The simple ears of noctuoid moths are tuned to the calls of their sympatric bat community

Abstract

SUMMARYInsects with bat-detecting ears are ideal animals for investigating sensory system adaptations to predator cues. Noctuid moths have two auditory receptors (A1 and A2) sensitive to the ultrasonic echolocation calls of insectivorous bats. Larger moths are detected at greater distances by bats than smaller moths. Larger moths also have lower A1 best thresholds, allowing them to detect bats at greater distances and possibly compensating for their increased conspicuousness. Interestingly, the sound frequency at the lowest threshold is lower in larger than in smaller moths, suggesting that the relationship between threshold and size might vary across frequencies used by different bat species. Here, we demonstrate that the relationships between threshold and size in moths were only significant at some frequencies, and these frequencies differed between three locations (UK, Canada and Denmark). The relationships were more likely to be significant at call frequencies used by proportionately more bat species in the moths' specific bat community, suggesting an association between the tuning of moth ears and the cues provided by sympatric predators. Additionally, we found that the best threshold and best frequency of the less sensitive A2 receptor are also related to size, and that these relationships hold when controlling for evolutionary relationships. The slopes of best threshold versus size differ, however, such that the difference in threshold between A1 and A2 is greater for larger than for smaller moths. The shorter time from A1 to A2 excitation in smaller than in larger moths could potentially compensate for shorter absolute detection distances in smaller moths.

Evolutionary escalation: the bat–moth arms race

“…A frequently cited but untested hypothesis for the neural basis of evasive flight in noctuid moths is that the more sensitive receptor (A1) triggers directional flight, whereas the less sensitive receptor (A2) triggers last-ditch behaviour (Roeder, 1974b). This hypothesis implies that A1 and A2 encode different types of information about predation risk: potentially 'I am not yet detected by the bat' and 'I am now detectable by the bat' (ter Hofstede et al, 2013). Other authors (Surlykke, 1984;Ratcliffe et al, 2009) have suggested that A2 might only increase the dynamic range of the ear, i.e.…”

“…Larger moths, however, have more sensitive ears and detect bats at greater distances than do smaller moths, essentially compensating for their increased conspicuousness. This relationship between size and sensitivity is strongest for frequencies that are used by a large number of sympatric bats for echolocation (ter Hofstede et al, 2013). Forrest et al (1995) suggest that this pattern of size and sensitivity may apply across all insects with bat-detecting ears.…”

“…3A; Roeder, 1967). The difference between the most sensitive receptor and the next most sensitive receptor is ∼2-6 dB in pyralids (Skals and Surlykke, 2000), 15 dB in geometrids (Roeder, 1974a;Surlykke and Filskov, 1997) and 15-20 dB in noctuids (ter Hofstede et al, 2013). These differences in threshold between afferents increase the range of amplitudes to which the ear can respond by allowing the less sensitive afferent to continue encoding increasing sound amplitude once the most sensitive afferent has reached its maximum firing capability.…”

“…For example, the ears of Hawaiian moths have a much narrower tuning curve than those of moths found elsewhere, and they are closely tuned to the echolocation frequency of the one bat species in Hawaii, Lasiurus cinereus semotus (Fullard, 1984a). Horseshoe bats, if present, usually have the highest frequency echolocation calls in a community, and their presence appears to select for improved higher frequency hearing in local moth populations (Jacobs et al, 2008;ter Hofstede et al, 2013) and several Old World mantis species (Triblehorn and Yager, 2001).…”

Simple ears – flexible behavior: Information processing in the moth auditory pathway

“…A further common feature of all moth ears is that, given the few receptor cells present, moths cannot discriminate frequencies. Nevertheless, the ears might be tuned to a "best frequency" (Hofstede et al, 2013). However, other anatomical details, i.e.…”