If a bird flies in the forest, does an insect hear it?

Abstract

Birds are major predators of many eared insects including moths, butterflies, crickets and cicadas. We provide evidence supporting the hypothesis that insect ears can function as 'bird detectors'. First, we show that birds produce flight sounds while foraging. Eastern phoebes (Sayornis phoebe) and chickadees (Poecile atricapillus) generate broadband sounds composed of distinct repetitive elements (approx. 18 and 20 Hz, respectively) that correspond to cyclic wing beating. We estimate that insects can detect an approaching bird from distances of at least 2.5 m, based on insect hearing thresholds and sound level measurements of bird flight. Second, we show that insects with both high and low frequency hearing can hear bird flight sounds. Auditory nerve cells of noctuid moths (Trichoplusia ni) and nymphalid butterflies (Morpho peleides) responded in a bursting pattern to playbacks of an attacking bird. This is the first study to demonstrate that foraging birds generate flight sound cues that are detectable by eared insects. Whether insects exploit these sound cues, and alternatively, if birds have evolved sound-reducing foraging tactics to render them acoustically 'cryptic' to their prey, are tantalizing questions worthy of further investigation.

Evolutionary escalation: the bat–moth arms race

“…First, bat avoidance is the sole function of ears in most moth species (Fullard, 1988), and sound-triggered evasive flight provides a survival advantage for moths under attack by bats (Roeder and Treat, 1962;Acharya and Fenton, 1999;Fullard, 2001). Other uses, such as detecting insect-eating birds or intraspecific communication, are likely to be derived (Conner, 1999;Jacobs et al, 2008;Fournier et al, 2013). That said, ever more moth species are being reported to use sound for communication, and this function might be much more common than previously realized (Nakano et al, 2009).…”

“…Erratic flight is a pervasive strategy for predator avoidance for many flying insects, providing defence against birds (Jacobs et al, 2008;Fournier et al, 2013) and bats (Roeder, 1967;Acharya and Fenton, 1999) alike. Compared with eared moths, earless moths rely more on passive defences, such as flying less at night (Morrill and Fullard, 1992;Fullard and Napoleone, 2001;Soutar and Fullard, 2004), closer to vegetation (Lewis et al, 1993;Rydell, 1998), more erratically (Lewis et al, 1993;Rydell and Lancaster, 2000) or at times when bats are not active (Yack, 1988;Morrill and Fullard, 1992;Lewis et al, 1993).…”

Selective forces on origin, adaptation and reduction of tympanal ears in insects

“…For instance, terrestrial mammals or reptiles have been discussed as predators which generated noise by moving in the habitat, touching plants and stones and so onand this noise definitely will include ultrasound (Flook et al 2000). Recently, birds have been discussed as a potential selection pressure on ears as their wing beats peaking at lower frequencies but also extending into the ultrasound are potentially audible for insects (Jacobs et al 2008;Fournier et al 2013). Flying birds have been present on the scene since about 150 million years ago and insect eating might have been a heritage of their already rather small dinosaurian ancestors (e.g.…”

“…It is likely that the main pressure came from bats (e.g. Hoy 1992;Fullard 1998;Miller and Surlykke 2001;Conner and Corcoran 2012), but it was shown recently for moths that they can hear flying birds as well (Fournier et al 2013). The tympanal organ in the diurnal butterfly (Morpho peleides) responds to low frequencies and has been suggested as a specific "bird detector" (Lane et al 2008).…”

Specialized primary feathers produce tonal sounds during flight in rock pigeons (Columba livia)

“…strut displays in greater sage grouse, wing-snapping displays in manakins; Clark and Prum, 2015;Prum, 1998). These non-vocal acoustic signals, or sonations, are common among birds, perhaps because of the inherently noisy nature of feathers, wings and flight (Clark and Prum, 2015;Fournier et al, 2013;Wei et al, 2013).…”