Environmental acoustic cues guide the biosonar attention of a highly specialised echolocator

Abstract

Sensory systems experience a trade-off between maximizing the detail and amount of sampled information. This trade-off is particularly pronounced in sensory systems that are highly specialised for a single task and thus experience limitations in other tasks. We hypothesised that combining sensory input from multiple streams of information may resolve this trade-off and improve detection and sensing reliability. Specifically, we predicted that perceptive limitations experienced by animals reliant on specialised active echolocation can be compensated for by the phylogenetically older and less specialised process of passive hearing. We tested this hypothesis in greater horseshoe bats, which possess morphological and neural specialisations allowing them to identify fluttering prey in dense vegetation using echolocation only. At the same time, their echolocation system is both spatially and temporally severely limited. Here, we show that greater horseshoe bats employ passive hearing to initially detect and localise prey-generated and other environmental sounds, and then raise vocalisation level and concentrate the scanning movements of their sonar beam on the sound source for further investigation with echolocation. These specialised echolocators thus supplement echo-acoustic information with environmental acoustic cues, enlarging perceived space beyond their biosonar range. Contrary to our predictions, we did not find consistent preferences for prey-related acoustic stimuli, indicating the use of passive acoustic cues also for detection of non-prey objects. Our findings suggest that even specialised echolocators exploit a wide range of environmental information, and that phylogenetically older sensory systems can support the evolution of sensory specialisations by compensating for their limitations.

Neural representation of bat predation risk and evasive flight in moths: A modelling approach

“…in the range of the sonar beam directionality or even narrower. More data on hearing directionality, hearing direction, their variation due to ear movements (e.g., Griffin et al 1962;Kugler et al 2017, Lattenkamp et al 2018, Yin & Mülller 2019, and on natural scanning behaviour will be required to estimate the average prey detection cone of free-flying bats.…”

The challenge of detecting prey: Private and social information use in predatory bats

“…Bats targeting the fluttering sounds of moths are not surprising given the nocturnal habits of both groups; indeed, many bat species exploit this sensory strategy (e.g., Myotis septentrionalis , Myotis lucifugus [Ratcliffe & Dawson, ]; Myotis evotis [Faure & Barclay, ]; Plecotus auritus [Anderson & Racey, , ]). Even bats with highly specialized neurological and morphological adaptations to use echolocation to detect fluttering moths also attend to the sounds produced by moth movements, underlying the importance of simply listening for prey‐emitted locomotion cues (e.g., Rhinolophus ferrumequinum , Lattenkamp et al, ).…”

“…Phylogeny adapted from Kaňuch, Aghová, Meheretu, Šumbera, and Bryja (), Roehrs, Lack, and Bussche (), Rojas, Warsi, and Dávalos () and Stadelmann, Lin, Kunz, and Ruedi (). References for prey cue and signal use by bat species: 1 Lattenkamp et al (); 2 Raghuram et al (); 3 Ryan and Tuttle (); 4 Fiedler (); 5 Marimuthu and Neuweiler (); 6 Marimuthu et al (); 7 Fenton et al (); 8 Bell (); 9 Vehrencamp, Stiles, and Bradbury (); 10 Schmidt et al (); 11 Gröger and Wiegrebe (); 12 Heffner et al (); 13 Jones et al (); 14 Bell (), 15 Fuzessery et al (); 16 Holderied et al (); 17 Anderson and Racey (); 18 Anderson and Racey (); 19 Coles et al (2004); 20 Siemers et al (); 21 Jones et al (); 22 Arlettaz et al (); 23 Faure and Barclay (); 24 Ratcliffe and Dawson (); 25 ter Hofstede, Ratcliffe, and Fullard (); 26 Alem et al (); 27 Belwood and Morris () (note that in this study, Micronycteris microtis is referred to as Micronycteris megalotis and Lophostoma silvicolum as Tonatia silvicola , reflecting the phylogenetic understanding at the time); 28 Falk et al (); 29 Page and Jones (); 30 Patriquin et al (); 31 Bailey and Haythornthwaite (); 32 Buchler and Childs ()…”

Brief exposure to intense turbulence induces a sustained life-history shift in echinoids

“…Previous studies on a range of behaviors have demonstrated how terrestrial and aquatic animals utilize and integrate multiple cue modalities (e.g. Dusenbery, 1992;Pluta and Kawasaki, 2008;Harley et al, 2011;Igulu et al, 2013;Ravi et al, 2016;Lattenkamp et al, 2018), and specifically how cue hierarchies can lead to optimal decisions in dynamic marine environments (e.g. Kingsford et al, 2002;Woodson et al, 2007;Fuchs et al, 2010;Seuront, 2013).…”