THE EVOLUTIONARY ECOLOGY OF INTRASPECIFIC TRAIT VARIATION IN LARVAL AMPHIBIANS

135 Pages·2014·1.38 MB·English

by  Brad Carlson

The Pennsylvania State University
The Graduate School
Intercollege Graduate Degree Program in Ecology

THE EVOLUTIONARY ECOLOGY OF INTRASPECIFIC TRAIT VARIATION
IN LARVAL AMPHIBIANS

A Dissertation in
Ecology
by
Bradley E. Carlson

© 2014 Bradley E. Carlson

Submitted in Partial Fulfillment
of the Requirements
for the Degree of

Doctor of Philosophy

May 2014
The dissertation of Bradley E. Carlson was reviewed and approved* by the following:

Tracy Langkilde
Associate Professor of Biology
Dissertation Advisor, Chair of Committee

Victoria Braithwaite
Professor of Fisheries and Biology

James Marden
Professor of Biology

John Tooker
Assistant Professor of Entomology

Durland Shumway
Research Associate and Faculty Consultant of Statistics

David Eissenstat
Professor of Woody Plant Physiology
Chair, Intercollege Graduate Degree Program in Ecology

*Signatures are on file in the Graduate School
ii
ABSTRACT

Individual organisms of the same species can differ from each other in a variety of
phenotypic traits (“intraspecific trait variation”), a phenomenon that is increasingly
understood to impact our understanding of natural ecological systems. Behavior is often a
particularly variable trait and is important for mediating the interactions of animals with
their environment. In this dissertation, I used tadpoles as a system to explore two general
questions: why do conspecifics differ in behavior, and what are the ecological
implications of behavioral variation? I characterized consistent individual differences in
behavior in tadpoles, and found that experimental artifacts (marking effects), hunger, and
population of origin all influence tadpole behavior. Counterintuitively, individual
differences in boldness didn’t impact survival of predation. Antipredator responses of
tadpoles in simulated ponds apparently increased the abundance of their resources but,
unexpectedly, differences in behavior between populations did not alter the strength of
this ecological impact. Together, these findings reveal multiple factors influencing
behavioral variation and demonstrate the complexity of the impacts of behavioral
diversity on ecological interactions.
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TABLE OF CONTENTS

List of figures ........................................................................................................ vi
List of tables ...................................................................................................... viii
Acknowledgements ................................................................................................ ix

Chapter 1. INTRODUCTION ..................................................................................1
Thesis overview ...............................................................................1
References ........................................................................................3

Chapter 2. PERSONALITY TRAITS ARE EXPRESSED IN BULLFROG TADPOLES
DURING OPEN-FIELD TRIALS ...........................................................................5
Abstract ............................................................................................5
Introduction ......................................................................................5
Methods............................................................................................7
Results ............................................................................................12
Discussion ......................................................................................12
References ......................................................................................17
Tables & Figures ............................................................................22

Chapter 3. A COMMON MARKING TECHNIQUE AFFECTS TADPOLE BEHAVIOR
AND PREDATION RISK .....................................................................................24
Abstract ..........................................................................................24
Introduction ....................................................................................24
Methods..........................................................................................28
Results ............................................................................................34
Discussion ......................................................................................35
References ......................................................................................40
Tables & Figures ............................................................................46

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Chapter 4. NO EVIDENCE OF SELECTION BY PREDATORS ON TADPOLE
BOLDNESS ........................................................................................................48
Abstract ..........................................................................................48
Introduction ....................................................................................48
Methods..........................................................................................52
Results ............................................................................................60
Discussion ......................................................................................61
References ......................................................................................65
Tables & Figures ............................................................................71

Chapter 5. FOOD OR FEAR: HUNGER MODIFIES RESPONSES TO ALARM CUES
IN TADPOLES ......................................................................................................77
Abstract ..........................................................................................77
Introduction ....................................................................................77
Methods..........................................................................................79
Results ............................................................................................82
Discussion ......................................................................................83
References ......................................................................................88
Tables & Figures ............................................................................94

Chapter 6. PREDATION RISK IN TADPOLE POPULATIONS SHAPES
BEHAVIOURAL RESPONSES OF PREY BUT NOT STRENGTH OF TRAIT-
MEDIATED INDIRECT INTERACTIONS .........................................................98
Abstract ..........................................................................................98
Introduction ....................................................................................98
Methods........................................................................................101
Results ..........................................................................................107
Discussion ....................................................................................108
References ....................................................................................114
Tables & Figures ..........................................................................118
Appendix ......................................................................................................123
v
LIST OF FIGURES

Figure 2.1. Individual bullfrog tadpole behavioral scores for activity (A), boldness (B),
and exploration (C). Points and lines depict means ± one standard error.
........................................................................................................23
Figure 3.1. Effects of marking with methylene blue and olfactory cues from predators
(newts and dragonflies combined) on tadpole (A) activity, (B) distance
moved, (C) speed of movement, and (D) avoidance. C = control (baseline)
conditions, P = after addition of predator cues ..............................47
Figure 4.1. Diagram of experimental setups for a) assaying behavior in an open-field,
and b) predator selection trials. ......................................................73
Figure 4.2. Distributions of behavioral scores for a) activity level in the absence and b)
presence of predator cues, and c) avoidance of predator cues. Activity
levels represent the number of observations (out of 30) in which tadpoles
were observed moving, while low numbers indicate avoidance of the
predator cues. .................................................................................74
Figure 4.3. Distribution of durations of predator selection trials used in the analyses.
Trials were terminated when one tadpole was captured or eaten. .75
Figure 4.4. Relationships between survival of focal tadpoles in predation trials and
relative differences in boldness-related behavior between the focal tadpole
and the conspecific with which it was paired during a trial. Behaviors are
a) activity level in the presence of predator cues, b) responsiveness
(change in activity after adding predator cues), and c) spatial avoidance of
predator cues. .................................................................................76
Figure 5.1. Test arenas used for measuring responses of tadpoles to injured or uninjured
conspecific cues. ............................................................................96
Figure 5.2. Effects of hunger status (fed vs. unfed) and cue type (uninjured vs. injured
conspecifics) on a) activity levels and b) attraction to the cue (mean zone
location, with lower values indicating avoidance of the cue). .......97
Figure 6.1. Population mean visibility (± 1 SE) of tadpoles in mesocosms and predation
risk index (PRI) in source ponds. Open circles indicate control (predator-
vi
free) mesocosms and closed circles indicate mesocosms with caged (non-
lethal) larval dragonfly predators. Lines represent fitted relationships using
GLMMs with Poisson error distributions; the slope was only significantly
different from 0 in predator mesocosms. .....................................119
Figure 6.2. Population mean movement rates (± 1 SE) of visible tadpoles plotted against
predation risk index (PRI) in population source ponds (open circles =
control mesocosms, and closed circles = predator-treated mesocosms).
Lines are GLMM fitted relationships (both non-significant), and the
vertical axis (counts of moving tadpoles) is presented on a logarithmic
scale..............................................................................................120
Figure 6.3. The percent difference in periphyton dry biomass in predator mesocosms
(compared to control mesocosms with tadpoles from the same population)
in relationship to a) the percent difference in tadpole visibility in predator
compared to control mesocosms, b) the percent difference in number of
visible tadpoles that are moving, and c) the source pond PRI of tadpoles
from that population ....................................................................121
Figure 6.4. Periphyton biomass and a) the proportion of tadpoles visible and b) the
proportion of visible tadpoles moving across all mesocosms. Open circles
and closed circles indicate control and predator-treated mesocosms,
respectively. Activity levels are mesocosm means, averaged across five
observations. ................................................................................122
vii
LIST OF TABLES

Table 4.1. Summary of logistic regression models predicting survival of the unmarked
tadpoles. ‘Behavior’ includes all three measures of boldness (activity,
responsiveness, and avoidance). All statistical tests are likelihood ratio
tests (LRT) comparing fitted models to either a null model (to evaluate
overall significance of all parameters) or Model 1 (to test marginal
improvement in fit over the reduced model). .................................71
Table 5.1. Effects of hunger status (fed or unfed), cue type (uninjured or injured
conspecific), and block on wood frog tadpole a) activity and b) attraction
to cue ..............................................................................................94
Supplementary Table 2.1. Summary of statistical analyses of bullfrog tadpole
personality traits. Analyses were conducted as ANCOVAs with a random
intercept for tadpole identity, fit as linear mixed models with the lmer
function in the R package “lme4”. Tests were conducted as likelihood
ratio tests comparing nested models that differed only in the presence of
the tested predictor variable .........................................................123
Supplementary Table 3.1 Summary of statistical analyses of marking effects on tadpole
behavior. Analyses were conducted as ANOVAs with cue treatment
effects nested within individual tadpoles. ....................................124
Supplementary Table 6.1. Summary of analyses of effects of predation risk on tadpole
behavior. Values are derived from generalized linear mixed models fit
with quasi-Poisson distributions. .................................................125

viii
ACKNOWLEDGEMENTS

First, I am grateful to my advisor, Tracy Langkilde, who has provided
support to me in innumerable ways over the past 5 years. She has guided me in
developing interesting questions, energized me with her enthusiasm, sharpened my
writing, and served as a therapist when things went awry. She has been a mentor, role
model, and friend, and a critical element of my positive experience in graduate school. I
also thank my committee members for all their contributions. Victoria Braithwaite
provided keen insights into behavioral biology and an invaluable teaching experience.
Jim Marden and John Tooker stretched my thinking with their perspectives, challenging
me to examine key questions and place my work in a much larger context. Durland
Shumway graciously offered his time to helping me earn a statistics minor and introduced
me to statistical ideas that I will carry with me for many years.
Sigma Xi, the American Society of Ichthyologists and Herpetologists, the
Animal Behavior Society, and the NSF all contributed funding to my work, and I
couldn’t have done it without their generosity. Thanks also to the Ecology Program and
Biology Department, which provided many forms of support – from funding to helping
with paperwork. The camaraderie and help of other graduate students, and especially of
the Langkilde Lab, will always be treasured. Lindsey, Renee, Jenny, Kelly, Chris, Gail,
Travis, and Sean – it’s been a pleasure teaming up with all of you on both projects and
hijinks. Numerous undergraduate students provided help at various times and though
space doesn’t permit naming individuals, I have appreciated each of them.
Finally, I thank my parents for all their love and support, both currently
and as a child when I was first catching frogs and conducting “experiments” with cooking
supplies. To my in-laws, I am grateful for all their encouragement and interest in my
work. Most of all, I thank my wife, Gwen, and daughter, Nora, for being there for me,
making me smile, and giving me a reason to work hard.
ix
Chapter 1: INTRODUCTION

Thesis overview
It is readily apparent that individual organisms of the same species often differ
from each other in size, morphology, physiology, behavior, life history, and other traits.
This has been recognized at least since the formulation of the theory of evolution by
natural selection (Darwin 1859), which depends on substantive phenotypic variation
within species to operate. As expected given the significance of phenotypic differences
for evolutionary fitness, variable traits often mediate ecological interactions, resulting in
a diversity of ecological impacts and niches within species (Bolnick et al. 2003).
Accordingly, a growing body of evidence demonstrates that phenotypic differences
between populations, among individuals, and within individuals (over time) have
important consequences for communities and ecological processes (Bolnick et al. 2011,
Bassar et al. 2010), with impacts on areas of applied interest such as agriculture (Tooker
and Frank 2012) and conservation (Forsman 2014). Recognition of the ecological
significance of “intraspecific trait variation” (Bolnick et al. 2011) necessitates a more
expansive approach to ecology, in which phenotypic and genetic variation within species
is incorporated into the well-established research program on the origins and impacts of
biodiversity at the species level (Hughes et al. 2008).
Behavior is especially variable in animals. Recent research has uncovered
substantial within-species diversity in basic behavioral traits such as activity levels,
boldness, and sociality, with consistent individual differences in these traits variously
considered “personality” (Gosling 2001), “temperament” (Réale et al. 2007), or
“behavioral syndromes” (Sih et al. 2004b). As with studies of intraspecific trait variation
in general, a deeper recognition of the variation that surrounds the “average” behavioral
phenotype has presented exciting new challenges for ecologists. Two key issues are how
ecological interactions shape production of diverse behaviors (both by processes acting
over evolutionary time and within generations; Dall et al. 2004), and consequences of
behavioral diversity for ecological processes in complex communities (Sih et al. 2012,
Sih et al. 2004a, Wolf and Weissing 2012).