SONAR JAMMING IN THE BAT-MOTH ARMS RACE BY AARON J. CORCORAN A Dissertation ...

185 Pages·2013·3.6 MB·English

SONAR JAMMING IN THE BAT-MOTH ARMS RACE
BY
AARON J. CORCORAN
A Dissertation Submitted to the Graduate Faculty of
WAKE FOREST UNIVERSITY GRADUATE SCHOOL OF ARTS AND SCIENCES
in Partial Fulfillment of the Requirements
for the Degree of
DOCTOR OF PHILOSOPHY
Biology
May, 2013
Winston-Salem, North Carolina
Approved By:
William E. Conner, Ph.D., Advisor
Nickolay Hristov, Ph.D., Chair
Miriam Ashley-Ross, Ph.D.
Robert Browne, Ph.D.
Susan Fahrbach, Ph.D.
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DEDICATION
To the late James Fullard, the primary proponent of the jamming hypothesis. You meant
so much to me, despite our brief acquaintance.
iii
ACKNOWLEDGEMENTS
To say thank you is not nearly enough for the numerous people who have inspired
me, taught me, challenged my thinking repeatedly in the kindest of ways, and worked by
my side night after night until the sun rose. But here I attempt to do just that.
First, I thank Dr. William ((cid:147)Bill(cid:148)) Conner, my academic advisor and mentor over
the last five years. You taught me what it means to be a scientist in the most complete
sense of the word. Somehow you always knew when to give me a push and when to let
me find my own way (usually the latter). I know few people with your breadth of
knowledge from genes to neurons to behaviors to ecosystems and more. And you have an
uncanny ability to relate that knowledge to your students whether in the classroom or
one-on-one. You taught me how to simplify a problem into its constituent parts and
dissect it experimentally with the skill of a surgeon. Your door was always wide open,
literally and figuratively and you treated me as a friend and colleague from day one.
I thank my academic committee (cid:150) Drs. Miram Ashley-Ross, Robert Browne,
Susan Fahrbach, and Nickolay Hristov (cid:150) for pushing my boundaries as a scientist. I must
also thank my master(cid:146)s advisor, Dr. Joe Szewczak, for sharing his love of bats with me;
my brothers Dan and Tim Corcoran and Tom Brown Jr. for inspiring in me a love of all
things wild; and my mom and dad for teaching me to always follow my heart and for
unending faith that I would find my path in life. I thank my wife, Lauren, for keeping me
grounded and humble through this journey.
Many others contributed directly to my research. Dr. Jesse Barber and Dr.
Nickolay Hristov, my academic elder brothers, set the stage for this work with their
ground-breaking studies on bats and moths. They also selflessly helped me at every turn,
be that training me how to care for and raise baby bats, how to use high-speed cameras or
develop 3-D models, or whatever the moment demanded. I had five extraordinary Wake
Forest undergraduate researchers (cid:150) Megan Cullen, Wesley Johnson, Ryan Wagner,
Zachary Walker, and Kaitlyn Roman (cid:150) work with me over the summers at Wake and in
southern Arizona. I could not have asked for a harder working or more insightful and
intelligent group to work with than you. I am especially thankful to Ryan Wagner, whose
exceptional devotion to the project led to chapter five of this dissertation. My good
friends Jean-Paul Kennedy and Nick Dowdy also worked with me in the field in Arizona
and your companionship and dedication made all the difference, especially on those
nights when everything seemed to go wrong and all there was left to do was crack open a
beer and watch the sun rise.
I am also especially grateful to the staff, interns and fellow researchers at the
Southwestern Research Station where I spent four summers studying bats and moths.
There are too many of you to name here, but your help and comradery brought me joy as
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much as did the charismatic bats and moths I got to know so well. Several people also
helped with the many technological challenges of this work. Most notably, Jeff Muday
was always at hand to fix a computer glitch, or even build a new computer. Mark Jenson
built a custom microphone to specification for chapter five; Manfred Berger provided
assistance with his Maxtraq software and Brad Chadwell graciously provided computer
code and gave me lessons on 3D Geometry. Finally, I must thank Mindy Conner, who
graciously edited many of the pages of this work. Of course any errors left here are mine
alone.
Chapter-specific acknowledgements
Chapter II -- I thank F. Insana and the staff of the Southwestern Research Station for
assistance collecting B. trigona; M. Cullen for providing bat care and training; N. Hristov
and J. Muday for technical assistance; and B. Chadwell for software. M. Conner, J.-N.
Jasmin, T. Eisner, and the Wake Forest University ecology group provided editorial
comments. Funding for research was provided by National Science Foundation Grant
IOB-0615164 to W.E.C. and a W.F.U. Dean(cid:146)s Fellowship to A.J.C.
CHAPTER III (cid:150) I am most grateful to Frank Insana, Jeff Paull, and the staff of the
Southwestern Research Station for assistance collecting B. trigona; Megan Cullen for bat
care; Jeff Muday for technical support; and Brad Chadwell for software development.
Two anonymous reviewers provided several insightful and constructive comments.
Funding was provided by grant #IOB-0615164 to W. E. C. by the National Science
Foundation.
CHAPTER IV -- I thank Wesley Johnson, Ryan Wagner, Zachary Walker, Jean-Paul
Kennedy, Nick Dowdy and several Southwestern Research Station interns for assistance
in the field. Brad Chadwell provided software for 3-D calculations. Nickolay Hristov
helped develop our field recording setup. Jeff Muday provided technical assistance, and
the staff of the Southwestern Research Station provided valuable logistical support.
Melinda Conner edited the manuscript, and two anonymous reviewers provided
numerous valuable comments.
CHAPTER V -- I thank the staff and interns of the Southwestern Research Station of the
American Museum of Natural History for logistical support. Dr. Bradley Chadwell
provided software for 3-D analysis. Jeffrey Muday provided technical computing support.
Funding was provided by National Science Foundation grant number IOS-0615164 and
IOS-0951160 to W. E. C.
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TABLE OF CONTENTS
Page
DEDICATION .................................................................................................................... ii
ACKNOWLEDGEMENTS ............................................................................................... iii
LIST OF FIGURES ......................................................................................................... viii
LIST OF TABLES ............................................................................................................. xi
ABSTRACT ...................................................................................................................... xii
CHAPTER I
Bats and tiger moths: an introduction ......................................................................1
CHAPTER II
Tiger moth jams bat sonar
Published in Science (2009)
ABSTRACT ...............................................................................................17
INTRODUCTION .....................................................................................18
METHODS ................................................................................................20
RESULTS/DISCUSSION..........................................................................21
REFERENCES AND NOTES ...................................................................24
SUPPORTING MATERIAL .....................................................................29
CHAPTER III
How do tiger moths jam bat sonar?
Published in Journal of Experimental Biology (2011)
ABSTRACT ...............................................................................................42
INTRODUCTION .....................................................................................43
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MATERIALS AND METHODS ...............................................................46
RESULTS ..................................................................................................53
DISCUSSION ............................................................................................58
CONCLUSION ..........................................................................................64
REFERENCES ..........................................................................................66
CHAPTER IV
Sonar jamming in the field: Effectiveness and behavior of a unique prey defense
Published in Journal of Experimental Biology (2012)
ABSTRACT ...............................................................................................83
INTRODUCTION .....................................................................................84
MATERIALS AND METHODS ...............................................................87
RESULTS ..................................................................................................93
DISCUSSION ............................................................................................96
CONCLUSION ........................................................................................105
REFERENCES ........................................................................................108
CHAPTER V
Optimal predator risk assessment by the sonar-jamming moth Bertholdia trigona
ABSTRACT .............................................................................................125
INTRODUCTION ...................................................................................126
MATERIALS AND METHODS .............................................................131
RESULTS ................................................................................................139
DISCUSSION ..........................................................................................143
REFERENCES ........................................................................................149
vii
CONCLUSIONS AND FUTURE DIRECTIONS...........................................................165
CURRICULUM VITAE ..................................................................................................169
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LIST OF FIGURES
CHAPTER I
Figure 1.1 Spectrogram of an echolocation attack sequence of a Myotis bat .............15
CHAPTER II
Figure 2.1 Jamming acoustic complex ........................................................................26
Figure 2.2 Predicted and observed success rates for Eptesicus fuscus attacking moths
using various defensive strategies. ............................................................27
Figure 2.3 Example echolocation attack sequence of a bat being jammed by
Bertholdia trigona .....................................................................................28
Figure 2.S1 Attack persistence of Eptesicus fuscus on clicking moths through
successive foraging nights .........................................................................36
Figure 2.S2 Oscillogram of a Bertholdia trigona click modulation cycle. ...................37
CHAPTER III
Figure 3.1 Diagram illustrating bat flight parameters. ................................................72
Figure 3.2 Example pulse interval graph of a big brown bat unsuccessfully attacking
a sonar-jamming moth. ..............................................................................73
Figure 3.3 Oscillograms, spectrograms and power spectra of an approach phase
echolocation call of a big brown bat (Eptesicus fuscus) and two
overlapping click modulation cycles of Bertholdia trigona. .....................74
Figure 3.4 Three categories of bat behavioral responses to moth clicks, as illustrated
by bat flight and echolocation behavior. ....................................................75
Figure 3.5 The distribution of bat responses to moth jamming changed after the first
two nights of the experiment......................................................................76
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Figure 3.6 Spectrograms of three attacks on silent control or clicking experimental
moths. .........................................................................................................77
Figure 3.7 Simulations of competing hypotheses of sonar-jamming mechanisms .....79
CHAPTER IV
Figure 4.1 Diagram of field recording setup .............................................................115
Figure 4.2 Ethogram showing results of bats attacking clicking and silenced
Bertholdia trigona. ...................................................................................116
Figure 4.3 Three-dimensional flight trajectories of bats attacking clicking, and
silenced Bertholdia trigona exhibiting defensive maneuvers. .................117
Figure 4.4 Percentage of bat attacks in which Bertholdia trigona exhibited defensive
behaviors, and bat capture rates on moths exhibiting different
combinations of behaviors .......................................................................118
Figure 4.5 Percentage of moths diving, and captured by bats relative to moth distance
from a light source. ..................................................................................119
Figure 4.6 Box plots of bat-moth distances and bat echolocation pulse intervals at the
initiation of Bertholdia trigona defenses and bat approaching behavior .120
Figure 4.7 Directionality of Bertholdia trigona diving behavior in response to bat
attack ........................................................................................................121
Figure 4.8 Cross-species comparison of the effectiveness of insect defenses at
preventing capture by bats. ......................................................................122
CHAPTER V
Figure 5.1 Hypothesized predator risk level as it relates to predation stage .............156
Figure 5.2 Three-dimensional simulation of the sonar beam of a bat attacking a moth,
and a spectrogram of the bat echolocation sequence with two-dimensional
plots of the bat(cid:146)s echolocation beam shape and direction relative to the
target ........................................................................................................157
x
Figure 5.3 Three-dimensional schematic of field setup for recording bat attacks on
tethered and free-flying moths .................................................................158
Figure 5.4 Acoustic and kinematic characterization of (cid:147)real(cid:148) and (cid:147)false(cid:148) threats ....159
Figure 5.5 Predicted and actual clicking thresholds for different bat echolocation
pulse-intervals in Bertholdia trigona .......................................................161
Figure 5.6 Discrimination of bat passes that did or did not elicit clicking by tethered
Bertholdia trigona in the field. ................................................................162
Figure 5.7 Cost-benefit models of escape behavior with varying prey knowledge of
predator attack stage ................................................................................164