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Electrocommunication, Sensory Ecology, and Group Dynamics in a Mormyrid Weakly Electric Fish

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Electrocommunication, Sensory Ecology, and Group Dynamics in a Mormyrid Weakly Electric Fish Animal–Robot Interactions: Electrocommunication, Sensory Ecology, and Group Dynamics in a Mormyrid Weakly Electric Fish Dissertation zur Erlangung des Doktorgrades (Dr. rer. nat.) der Mathematisch-Naturwissenschaftlichen Fakultät der Rheinischen Friedrich-Wilhelms-Universität Bonn vorgelegt von Martin Worm aus Gießen Bonn 2018 Angefertigt mit Genehmigung der Mathematisch-Naturwissenschaftlichen Fakultät der Rheinischen Friedrich-Wilhelms-Universität Bonn. 1. Gutachter: Prof. Dr. Gerhard von der Emde 2. Gutachter: Prof. Dr. Wolfgang Alt Tag der Promotion: 2. Oktober 2018 Erscheinungsjahr: 2018 i Erklärung Hiermit erkläre ich, die vorliegende Arbeit persönlich, selbstständig und nur unter Zuhil- fenahme der angegebenen Mittel angefertigt zu haben. Inhaltliche und wörtliche Über- nahmen anderer Werke wurden durch Zitate als solche gekennzeichnet. Bonn, den 25. Mai 2018 Martin Worm ii Teile dieser Arbeit sind veröffentlicht oder zur Veröffentlichung eingereicht: 1. Worm, M., Landgraf, T., Prume, J., Nguyen, H., Kirschbaum, F., and von der Emde, G. (2018). Evidence for mutual allocation of social attention through interactive signaling in a mormyrid weakly electric fish. Proceedings of the National Academy of Sciences (Accepted). 2. Worm, M., Kirschbaum, F. and von der Emde, G. (2018). Disembodying the invisible: Electrocommunication by passive reception of a moving playback signal. Journal of Experimental Biology 221: jeb-172890. 3. Worm, M., Kirschbaum, F. and von der Emde, G. (2017). Social interactions between live and artificial weakly electric fish: Electrocommunication and locomotor behavior of Mormyrus rume proboscirostris towards a mobile dummy fish. PLOS ONE 12 (9): e0184622. 4. Donati, E., Worm, M., Mintchev, S., van der Wiel, M., Benelli, G., von der Emde, G. and Stefanini, C. (2016). Investigation of collective behaviour and electrocommunication in the weakly electric fish, Mormyrus rume, through a biomimetic robotic dummy fish. Bioinspiration & Biomimetics 11: 066009. iii Teile dieser Dissertation basieren auf veröffentlichten (Kapitel 4, 8 und 9), bzw. zur Veröffentlichung angenommen Manuskripten (Kapitel 5). Die Literaturquellen aller Kapitel sind am Ende der Arbeit zusammengefasst. Diese Arbeit enthält außerdem Daten und Ergebnisse, die von Studentinnen im Rahmen ihrer Abschlussarbeiten am Zoologischen Institut in der Abteilung Neuroethologie/Sensorische Ökologie erhoben wurden. Diese Arbeiten wurden im Rahmen meines Dissertationsprojektes angefertigt und wurden während aller Phasen ihrer Entstehung durch mich mitbetreut: 1. Die Daten der Versuche mit konstanten Entladungsfrequenzen (Kapitel 4) wurden von Rowena Toma für ihre Bachelorarbeit "Auswirkungen verschiedener Dummy- generierter Playbacks auf die motorische und elektrische Antwort von Mormyrus rume (Mormyridae, Teleostei)" (Toma, 2014b) erhoben. 2. Die Kontestversuche zur Untersuchung der Kommunikationsfunktion elektrischer Doppelpulse (Kapitel 4) wurden von Anna Kersten im Rahmen ihrer Projektarbeit "Das motorische und elektrische Kommunikationsverhalten von Mormyrus rume: Antagonistische Begegnungen in Zweiergruppen" (Kersten, 2017a) durchgeführt und ausgewertet. 3. Das Programm zur Imitation der Echoantwort (Kapitel 5 und 11) wurde von Julia Prume mitentwickelt und kam bei der Anfertigung iher Projektarbeit "Elektrische und motorische Reaktionen des freischwimmenden, schwach elektrischen Fisches Gnathonemus petersii auf aggressive Signale und interaktive "Echo Antworten" einer elektrokommunizierenden Attrappe" (Prume, 2015b) und ihrer Bachelorarbeit "Elektrische Reaktionen des freischwimmenden schwach elektrischen Fisches Gnathonemus petersii auf interaktive 'Echo Responses' und statische Playbacks einer elektrokommunizierenden Attrappe" (Prume, 2015a) erstmals zur Anwendung. Alle Übernahmen sind an entsprechender Stelle als solche kenntlich gemacht. iv TABLE OF CONTENTS Table of Contents I. General Introduction .................................................................................................................................. 1 1. Weakly Electric Fish as Model Organisms .................................................................................... 3 1.1 Electroreception in aquatic vertebrates .............................................................................. 3 1.2 Electrogenic fishes ........................................................................................................................ 5 1.3 The electric sense of mormyrid weakly electric fish ...................................................... 7 1.4 Habitat and sensory ecology of weakly electric fishes ................................................ 14 2. Study Aims and Objectives: Mobile Dummy Fish for the Investigation of Electrocommunication ....................................................................................................................... 19 II. Part One: Communication ..................................................................................................................... 21 3. Introduction to Animal Communication ..................................................................................... 23 3.1 Definitions and the evolution of communication systems ........................................ 23 3.2 Classification of communication signals ........................................................................... 27 3.3 Communication in fishes ......................................................................................................... 30 3.3.1 Visual communication .................................................................................................... 30 3.3.2 Acoustic communication ............................................................................................... 32 3.3.3 Chemical communication .............................................................................................. 34 3.3.4 Communication through tactile stimuli and the lateral line ........................... 36 3.4 Electrocommunication ............................................................................................................. 37 3.4.1 Communication via pulse-type electric signals in Gymnotiformes .............. 38 3.4.2 Communication via wave-type electric signals in Gymnotiformes .............. 38 3.5 Electrocommunication in Mormyriformes ...................................................................... 39 3.5.1 Communication via EOD-waveform information in mormyrids ................... 40 3.5.2 Communication via IDI-variation in mormyrids ................................................. 41 4. Project 1: Social Interactions between Live and Artificial Weakly Electric Fish: Electrocommunication and Locomotor Behavior of Mormyrus rume towards a Mobile Dummy Fish ............................................................................................................................ 45 4.1 Introduction .................................................................................................................................. 46 4.2 Materials and methods ............................................................................................................. 49 v TABLE OF CONTENTS 4.2.1 Animals ..................................................................................................................................49 4.2.2 Experimental setup and electrical playback generation ...................................49 4.2.3 Experimental protocol ....................................................................................................51 4.2.4 Data acquisition .................................................................................................................52 4.2.5 Hierarchy determination ...............................................................................................52 4.2.6 Locomotor behavior .........................................................................................................53 4.2.7 EOD data analysis ..............................................................................................................53 4.2.8 Video tracking .....................................................................................................................55 4.3 Results .............................................................................................................................................56 4.3.1 Dominance hierarchy ......................................................................................................56 4.3.2 Following-behavior ..........................................................................................................56 4.3.3 Electrical responses .........................................................................................................58 4.3.4 Electrical discharge interactions and synchronizations ...................................70 4.3.5 Motor interactions with the dummy fish ................................................................72 4.4 Discussion ......................................................................................................................................79 5. Project 2: Evidence for Mutual Allocation of Social Attention through Interactive Signaling in a Mormyrid Weakly Electric Fish ..........................................................................89 5.1 Introduction ..................................................................................................................................90
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