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Path Integration Error and Adaptable Search Behaviors in a Mantis Shrimp Rickesh N © 2020. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2020) 223, jeb224618. doi:10.1242/jeb.224618 RESEARCH ARTICLE Path integration error and adaptable search behaviors in a mantis shrimp Rickesh N. Patel* and Thomas W. Cronin ABSTRACT Many stomatopod crustaceans, more commonly known as mantis Mantis shrimp of the species Neogonodactylus oerstedii occupy shrimp, are central place foragers that inhabit benthic marine small burrows in shallow waters throughout the Caribbean. These environments. These animals occupy burrows in marine substrates, animals use path integration, a vector-based navigation strategy, to where they reside between foraging bouts (Dominguez and Reaka, return to their homes while foraging. Here, we report that path 1988; Basch and Engle, 1989; Caldwell et al., 1989). Mantis shrimp integration in N. oerstedii is prone to error accumulated during of the species Neogonodactylus oerstedii employ path integration to outward foraging paths and we describe the search behavior that efficiently navigate back to their burrows while foraging. During N. oerstedii employs after it fails to locate its home following the route path integration, N. oerstedii exhibit homeward paths that are well provided by its path integrator. This search behavior forms oriented and are approximately equal in length to the direct distance continuously expanding, non-oriented loops that are centered near from the point where they initiate their return trip to the burrow (Patel the point of search initiation. The radius of this search is scaled to the and Cronin, 2020). However, the return paths guided by their home animal’s positional uncertainty during path integration, improving the vectors often do not lead them directly to their burrows. When this effectiveness of the search. The search behaviors exhibited by happens, N. oerstedii initiate searches to find their homes (Patel and N. oerstedii bear a striking resemblance to search behaviors in other Cronin, 2020). Here, we investigated the source of the home vector animals, offering potential avenues for the comparative examination error in N. oerstedii and evaluated the means by which N. oerstedii – of search behaviors and how they are optimized in disparate taxa. copes with this error the strategies that shape its search pattern. KEY WORDS: Navigation, Search Pattern, Animal Behavior, MATERIALS AND METHODS Orientation, Stomatopod, Homing All data in this study were collected from experiments reported in Patel and Cronin (2020). Specifically, foraging behaviors from the INTRODUCTION ‘not manipulated’ and ‘animal displaced’ groups of trials enacted in Path integration is an efficient navigational strategy that many the greenhouse on the University of Maryland Baltimore County animals use to return to a specific location. During path integration, (UMBC) campus in Patel and Cronin (2020) were used in the an animal monitors its body orientation and the distance it travels current study. from a reference point using a biological compass and odometer. From this information, a home vector (the most direct path back to Animal care the reference point) is continuously updated, allowing the animal to Individual Neogonodactylus oerstedii (Hansen 1895) collected in return to its original location (Seyfarth et al., 1982; Müller and the Florida Keys, USA, were shipped to UMBC. Animals were Wehner, 1988; Seguinot et al., 1993). Path integration is especially housed individually in 30 ppt sea water at room temperature under a useful for central place foragers, animals which return to a home 12 h:12 h light:dark cycle. Animals were fed whiteleg shrimp, location between foraging bouts. Litopenaeus vannamei, once per week. Data were collected from 13 Because of small errors made in angular and odometric individuals (5 male and 8 female). All individuals were between 30 measurements during path integration, the home vector is prone to and 50 mm long from the rostrum to the tip of the telson. error accumulated over the course of an animal’s outward path (the path from the animal’s start location to the site of home vector Experimental apparatus initiation). Therefore, with a longer outward path, an increased error Four relatively featureless, circular navigation arenas were of the home vector is expected (Müller and Wehner, 1988; Cheung constructed from 1.5 m diameter plastic wading pools that were et al., 2007; Heinze et al., 2018). To account for this error, some filled with pool filter sand and artificial seawater (30 ppt; Fig. 1A). path-integrating animals initiate a stereotyped search behavior if Arenas were placed in a glass-roofed greenhouse on the UMBC they fail to reach their goal after traveling the distance indicated by campus. The spectral transmittance of light through the greenhouse their path integrator (Wehner and Srinivasan, 1981; Hoffmann, glass was nearly constant for all wavelengths, excluding the deep-UV 1983; Zeil, 1998; Durier and Rivault, 1999). wavelength range (280–350 nm; Fig. S2A). Celestial polarization information was transmitted through the glass roof of the greenhouse (Fig. S2B–D). Vertical burrows created from 2 cm outer-diameter PVC pipes were buried in the sand 30 cm from the periphery of the UMBC Department of Biological Sciences, The University of Maryland, Baltimore County, 1000 Hilltop Circle, Baltimore, MD 21250, USA. arena so that they were hidden from view when experimental animals were foraging. Trials were recorded from above using C1 Security *Author for correspondence ([email protected]) Cameras (Foscam Digital Technologies LLC) mounted to tripods R.N.P., 0000-0002-5323-2062 placed above the arenas. During animal displacement experiments, a thin 11×82 cm acrylic track with a movable platform was placed Received 4 March 2020; Accepted 9 June 2020 30 cm from the wall of the arena at its closest edge. Journal of Experimental Biology 1 RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb224618. doi:10.1242/jeb.224618 AB C 30 Path integration error 25 Camera Outward path 20 15 Burrow Homeward path before search 10 Food Food Search path 5 Burrow Path integration error (cm) y=5log(x)+9.9 Food 0 25 cm 100 200 500 1000 2000 5000 25 cm Burrow Outward path length (cm) Fig. 1. Error accumulated during outward foraging paths leads to error in the home vector. (A) Navigation arenas, 150 cm in diameter, contained a burrow (empty circle) buried in the base of the arena, 30 cm from the arena’s periphery. During trials when animals were not manipulated, food was placed at one of two positions 50 cm from the periphery of the arena (filled circles). Trials were video recorded from above. (B) Example of a foraging path of Neogonodactylus oerstedii. The distance from the point where search behaviors were initiated to the burrow location is the error of the animal’s path integrator. (C) Correlation between outward path lengths (log axis) and the path integration error during trials in which the animals were not manipulated (P=0.017, R=0.67, n=12). Experimental procedures behavior initiation to the burrow (the path integration error) was also Individual N. oerstedii were placed in each arena and were allowed to measured using the MTrackJ plugin. familiarize themselves with the arena for 24 h. During familiarization, Search behaviors lasting over 10 s with at least one completed a vertical 2 cm diameter PVC column with alternating 1 cm thick loop were analyzed from all trials when animals were not black and white horizontal stripes was placed adjacent to the burrow, manipulated (n=4) and/or were displaced to a new location in marking it during the animal’s initial explorations of the arena. the arena (n=7, n=11 total). We defined a loop in the search as a After familiarization, the column marking the burrow was path that increased in distance from the point of search initiation removed from the arena. Empty Margarites sp. snail shells stuffed before the animal turned and moved back toward the search with pieces of food (whiteleg shrimp) were placed at fixed locations initiation point. The loop was determined to be completed when an in the arena. During experiments when animals were not animal moved closest to the point of search initiation before once manipulated, food was placed at one of two locations, 50 cm from again moving away from the search initiation point or when an the periphery of the burrow. During experiments in which animals animal turned more than 90 deg from its trajectory back towards were displaced, food was placed on the movable platform on which the search initiation point after returning halfway back to it, animals were translocated. Each animal was allowed three whichever occurred first. successful foraging excursions (i.e. food placed in the arena was The radii of search behaviors were measured as the farthest found) before foraging paths were used for analyses. If an individual distance of a search from the original point of search initiation (i.e. did not successfully locate food within 1 week in the arena, it was the end point of the home vector) using ImageJ. The radii of all replaced with a new individual. searches were measured over three time ranges after search During experiments when animals were not manipulated, food initiation: 0–20 s, 21–60 s and 61–180 s. The radii of individual was placed in the arena between 2 and 3 h after sunrise and removed searches lasting at least 60 s were also measured from the beginning from the arena following sunset. Animal displacement experiments to the end of the search, every 10% of the total search time until the were run from sunrise to 4 h following sunrise and from 4 h search was completed (up to 10 min). As individuals traveled at preceding sunset to sunset. During animal displacement different speeds during their searches, search time (in seconds) was experiments, food was removed from the arena during the middle multiplied by the individual’s mean velocity during the search of the day.
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