The bat signal: Can cricket ears hear their predators?

(This was originally published here in 2005.)

Few events in animal behaviour evoke an observer’s visceral response as interactions between predators and prey, leading to poetic metaphors like, “nature red in tooth and claw.” The mechanisms through which prey avoid being caught and eaten provide some of the best examples of behaviours whose neural basis is reasonably well understood. For example, in fish, the Mauthner cells are key players in generating C-start escape responses (Korn and Faber 2005); in crayfish, the lateral and medial giant interneurons generate escape tailflips (Edwards et al. 1999). Surprisingly, however, our knowledge of when these well studied circuits are triggered by actual predators in the wild is rather limited, though those gaps are beginning to close (Herberholz et al. 2004).

Crickets have neurons that trigger escape responses, named AN2 (also referred to as Int-1). Unlike fishes’ Mauther neurons or crayfish’s giant interneurons, which can be triggered by a wide range of sudden stimuli, AN2 neurons appear to serve as detectors for one particular type of predator, namely echolocating bats (Nolen and Hoy 1984, 1987). While AN2 neurons respond to a wide range of sound frequencies, they are particularly sensitive to ultrasound, that is, sound frequencies that are too high for human ears to hear (Nolen and Hoy 1987). This is the approximately the same range of sound frequencies that echolocating bats use when foraging. But, as a recent paper by Fullard and colleagues (Fullard et al. 2005) notes, the key word is “approximately.” There are many species of bats, which differ in their foraging tactics, and emit a wide range of sounds as they do so. Most lab studies, for understandable reasons of simplicity and convenience, have used pure tones generated by computers to trigger crickets’ auditory neurons.

Fullard and colleagues studied Teleogryllus oceanicus, a cricket species found across much of the western Pacific. They recorded the calls of a half-dozen species of bats that share habitat with this cricket, then recorded AN2 neurons as they played back the bat calls at different sound intensities.

The crickets’ AN2 neurons responded to calls from all six bat species, if the sound intensity was 80 decibels sound pressure level (dB SPL) or more, although they did not react equally to all bat search calls.

Simply firing the AN2 neuron, however, does not determine if the cricket can avoid a foraging bat, because a single spike of AN2 is not sufficient to trigger an escape response (Nolen and Hoy 1984). By examining the pattern of firing in more detail, the authors were able to estimate how far away a bat call might trigger an escape response. Only calls by three of the bat species fired AN2 neurons strongly enough to generate escape responses before the bat would be aware of the cricket's echo.

If the AN2 is indeed a “bat detector,” it is reasonable to hypothesize that it has been shaped by natural selection to detect bat species living in the same habitat. All bat calls tested were from species that live in the same regions as T. oceanicus (i.e., sympatric species), but one might reasonably predict that AN2 should be less responsive to calls of bats that do not live in the same regions (i.e., allopatric species). That T. oceanicus has such a wide distribution, however, might mean that its auditory system has remained a bat “generalist.” Another prediction of the “bat detector” hypothesis would be that the bats that AN2 detects best would be those of species that are the most successful predators of crickets. In this case, the bat species Tadarida australis generated the greatest AN2 responses, raising the question of what the natural ecological interactions are between the cricket and the bat.

The bat species that is arguably the least conspicuous to crickets demonstrates the importance of understanding natural ecology in interpreting patterns of neural activity. Of the six species of bat whose calls were tested, the least conspicuous to crickets was Nyctophilus geoffroyi, because the echolocating calls of this species are too short and too high frequency for the crickets’ ears to detect reliably. The simple hypothesis might be that this bat species is a mammalian “stealth bomber:” by using echolocation calls that are almost undetectable by crickets, the bat would seem to be well equipped to pluck crickets from the air at will. Instead, N. geoffroyi seems to forage primarily by “gleaning,” i.e., locating insects by the sounds they emit and picking them off the ground (Bailey and Haythornthwaite 1998), a tactic that circumvents crickets’ tuned AN2 “bat detector” almost entirely.

References

Bailey WJ & Haythornthwaite S. 1998. Risks of calling by the field cricket Teleogryllus oceanicus; potential predation by Australian long-eared bats. 513. Journal of Zoology 244(4): 505-513

Edwards DH, Heitler WJ, & Krasne FB. 1999. Fifty years of a command neuron: the neurobiology of escape behavior in the crayfish. Trends in Neurosciences 22(4): 153-160.

Fullard JH, Ratcliffe JM, & Guignion C. 2005. Sensory ecology of predator-prey interactions: responses of the AN2 interneuron in the field cricket, Teleogryllus oceanicus to the echolocation calls of sympatric bats. Journal of Comparative Physiology A 191(7): 605-618.

Herberholz J, Sen MM, & Edwards DH. 2004. Escape behavior and escape circuit activation in juvenile crayfish during prey-predator interactions. The Journal of Experimental Biology 207(11): 1855-1863.

Korn H & Faber DS. 2005. The Mauthner Cell half a century later: A neurobiological model for decision-making? Neuron 47(1): 13-28.

Nolen TG & Hoy RR. 1984. Initiation of behavior by single neurons: The role of behavioral context. Science 226(4677): 992-994.

Nolen TG & Hoy RR. 1987. Postsynaptic inhibition mediates high-frequency selectivity in the cricket Teleogryllus oceanicus: implications for flight phonotaxis behavior. The Journal of Neuroscience 7(7): 2081-2096.