The effects of predation on electric fish signals Minh Tuan Alex Tran Department of Biology McGill

72 Pages·2015·3.77 MB·English

The effects of predation on electric fish signals

Minh Tuan Alex Tran
Department of Biology
McGill University
Montréal

December 2014

A thesis submitted to McGill University in partial fulfillment of the requirements of the degree
of Master of Science in Biology (Neotropical Environment Option)

© Alex Tran 2014
TABLE OF CONTENTS

Abstract / Résumé 2
Acknowledgements 4
Preface 6
General introduction 7
I: Evidence for crypsis in electric signals 11
Abstract 12
Introduction 13
Methods 16
Results 20
Discussion 22
Tables & Figures 26
Linking statement 36
II: Effects of tail loss and regeneration in electric fish 37
Abstract 38
Introduction 39
Methods 42
Results 45
Discussion 47
Tables & Figures 53
General conclusion 62
Bibliography 64
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ABSTRACT

Electric fish produce electric signals for navigation, prey location, and communication. These
signals vary widely among species, but the forces that have led to this diversity remain unclear.
Predation has been proposed as a potential evolutionary force shaping electric fish signals, but
this has not been tested in the field. The purpose of this thesis is to explore the ways in which
predators affect electric fish signals. In the first chapter, we provide field evidence supporting the
hypothesis that predators are driving the evolution of electric fish signals. In the second chapter,
we explore the more acute effects of predation. Caudal injuries are frequently observed in some
electric fish, presumably as the result of sublethal encounters with predators. We show how this
sublethal predation affects electric signals and discuss the implications for the fish.

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RÉSUMÉ

Les poissons électriques produisent des signaux électriques afin de naviguer, localiser leurs
proies, et communiquer. Ces signaux varient fortement entre les espèces, mais les méchanismes
ayant conduit à cette diversité demeurent inconnus. La prédation pourrait potentiellement être un
agent évolutif capable d’influencer l’évolution des signaux électriques, bien que cette hypothèse
n’a jamais été examinée sur le terrain. Le but de cette thèse est d’explorer différents moyens par
lesquels les prédateurs des poissons électriques influencent leurs signaux électriques. Le premier
chapitre présente une étude de terrain qui supporte l’hypothèse voulant que les prédateurs
puissent influencer l’évolution des signaux chez les poissons électriques. Dans le deuxième
chapitre, nous explorons les effets plus immédiats de la prédation. Des blessures caudales sont
fréquemment observées chez quelques espèces de poissons électriques, celles-ci étant
probablement causées par des attaques de prédateurs sublétales. Nous démontrons les effets de
cette prédation sublétale sur les signaux électriques et discutons ses implications pour les
poissons.
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ACKNOWLEDGEMENTS

I thank my second home, the Panamanian rainforest, and its inhabitants – the howler monkeys,
toucans, kingfishers and iguanas – for entertaining me while I collected data. I specifically do not
wish to thank the 14 snakes I encountered during the last 2 years. I thank the electric fish for
their patience and collaboration, with an honourable mention to fish #262.

The first human to thank is Rüdiger Krahe for his supervision, his support during (and also
before) my degree, and for allowing me to discover the wonderful world of electric fish in his
Animal Communication class. Aside from his academic support, he is an excellent and reliable
source of humour, sarcasm, and coffee in my life. I also thank my co-supervisors in Panama:
Luis Fernando de León, who was able to jump in on a short notice to give great advice, help me
on the field and allowing me to discover that empanada restaurant, and Biff Bermingham for his
insight and welcoming me at STRI. My committee members Andrew Hendry and Rachel Page
gave me great suggestions, which helped me focus my thesis. I am in debt to Sophie Picq, the
student who paved the way for my project with her own research on electric fish. Without
Rigoberto Gonzalez, his people skills, and his encyclopedic knowledge on freshwater fish, I
would still be driving around in Panama trying to find good field sites as you read this. Fernando
Alda and Gisela Ruth Reina trained me in the lab and on the field, transforming me from danger-
hazard to competent. I’m grateful to all the families and the Peña Bijagual community who
hosted me in the field and allowed me to camp in their backyard. Thank you previous and current
members of the Krahe, Bermingham and de León labs (special shout-out to Kerri-Lynn Ackerly).
Gracias también a mi compañero de oficina Felipe Dargent por ayudarme con mi análisis
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estadístico y mi español, et Vincent Fugère qui m’a aidé avec mon résumé de thèse. Thank you
family, roommates in the Jaula, friends, and everyone who helped and endured me in the field:
Kent Dunlap, Diana Sharpe, Eric Moody, Cassandra Wesseln, Gina Contolini, Celestino
Martinez, Ian Sharpe, Jan Benda, Haleh Fotowat, Jorge Molina, and last but definitively not
least, Claudia Atomei.

The research was supported by TAships and grants from Natural Sciences and Engineering
Research Council of Canada (NSERC) through Dr. Rüdiger Krahe, Fonds de recherche du
Québec – Nature et Technologies (FQRNT), Tomlinson Master’s Fellowship, GREAT Travel
Awards, NEO fellowship and the McGill University Biology Department.

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PREFACE

Thesis format
This thesis is submitted as a manuscript-based thesis, a compilation of publications of which I
am the lead author. Both chapters are independent articles, but are integrated by a general
introduction, linking statement and general conclusion.

Contribution of authors
Chapter I: Evidence for crypsis in electric signals.
Tran, A., de León, L.F., Bermingham, E. & Krahe, R.
Alex Tran designed and performed the experiments, analyzed the data and wrote the
manuscripts. Dr. Luís Fernando de León contributed to the data collection and reviewed the
manuscript. Dr. Eldredge Bermingham co-supervised the project. Dr. Rüdiger Krahe designed
the experiments, contributed to the data collection, wrote the MATLAB scripts for signal
analysis, reviewed the manuscript, provided funding for the research and co-supervised the
project.

Chapter II: Effects of tail loss and regeneration on electric fish signals.
Tran, A. & Krahe, R.
Alex Tran designed and performed the experiments, analyzed the data and wrote the
manuscripts. Dr. Rüdiger Krahe designed the experiments, contributed to the data collection,
wrote the MATLAB scripts for signal analysis, reviewed the manuscript, provided funding for
the research and supervised the project.
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GENERAL INTRODUCTION

There is an impressive range of signals within and across signal modalities in the animal
kingdom. Signals encode information about the sender, such as its reproductive fitness, resource
holding potential, or intent, but they can also reflect the physiological, physical, and
environmental constraints acting on signal design (Bradbury and Vehrencamp, 1998). Therefore,
by studying how animal signals change over time and in different contexts, biologists can infer
information about both the senders and the environment, such as the selective forces acting on
the animals and the direction of evolution (Endler, 1992; Endler, 2000).

Electric communication signals, produced by weakly electric fish (Gymnotiformes and
Mormyriformes), are excellent models to study the evolutionary forces acting on animals and
shaping signal design. These electric signals, also known as electric organ discharges (EODs),
are highly diverse across species of electric fish (Hopkins, 1981; Albert and Crampton, 2005),
yet they can be compared within and across species, since they are easily recorded and
quantified, and continuously produced (Turner et al., 2007). Unlike signals of other modalities,
EODs are also used by electric fish to navigate and locate prey (Moller, 1995). Electric fish do
this by using their electroreceptors to sense the distortions in their electric field, which are
produced when objects with electrical properties different than water approach them (Bullock et
al., 2005). They can also detect EODs produced by other fish and discriminate among EODs that
vary in measurable signal parameters such as firing rate, spectral properties, and pulse duration
(Bullock et al., 1972; Hopkins and Bass, 1981; Shumway and Zelick, 1988; McGregor and
Westby, 1992). Electric fish use some of these parameters for species recognition (Feulner et al.,
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2009; Fugère and Krahe, 2010), and because some parameters correlate with body size or
dominance (Hagedorn and Zelick, 1989; Fugère et al., 2011), they may be used to assess the
fitness and condition of potential mates (Curtis and Stoddard, 2003). Within an individual,
signals can also vary depending on the social context (Hagedorn and Zelick, 1989; Franchina et
al., 2001; Salazar and Stoddard, 2009; Gavassa et al., 2012), the environmental variables (Squire
and Moller, 1982; Dunlap et al., 2000) and the time of day (Hagedorn, 1995; Franchina and
Stoddard, 1998).

Electric fish bear an interesting constraint on the evolution of their signals. Because they rely on
EODs for both electrocommunication and electrolocation, there may be a compromise between
different selecting forces if, for example, the signal design for optimal mate recognition differs
from the one for optimal active sensing. The signal diversity observed in electric fish may thus
reflect the ecological specialization and diversification of species (Albert and Crampton, 2005).
Stoddard (2002) explored several potential evolutionary origins of signal complexity in EODs,
such as sexual selection, electrolocation, and species isolation. He found that crypsis from
electroreceptive predators had the best support as the main driving force behind signal
complexity, and proposed that this may have contributed to the diversity of electric fish signals
and species observed today.

It is widely accepted that predators exploit communication signals produced by their prey (Zuk
and Kolluru, 1998; Espmark et al., 2000; Peake, 2005). In some cases, predation can be an
important selective force driving the evolution of signals (Tuttle and Ryan, 1981; Belwood and
Morris, 1987; Endler, 1995; Briskie et al., 1999; Prohl et al., 2013). In the framework that
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Stoddard proposed, electroreceptive predators eavesdrop on the continuously produced EODs,
allowing them to locate and prey on the electric fish (Stoddard, 1999; Stoddard and Markham,
2008). When comparing signals from more basal electric fishes to signals from more derived
electric fishes, there is an increasing trend in signal peak frequency, and lab experiments have
shown that high signal peak frequencies are less detectable for electroreceptive predators
(Hanika and Kramer, 1999; Stoddard, 1999). There is also circumstantial field evidence that
supports this hypothesis: many gymnotiform electric fish producing signals with spectral
properties within the detection range of these predators are found with missing, damaged, or
regenerating tails (Hopkins et al., 1990; Picq, 2013; Sullivan et al., 2013). This is particularly
interesting because it also shows a second way in which predation, although sublethal, can affect
electric signals. In gymnotiforms, the electric organ is located in the tail of the fish, and if these
caudal injuries affect the production or shape of EODs, there could be major repercussions for
the fish.

In my thesis, I explore these two ways in which predators can affect electric fish signals. The
first chapter of my thesis explores signal evolution in weakly electric fish. Specifically, I tested
Stoddard’s hypothesis of signal evolution driven by electroreceptive predation in populations of
Brachyhypopomus occidentalis (Gymnotiformes: Hypopomidae). The spatial distribution of B.
occidentalis in Panama into discrete streams across independent drainages (Picq et al., 2014)
offers an ideal opportunity to observe the influences of natural variations in evolutionary forces
on electric signals. B. occidentalis, like its congeners, produces signals within the detection range
of electroreceptive predators (Peters and Buwalda, 1972; Stoddard, 1999), and is found with a
high occurrence of tail injuries (Picq, 2013), making them an excellent candidate to test this
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