the relative importance of population size, colonist quality, and colonist arrival frequency for ...

179 Pages·2017·3.07 MB·English

THE RELATIVE IMPORTANCE OF POPULATION SIZE, COLONIST
QUALITY, AND COLONIST ARRIVAL FREQUENCY FOR
POPULATION SUCCESS

by

James Stewart Sinclair

A thesis submitted to the Department of Biology
In conformity with the requirements for
the degree of Doctor of Philosophy

Queen’s University
Kingston, Ontario, Canada
February, 2018

Copyright © James Stewart Sinclair, 2018
Abstract
Colonization is a fundamental ecological process structuring populations, communities, and
ecosystems. Promoting, or preventing, colonization is also integral to solving applied ecological
problems, such as biocontrol, invasive species, community recovery, and conservation. Because of its
central role in many of the theory and applications of ecology, it is essential that we determine what
drives colonization success. One of the primary, and most commonly managed, factors influencing
colonist success is population size. Larger populations are more likely to colonize because they are less
vulnerable to the demographic, environmental, and genetic processes that can drive extinction. However,
there are other, less studied, factors that could also affect colonist success, such as the quality of colonists
or the frequency with which new individuals arrive, but we do not know their relative importance
compared to that of population size. This is a crucial piece of missing information necessary for
improving our understanding, and management, of the colonization process. I conducted three field
experiments that examined variation in the importance of multiple colonist characteristics for success in
new populations. The first investigated the relative importance of population size and arrival frequency in
introduced populations of Hemimysis anomala. The second investigated whether the relative importance
of population size, colonist quality, and arrival frequency varied between two zooplankton species
(Daphnia pulicaria and Skistodiaptomus oregonensis). The third experiment determined whether the
benefits of increasing colonist quantity and genetic diversity varied based on colonist identity. These
experiments showed that the value of colonist quantity, quality, arrival frequency, and/or genetic diversity
can depend upon the species and individuals involved. Additionally, I reviewed the mechanisms that drive
specific colonists to enter, survive, and exit from human vectors. Human-mediated dispersal is a common
driver of both intentional and unintentional colonization, and this review details how human-assisted
colonization is caused by the interplay between biological- (e.g. organism characteristics and their
abiotic/biotic interactions) and human-based (e.g. human movement ecology) processes.
ii
Co-Authorship
This thesis conforms to the publication format as outlined in the Department of Biology Guide to
Graduate Studies, with consolidated Acknowledgements and Literature Cited sections. The contributions
made by co-authors are outlined below:

Chapter 2 Dr. Shelley Arnott provided assistance with experimental design, interpretation of data
analysis, and manuscript preparation.

Chapter 3 Dr. Shelley Arnott provided assistance with experimental design, interpretation of data
analysis, and manuscript preparation.

Chapter 4 Dr. Shelley Arnott provided assistance with experimental design, interpretation of data
analysis, and manuscript preparation. Katie Millette performed clone genotyping, genetic analysis, and
assisted with manuscript preparation. Dr. Melania Cristescu provided assistance with experimental design
and manuscript preparation.

Chapter 5 Dr. Julie Lockwood edited the manuscript and wrote portions of it. Dr. Shelley Arnott
provided advice on framework design and edited the manuscript. Sarah Hasnain assisted with background
research and edited the manuscript.

Manuscripts directly from this thesis
Sinclair, J. S., and S. E. Arnott. 2016. Strength in size not numbers: propagule size more important than
number in sexually reproducing populations. Biological Invasions 18:497–505.
Sinclair, J. S., and S. E. Arnott. 2017. Relative importance of colonist quantity, quality, and arrival
frequency to the extinction of two zooplankton species. Oecologia 184:441–452.
iii
Sinclair, J. S., S. E. Arnott, K. L. Millette, and M. E. Cristescu. Colonist identity determines the benefits
of increased quantity and genetic diversity in the success of new Daphnia populations. Under review
for Ecology. Re-submitted with revisions on November 10th, 2017. #ECY17-1262
Sinclair, J. S., J. L. Lockwood, S. E. Arnott, and S. Hasnain. A framework for predicting which
individuals and species are introduced as non-natives. In prep.

Manuscripts from experiments conducted alongside thesis
Sinclair, J. S., S. E. Arnott, and A. Cox. 2016. The quick and the dead: copepods dominate as cladocerans
decline following invasion by Hemimysis anomala. Canadian Journal of Fisheries and Aquatic
Sciences 73:793–803.
Sinclair, J. S., and S. E. Arnott. Local context and connectivity determine the response of zooplankton
communities to salt contamination. In prep.

iv
Acknowledgements
A majority of this work was funded by the Ontario government and the Natural Sciences and Engineering
Research Council of Canada. My research would not have been possible without their financial support,
and that of the Canadian taxpayer.

I am also indebted to my co-authors, the members of the Arnott lab, and the faculty of the Department of
Biology at Queen’s University for their help, scientific advice, education, encouragement, and criticism
that has greatly improved my work. I would also like to thank my three field students, Amelia Cox, Emily
Drinkwater, and Kaitlyn Brougham, without whom my experiments would have failed spectacularly.

I am eternally grateful to my family, David, Evelyn, and Iain, and my partner, MJ. They haven’t read a
word of anything I’ve written, but they provided constant support and sincere attempts at interest along
the way.

Finally, none of this would have been remotely possible without my supervisor, Dr. Shelley Arnott. She
taught me how to ask the right questions and focus on the bigger picture. She will always be better at this
than I ever could be.
v
Table of Contents
Abstract ......................................................................................................................................................... ii
Co-Authorship.............................................................................................................................................. iii
Acknowledgements ....................................................................................................................................... v
List of Figures .............................................................................................................................................. ix
List of Tables ................................................................................................................................................ x
List of Abbreviations, Acronyms, and Symbols .......................................................................................... xi
Glossary ...................................................................................................................................................... xii
Chapter 1 General Introduction..................................................................................................................... 1
Colonization .............................................................................................................................................. 1
The colonization process ........................................................................................................................... 2
Drivers of success or failure in colonizing populations ............................................................................ 5
The importance of population size ............................................................................................................ 5
Colonist quality and arrival frequency ...................................................................................................... 7
Relative importance of colonizer characteristics ...................................................................................... 8
Research and chapter objectives ............................................................................................................. 10
Chapter 2 Strength in size not numbers – propagule size more important than number in sexually
reproducing populations .............................................................................................................................. 14
Abstract ................................................................................................................................................... 15
Introduction ............................................................................................................................................. 15
Methods .................................................................................................................................................. 18
Sampling protocol ............................................................................................................................... 20
Statistical analysis .............................................................................................................................. 20
Results ..................................................................................................................................................... 21
Discussion ............................................................................................................................................... 22
Implications ......................................................................................................................................... 25
Chapter 3 Relative importance of colonist quantity, quality, and arrival frequency to the extinction of two
zooplankton species .................................................................................................................................... 29
Abstract ................................................................................................................................................... 30
Introduction ............................................................................................................................................. 30
Methods .................................................................................................................................................. 34
Experiment 1 – Daphnia pulicaria ...................................................................................................... 37
Multiple additions ........................................................................................................................... 37
vi
Single additions ............................................................................................................................... 38
Experiment 2 – Skistodiaptomus oregonensis ..................................................................................... 38
Multiple additions ........................................................................................................................... 39
Single additions ............................................................................................................................... 39
Sampling protocol ............................................................................................................................... 40
Statistical analysis .............................................................................................................................. 41
Results ..................................................................................................................................................... 43
Experiment 1 – Daphnia pulicaria ...................................................................................................... 43
Experiment 2 – Skistodiaptomus oregonensis ..................................................................................... 44
Discussion ............................................................................................................................................... 44
Implications ......................................................................................................................................... 48
Chapter 4 Colonist identity determines the benefits of increased quantity and genetic diversity in the
success of new Daphnia populations .......................................................................................................... 55
Abstract ................................................................................................................................................... 56
Introduction ............................................................................................................................................. 56
Methods .................................................................................................................................................. 61
Life-history trials ................................................................................................................................ 62
Experiment .......................................................................................................................................... 62
Sampling protocol ............................................................................................................................... 64
Statistical analysis .............................................................................................................................. 65
Results ..................................................................................................................................................... 68
Effect of quantity on population success ............................................................................................. 68
Effect of genetic diversity on population success ................................................................................ 69
Correlations with source habitat characteristics and life-history traits ............................................. 69
Genotype persistence in high diversity populations ............................................................................ 70
Discussion ............................................................................................................................................... 71
Implications ......................................................................................................................................... 75
Chapter 5 A framework for predicting which individuals and species are introduced as non-natives ....... 82
Abstract ................................................................................................................................................... 83
Aim ..................................................................................................................................................... 83
Location .............................................................................................................................................. 83
Methods............................................................................................................................................... 83
Results ................................................................................................................................................. 83
Main conclusion .................................................................................................................................. 84
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Introduction ............................................................................................................................................. 84
An integrated framework for the pre-introduction invasion stages..................................................... 85
Part I – The biological processes that influence introduction ................................................................. 87
Uptake filter ........................................................................................................................................ 87
Survival filter ...................................................................................................................................... 88
Release filter ....................................................................................................................................... 89
The framework so far .......................................................................................................................... 90
Part II - human movement ecology ......................................................................................................... 90
Uptake filter ........................................................................................................................................ 92
Survival filter ...................................................................................................................................... 94
Release filter ....................................................................................................................................... 95
The framework so far, part II .............................................................................................................. 96
Using the framework ............................................................................................................................... 97
Example 1 – Intentional transport of pet reptiles, Fig. 5.5a ............................................................... 97
Biological processes ........................................................................................................................... 97
Human movement ecology .................................................................................................................. 98
Example 2 – Unintentional dispersal of plant seeds on clothing, Fig. 5.5b ....................................... 99
Biological processes ......................................................................................................................... 100
Human movement ecology ................................................................................................................ 100
Estimating introduction risk.............................................................................................................. 101
Conclusions ........................................................................................................................................... 103
Chapter 6 General Conclusions................................................................................................................. 110
Summary ............................................................................................................................................... 110
Implications and future directions......................................................................................................... 111
References ................................................................................................................................................. 113
Appendix A Lake characteristics, summary statistics, and temperature variability for Chapter 2 ........... 147
Appendix B Lake characteristics, summary statistics, and information on Daphnia abundance for Chapter
3 ................................................................................................................................................................ 152
Appendix C Lake characteristics, summary statistics, life-history methods, and genotyping methods for
Chapter 4 ................................................................................................................................................... 157

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List of Figures
Figure 1.1 The stages and barriers of the colonization process ................................................................... 4
Figure 1.2 Site and general layout of mesocosm experiments at the Queen’s University Biological Station
(QUBS) ....................................................................................................................................................... 11
Figure 2.1 Change in Hemimysis abundance with increasing propagule size across all sampling weeks for
populations divided over one, two, or four introduction events ................................................................. 27
Figure 2.2 Presence/absence of Hemimysis in the final sampling week .................................................... 28
Figure 3.1 Effects of the quality treatments and time on D. pulicaria density across all sampling weeks
for good and poor quality populations ........................................................................................................ 53
Figure 3.2 Effect of the quantity/frequency treatments on S. oregonensis density and presence/absence
from the final sampling week ..................................................................................................................... 54
Figure 4.1 Density of single Daphnia pulex genotypes and mixed genotype populations for introductions
of 1 colonist or 9 colonists at the conclusion of the experiment ................................................................. 79
Figure 4.2 Cliff’s δ for the treatment effects of quantity and genetic diversity within each genotype ...... 80
Figure 4.3 Relationships between the effect sizes of quantity and genetic diversity for each genotype and
their respective intrinsic rates of increase, mean body sizes at first reproduction, and habitat similarities 81
Figure 5.1 Stage- and filter-based invasion framework of the first three stages of the invasion process 105
Figure 5.2 Conceptual interaction between the biological processes and aspects of human movement
ecology that determine which individuals will successfully pass through the uptake, survival, and release
filters of the human mediated dispersal process ....................................................................................... 106
Figure 5.3 Propagule deposition patterns for two types of vectors that are interacting with the same
organism .................................................................................................................................................... 107
Figure 5.4 Hypothetical differences in propagule deposition patterns between ground versus air vectors
.................................................................................................................................................................. 108
Figure 5.5 High-risk profiles of the biological and human mechanisms that interact in the intentional
transport of pet reptiles and the unintentional dispersal of plant seeds on clothing .................................. 109

ix
List of Tables
Table 3.1 Experimental studies that have investigated the relative effects of colonist quantity, quality, or
frequency on the establishment and growth of new populations ................................................................ 50
Table 3.2 Schedule of experimental introductions for each treatment, with both species following the
same introduction schedule ......................................................................................................................... 51
Table 3.3 Minimum adequate model structure, statistical methodology, and descriptive statistics for
abundance and presence/absence models ................................................................................................... 52
Table 4.1 Origin and trait values from the 21-day life-history trials for each Daphnia pulex genotype
involved in the experiment .......................................................................................................................... 77
Table 4.2 Presence/absence of unique alleles for each Daphnia pulex genotype determined across 12
microsatellite loci in each high-diversity mesocosm, along with the proportion of all replicates in which
each genotype was determined to be present. ............................................................................................. 78

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