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Sensory ecology of predator–prey interactions: responses of the AN2 interneuron in the field cricket, Teleogryllus oceanicus to the echolocation calls of sympatric bats

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Abstract

We observed the responses of the AN2 interneuron in the Pacific field cricket, Teleogryllus oceanicus, a cell implicated in eliciting avoidance flight away from bats, to acoustic stimuli representing the echolocation calls of bats as well as field recordings of search and gleaning attack calls of six species of insectivorous sympatric bats (West Australia, Australia: Tadarida australis, Chalinolobus goudii, Nyctophilus geoffroyi; Queensland, Australia: Vespadelus pumilus, Myotis adversus; Kaua‘i, Hawai‘i: Lasiurus cinereus). The broad frequency sensitivity of the AN2 cell indicates that T. oceanicus has evolved to detect a wide range of echolocation call frequencies. The reduced sensitivity of this cell at frequencies higher than 70 kHz suggests that some bats (e.g., the gleaning species, N. geoffroyi) may circumvent this insect’s auditory defences by using frequency-mismatched (allotonic) calls. The calls of the freetail bat, T. australis evoked the strongest response in the AN2 cell but, ironically, this may allow this bat to prey upon T. oceanicus as previous studies report that under certain conditions, flying crickets exhibit ambiguous directional responses towards frequencies similar to those emitted by this bat. Short duration calls (1–2 ms) are sufficient to evoke AN2 responses with instantaneous spike periods capable of causing defensive flight behaviours; most bats tested emit calls of durations greater than this. The short calls of N. geoffroyi produced during gleaning attacks may reduce this species’ acoustic conspicuousness to this cricket.

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Abbreviations

AN2:

Ascending neuron 2

dB peSPL:

Decibel, peak equivalent sound pressure level

source level dB:

Decibel intensity measured at 10 cm

IP:

Instantaneous period

kHz:

Kilohertz

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Acknowledgements

We are indebted to Gerald Pollack (McGill University) for the gift of the crickets in this study and for his insightful comments on the manuscript. We also thank Hannah ter Hofstede for data analyses. This study was funded by Discovery and Equipment grants from the Natural Sciences and Engineering Council of Canada to JHF and scholarships from the University of Toronto and the Ontario Government to JMR. The experiments described in this paper comply with the “Principles of animal care”, publication No. 86-23, revised 1985 of the National Institutes of Health and with the guidelines described in the “Canadian Council on Animal Care guide to the care and use of experimental animals” Vol 1, 2 ed 1993.

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Fullard, J.H., Ratcliffe, J.M. & Guignion, C. Sensory ecology of predator–prey interactions: responses of the AN2 interneuron in the field cricket, Teleogryllus oceanicus to the echolocation calls of sympatric bats. J Comp Physiol A 191, 605–618 (2005). https://doi.org/10.1007/s00359-005-0610-3

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