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.