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Diel Flight Periodicity and the Evolution of Auditory Defences in the Macrolepidoptera

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Diel Flight Periodicity and the Evolution of Auditory Defences in the Macrolepidoptera ANIMAL BEHAVIOUR, 2001, 62, 349–368 doi:10.1006/anbe.2001.1753, available online at http://www.idealibrary.com on Diel flight periodicity and the evolution of auditory defences in the Macrolepidoptera JAMES H. FULLARD & NADIA NAPOLEONE Department of Zoology, Erindale College, University of Toronto (Received 18 February 2000; initial acceptance 3 May 2000; final acceptance 24 January 2001; MS. number: A8729R) We measured the 24-h flight activity patterns of 84 species of Nearctic Lepidoptera representing 12 ultrasound-earless and seven ultrasound-eared families to examine the evolution of the diel flight periodicities (DFPs) and auditory defences of these insects. Most species tested showed mixed DFPs (flight during day and night hours) with few being exclusively nocturnal. With the exception of one geometrid moth and one arctiid moth, only the butterflies (Papilionoidea+Hesperioidea) were exclusively diurnal, supporting the hypothesis that this trait has resulted from their lack of ultrasound-sensitive ears, structures that in most other Macrolepidoptera provide auditory defence against aerially foraging, insectivorous bats. Eared species showed the highest tendency to fly during both day and night, a trait we suggest results from their possession of both visual and auditory defences. Earless moths were almost exclusively nocturnal and may be constrained to the night because of their size and tendency for ground-hugging flight, which may provide protection against bats, but would be liabilities against diurnal, visually hunting predators. Ultrasound sensitivity not only appears to protect eared moths from aerial predators (bats) but also protects them from terrestrial predators by allowing the moths to remain in the air during the night, and, we suggest, is responsible for the success of this group of Macrolepidoptera. 2001 The Association for the Study of Animal Behaviour Diel periodicity, the patterning of 24-h activity, is a studies focus upon the activities of species (usually fundamental characteristic of insect biology that has economically important ones) during only the day attracted research at both proximate (e.g. physiological) (photophase) or night (scotophase) portions of their diel and ultimate (e.g. evolutionary) levels (for reviews see cycle, with the result that many taxa have been labelled Dreisig 1986; McNeil 1991). While ‘activity’ includes ‘diurnal’ or ‘nocturnal’ without knowledge of their com- relatively inconspicuous behaviours such as feeding or plete 24-h activity patterns (Ehnbom 1948; Powell 1973; pheromone release, it is the act of moving (e.g. flight) Dreisig 1986; Chinery 1989; Nielsen & Common 1991; that presumably most exposes animals to their would-be Aiello 1992; Svensson et al. 1999). If these labels are used predators (Sakaluk & Belwood 1984; Fleishman 1986; to imply specific diel periodicities (e.g. ‘diurnal’ means no Acharya & McNeil 1998). Because the day and the night nocturnal activity), this may lead to assumptions about present considerably different types of potential preda- their sensory adaptations (Ehnbom 1948; Powell 1973; tors, the sensory defences of flying insects should be Horridge et al. 1977; Cutler et al. 1995; Kreusel & Ha¨user influenced by their (and their predators’) diel flight 1997; Schmitz & Bleckmann 1998; Fullard & Dawson periodicity (DFP). For primary defences (i.e. those that 1999). operate before a predator is aware of a potential prey; Lepidoptera can serve as useful models for these ques- Edmunds 1974), diurnally flighted insects should rely tions because they show a diversity of both flight habits more upon vision to detect the approach of potential and sensory adaptations (Svensson et al. 1999). As most predators, whereas nocturnal taxa should favour auditory Lepidoptera have short adult life spans, selection should or chemical systems (Svensson 1996). To examine the favour traits that enable individuals to maximize their evolution of diel sensory adaptations in insects it is time flying in search of mates and oviposition sites. necessary to know their entire 24-h flight patterns, but Sensory defences against diurnal and nocturnal preda- such observations are surprisingly few. Most periodicity tors should be important factors in maximizing this Correspondence: J. Fullard, Department of Zoology, Erindale College, flight time. A profound sensory difference within the University of Toronto, 3359 Mississauga Road, Mississauga, Ontario Lepidoptera is the presence of ultrasound-sensitive ears in L5L 1C6, Canada (email: [email protected]). most moths compared to their absence in most butterflies 0003–3472/01/080349+20 $35.00/0 349 2001 The Association for the Study of Animal Behaviour 350 ANIMAL BEHAVIOUR, 62, 2 (Scoble 1992) (the purported ears of certain nymphalid cylinders measuring 15.2 cm tall with a 6.5 cm radius and butterflies (Otero 1990) are not ultrasound sensitive backed by white Styrofoam. We inserted a microcentri- (Swihart 1967; Ribaricˇ & Gogala 1996) and appear to be fuge tube filled with a dilute sucrose solution through the used in a social context (Monge-Na´jera et al. 1998; Yack back of the chamber and allowed the insects to feed et al. 2000)). Ultrasound-sensitive ears alert their owners ad libitum for the 24-h observation period. Cages were (usually moths, but see Yack & Fullard 2000)tothe visually separated from each other by sheets of card- presence of echolocating, insectivorous bats (Roeder board. We placed the chambers in a 220270200 cm 1967) and their absence in most butterflies (Rhopalocera) plastic screen tent in a partially open forest that was has been argued to have selected for these insects’ pre- isolated from human activity and exposed to ambient sumed diurnal preferences (Fullard 1988, 1998; Morrill & environmental conditions. Temperatures recorded in- Fullard 1992; Fullard et al. 2000; Yack & Fullard 2000). side and outside the tent three times every day of The basic assumption of this hypothesis however is testing never differed by more than 2 throughout the untested because the DFPs of most butterflies are summer months. unknown and the nocturnal activity of certain hedyloid We positioned an automatic light-sensing video camera butterflies (Aiello 1992) suggests that night-flight may be (Sanyo VDC-9212) 60 cm in front of the chambers and more common than believed in the Rhopalocera. focused it on the moths within the chambers (Fullard & In this paper, we use a modified technique (Fullard & Dawson 1999). The camera uses ambient light during the Dawson 1999) of near infrared video recording (Conner & day and automatically converts to a built-in set of near Masters 1978; Webster & Conner 1986; Riley et al. 1990, infrared lights during the night (=980 nm, wavelengths 1992) to monitor the 24-h flight activity patterns of 84 not received by lepidopteran eyes: Horridge et al. 1977; species of Nearctic Lepidoptera. We use the resultant Scherer & Kolb 1987; Arikawa et al. 1999). We allowed the flight actograms to test the assumption of diurnality in animals to be tested to acclimatize in their cages for butterflies and to test whether eared Lepidoptera differ in 30 min (without observers present) before we began their diel flight periodicities from those of earless species. videotaping and at no time throughout the 24 h were the We also map our flight characters onto recently published moths disturbed. Whenever possible, no two individuals phylogenies of the Lepidoptera (Kristensen & Skalski of the same species were used on the same day and to 1998; Weller et al. 1994) to examine the evolution of DFP avoid possible pheromonal interactions, we never tested and auditory defences in the Macrolepidoptera. different conspecific genders on the same day. The output of the camera was fed into a video-cassette recorder at another location and the 24-h activities were recorded METHODS using 10-h tapes (BASF T-200). After the insects had Animals been observed for one 24-h period, they were cold- anaesthetized, killed and preserved by injection with 70% We conducted this study during the summer months ethyl alcohol (only the data from animals that were (June–September) from 1997 to 2000 at the Queen’s not dead or moribund following the observation period University Biological Station (QUBS) in southeastern were used). Ontario, Canada (4434N, 7915W). We collected Lepi- For analysis, we played the tapes back at high speed and doptera from wild populations using hand nets during recorded flight as the number of minutes per 10-min the day or from ultraviolet lights erected on the QUBS period (bin) that an individual showed at least one property during the night. We identified species using movement of at least one body length accompanied by Forbes (1960), Covell (1984), Ward et al. (1974), Riotte wing beats during the minute (e.g. a score of 50% indi- (1992) and Opler (1998) and compared them to vouchers cates an animal that showed at least one flight movement in the insect collections at QUBS. We categorized species during 5 of the 10 min but not necessarily for the entire as eared if they possessed an externally visual tympanic 5 min of that period). We express DFP as the degree of membrane, or belonged to families with species that have nocturnality, that is, the percentage of an individual’s been demonstrated to show an auditory sense (for reviews 24-h flight activity that occurred from the end of twilight see Eggers 1919; Roeder 1974) because exceptions to these in the evening to 40 min past sunrise in the morning ear classifications are rare and exist only in taxa with (individual twilight times for the testing day of each extremely unusual life histories (e.g. bat-free habitats: specimen were provided by the Herzberg Institute of Clarke 1971; Fullard 1994; Surlykke et al. 1998). Astrophysics, National Research Council of Canada Air temperatures are continuously recorded at QUBS as <http://www.hia.nrc.ca>). We explain our reasons for part of the meteorological monitoring function of the choosing these times below (see Results). Diurnal move- station.
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