Early erratic flight response of the lucerne moth to the quiet echolocation calls of distant bats

Abstract

Nocturnal insects have evolved ultrasound-sensitive hearing in response to predation pressures from echolocating insectivorous bats. Flying tympanate moths take various evasive actions when they detect bat cries, including turning away, performing a steering/zigzagging flight and ceasing flight. In general, infrequent ultrasonic pulses with low sound intensities that are emitted by distant bats evoke slight turns, whereas frequent and loud ultrasonic pulses of nearby bats evoke erratic or rapid unpredictable changes in the flight path of a moth. Flight cessation, which is a freezing response that causes the moth to passively dive (drop) to the ground, is considered the ultimate last-ditch evasive behaviour against approaching bats where there is a high predation threat. Here, we found that the crambid moth Nomophila nearctica never performed passive dives in response to frequent and loud ultrasonic pulses of >60 dB sound pressure level (SPL) that simulated the attacking echolocation call sequence of the predominant sympatric insectivorous bat Eptesicus fuscus, but rather turned away or flew erratically, regardless of the temporal structure of the stimulus. Consequently, N. nearctica is likely to survive predation by bats by taking early evasive action even when it detects the echolocation calls of sympatric bats hunting other insects at a distance. Since aerially hawking bats can track and catch erratically flying moths after targeting their prey, this early escape strategy may be common among night-flying tympanate insects.

Fig 1. Temporal structures of echolocation pulses emitted by the big brown bat, Eptesicus fuscus.

Circles denote the ultrasonic pulses of echolocating bats in a foraging sequence that were recorded in the field. Triangles represent the simulated ultrasonic pulses that were broadcast to moths during the behavioural experiment. Note that E. fuscus is currently a major insectivorous bat species in the area in which we collected the lucerne moth, Nomophila nearctica.

Fig 2. Active times of the bat Eptesicus fuscus and the moth Nomophila nearctica.

(a) Early in the night, E. fuscus frequently echolocated in the field, with 1571 sound files being recorded over 14 clear nights in June to July 2014 and 2015. Bars beneath the x-axis denote daytime (white), twilight (grey) and nighttime (black) in early July in Ontario, Canada. (b, c) In the early scotophase (16L:8D), i.e. shortly after lights-off, both male (b) and female (c) N. nearctica exhibited active locomotion, with a standardised active rate (i.e. nocturnality; see Methods) of 98.6% for male (N = 16) and 99.2% for female (N = 18). Error bars in (b) and (c) indicate the standard error of the mean, and white and black bars beneath the x-axis denote photophase (daytime) and scotophase (nighttime), respectively, in the experimental room. Activity was significantly different between the photophase and scotophase.

Fig 3. Mode of evasive action taken by flying Nomophila nearctica following the broadcast of a 30-kHz pure tone pulse with a similar temporal structure to the echolocation calls of Eptesicus fuscus.

(a) Search phase pulse, (b) early-approach phase pulse, (c) middle-approach phase pulse, (d) late-approach phase pulse, (e) early-terminal phase pulse and (f) middle-terminal phase pulse. Grey bars indicate a turning-away response and white bars indicate an erratic response in the flying moth. Sample sizes are given in parentheses beneath the sound levels and the y-axis denotes the proportion of moths showing each type of response. Multiple comparisons among all combinations of pulse types showed that there was no significant difference in the evasive manoeuvres performed.

Fig 4. Effect of sound level on the evasive responses of flying Nomophila nearctica.

(a) The proportion of pooled turning and erratic responses significantly differed among sound levels. (b) The proportion of turning responses did not differ among sound levels. (c) The proportion of erratic responses significantly differed among sound levels. The same dataset was used as in Fig 3. Circles identify the averages and the lattice represents the average spline deduced by generalized additive models. ‘Se.’ to ‘M.-te. Buzz’ in (b) and (c) are abbreviations of the echolocation call phases shown in (a).