Sensorimotor behavior under informational constraints: a robotic model of prey localization in the bat Micronycteris microtis

Action and perception are complicated by the fact that sensory information is often incomplete. Despite these informational constraints, animals interact intelligently and robustly with the world. Echolocating bats can be assumed to operate under substantial informational constraints as the information acquired by their sonar system is limited and sparse. Nevertheless, they fly swiftly through complex habitats and forage on the wing in complete darkness. Recently, the small tropical bat Micronycteris microtis was documented to glean motionless prey from vegetation. Its ability to precisely localize insects has been interpreted as evidence for the bat acquiring a detailed acoustic image of the target. Given the limitations of the sonar system, it is unclear how this detailed image would be obtained. In this paper, we present a robotic model testing an alternative hypothesis. We propose that echo loudness (differences) contain sufficient information to localize a prey item perched on a leaf. Our robot can localize prey with a precision similar to that of the bat, relying only on echo loudness. We conclude that the documented behavior of M. microtis might not require a detailed acoustic image of the prey. Informational constraints The extraordinary behavioral feats of echolocating bats have led researchers to speculate about the representations they infer from echoes. Some have suggested that the information acquired through sonar is highly detailed (Simmons, 2012; Ulanovsky and Moss, 2008; Geipel et al., 2013), containing information about object location and shape. Moreover, it has been suggested that their behaviors indicate that sonar enables bats to perceive complex scenes as integrated wholes (Barchi et al., 2013). And that the comprehensive acoustic images (Clare and Holderied, 2015) of the environment (Lee et al., 2017) build from echo data compare well with those enabled by vision (Moss and Surlykke, 2001). Despite the preceding interpretations of sonar-based behavior, bats can be assumed to operate under significant informational constraints, just like other animals. The world is full of intricate, ill-defined problems animals must solve to survive. Animals have to flexibly adjust their sensorimotor behavior to the moment-to-moment contingencies which arise in interaction with the environment (e.g., Brooks, 1999; Beer, 1990; Pfeifer and Bongard, 2006; Di Paolo et al., 2017). Critically, action and perception have to proceed in the face of substantial informational deficiency (Brooks, 1990; Sterling and Laughlin, 2015). Indeed, animals can not be assumed to have access to complete knowledge about (the dynamics of) their bodies or the environment. This informational constraint encumbers action-perception in all animals (Marks et al., 1988; Sterling and Laughlin, 2015), including mammals, and is one of the primary reasons direct interaction with the world is challenging (Alterovitz et al., 2016). The view that bat echolocation yields highly detailed information about the environment probably has its origin in experimental findings showing that bats can locate single targets (typically, a small sphere) with high accuracy (e.g., Simmons et al., 1983; Lawrence and Simmons, 1982; Wotton and Simmons, 2000). However, the ability to locate and identify isolated objects under favorable conditions does not necessarily imply that bats can reconstruct the layout of multiple complex reflectors (e.g., trees and shrubs) under natural conditions. In contrast to the artificial targets used in experiments, most natural objects, including vegetation and human-made objects, typically return many overlapping echoes (Yovel et al., 2011, 2009; Vanderelst et al., 2016; Warnecke et al., 2018). Over the past few years, we have shown that for a range of sonar-based activities, bats do not require an interpretation of echoes in terms of identifiable objects in the environment or acoustic image (e.g., Vanderelst et al., 2015, 2016; Steckel and Peremans, 2013; Mansour et al., 2019; Adarsh Chitradurga Achutha and Vanderelst, 2021). We maintain that bat sonar is inherently limited in the amount of information it can extract about natural environments’ structure. The presumed ability of bats to reconstruct acoustic images from echoes is questionable due to their small field of view (Surlykke et al., 2009; Jakobsen et al., 2012, 2013) and low update rate (Holderied et al., 2006; Seibert et al., 2013). However, the most severe barrier stems from the temporal resolution of the sonar system (Simmons et al., 1989; Wiegrebe and Schmidt, 1996; Surlykke and Bojesen, 1996). D ow naded rom httpdirect.m it.edu/isal/proceedin33/61/1929883/isal_a_00374. pdf by gest on 27 Sptem er 2021 It follows that bats probably cannot extract much information about the 3D layout of the environment most of the time. Gleaning prey from substrate Recently, Geipel et al. (2013, 2019) reported on prey capture behavior in the small neotropical bat Micronycteris microtis (see fig. 1a). This bat hunts for insects perched on the leaves of understory vegetation in the rainforest. This behavior is remarkable as echoes from the leaves overlap with any echoes returning from potential prey (Jones, 2013). The overlapping echoes should make it difficult to detect and localize the prey. Geipel et al. (2013, 2019) presented some hypotheses about how M. microtis can hunt for motionless prey resting on leaves. Ensonification experiments confirmed that leaves with an insect on them return louder echoes than unoccupied leaves, especially when approached under an oblique angle (Geipel et al., 2019). While this might explain how M. microtis detects prey (or, rather, leaves occupied by prey), it does not explain how the bat localizes and homes in on the target. Geipel et al. (2013) suggested that the bat’s ability to localize the insect indicates that they form acoustic images from temporal and spectral echo information (see also Geipel, 2007; Jones, 2013). Likewise, Simon et al. (2014) interpreted the findings of Geipel et al. (2013) as evidence for fine echo-acoustic resolution. If the bat can form a 2D or 3D representation of the leave, the insect, or combination thereof, it could use this to approach the insect. However, we think it is unlikely that M. microtis can infer the insect’s 3D geometry and leaf from echoes for the reasons outlined above. In this paper, we test the alternative hypothesis that a strategy based on echo amplitude allows M. microtis to approach prey perched on a leaf. We test this hypothesis using a robotic model operating under conditions mimicking the experiments presented by Geipel et al. (2013, 2019).