Variation in ecological impacts of invasive alien species

169 Pages·2015·1.31 MB·English

Variation in ecological impacts of invasive alien species

Josephine C. Iacarella

Department of Biology
McGill University
Montreal, QC, Canada

June 2015

A thesis submitted to McGill University
in partial fulfillment of the requirements of the degree of
Doctor of Philosophy

© Josephine C. Iacarella 2015
ACKNOWLEDGEMENTS
I would first like to thank my supervisor Anthony Ricciardi for his unfailing enthusiasm
for research. He taught me to look for the positive in what seemed to be set-backs, and facilitated
many amazing opportunities, including field work and conferences abroad. Jaimie Dick also
played an important role in my thesis, providing a tremendous amount of feedback on
experimental ideas and writing. I would also like to thank my committee members Lauren
Chapman and Gregor Fussmann for their many insightful comments and questions.
I would like to acknowledge the funding sources that contributed to my research and
international opportunities, including the Dr. Richard H. Tomlinson Award, the Canadian
Aquatic Invasive Species Network, the National Geography Young Explorer’s Grant, the Fumi
Takano Award on behalf of the International Federation of University Women and McGill travel
and research awards.
I thank my parents, Ann Iacarella and David Gilden, for teaching me to aim high and
for always believing in me, Franklin for being an awesome little brother and my extended family
for their support. I thank my friends, labmates and the biology graduate student community for
making this journey a happy one – particularly Aerin Jacob and Ahdia Hassan for always being
available to make me smile, and Morgan Boenke for providing encouragement and laughter
through the trials and tribulations of every last chapter. I dedicate this thesis to the memory of
Anton Pokhil and to my dear friends in Minneapolis.

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TABLE OF CONTENTS
ACKNOWLEDGEMENTS .................................................................................................................... i
TABLE OF CONTENTS ............................................................................................................. ii
LIST OF TABLES ...............................................................................................................................v
LIST OF FIGURES .................................................................................................................. vi
PREFACE ............................................................................................................................ viii
Thesis structure ...................................................................................................................... viii
Contribution of authors.......................................................................................................... viii
Original scholarship .............................................................................................................. viii
ABSTRACT ....................................................................................................................................... x
RÉSUMÉ ......................................................................................................................................... xi
GENERAL INTRODUCTION .............................................................................................................. 1
Impacts are context dependent ...................................................................................................1
Thesis outline .............................................................................................................................6
CHAPTER 1 ............................................................................................................................ 9
Ecological impacts of alien species along temperature gradients: testing the role of
environmental matching
Abstract ....................................................................................................................................10
Introduction..............................................................................................................................11
Methods ....................................................................................................................................14
Results ......................................................................................................................................21
Discussion ................................................................................................................................23
Acknowledgements ...................................................................................................................32
CONNECTING STATEMENT 1-2 ......................................................................................................33
CHAPTER 2 .....................................................................................................................................34
Dissolved ions mediate the growth and predatory response of an invasive fish
Abstract ....................................................................................................................................35
Introduction..............................................................................................................................36
Methods ....................................................................................................................................38
Results ......................................................................................................................................42
Discussion ................................................................................................................................43
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Acknowledgements ...................................................................................................................50
CONNECTING STATEMENT 2-3 ......................................................................................................51
CHAPTER 3 .....................................................................................................................................52
A spatio-temporal contrast of the predatory impact of an invasive freshwater crustacean
Abstract ....................................................................................................................................53
Introduction..............................................................................................................................55
Methods ....................................................................................................................................59
Results ......................................................................................................................................64
Discussion ................................................................................................................................69
Acknowledgements ...................................................................................................................74
CONNECTING STATEMENT 3-4 ......................................................................................................75
CHAPTER 4 .....................................................................................................................................76
Negative competitive effects of invasive plants change with time since invasion
Abstract ....................................................................................................................................77
Introduction..............................................................................................................................78
Methods ....................................................................................................................................80
Results ......................................................................................................................................85
Discussion ................................................................................................................................86
Acknowledgements ...................................................................................................................91
CONNECTING STATEMENT 4-5 ......................................................................................................92
CHAPTER 5 .....................................................................................................................................93
Predatory behaviour of an invasive amphipod in response to the presence of conspecifics
and predation risk
Abstract ....................................................................................................................................94
Introduction..............................................................................................................................95
Methods ....................................................................................................................................97
Results ....................................................................................................................................102
Discussion ..............................................................................................................................103
Acknowledgements .................................................................................................................110
FINAL CONCLUSIONS AND FUTURE RESEARCH ..........................................................................112
REFERENCES ................................................................................................................................115
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APPENDICES .................................................................................................................................139
Appendix A. Details of the studies and data included in the meta-analysis on alien freshwater
crustacean and fish impacts (Chapter 1) ................................................................................139
Appendix B. Details of the studies and data included in the meta-analysis on competitive
effects of invasive terrestrial plants (Chapter 2) ....................................................................149

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LIST OF TABLES
CHAPTER 1
TABLE 1. Studies indicating alien species have higher impacts in environmental conditions for
which they are evolutionarily adapted ...........................................................................................27
CHAPTER 2
TABLE 1. Functional responses (FR) of Round Gobies in high and low acclimation and FR
calcium concentrations…………………………………………………………………………..45
CHAPTER 3
TABLE 1. Tests of traits of invasive animals along temporal invasion gradients showing physical
and behavioural differences ...........................................................................................................56
TABLE 2. Functional responses of H. anomala from invasion front and well-established sites in
Ireland ............................................................................................................................................67
TABLE 3. Prey selection of invasion front and well-established H. anomala when preying on
zooplankton at both sites ............................................................................................................................. 68
CHAPTER 4
TABLE 1. Model values for the best fit model and separate main effect models ...........................87
TABLE 2. Studies that have tested the effect of time since invasion on impacts of invasive species
across their invaded ranges ............................................................................................................90
APPENDICES
TABLE A1. Impact and thermal optima data for 16 alien species that directly impact native
populations through predation or herbivory in inland water systems ..........................................139
TABLE B1. Impact and time since invasion data for 36 invasive terrestrial plants within 27 studies
on competition with native plants ................................................................................................149
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LIST OF FIGURES
GENERAL INTRODUCTION
FIGURE 1. Hypothesized causal links between the attributes of an invader, the context of invasion
and the ecological impact of an invader ..........................................................................................3
CHAPTER 1
FIGURE 1. Ecological impacts (negative log response ratios) of alien species decline significantly
with an increasing absolute difference between their thermal optima and ambient study
temperatures ...................................................................................................................................22
FIGURE 2. Functional responses of Hemimysis anomala from 5-28°C and Mysis diluviana from
5-15°C on Daphnia pulex ..............................................................................................................24
FIGURE 3. Maximum feeding rates of Hemimysis anomala and Mysis diluviana along
temperature gradients .....................................................................................................................25
CHAPTER 2
FIGURE 1. Round Gobies consumed significantly more shrimp pellets during the high-calcium
concentration ([Ca]) acclimation treatment than fish in the low-[Ca] treatment ...........................44
FIGURE 2. Round Gobies in high-calcium concentration ([Ca]) acclimation and functional
response treatments gained more mass than fish in only low-[Ca] treatments ..............................44
FIGURE 3. Round Gobies had the highest predatory impact on amphipod prey in high-calcium
concentration functional response treatments ................................................................................45
FIGURE 4. Type II functional response curves of Round Gobies on amphipod and mayfly nymph
prey ................................................................................................................................................46
CHAPTER 3
FIGURE 1. Sites along an invasion gradient of Hemimysis anomala in Ireland .............................60
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FIGURE 2. Predation rates of invasion front and well-established H. anomala at zooplankton
densities across invasion front and well-established sites and experimental nights ......................66
FIGURE 3. Type II functional responses on Daphnia magna for invasion front and well-
established H. anomala ..................................................................................................................67
FIGURE 4. Rarefaction curves of Simpson’s diversity index for zooplankton in Ireland ...............68
CHAPTER 4
FIGURE 1. Negative competitive effects (log response ratios) of invasive terrestrial and forbs,
herbs and shrubs declined with time since invasion across invaded ranges ..................................87
Chapter 5
FIGURE 1. Map of sites surveyed from Lough Neagh to the Atlantic Ocean along the Bann River
in Northern Ireland .........................................................................................................................98
FIGURE 2. Per capita predation rates of Gammarus pulex on dipteran larvae were higher in the
presence of conspecifics in field microcosms and in lab experiments ........................................105
FIGURE 3. With increasing group size, the time Gammarus pulex spent swimming declined and
time spent interacting increased ...................................................................................................105
FIGURE 4. Fish presence in field experiments reduced per capita predation rates of Gammarus
pulex .............................................................................................................................................106
FIGURE 5. Gammarus pulex had lower predation rates at the Salterstown R. site than at the Bann
R. site in field microcosm experiments........................................................................................106

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PREFACE
Thesis structure
This thesis is written in manuscript-based format, following McGill University’s
regulations. All chapters are in review or published in peer-reviewed scientific journals: Chapter
1 is published in Ecological Applications, Chapter 2 is in review with Biological Invasions,
Chapter 3 is in press with Diversity and Distributions, Chapter 4 is in press with Ecosphere and
Chapter 5 is in preparation. The thesis is formatted in the style of the scientific journal Ecology.

Contribution of authors
The research was conceived of in collaboration with Anthony Ricciardi and Jaimie
Dick. I led all experiments, analyses and writing. Research conducted in the U.K. and Ireland
was supported logistically by Jaimie Dick’s lab at Queen’s University Belfast. Undergraduate
(independent study) students, Phoebe Mankiewicz and Emma Hudgins, conducted analysis under
my supervision that contributed to Chapters 4 and 5. Mhairi Alexander aided in the statistical
analysis of functional response curves used in Chapter 1. Fish used in the U.K. were handled by
Gillian Riddel and Rachel Paterson (Chapter 5), whereas all other animals were handled by me
following animal use protocols.

Original scholarship
My thesis tests two novel hypotheses, the Environmental Matching Hypothesis
(proposed by Ricciardi et al. 2013) and the Invasion Front Hypothesis, to better understand how
impacts of alien species vary across invasion contexts. Neither hypothesis has been explicitly
tested before. Here, I find support for both hypotheses. In the first meta-analytical test of the
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Environmental Matching Hypothesis, I show that high consumptive impacts are more likely to
arise from a closer match between ambient physico-chemical conditions and the invader’s
growth optimum. Testing the Invasion Front Hypothesis both experimentally and through meta-
analysis, I find that consumptive and competitive effects of invasive species decline with time
since invasion.
Adopting a mechanistic approach to assessing the effect of biotic interactions on
predatory impacts, I find that per capita predation rates and consumption times are affected by
the presence of conspecifics and predation-risk cue; predatory behaviour is rarely assessed at this
scale, and behavioural responses are often inferred. My research also provides the first
demonstration of the impacts of a potential global invader, the crustacean Hemimysis anomala,
in a natural waterbody. Finally, in collaboration with Jaimie Dick’s lab at Queen’s University
Belfast, I develop functional response analysis as a tool for comparing impacts of alien species
across abiotic and biotic gradients.

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