Developing a Phonotaxis Performance Index to Uncover Signal Selectivity in Walking Phonotaxis

Abstract

Any sensory strategies that prey take to avoid eavesdropping predators will depend on the behavioral decisions of eavesdroppers. As these decisions are guided by the sensory processing of communication signals, accurate measurements of sensorimotor output will provide insights into signal preferences, parameters evaluated for signal recognition, and the perceptual and cognitive capacity of receivers. A number of techniques have been proposed for measuring walking phonotaxis (and taxis behavior more generally). Consistent limitations of such measures are (1) that some animals cannot discriminate alternative signals when they occur simultaneously (i.e., overlapping in the spectral and temporal domain), or (2) some animals respond with low selectivity to stimuli presented in isolation, and (3) identifying appropriate dimensions of response variability is not straightforward. Here we document an approach to develop a sensitive phonotaxis performance index to quantify pulse rate selectivity in two distinct populations of the acoustic parasitoid fly Ormia ochracea. Using a spherical treadmill to measure tethered walking phonotaxis, we examined the ability of flies to track a switch in the broadcast location of test songs with varying pulse-rates. By applying an information-theoretic approach, we identified a set of response parameters that best predict a previously described pulse-rate preference. These parameters were incorporated into an index to describe temporal pattern selectivity during walking phonotaxis. Our study also revealed that in Floridian Ormia ochracea, the pulse rate preference function is not affected by the locomotor mode (walking vs. flying) used in phonotaxis. Furthermore, we describe for the first time, pulse rate selectivity in Californian Ormia ochracea. Both populations have pulse rate preference functions with peak selectivity between 50 and 60 Pulses/s (pps). Previous studies demonstrating natural differences in host song preferences (Floridian O. ochracea preferring Gryllus rubens and Californian O. ochracea preferring Gryllus lineaticeps calling songs) may be based on other temporal parameters aside from pulse rate. Finally, we discuss the advantages and limitations of our approach in quantifying signal selectivity. This approach can be applied broadly to study signal preferences in other acoustic parasitoid flies and potentially other eavesdroppers that exhibit taxis behaviors in response to the communication signals of prey.

Effects of Ambient Temperature on the Recognition and Preferences for Host Song Pulse-rate by the Acoustic Parasitoid FlyOrmia ochracea

“…This optical mouse sensor registers motion as changes in x and y pixel units at a sampling rate of 2160 Hz [56]. In a previous study [49], we confirmed that O. ochracea never caused the spherical treadmill to rotate on its axis and thus a single sensor system is sufficient for recording O. ochracea walking phonotactic responses. Data captured from the treadmill system was synchronized with sound presentation using software (StimProg V6) developed in MATLAB (R2018a, The MathWorks Inc., USA) that interfaced with National Instruments Data Acquisition hardware (NI USB-6363, USA).…”

“…Walking phonotactic responses were recorded from flies tethered and held on top of a spherical treadmill system previously described in [56] and [49]. This treadmill system consists of a spherical ping-pong ball held afloat in a custom holder with a continuous air stream.…”

“…Most of the primary auditory afferents are type 1 receptors, which exhibit phasic, low jitter spikes that are timed with the onset of sound pulses and are ideal for copying the temporal pattern of cricket songs [45]. Song recognition is based on evaluating the temporal patterning of sound pulses [40,46]. In Florida, Gryllus rubens is the preferred cricket host [47,48], which produces calling songs characterized by a pulse rate of about 45-50 pulses per second (pps).…”

“…In Florida, Gryllus rubens is the preferred cricket host [47,48], which produces calling songs characterized by a pulse rate of about 45-50 pulses per second (pps). Floridian O. ochracea exhibit pulse rate preference functions that peak at the same range of pulse rates [49]. Upon detection of appropriate calling songs, gravid female flies will perform flying and walking phonotaxis to the source location [50][51][52], where they deposit first instar planidia near or on top of the host.…”

Parasitism of Neoconocephalus katydids by the parasitoid fly, Ormia lineifrons

“…On the one hand, it is possible that host recognition is broadly tuned, accepting differences of call characteristics of multiple host species (sensu Lee et al, 2019;Sakaguchi & Gray, 2011). Based on the hosts from our study, O. lineifrons was attracted to calls that were either interrupted ("versed") or continuous and consisted of single or double pulses.…”