, M. D. &Ryan,
M. J. 1981. Bat predation
and the
evolution
of frog vocalizations
in the neotropics.
Science. 214, 677678.
Wagner,
D. L. & Powell, J. A. 1988. A new Produxus
from
Yucca baccara:
first report
of a leaf-mining
prodoxine
(Lepidoptera:
Prodoxidae).
Ann. enromol.
Sot. Am., 81, 547-553.
49,
6
Weissling,
T. J. & Knight,
A. L. 1994. Passive trap for
monitoring
codling
moth (Lepidoptera:
Tortricidae)
flight activity.
J. econ. Entomol..
87. 103-107.
Whitaker,
J. O., Jr. 1988. Food
habits
analysis
of
insectivorous
bats.
In: Ecological
and Behavioral
Methods for the Study of Bats (Ed. by T. H. Kunz),
pp.
171-189.
Washington,
D.C.:
Smithsonian
Institution
Press.
Wiklund,
C. & Fagerstrom,
T. 1977. Why do males
emerge before females? A hypothesis
to explain
the
incidence
of protandry
in butterflies.
Oecologia
(Berl.),
31, 153-158.
Williams,
C. B. 1935. The times of activity
of certain
nocturnal
insects, chiefly
Lepidoptera,
as indicated
by a light-trap.
Trans. R. enromol.
Sot. Lo&,
83,
523-555.
Williams,
C. B. 1939. An analysis
of four years capture
of insects
in a light trap. I. General
survey;
sex
proportion
phenology;
and time of flight. Trans. R.
enromol. Ser. Land.. 89, 79-131.
Yager.
D. D. 1990. Sexual
dimorphism
of auditory function
and structure
in praying
mantises
(Mantodea;
Dictyoptera).
J. Zoo/., Lond., 221, 517537.
Yager,
D. D., May,
M. L. & Fenton,
M. B. 1990.
Ultrasound-triggered,
flight-gated
evasive maneuvers
in the praying mantis Parasphendale
agrionina.
J. exp.
Biol., 152, 17-39.