Behavioral Ecology Advance Access originally published online on June 16, 2004
Behavioral Ecology 2004 15(6):1016-1022; doi:10.1093/beheco/arh103
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Nocturnal anti-predator adaptations in eared and earless Nearctic Lepidoptera
Department of Biology, University of Toronto at Mississauga, 3359 Mississauga Rd., Mississauga, Ontario L5L 1C6, Canada
Address correspondence to J. Fullard. E-mail: jfullard{at}utm.utoronto.ca.
Received 28 July 2003; revised 1 March 2004; accepted 5 March 2004.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Nocturnal flight exposes insects to selection pressures that include reduced light and the hunting behavior of insectivorous bats. Using a phylogenetically based selection of wild moths collected from a Nearctic site, we report that earless species fly less throughout the night than eared species. This supports the hypothesis that this behavior has evolved as a passive defense against the transient attacks of aerially foraging bats in insects that do not possess long-range auditory detection abilities. We measured the eyesize of a selection of moths whose 24-h flight activities are known and confirm that nocturnal lifestyle results in larger eyes. With the exception of hawkmoths, there is no eyesize difference between eared and earless moths, suggesting that earless moths do not preferentially use vision to detect the approach of bats.
Key words: auditory state, bats, defense, eyesize, flight, moths.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Animals are active at various times of the 24-h day (diel periodicity) and experience different selection pressures arising from the predators they encounter during those times. Insects, with their diversity of lifestyles and short generation times, can be used to study the effects of diel selection pressures on the evolution of defenses (Joron and Mallet, 1998
; Roeder, 1952). The Lepidoptera (moths and butterflies) is a speciose taxon exhibiting a wide variety of lifestyles and diel periodicities (Dreisig, 1986) and is well suited for these studies. Diurnal predators of Lepidoptera have selected for many well-studied, visually governed primary and secondary defenses (i.e., those that function before and after the predator has discovered them [Edmunds, 1974; Endler, 1991]), such as crypsis (Majerus et al., 2000; Sargent, 1969) and startle behavior (Ford, 1976; Sargent, 1990; Schlenoff, 1985).
Being active at night exposes insects to predators that rely more on hearing and smell to detect their intended prey, and some of the most studied of these are insectivorous bats, ecologically diverse mammals that inhabit almost every terrestrial habitat on the planet (Kunz and Fenton, 2003; Nowak, 1994). Aerially foraging (AF) bats prey on flying insects by locating them using ultrasonic echolocation calls, and as a primary defense many insects have evolved ultrasonically sensitive ears to detect these calls (for reviews see Fullard, 1998; Jones and Rydell, 2003; Miller and Surlykke, 2001). Less understood, however, are the defenses used by earless insects to reduce the predation potential of AF bats. Since the rapid flight of AF bats renders them transient predators whose threat is temporary, earless insects can lessen the chance of being detected by modifying their own flight patterns. Roeder (1974) hypothesized that earless moths could protect themselves by flying erratically or in areas where bats do not normally hunt (e.g., close to the ground), ideas that have been supported by studies on moths (Andersson et al., 1998; Lewis et al., 1993; Rydell, 1998) and water striders (Svensson et al., 2002). Morrill and Fullard (1992) proposed that earless moths protect themselves by being less likely to fly than eared moths, and Yack (1988) tested the hypothesis that seasonal isolation provides a defense by demonstrating the greater tendency of earless Nearctic moths to fly in the early summer, before bats have returned from their overwintering sites.
Another source of potential nocturnal predation pressure arises from substrate-gleaning (SG) bats (or AF bats who switch to this strategy), which hunt by flying close to the ground or vegetation while listening for prey-generated sounds (Faure and Barclay, 1994; Ratcliffe and Dawson, 2003). The characteristics of the echolocation calls of these bats render them acoustically inconspicuous to the eared defenses of their prey (Faure et al., 1993; but see Greenfield and Baker, 2003). As a primary defense against SG bats, ultrasound-deaf, Neotropical frogs (Physalaemus pustulosus) watch for foraging SG bats and cease calling when they are present (Tuttle et al., 1982). It is possible, therefore, that moths could use vision to detect bats, in which case we would expect that earless species would rely more heavily on this defense than eared species. In general, the evolutionary effect of nocturnality on eyes has not been phylogenetically tested. Studies suggest that nocturnally active insects have larger eyes (Caveney and McIntyre, 1981; Maschwitz and Hanel, 1988; McIntyre and Caveney, 1998), and this character is used as an indicator of diel periodicity nocturnality (e.g., Miller, 1991), but none have tested whether there is a relationship between the time spent active at night and eyesize using a phylogenetically diverse selection of insects.
The purpose of this paper is to examine the behavioral and morphological adaptations that facilitate a nocturnal lifestyle in a community of Nearctic moths, with particular attention to the predation pressure of insectivorous bats. Two recent improvements in our understanding of the basic biology of the Lepidoptera allow for such a study. The first is a phylogeny of the Lepidoptera resolved to the superfamily level (Kristensen and Skalski, 1999) and the second is a survey of Nearctic Lepidoptera using this phylogeny (Fullard and Napoleone, 2001), which quantified the different levels of nocturnality in these insects by using the 24-h timing of their flight patterns. In our current study we measure the total amount of nocturnal flight in a phylogenetically diverse selection of these moths to test the following predictions: (1) earless moths exhibit less total nocturnal flight than eared species to avoid detection by AF bats, (2) nocturnal flight activity has resulted in larger eyes in the Lepidoptera, and (3) earless moths possess larger eyes than eared species as a primary defense against the attacks of bats.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Flight
Animals
We conducted this study from 5 June to 12 August 2001 at the Queen's University Biological Station (QUBS), Chaffey's Lock, Ontario, Canada (44°34' N, 79°15' W). Nocturnal moths were collected at ultraviolet light traps and sugared trees (Holland, 1968
) and diurnal moths were captured with handnets; all were identified according to Covell (1984), Handfield (1999), Riotte (1992), and Ward et al. (1974). We captured only individuals that were in good condition (e.g., no wing wear) and excluded females from the study to eliminate pheromone interactions and because in some species females fly less than males or not at all (Sattler, 1991) and may not be subject to the same predation influences as males (Acharya and McNeil, 1998).
Auditory state was based on known presence or absence of ears or on family affiliation (e.g., all Noctuidae were considered eared [Roeder, 1974; Scoble, 1992]). We considered all of the hawkmoths (Sphingidae) to be earless, as the only known eared species in this family (Göpfert et al., 2002; Roeder et al., 1968) do not exist locally. Microlepidopteran families other than pyralids were excluded due to the inability to resolve extremely small moths on video. In the absence of a species-level lepidopteran phylogeny (Kristensen and Skalski, 1999), we used families as the finest unit of resolution. We recognize that this may pseudoreplicate families if they are later found to be closely related, and we have attempted to limit this effect by sampling all of the superfamilies that were available to us at our study site.
Flight recordings
All moths were tested in a cage made of wooden doweling, measuring 1.8 m long, 1.2 m high, and 0.6 m deep, divided into two side-by-side chambers by an opaque wooden wall. The bottom of the room was open and placed over grass and short undergrowth. All other walls were covered with white acrylic mesh, with a resealable opening at the end of each chamber to permit access to moths. The flight room was contained within a plastic screened tent (4x4x2.1 m) with mesh walls, keeping the area dry but preserving ambient temperatures. The setup was located in a small forest clearing so as to reduce wind disturbance. Cage size does not appear to compromise moth flight, as flight times were similar between our study and those reported by Fullard and Napoleone (2001), who used smaller cages (other justifications for the use of cages in measuring flight are discussed in Fullard and Napoleone [2001]). Naturally hunting bats are not common in the enclosed forest location of the cage (Fenton, 1970), and the site would have exposed all moths to the same probability of occasional external influence.
Approximately one hour before dusk (daily times obtained from tables published by the Herzberg Institute of Astrophysics, National Research Council of Canada; http://hia-iha.nrc-cnrc.gc.ca/main_e.html), we placed one moth into each chamber. The flight room was illuminated (Extreme CCTV Surveillance Systems, model EX12LED) at wavelengths of 850 or 940 nm, to which Lepidoptera are insensitive (Horridge, 1977), and flight was video-recorded until one hour after dawn using a Sanyo CB-3574IR camera. Flight time was measured as the number of seconds each moth moved at least one body length while flapping wings during a 10-min period. The data from moths that moved for less than five mins during a nightly trial or had died during the trial were excluded. As we were only interested in bat-influenced flight patterns, flight times were analyzed from the end of twilight to 40 min past sunrise, encompassing the nightly flight period of the most common sympatric bat in the area, Myotis lucifugus (Fullard and Napoleone, 2001).
Statistical analyses
To control for the different sizes of moths in our study we first determined that flight time and wingspan were not correlated (Pearson r = –.17, p =.19, n = 60). We then excluded wingspan from subsequent two-factor nested general linear model (GLM) ANOVAs to compare the nocturnal flight times of eared versus earless moths. The five replicated flight times for each species were nested within auditory state (eared or earless). We were interested in comparing species within each auditory state (e.g., multiple comparisons of only earless species), but since no method exists for performing multiple comparisons within specific levels of a nested effect, ANOVAs were performed on each auditory level individually. All statistical analyses were performed using SAS v. 6.12 (licensed to the University of Toronto).
Eyesize
Animals and measurements
Male moths (other than those used for the flight trials) were collected as described above and immediately frozen. Upon thawing, the head and left metathoracic femur of each moth were removed and dried. Field-collected samples were supplemented with specimens from QUBS and the Canadian National Collection of Insects, Arachnids and Nematodes (Ottawa). We measured the estimated eye surface area (EESA) of five individuals from each species as described for butterflies by Rutowski (2000). For the left eye of each specimen, five lengths were measured under a dissecting microscope: eye height, eye span, and three eye radii. In accordance with Rutowski (2000) we used femur lengths as indicators of body size for control purposes in subsequent analyses. We measured only those species for which Fullard and Napoleone (2001) had determined 24-h flight periodicities and ranked them according to their study's categories: (1) exclusively diurnal (0–10% nocturnal flight); (2) mixed, primarily diurnal (10–50% nocturnal flight); (3) mixed, primarily nocturnal (50–90% nocturnal flight); and (4) exclusively nocturnal (90–100% nocturnal flight).
Flight activity was analyzed for five replicates of every species. Within the primarily diurnal category, the number of eared and earless species tested was limited by the availability of species at our study site, and we were able to analyze only two earless and three eared species within this category. Species from the same family within the same nocturnality category were combined, making the analysis more conservative. The effect of family was also included in the analysis since families were repeated over different nocturnality classes within an auditory condition.
Statistical analyses
We performed GLM ANOVAs on eyesize with four levels: femur length, auditory condition, nocturnality category, and family, nested within a combination of auditory category and nocturnality category. When we added the two species of exclusively diurnal moths to the data set, we performed an independent ANOVA, removing auditory state as a variable as there are no confirmed exclusively diurnal earless moths available locally to statistically balance the analysis. Butterflies (Papilionoidea) and skippers (Hesperioidea) are both exclusively diurnal superfamilies at our study site (Fullard and Napoleone, 2001) and were excluded from these analyses because we were interested in examining the eyesizes of only those Lepidoptera that exhibit different degrees of nocturnality. All multiple comparisons in this study were performed using Tukey-Kramer tests on least-squares means (LS-means), as the nested effect was unbalanced, and we were interested in multiple comparisons within this effect. Because the data were unbalanced, only F and p values from the Type III sums of squares and LS-means are reported, as these values are adjusted for all variables and are independent of the number of values for each cell of the analysis (Searle et al., 1980). LS-means also permitted multiple comparisons within the unbalanced and nested levels.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Flight
We measured the total nocturnal flight time of 60 individual male moths representing seven species of eared moths and five species of earless moths (Figure 1, Table 1). There were significant differences in total nocturnal flight times among all of the species used in the trials (F10, 58 = 3.52, p =.0015), and eared moths flew for significantly longer times than earless moths (means (s) ± SE: eared = 89.4 ± 23.8; earless = 34.8 ± 8.7; F1, 58 = 20.09, p =.0001).
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Eyesize
We calculated the EESAs of 135 moths of all diel categories, representing 27 species from 14 families (Table 2). As expected from Rutowski (2000)
, femur length as an indicator of body size was positively correlated to EESA (F1,109 = 25.72, p =.0001; Pearson post hoc r =.75, p =.0001; Figure 2). Body size was therefore controlled for throughout the subsequent analyses. While Figure 2 illustrates the individual moth values to demonstrate data variability, statistical analyses were performed with untransformed species means after data were determined to be normally distributed (box plots; Minitab v. 13.0).
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Effect of nocturnality
When examining all moths (n = 125) exhibiting any nocturnal flight (categories 2, 3, and 4), their EESAs were significantly different (F2, 101 = 77.47, p =.0001; Figure 3A), with larger eyes associated with increased nocturnality. Box plots and multiple comparison results within families suggested that the large EESAs of sphingid moths were outliers. When we reran the ANOVAs after excluding sphingids (n = 115), we found that the overall effects of nocturnality on EESA remained significant (F2, 91 = 19.47, p =.0001; Figure 4A) but the differences between categories 2 and 3 became insignificant (post hoc Tukey-Kramer, p = 0.06).
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We examined the relationship between 24-h activity and eyesize including the data from the two species of exclusively diurnal moths, with and without sphingids. In both cases, exclusively diurnal moths had the smallest eyes of all other diel categories (post hoc Tukey-Kramer, p =.0001; Figure 3B).
Effect of ears
Initially, we found that for species exhibiting any night-flight (categories 2, 3, and 4), earless moths had significantly greater EESAs than eared moths (F1, 101 = 94.0, p =.0001; Figure 4). In keeping with the possible outlier status for sphingid eyes (see above), we reanalyzed the data excluding these moths and then found no significant EESA difference between eared and earless moths (F1, 91 = 1.83, p =.18).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Our study represents the first comparative examination of proposed nocturnal adaptations in moths that is based on a phylogenetically diverse selection of species and therefore allows for a quantitative analysis of the evolution of these defenses. We caution that our findings are based on a single community of Nearctic moths and that other lepidopteran defenses exist that we were not able to include in our comparisons (e.g., ears in Neotropical nocturnal butterflies [Yack and Fullard, 2000
]).
Flight
Our finding that earless moths fly less during the night than eared moths quantitatively supports Morrill and Fullard's (1992) hypothesis that reduced flight evolved as a passive primary defense in earless moths. We suggest that eared moths actively assess levels of local predation risk (e.g., bats vs. no bats) by listening for echolocation calls and make behavioral decisions (i.e., fly vs. don't fly) that allow them to maximize their nocturnal flight time. Earless moths, without early-warning sensory defenses, are therefore constrained to passive anti-bat flight adaptations such as reduced nightly flight (Morrill and Fullard, 1992). Reduced flight provides two anti-bat defenses, depending on the type of bat being avoided. First, stationary moths are physically and perceptually isolated from AF bats since these bats typically avoid closed zones where collisions pose a threat and acoustic clutter renders echoes less reliable (Fenton, 1990; Schnitzler and Kalko, 2001). Second, for SG bats that cannot detect silent prey, motionless moths are acoustically cryptic (Arlettaz et al., 2001). Counteracting this defense, however, is the case of moths that warm up by wing-fanning before flying (Heinrich and Bartholomew, 1971), since the noise that results from this activity will expose them to SG bats (Faure and Barclay, 1992; Ratcliffe and Dawson, 2003).
If reduced flight is adaptive as an anti-bat defense, the question arises as to how this strategy can be tolerated in short-lived animals that depend on flight for mating and egg-laying opportunities. As compensation for their reduced nightly flight time, earless moths may avoid bats by using short bouts of fast and erratic flight (Roeder, 1974; Roeder and Treat, 1962). We suggest that earless nocturnal moths have longer lifespans or possess mate-searching sensory strategies that require less continual flight, such as increased pheromonal sensitivity in males that allows for more efficient localization of females. Body size is positively correlated with antennal size in some insects (e.g., carabid beetles [Bauer and Kredler, 1993]), and considering that large antennae increase pheromonal uptake in silkworm moths (Kaisslin and Priesner, 1970), the large size and antennae of earless moths may reflect a greater use of pheromones in their mating behavior.
Eyesize
Nocturnality and eyesize
Our findings support the generally held but untested belief that nocturnal insects have larger eyes, and we have shown that this adaptation exists in a graded fashion, that is, the more nocturnal the insect, the larger the eye. As discussed in Land and Nilsson (2002), visual quality (i.e., sensitivity, resolution, and size of visual field) will increase with greater eyesize and number of ommatidia (the basic visual unit of a compound eye). While we cannot conclude which of these qualities are optimized in moths with larger eyes, we conclude that increased eyesize is a nocturnal adaptation that increases visual quality in dim-light conditions.
Auditory state and eyesize
We initially predicted that if earless moths use vision to detect bats, to compensate for their auditory deficiency, their eyes would be larger than those of eared moths. After removing the large eyes of sphingids from our data we found no difference, implying that this defense, if it exists, has not been favored by earless moths. Because eyesize is positively related with moth size and degree of nocturnality, it is possible that all large moths use vision to detect approaching bats. In noctuid (eared) moths, larger species possess greater auditory sensitivities, an adaptation proposed by Surlykke et al. (1999) to be a compensation for the stronger echoes their bodies provide to searching bats (Norman and Jones, 2000), and we suggest that any large moth would benefit from being able to see the approach of distant bats before they were detected.
Our finding that sphingid moths have significantly larger eyes than other moths raises the question of whether these moths alone have evolved this adaptation in response to bats. Sphingids frequently supplement their energy needs with flower nectar (O'Brien, 1999) that they consume while hovering (Wicklein and Strausfeld, 2000). Certain sphingids purportedly use ears at this time to detect the attacks of bats (Roeder et al., 1968), so it is possible that earless sphingids use their large eyes to see bats. Alternatively, large eyes may perform nocturnal functions unrelated to interactions with bats. Sphingids are active fliers and are presently the only animal known that use color vision at nocturnal illumination levels (Kelber et al., 2002), traits that might require large eyes. Most studies of moth vision have used sphingids (e.g., Bennett, 1997; Brantjes and Boss, 1980; Cutler et al., 1995; Kelber et al., 2002; Milde, 1993; Raguso and Willis, 2002; White et al., 1983) and, considering the unusual anatomy of the eyes of these moths, we caution that the findings of these studies should not be applied to other moths until phylogenetically-based comparative visual studies are done on a diversity of moths.
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ACKNOWLEDGEMENTS |
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We thank Raleigh Robertson, Frank Phelan, and Floyd Connor of Queen's University for permission to use their facilities and Cassandra Guignion, Kit Muma, John Ratcliffe, and Christine Belanger for their assistance in the field and in the lab. We also thank Jerry Brunner for his statistical help. This study was funded by a research grant from the Natural Sciences and Engineering Research Council of Canada (to J.H.F.).
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REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Acharya L, McNeil JN, 1998. Predation risk and mating behavior: the responses of moths to bat-like ultrasound. Behav Ecol 9:552-558.
Andersson S, Rydell J, Svensson MGE, 1998. Light, predation and the lekking behaviour of the ghost swift Hepialus humuli (L.) (Lepidoptera: Hepialidae). Proc R Soc Lond B 265:1345-1351.
Arlettaz R, Jones G, Racey PA, 2001. Effect of acoustic clutter on prey detection by bats. Nature 414:742-745.[CrossRef][Medline]
Bauer T, Kredler M, 1993. Morphology of the compound eyes as an indicator of life-style in carabid beetles. Can J Zool 71:799-810.
Bennett RR, White RH, Meadows J, 1997. Regional specialization in the eye of the sphingid moth Manduca sexta: Blue sensitivity of the ventral retina. Vis Neurosci 14:523-526.[Web of Science][Medline]
Brantjes NBM, Boss JJ, 1980. Hawkmoth behavior and flower adaptation reducing self-pollination in two Liliflorae. New Phytol 84:139-143.[CrossRef][Web of Science]
Caveney S, McIntyre P, 1981. Design of graded-index lenses in the superposition eyes of scarab beetles. Phil Trans R Soc London B 294:589-632.
Covell CV, Jr, 1984. A field guide to the moths of Eastern North America. Boston: Houghton Mifflin Co.
Cutler DE, Bennett RR, Stevenson RD, White RH, 1995. Feeding-behavior in the nocturnal moth Manduca sexta is mediated mainly by blue receptors, but where are they located in the retina? J Exp Biol 198:1909-1917.
Dreisig H, 1986. Timing of daily activities in adult Lepidoptera. Ento Gener 12:25-43.
Edmunds M, 1974. Defence in animals. New York: Longman Group Ltd.
Endler JA, 1991. Interactions between predators and prey. In: Behavioural ecology: an evolutionary approach (Krebs JR, Davies NB, eds). Boston: Blackwell Scientific Publications; 169–196.
Faure PA, Barclay RMR, 1992. The sensory basis of prey detection by the long-eared bat, Myotis evotis, and the consequences for prey selection. Anim Behav 44:31-39.
Faure PA, Barclay RMR, 1994. Substrate-gleaning versus aerial-hawking—plasticity in the foraging and echolocation behavior of the long-eared bat, Myotis evotis. J Comp Physiol A 174:651-660.[Medline]
Faure PA, Fullard JH, Dawson JW, 1993. The gleaning attacks of the northern long-eared bat, Myotis septentrionalis, are relatively inaudible to moths. J Exp Biol 178:173-189.[Abstract]
Fenton MB, 1970. A technique for monitoring bat activity with results obtained from different environments in southern Ontario. Can J Zool 48:847-851.[CrossRef]
Fenton MB, 1990. The foraging behaviour and ecology of animal-eating bats. Can J Zool 68:411-422.[CrossRef]
Ford EB, 1976. Moths. London: Collins.
Fullard JH, 1998. The sensory coevolution of moths and bats. In: Comparative hearing: insects (Hoy RR, Popper AN, Fay RR, eds). New York: Springer-Verlag; 279–326.
Fullard JH, Napoleone N, 2001. Diel flight periodicity and the evolution of auditory defences in the Macrolepidoptera. Anim Behav 62:349-368.[CrossRef]
Göpfert MC, Surlykke A, Wasserthal LT, 2002. Tympanal and atympanal ‘mouth-ears’ in hawkmoths (Sphingidae). Proc R Soc Lond B 269:89-95.[Medline]
Greenfield MD, Baker M, 2003. Bat avoidance in non-aerial insects: the silence response of signaling males in an acoustic moth. Ethology 109:427-442.[CrossRef][Web of Science]
Handfield L, 1999. Le guide des papillons du Québec. Boucherville: Broquet.
Heinrich B, Bartholomew GA, 1971. An analysis of pre-flight warm-up in the sphinx moth, Manduca sexta. J Exp Biol 55:223-239.
Holland WJ, 1968. The moth book: a guide to the moths of North America. New York: Dover Publications, Inc.
Horridge GA, 1977. Compound eye of insects. Sci Am 237:108-118.[Web of Science][Medline]
Jones G, Rydell J, 2003. Attack and defense: interactions between echolocating bats and their insect prey. In: Bat ecology (Kunz TH, Fenton MB, eds). Chicago: University of Chicago Press; 301–345.
Joron M, Mallet JLB, 1998. Diversity in mimicry: paradox or paradigm? Trends Ecol Evol 13:461-466.[CrossRef]
Kaisslin KE, Priesner E, 1970. Olfactory threshold of silk moths. Naturwissenschaften 57:23-28.[CrossRef][Web of Science][Medline]
Kelber A, 2002. Pattern discrimination in a hawkmoth: innate preferences, learning performance and ecology. Proc R Soc Lond B 269:2573-2577.[Medline]
Kelber A, Balkenius A, Warrant EJ, 2002. Scotopic colour vision in nocturnal hawkmoths. Nature 419:922-925.[CrossRef][Medline]
Kristensen NP, Skalski AW, 1999. Phylogeny and palaeontology. In: Lepidoptera, moths and butterflies (Kristensen NP, ed). Berlin: Walter de Gruyter; 7–25.
Kunz TH, Fenton MB, 2003. Bat ecology. Chicago: University of Chicago Press.
Land MF, Nilsson DE, 2002. Animal eyes. New York: Oxford University Press.
Lewis FP, Fullard JH, Morrill SB, 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.
Majerus MEN, Brunton CFA, Stalker J, 2000. A bird's eye view of the peppered moth. J Evol Biol 13:155-159.[CrossRef][Web of Science]
Maschwitz U, Hanel H, 1988. Biology and the southeast asian nocturnal wasp, Provespa anomala (Hymenoptera, Vespidae). Entomol Gen 14:47-52.
McIntyre P, Caveney S, 1998. Superposition optics and the time of flight in onitine dung beetles. J Comp Physiol A 183:45-60.[CrossRef]
Milde JJ, 1993. Tangential medulla neurons in the moth Manduca sexta—structure and responses to optomotor stimuli. J Comp Physiol A 173:783-799.[CrossRef]
Miller JS, 1991. Cladistics and classification of the Notodontidae (Lepidoptera: Noctuoidea) based on larval and adult morphology. Bull Am Mus Nat Hist 204:1-230.
Miller LA, Surlykke A, 2001. How some insects detect and avoid being eaten by bats: tactics and countertactics of prey and predator. Bioscience 51:570-581.[CrossRef][Web of Science]
Morrill SB, Fullard JH, 1992. Auditory influences on the flight behavior of moths in a Nearctic site. 1. Flight tendency. Can J Zool 70:1097-1101.[CrossRef][Web of Science]
Norman AP, Jones G, 2000. Size, peripheral auditory tuning and target strength in noctuid moths. Physiol Entomol 25:346-353.[CrossRef]
Nowak RM, 1994. Walker's bats of the world. Baltimore, MD: Johns Hopkins University Press.
O'Brien DM, 1999. Fuel use in flight and its dependence on nectar feeding in the hawkmoth Amphion floridensis. J Exp Biol 202:441-451.[Abstract]
Raguso RA, Willis MA, 2002. Synergy between visual and olfactory cues in nectar feeding by naive hawkmoths, Manduca sexta. Anim Behav 64:685-695.[CrossRef]
Ratcliffe JM, Dawson JW, 2003. Behavioural flexibility: the little brown bat, Myotis lucifugus and he northern long-eared bat, M. septentrionalis, both glean and hawk prey. Anim Behav 66:847-856.[CrossRef]
Riotte JCE, 1992. Annotated list of Ontario Lepidoptera. Royal Ontario Museum, Life Sciences Miscellaneous Publication.
Roeder KD, 1952. Insects as experimental material. Science 115:275-280.
Roeder KD, 1974. Acoustic sensory responses and possible bat-evasion tactics of certain moths. In: Proceedings of the Canadian Society of Zoologists Annual Meeting (June 2–5) (Burt MDB, ed). Frederick: University New Brunswick Press; 71–78.
Roeder KD, Treat AE, 1962. The acoustic detection of bats by moths. In: Proceedings of the XI International Congress of Entomology, Vienna, Austria, 1960 (Strouhal H, Beier M, eds). Vienna, Austria: Naturhistorisches Museum; 7–11.
Roeder KD, Treat AE, Vandeberg JS, 1968. Auditory sense in certain sphingid moths. Science 159:331-333.
Rutowski RL, 2000. Variation of eye size in butterflies: inter- and intraspecific patterns. J Zool 252:187-195.[CrossRef]
Rydell J, 1998. Bat defense in lekking ghost swifts (Hepialus humuli), a moth without ultrasonic hearing. Proc R Soc Lond B 265:1373-1376.[Medline]
Sargent TD, 1969. Behavioral adaptations of cryptic moths. 2. Experimental studies on bark-like species. J NY Entomol Soc 77:75-79.
Sargent TD, 1990. Startle as an anti-predator mechanism, with special reference to the underwing moths, (Catocala). In: Insect defenses: adaptive mechanisms and strategies of prey and predators (Evans DL, Schmidt JO, eds). Albany, NY: State University of New York Press; 229–249.
Sattler K, 1991. A review of wing reduction in Lepidoptera. Bull Br Mus Nat Hist (Entomol) 60:243-288.
Schlenoff DH, 1985. The startle responses of blue jays to Catocala (Lepdioptera, Noctuidae) prey models. Anim Behav 33:1057-1067.[CrossRef]
Schnitzler HU, Kalko EKV, 2001. Echolocation by insect-eating bats. Bioscience 51:557-569.[CrossRef][Web of Science]
Scoble MJ, 1992. The Lepidoptera: form, function and diversity. New York: Oxford University Press.
Searle SR, Speed FM, Milliken GA, 1980. Population marginal means in the linear-model—an alternative to least-squares means. Am Stat 34:216-221.[CrossRef][Web of Science]
Surlykke A, Filskov M, Fullard JH, Forrest E, 1999. Auditory relationships to size in noctuid moths: bigger is better. Naturwissenschaften 86:238-241.[CrossRef][Web of Science]
Svensson AM, Danielsson I, Rydell J, 2002. Avoidance of bats by water striders (Aquarius najas, Hemiptera). Hydrobio 489:83-90.[CrossRef]
Tuttle MD, Taft LK, Ryan MJ, 1982. Evasive behavior of a frog in response to bat predation. Anim Behav 30:393-397.[CrossRef]
Ward PS, Harmsen R, Hebert PDN, 1974. The Macroheterocera of south-eastern Ontario. J Res Lepidoptera 13:23-42.
White RH, Banister MJ, Bennett RR, 1983. Spectral sensitivity of screening pigment migration in the compound eye of Manduca sexta. J Comp Physiol 153:59-66.[CrossRef]
Wicklein M, Strausfeld NJ, 2000. Organization and significance of neurons that detect change of visual depth in the hawk moth Manduca sexta. J Comp Neurol 424:356-376.[CrossRef][Web of Science][Medline]
Yack JE, 1988. Seasonal partitioning of atympanate moths in relation to bat activity. Can J Zool 66:753-755.[CrossRef][Web of Science]
Yack JE, Fullard JH, 2000. Ultrasonic hearing in nocturnal butterflies. Nature 403:265-266.[CrossRef][Medline]
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