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Poecilia Mexicana) in Light and Darkness Through the Use of a Biomimetic Robot

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Poecilia Mexicana) in Light and Darkness Through the Use of a Biomimetic Robot ORIGINAL RESEARCH published: 05 February 2018 doi: 10.3389/frobt.2018.00003 Insights into the Social Behavior of Surface and Cave-Dwelling Fish (Poecilia mexicana) in Light and Darkness through the Use of a Biomimetic Robot David Bierbach1,2*, Juliane Lukas1,2,3, Anja Bergmann1, Kristiane Elsner1, Leander Höhne1, Christiane Weber1, Nils Weimar1, Lenin Arias-Rodriguez4, Hauke J. Mönck5, Hai Nguyen2, Pawel Romanczuk6, Tim Landgraf5 and Jens Krause2,3 1 Humboldt-Universität zu Berlin, bologna.lab, Q-Team Programm, Berlin, Germany, 2 Department of Biology and Ecology of Fishes, Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Berlin, Germany, 3 Faculty of Life Sciences, Thaer Institute, Humboldt University of Berlin, Berlin, Germany, 4 División Académica de Ciencias Biológicas, Universidad Juárez Autónoma de Tabasco (UJAT), Villahermosa, Tabasco, Mexico, 5 Freie Universität Berlin, FB Mathematik u. Informatik, Berlin, Edited by: Germany, 6 Department of Biology, Institute for Theoretical Biology, Humboldt Universität zu Berlin, Berlin, Germany Andrew King, Swansea University, United Kingdom Biomimetic robots (BRs) are becoming more common in behavioral research and, if Reviewed by: Andrew Philippides, they are accepted as conspecifics, allow for new forms of experimental manipulations of University of Sussex, United Kingdom social interactions. Nevertheless, it is often not clear which cues emanating from a BR are Heiko Hamann, actually used as communicative signals and how species or populations with different University of Lübeck, Germany sensory makeups react to specific types of BRs. We herein present results from experi- *Correspondence: David Bierbach ments using two populations of livebearing fishes that differ in their sensory capabilities. [email protected] In the South of Mexico, surface-dwelling mollies (Poecilia mexicana) successfully invaded caves and adapted to dark conditions. While almost without pigment, these cave mollies Specialty section: This article was submitted to possess smaller but still functional eyes. Although previous studies found cave mollies Evolutionary Robotics, to show reduced shoaling preferences with conspecifics in light compared to surface a section of the journal mollies, it is assumed that they possess specialized adaptations to maintain some kind Frontiers in Robotics and AI of sociality also in their dark habitats. By testing surface- and cave-dwelling mollies with Received: 31 October 2017 Accepted: 15 January 2018 RoboFish, a BR made for use in laboratory experiments with guppies and sticklebacks, Published: 05 February 2018 we asked to what extent visual and non-visual cues play a role in their social behavior. Citation: Both cave- and surface-dwelling mollies followed the BR as well as a live companion Bierbach D, Lukas J, Bergmann A, Elsner K, Höhne L, Weber C, when tested in light. However, when tested in darkness, only surface-dwelling fish were Weimar N, Arias-Rodriguez L, attracted by a live conspecific, whereas cave-dwelling fish were not. Neither cave- nor Mönck HJ, Nguyen H, Romanczuk P, surface-dwelling mollies were attracted to RoboFish in darkness. This is the first study Landgraf T and Krause J (2018) Insights into the Social Behavior to use BRs for the investigation of social behavior in mollies and to compare responses of Surface and Cave-Dwelling Fish to BRs both in light and darkness. As our RoboFish is accepted as conspecific by both (Poecilia mexicana) in Light and Darkness through the Use of a used populations of the Atlantic molly only under light conditions but not in darkness, we Biomimetic Robot. argue that our replica is providing mostly visual cues. Front. Robot. AI 5:3. doi: 10.3389/frobt.2018.00003 Keywords: RoboFish, Poecilia mexicana, cave molly, Atlantic molly, biomimetic robot Frontiers in Robotics and AI | www.frontiersin.org 1 February 2018 | Volume 5 | Article 3 Bierbach et al. Social Interactions with BR INTRODUCTION should be generally less social toward (e.g., do not follow closely) live conspecifics and BRs compared to surface-dwelling mollies Biomimetic robots (BRs) are becoming more common in behav- in light but should be better able to maintain some sociality in ioral research (Webb, 2000; Krause et al., 2011; Butail et al., 2015). darkness with both a live conspecific and a BR compared to One of the major advantages of BRs is that social interactions surface-dwelling fish. Our study not only tests for differences in that are often characterized by mutual influences (Herbert-Read social behavior of surface and cave-dwelling fish but also tests et al., 2012; Jolles et al., 2017) and feedbacks between multiple whether BRs constructed as mobile replicas are accepted as con- individuals (Harcourt et al., 2009) become in part controllable by specifics when visual cues are omitted (as in darkness). the experimenter (Krause et al., 2011). Thus, standardized testing and new forms of experimental manipulations of social interac- tions can be achieved using BRs as interaction partners. However, MATERIALS AND METHODS investigations of social behavior become only meaningful when live animals accept BRs as conspecifics [(Landgraf et al., 2016), Test Fish and Their Maintenance see similar views for computer animations in behavioral ecology In this study, we used second-generation lab-reared descendants (Chouinard-Thuly et al., 2017)]. At the moment, the number of of wild-caught fish from two populations of the Atlantic molly animal species that respond to BRs as conspecifics is quite small. (P. mexicana) that were caught during field trips to the Tacotalpa Thus, it is urgently needed to explore which cues emanating from river system in Tabasco, Mexico (Tobler et al., 2011; Plath et al., BRs are crucial for the acceptance as a conspecific [reviewed in 2013). Our surface population originated from the Río Oxolotán, Landgraf et al. (2016)]. Tinbergen (1948) proposed that only a a tributary to the Río Grijalva, while our cave population stemmed small subset of perceivable cues are actual signals (“social releas- from chamber 7 of the cave Cueva del Azufres (Figure 1). Fish were ers”). They can be species specific, and animals often use sets of reared in randomly outbred mixed-sex stocks at the Laboratory multiple cues to assess their (social) environment (Candolin, of Genetics and Ecophysiology from the Academic Division for 2003). The identification of relevant cues and their realistic imita- Biological Sciences-UJAT. Some of them were transported to the tion is one of the most challenging parts in developing BRs (Krause Department of Biology and Ecology of Fishes at the Thaer-Institute et al., 2011). Since different species possess different sensory for Life Sciences at Humboldt University of Berlin for the present capabilities (Burnett, 2011), comparing the response of species experiment. For the rearing prior to any experiment, we used a with known differences in sensory ecologies toward BRs might light regime of 12 h light:12 h darkness that resembles the natural help developers to understand the cues that are most important surface habitats and maintained water temperature at 26°C. Prior to establish social acceptance of their respective BRs. As an obvi- to experiments, test fish were taken from their stock tanks (80-L) ous by-product, BRs can help researchers to gain a much better and transferred into 54-L tanks in groups of 20 individuals with understanding of social interactions in species, population, or equal sex ratio. Those 54-L tanks were covered with black plastic ecotypes with different ecological and evolutionary backgrounds. foil and could be run either with a 12:12 L:D light regime (6,000 In summary, both developers and biologists using BRs will benefit vs. 0 lux) or in total darkness (0 lux; in case fish were later tested from a broader list of species investigated with BRs. in darkness, see below). Fish were fed twice daily ad libitum with Here, we explored whether two populations of the Atlantic TetraMin flake food and live Chironomid larvae. Please note that molly (Poecilia mexicana, a cave-dwelling and a surface-dwelling all our test subjects have been raised under normal 12 h light:12 h ecotype) accept a BR as a conspecific that was initially developed dark conditions in the lab, and cave mollies thus might not show to meet the requirements of the closely related guppy (Poecilia exactly the same behaviors compared to their wild counterparts reticulata), a “model organism” in many different biological that spend their whole lives in darkness. This was necessary to fields (Magurran, 2005). Both populations of cave- and surface- facilitate maintenance work and to ensure that all fish tested in dwelling mollies differ in their evolutionary background and darkness experienced the same treatment since it is impossible consequently also in their assumed sensory capabilities and social to raise surface mollies in darkness without high mortality rates tendencies. Although cave mollies still possess functional albeit (Riesch et al., 2011). Nevertheless, we acclimated those fish smaller eyes than their surface-dwelling counterparts (Körner tested in darkness (surface and cave mollies) to complete dark et al., 2006; Eifert et al., 2014), their non-visual systems seem to be conditions for 1 week prior to our tests. Such an approach follows much better developed (Parzefall, 1969, 1970, 2001; Peters et al., previous protocols for that species (Plath et al., 2003, 2004). 1973; Parzefall et al., 2007) with recent investigations pointing out that both chemical and mechanosensory communication is The BR: RoboFish more pronounced in cave mollies compared to surface dwell- Our RoboFish system consists of a glass tank (88 cm × 88 cm) ers (Rüschenbaum and Schlupp, 2013; Jourdan et al., 2016). that is filled to a level of 15 cm with aged tap water. The tank Furthermore, cave mollies were previously found to be less is placed on an aluminum rack at about 1.40 m above ground attracted to conspecifics in dichotomous choice tests under nor- (Figure 2A). The two-wheeled differential drive robot moves mal light conditions and hence are assumed to be less social than below the tank on a transparent platform (Figure 2B).
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