I also express my deep love and gratitude for my sons---Matthew, Jacob, and Daniel. ...... macrophytes of Lake Vechten: structural and functional relationships.
HUMAN-MEDIATED DISPERSAL OF AQUATIC NONINDIGENOUS SPECIES: IMPACTS AND INTERVENTIONS
A Dissertation
Submitted to the Graduate School of the University of Notre Dame in Partial Fulfillment of the Requirements for the Degree of
Doctor of Philosophy by John D. Rothlisberger
David M. Lodge, Director
Graduate Program in Biological Sciences Notre Dame, Indiana August 2009
HUMAN-MEDIATED DISPERSAL OF AQUATIC NONINDIGENOUS SPECIES: IMPACTS AND INTERVENTIONS
Abstract by John D. Rothlisberger
The introduction and establishment of species beyond the boundaries of their native ranges is an environmental issue of increasing scope and seriousness. This dissertation examines the consequences of the establishment of aquatic nonindigenous species (NIS) in the Laurentian Great Lakes (GL) region and also investigates alternatives for reducing anthropogenic spread of nuisance aquatic NIS. I first investigate the pathways by which aquatic NIS are introduced to the GL to learn if introduction pathway is related to where species originate and how likely they are to have spread beyond the GL basin. My analysis shows that ballast water release is highly likely to introduce new aquatic NIS to North America, whereas unauthorized release of organisms in trade tends to introduce to the GL aquatic NIS already established in North America. Moreover, it appears that it is primarily a matter of time before novel NIS that become established in the GL appear in other North American waterways. I also consider the relationship between introduction pathway and species impacts, finding that
John D. Rothlisberger there is an apparent relationship, but that further study of species-specific impacts is needed to verify this finding. Given the importance of ballast water release in bringing novel species to the GL, I use a novel technique to estimate the economic impacts in the region of ecological changes caused by populations of aquatic NIS introduced by this pathway. This study concludes that the economic impacts of ballast water species are large, but are also uncertain. Nevertheless, policies that aim to reduce the likelihood of additional invasions via this pathway appear to be economically justifiable. As nuisance aquatic NIS in the GL region spread to other waterways, they bring with them ecological and economic impacts. The detrimental nature of these impacts motivates efforts to reduce the rate of spread. To inform such efforts, I test the efficacy of multiple methods for removing aquatic NIS from recreational boats and trailers. I found that visual inspection and hand removal is highly effective in removing the nuisance macrophyte Myriophyllum spicatum, but that high-pressure washing is needed to effectively remove small-bodied organisms, including the exotic predatory zooplankter Bythotrephes longimanus. Beyond the tactics of how to clean boats, I evaluate efforts to strategically place boat cleaning stations on the landscape. My results show that a common predictive model is limited in its ability to predict which uninvaded lakes cleaning stations should protect. Instead, it appears that placing cleaning stations at invaded lakes to block the transport of invasive propagules is generally more likely to reduce landscape-level spread than protecting uninvaded lakes.
John D. Rothlisberger Aquatic NIS are only one of many environmental and cultural factors that affect ecosystems and societal interactions with the natural environment. To put the importance of aquatic NIS in context with other potential drivers of change in GL fisheries over the next two decades, I interviewed experts on GL fisheries, asking them to predict changes and to identify the most likely drivers of the changes they predicted. This study revealed that changing cultural interests are the main reason for expected declines in GL fisheries, but that NIS are the predominant environmental driver of change. The ecological and social issues surrounding NIS are complex and multi-faceted. As human populations grow, causing global environmental changes and taxing the supply of natural resources, the line separating ecological concerns from social ones is increasingly blurred. In this dissertation, I have included humans as a key component of the ecosystems of the GL region and considered the ecological effects of human actions with respect to their introduction of and intervention against aquatic NIS. In so doing, this dissertation presents several case studies of aquatic NIS in the GL with the aim of providing insights regarding opportunities and pitfalls for efforts to improve NIS policy and management.
To my parents, Dana and Ann. Thank you for your love and support.
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CONTENTS
Figures............................................................................................................................... vii Tables .............................................................................................................................. xiii Acknowledgements ........................................................................................................... xv Chapter 1: Dissertation introduction ................................................................................... 1 1.1 A role for ecology in natural resource policy and management ....................... 1 1.2 Nonindigenous species...................................................................................... 6 1.3 Human influence on the ecology of the Laurentian Great Lakes region .......... 9 1.4 Matching scientific inquiries on ecological topics to pertinent policy and management questions ................................................................................... 14 1.5 Dissertation outline ......................................................................................... 15 Chapter 2: The Laurentian Great Lakes are a freshwater invasion beachhead: pathways of nonindigenous species introduction predict prior distribution, subsequent spread, and potential impacts ............................................................................................ 20 2.1 Abstract ........................................................................................................... 20 2.2 Introduction ..................................................................................................... 22 2.3 Methods........................................................................................................... 25 2.3.1 Pathway and distribution prior to discovery in Great Lakes.................. 25 2.3.2 Pathway and spread beyond the Great Lakes ........................................ 27 2.3.3 Pathway and impacts.............................................................................. 28 2.4 Results ............................................................................................................. 34 2.4.1 Pathway and distribution prior to discovery in Great Lakes.................. 34 2.4.2 Pathway and spread beyond the Great Lakes ........................................ 37 2.4.3 Pathway and impacts.............................................................................. 41 2.5 Discussion ....................................................................................................... 42 2.5.1 The Great Lakes as a beachhead ............................................................ 42 2.5.2 The Great Lakes as a melting pot .......................................................... 45 2.5.3 Pathways and impacts ............................................................................ 47 2.5.4 Conclusion ............................................................................................. 49 2.6 Acknowledgements ......................................................................................... 50
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Chapter 3: Ship-borne nonindigenous species diminish Great Lakes ecosystem services ............................................................................................................................... 51 3.1 Abstract ........................................................................................................... 51 3.2 Introduction ..................................................................................................... 51 3.3 Results ............................................................................................................. 54 3.4 Discussion ....................................................................................................... 64 3.5 Acknowledgements ......................................................................................... 68 Chapter 4: Aquatic invasive species transport via trailered boats: what is being moved, who is moving it, and what can be done ............................................................... 69 4.1 Abstract ........................................................................................................... 69 4.2 Introduction ..................................................................................................... 70 4.3 Methods........................................................................................................... 75 4.3.1 Observational study ............................................................................... 75 4.3.2 Mail survey ............................................................................................ 77 4.3.3 In-person Northwoods survey ................................................................ 78 4.3.4 Experiment ............................................................................................. 78 4.4 Results ............................................................................................................. 81 4.4.1 Observational study ............................................................................... 81 4.4.2 Mail survey ............................................................................................ 88 4.4.3 In-person Northwoods survey ................................................................ 89 4.4.4 Experiment ............................................................................................. 89 4.5 Discussion ....................................................................................................... 90 4.6 Acknowledgements ....................................................................................... 100 Chapter 5: Limitations of gravity models in predicting the spread of Eurasian watermilfoil (Myriophyllum spicatum) ............................................................... 101 5.1 Abstract ......................................................................................................... 101 5.2 Introduction ................................................................................................... 102 5.3 Methods......................................................................................................... 107 5.3.1 Relationship between propagule pressure and probability of establishment ......................................................................................... 108 5.3.2 Model validation .................................................................................. 111 5.3.3 Cost-effectiveness of alternative interventions .................................... 113 5.4 Results ........................................................................................................... 115 5.4.1 Relationship between propagule pressure and probability of establishment ......................................................................................... 115 5.4.2 Model validation .................................................................................. 115 5.4.3 Efficacy of alternative intervention strategies ..................................... 117 5.5 Discussion ..................................................................................................... 117 5.6 Management recommendations .................................................................... 129 5.7 Acknowledgements ....................................................................................... 129
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Chapter 6: Future declines of the binational Laurentian Great Lakes fisheries: recognizing the importance of environmental and cultural change ........................................ 130 6.1 Abstract ......................................................................................................... 130 6.2 Introduction ................................................................................................... 131 6.3 Methods......................................................................................................... 133 6.3.1 Expert selection and interviews ........................................................... 133 6.3.2 Analysis, combination, and reporting of results .................................. 135 6.4 Results ........................................................................................................... 141 6.4.1 US commercial fishery ........................................................................ 143 6.4.2 Canadian commercial fishery .............................................................. 143 6.4.3 US sport fishery ................................................................................... 145 6.4.4 Canadian sport fishery ......................................................................... 146 6.5 Discussion ..................................................................................................... 146 6.5.1 Drivers of change in Great Lakes fisheries .......................................... 146 6.5.2 Conclusions .......................................................................................... 149 6.6 Acknowledgements ....................................................................................... 150 Chapter 7: Dissertation conclusion ................................................................................. 151 7.1 Ecology and society ...................................................................................... 151 7.2 Dissertation overview ................................................................................... 152 7.3 Possibilities and pitfalls ................................................................................ 156 7.4 Conclusion .................................................................................................... 159 Appendix A: List of nonindigenous aquatic species established in the Great Lakes and data on these species compiled for analyses in Chapter Two ............................. 161 Appendix B: Supporting text for Chapter Three: ship-borne nonindigenous species diminish Great Lakes ecosystem services........................................................... 170 B.1 Methods ........................................................................................................ 170 B.1.1 Selection of experts ............................................................................. 170 B.1.2 Briefing book....................................................................................... 171 B.1.3 Individual interviews ........................................................................... 171 B.1.4 Performance measures and combination of expert judgments: the classical model ....................................................................................... 174 B.1.5 Percent impacts on ecosystem services ............................................... 180 B.1.6 Economic valuation of impacts ........................................................... 181 B.2 Results .......................................................................................................... 189 B.2.1 Economic valuation of impacts ........................................................... 194 B.2.2 Expert rationales .................................................................................. 199 Appendix C: Expert elicitation protocol for ecological and economic impacts of shipborne nonindigenous species on the Great Lakes ............................................... 208 C.1 Purpose ......................................................................................................... 208 C.2 Scope ............................................................................................................ 209 C.3 Method ......................................................................................................... 209 v
C.3.1 Format ................................................................................................. 209 C.3.2 What is a good probability assessor? .................................................. 211 C.3.3 Expert names ....................................................................................... 212 C.3.4 Assumptions ........................................................................................ 212 C.4 Questions ...................................................................................................... 213 C.4.1 Commercial fishing ............................................................................. 213 C.4.2 Commercial fishing effort ................................................................... 216 C.4.3 Sport fishing ........................................................................................ 218 C.4.4 Fouling water intake for power plants & industry .............................. 222 C.4.5 Wildlife watching ................................................................................ 223 C.5 Answers to training questions ...................................................................... 224 Literature cited ................................................................................................................ 225
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FIGURES
Figure 1.1. The multi-stage process of biological invasions (Panel A), general policy and management options for dealing with each stage of an invasions (Panel B), and selected research questions for which scientific inquiry can improve the policy and management of invasive species (Panel C). Each of these questions is addressed for specific cases in this dissertation. See the text in the Dissertation Outline section of this chapter for how each of these questions is addressed in the chapters specified above. Panels A and B are redrawn with permission from Lodge et al. (2006). ................................................................................................. 7 Figure 2.1. Proportion of nonindigenous freshwater species that came to the Great Lakes via major introduction pathways that either were first discovered in North America in the Great Lakes basin or, alternatively, outside of the Great Lakes basin. The total number of species introductions attributed to each pathway is shown above each bar. (GL = Great Lakes) ........................................................ 35 Figure 2.2. Nonindigenous freshwater species whose first North American discovery was in the Great Lakes (n = 63) that remain confined to the Great Lakes basin as well as those that have spread beyond the basin. Sub-plots group species according to their pathway of introduction and bars in each sub-plot group species according to their taxonomic category....................................................................................... 36 Figure 2.3. Misclassification rates as a function of the number of explanatory variables, from leave-one-out cross-validation for binary decision trees intended to predict the current distribution of nonindigenous freshwater species whose first discovery in North America was in the Great Lakes. ............................................................ 38 Figure 2.4. The binary decision tree with the lowest combined misclassification rates for species that are confined to and which have spread beyond the Great Lakes basin. This tree classifies observations according to a single explanatory variable: years since a species was discovered in the Great Lakes. If it has been less than 74 years since a species was discovered in the Great Lakes, then this model predicts that it is still confined to the basin. The numbers of species correctly and incorrectly classified are shown at the two terminal nodes of this tree (i.e., 55 species were classified as being confined to the Great Lakes basin, 48 correctly so and 7 incorrectly; 8 species were classified as having spread beyond the basin, 7 correctly and 1 incorrectly). .................................................................................. 39 vii
Figure 2.5. Current distribution (within or outside the Great Lakes) of nonindigenous freshwater species that were first discovered in North America in the Great Lakes versus years since initial discovery. Symbols depict the pathway that introduced each species to the Great Lakes (see Legend). The vertical position of species discovered in the same year has been adjusted to avoid hidden data. .................. 40 Figure 3.1. Distributions of ship-borne species percent impacts on US commercial fish landings (for each lake), sport fishing effort (for each lake) and expenditures (aggregated across all five lakes), and wildlife viewing effort (aggregated across all five lakes) in 2006. Distributions are performance-based combinations of expert assessments. Solid black lines designate medians, indicating the most likely percentage by which each quantity would have been greater if ship-borne species were not present........................................................................................ 56 Figure 3.2. Distributions of economic impacts as lost consumer surplus (fishing and wildlife viewing) or additional costs (raw water users), aggregated across lakes, of ship-borne nonindigenous species on ecosystem services in the Great Lakes in the US: A, commercial fishing; B, sport fishing; C, wildlife viewing; D, raw water use). Solid black lines indicate the median and dotted lines the 90% uncertainty range of each distribution. Note differences in scale of horizontal and vertical axes of plots. ......................................................................................................... 58 Figure 3.3. Ninety percent uncertainty ranges for economic impacts in the United States of ship-borne NIS on multiple ecosystem services in the Great Lakes. ............... 60 Figure 3.4. Scenarios of future cumulative ship-borne invasive species damage relative to cumulative transportation savings from ocean-going shipping into the GL. ........ 62 Figure 4.1. Aquatic vegetation found attached to boats and trailers during field survey. Panel A is a histogram of the total mass of fragments on individual boats (bin width = 1g). Panel B shows a histogram of the mass of individual vegetation fragments (bin width = 0.5g). ............................................................................... 83 Figure 4.2. Average number and type of small-bodied organisms washed from recreational boats and trailers arriving at (n= 36) or departing from (n= 49) lakes in the northern Wisconsin and the Upper Peninsula of Michigan. See Table 4.3 for further detail on taxa included in each taxonomic category............................ 84 Figure 4.3. Results of experimental removal of biological materials from boat and trailer via boat washing or visual inspection. Panel A shows removal of Myriophyllum spicatum with different wash pressures and durations, and with visual inspection and hand-removal. Panel B shows data from the same treatments for the removal of small-bodied organisms. ................................................................................... 91 viii
Figure 5.1. Number of Eurasian watermilfoil invasions in Wisconsin lakes larger than 25 ha between 1990 and 2006, inclusive. Bars show the number of new invasions in each year and the line graph shows the cumulative number of invasions in Wisconsin............................................................................................................ 110 Figure 5.2. Evaluation of the gravity model’s ability to accurately predict lake-specific probability of invasion. Each bin holds 100 lakes and bins are arranged from highest predicted probability of invasion on the left to lowest on the right. Bars indicate the number of lakes in each bin that were actually invaded. The average per lake predicted probability of invasion in the top 200 at-risk sites ( pˆ ) is shown for each year. Also shown for each year is the probability or p-value (p) of observing the actual number of newly invaded sites given the value of pˆ for that year. The vertical dashed line shows the cut-off to the left of which are the bins for the 200 lakes predicted most likely to be invaded in each year. ................... 114 Figure 5.3. Analysis of alternative intervention strategies for slowing the spread of aquatic invasive species. Contour lines show the percent reduction in average per site probability of invasion relative to no intervention versus number (x-axis) and cleaning efficacy (y-axis) of intervention sites deployed. Dashed lines show the protection strategy, where intervention is deployed to prevent introductions at the specified number of uninvaded sites identified by the gravity model as having the highest probability of invasion (i.e., greatest propagule pressure from invaded locations). Solid lines show the containment strategy, where intervention is deployed to keep propagules from leaving the specified number of invaded sites with the greatest probability of initiating new invasions (i.e., highest propagule pressure to uninvaded locations). ........................................................................ 118 Figure 6.1. Historical and projected commercial and recreational fisheries in the US and Canadian waters of the GL. Angler effort in recreational fisheries is shown as insets in the upper right of each panel. Vertical range bars are performance-based combinations of expert assessments where lower and upper limits show, respectively, 5th and 95th percentiles of the combined expert subjective probability distributions. Hollow circles depict the 50th percentile of each distribution. Note different vertical scales across countries, lakes, and fishery types. Canadian commercial catch (Panel i) is for all Canadian waters of the GL. Historical recreational fisheries data were taken from the USFWS National Survey of Fishing, Hunting, and Wildlife-associated Recreation. Commercial catch data dating back to 1971 were obtained for the US from the USGS Great Lakes Science Center and for Canada from the Department of Fisheries and Oceans. 136 Figure 6.2. Probability density functions of PBC-projected percent change between 2006 and 2025 in US and Canadian commercial fish landings (lbs landed) and sport fishing effort (angler-days) and expenditures (2007 US$). Black lines show median of each distribution. Dotted lines provide a reference to zero percent ix
change. Note that, even though most distributions extend to the left of -100%, the value of these variables in 2025 actually cannot be more than 100% less than they were in 2006. ....................................................................................................... 137 Figure 6.3. Individual and combined expert assessments for US commercial fish landings (left column) and sport fishing effort (right column) for 2006 and 2025 for each of the GL. The lakes are shown in the following order: Superior, Michigan, Huron, Erie, Ontario. Two rows of panels represent each lake, the first showing 2006 assessments and the second 2025. Dashed lines divide 2006 and 2025 estimates for each lake. Each panel shows the 5th to 95th percentile range graphs for individual and combined expert assessments, with filled circles showing 50th percentile estimates. Assessments are shown in the same order in each panel: top to bottom, Expert 1, 2, 3, 4, 5, 6, 7, 8, 9, equally-weighted combination, performance-based combination. For calibration variables, light gray vertical bars show the actual value of the variable being estimated, which became known after the elicitation was finished. Note differences in scale for each lake and fishery type. ..................................................................................................................... 138 Figure 6.4. Individual and combined expert assessments for Canadian commercial fish landings, aggregated across lakes (a, b), and sport fishing effort, divided by lake (c – j), for 2006 and 2025 for each of the GL. For sport fishing, the lakes are shown in the following order: Superior, Huron, Erie, Ontario. Two rows of panels represent each lake, the first showing 2006 assessments and the second 2025. Dashed lines divide 2006 and 2025 estimates for each lake. Each panel shows the 5th to 95th percentile range graphs for individual and combined expert assessments, with filled circles showing 50th percentile estimates. Assessments are shown in the same order in each panel: top to bottom, Expert 1, 2, 3, 4, 5, 6, 7, 8, 9, equally-weighted combination, performance-based combination. For calibration variables, light gray vertical bars show the actual value of the variable being estimated, which became known after the elicitation was finished. Note differences in scale for each lake and fishery type. ............................................ 139 Figure 6.5. Individual and combined expert assessments for US GL recreational fishing expenditures for 2006 (a) and 2025 (b). Each panel shows the 5th to 95th percentile range graphs for individual and combined expert assessments, with filled circles showing 50th percentile estimates. Assessments are shown in the same order in each panel: top to bottom, Expert 1, 2, 3, 4, 5, 6, 7, 8, 9, equallyweighted combination, performance-based combination. The vertical light gray bar shows actual 2006 expenditures (USFWS 2007), which became known after the elicitation was over. ...................................................................................... 140 Figure 6.6. Number of experts that mentioned various potential drivers of change in explaining their expectations for declines in US and Canadian commercial and recreational fisheries between 2006 and 2025. ................................................... 144 x
Figure 7.1. Scope and content of research projects presented in this dissertation. Chapter numbers accompany a graphical depiction of the topic of each chapter. Biological invasions are a multi-stage process that occur at multiple spatial and temporal scales. For example, the global transport of ballast water in shipping vessels introduces species to the Great Lakes region (Chapter 2) which have ecological and economic impacts in the Great Lakes (Chapter 3). Some of these species and others introduced to the region by other pathways (e.g., commerce in living organisms) spread to other waterways in and beyond the region via anthropogenic mechanisms (Chapters 4 and 5). The impacts of nonindigenous freshwater species in the Great Lakes region take place within a broader context of other environmental and cultural factors that also drive environmental change (Chapter 6). See the text in the Dissertation Overview section of this chapter for explanation of the subject and conclusions of each chapter. .............................. 154 Figure B.1. Schematic of welfare changes related to commercial fishing, illustrating the market model approach taken to estimate economic impacts of ship-borne species. ............................................................................................................................. 184 Figure B.2. Schematic of welfare changes related to outdoor recreation, illustrating the inferred market model approach used to estimate economic impacts of ship-borne species. ................................................................................................................ 188 Figure B.3. Individual and combined expert assessments showing the impact of shipborne species on US sport fishing effort (left column) and US commercial fish landings (right column) in 2006. There are two rows of panels for each lake with the first row showing expert assessments for the variable (i.e., angler-days or pounds of commercially landed fish) with ship-borne species (i.e., actual condition) and the second row showing assessments for the variable if ship-borne species had never been introduced (i.e., hypothetical condition). Dashed lines divide assessments with and without ship-borne species. The order of the lakes is, from top to bottom, Superior (a-d), Michigan (e-h), Huron (i-l), Erie (m-p), and Ontario (q-t). Within each panel expert assessments are arranged in order, from top to bottom, Expert 1, 2, 3, 4, 5, 6, 7, 8, 9, equally-weighted combination, and performance-based combination. Vertical light gray bars in panels a, b, e, f, i, j, m, n, q, and r show the realization of the variable in question, which was unknown at the time of the elicitation. Note that the scale of the horizontal axes varies. .................................................................................................................. 191 Figure B.4. Individual and combined expert assessments of the impact of ship-borne species on US wildlife viewing effort in 2006. The first row shows expert assessments given the presence of ship-borne species (i.e., actual condition) and the second row shows assessments for the variable if ship-borne species had never been introduced (i.e., hypothetical condition). Dashed lines divide assessments with and without ship-borne species. Within each panel, expert assessments are arranged in order, from top to bottom, Expert 1, 2, 3, 4, 5, 6, 7, 8, 9, equallyxi
weighted combination, and performance-based combination. The vertical light gray bar in panel a shows the actual number of wildlife viewing participant-days in 2006, which was unknown at the time of the elicitation. ............................... 192 Figure B.5. Individual and combined expert assessments of the annual per facility impacts of ship-borne species on US raw water users in 2006. The order of the raw water users, from top to bottom, is nuclear power plants (a), water treatment plants (c), fossil fuel power plants (e), and industrial facilities (g). Within each panel expert assessments are arranged in order, from top to bottom, Expert 1, 2, 3, 4, 5, 6, 7, 8, 9, 10, equally-weighted combination, and performance-based combination. Note that the scale of the horizontal axis is different for each user type. ..................................................................................................................... 193
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TABLES
Table 2.1. Summary of scientific literature documenting ecological and economic impacts attributable to ballast water species established in the Great Lakes ........ 30 Table 2.2. Summary of scientific literature documenting ecological and economic impacts attributable to nonindigenous freshwater species introduced by commerce in living organisms to the Great Lakes ................................................................. 32 Table 3.1 Summarized distributions of percent impacts of ship-borne nonindigenous species on ecosystem services on ecosystem services in the Great Lakes in the United States in 2006 ............................................................................................ 55 Table 4.1. Questions and responses from mail and in-person surveys. ............................ 79 Table 4.2. Aquatic plant species and the respective number of fragments of each found on boats and trailers during observational field survey in Northern Wisconsin in Summer 2006 ........................................................................................................ 85 Table 4.3. Taxa collected from boats and trailers during field survey in northern Wisconsin in 2006................................................................................................. 86 Table 4.4. Nonindigenous species established in the Great Lakes that are morphologically similar to species collected in boat washing samples. .......................................... 95 Table 6.1. Experts interviewed and the professional title, affiliation, and qualifications of each (listed alphabetically). ................................................................................ 134 Table 6.2. Calibration, informativeness, and weights of the nine experts, their equalweight combination (EQUAL), and their performance-based combination (PBC) for changes in Great Lakes fisheries between 2006 and 2025 ............................ 142 Table A.1. Nonindigenous aquatic species established in the Great Lakes as of 2008 .. 162 Table B.1. Experts interviewed and the professional title, affiliation, and qualifications of each (listed alphabetically). ................................................................................ 172 xiii
Table B.2 Summary statistics on values drawn from the literature on own-price elasticity of demand of commercial fish, the value of sport fishing in the Great Lakes, and the value of wildlife viewing in the Great Lakes region ..................................... 186 Table B.3. Calibration, informativeness, and weights of the nine experts, their equalweight combination (EQUAL), and their performance-based combination (PBC) for the impacts of ship-borne species on the Great Lakes in 2006 ..................... 190 Table B.4. Summaries of commercial fishery consumer surplus prediction distributions in the Great Lakes in the United States in 2006 ...................................................... 195 Table B.5. Summaries of outdoor recreation consumer surplus prediction distributions in the Great Lakes in the United States in 2006 ...................................................... 196 Table B.6. Additional annual operating costs to raw water users attributable to shipborne species in the Great Lakes region in the United States in 2006 ................ 200
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ACKNOWLEDGEMENTS
I offer my sincere gratitude to my PhD advisor, Dr. David M. Lodge, for his mentorship during my studies at the University of Notre Dame. His example and intellect have benefited me profoundly, both professionally and personally. My completion of this degree would not have been possible without his guidance and encouragement. I hope to represent him well as I move forward in my career. I also thank my other committee members---Gary Belovsky, Jessica Hellmann, and Gary Lamberti---for their assistance and input. My associations with these professors have consistently motivated me to improve my work and myself. I have the utmost respect for each of them. I have also had the opportunity to work closely with senior researchers at other academic institutions. Roger Cooke of Resources for the Future and the Technical University of Delft and David Finnoff of the University of Wyoming have generously shared their time and expertise with me. Their help has made parts of this dissertation possible that would not otherwise have been so. I am grateful for the friendly culture and spirit of cooperation that exist in the Lodge lab and for the opportunity that I have had to interact with many excellent lab members during my graduate career. I thank Joanna McNulty for all she has done to help the projects and grants I have worked on flow smoothly. The positive experiences I have had as a doctoral student have largely been shaped by my interactions with the xv
postdoctoral researchers in the lab---Jon Bossenbroek, Kevin Drury, Darren Yeo, Chris Jerde, and Andy Mahon---and with my fellow graduate students---Sadie Rosenthal, Reuben Keller, Jody Peters, James Larson, Konrad Kulacki, Brett Peters, Matthew Barnes, Andrew Deines, and Ashley Baldridge. As an honorary lab member, Lindsay Chadderton also belongs on this list. I thank each of these individuals for their constructive influence on my life, as colleagues and as friends. Many technicians have helped to bring about this research. Mark Drew, Penny Nichols, Sarah Sutton, Tim Campbell, Mike McCann, and Rebecca Hale have all made significant contributions to this work. I also thank Sheila Kennedy, Jeff Delfeld, Brandon Feasel and Neil Wallace for their data collection efforts. Finally and always, I am most grateful to my wife, Emily, for her love and support during our pursuit of this degree. She is everything to me. I also express my deep love and gratitude for my sons---Matthew, Jacob, and Daniel.
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CHAPTER 1: DISSERTATION INTRODUCTION
1.1 A Role for Ecology in Natural Resource Policy and Management Among the most significant current challenges for the science of ecology are issues involving the interactions of humans with the natural environment (May 1999, NRC 2001, MEA 2005). Given the significant effects of humans on biodiversity and ecological processes, there is a great need for ecological guidance in addressing current and future environmental crises (Ehrlich and Ehrlich 2004, Cabrera et al. 2008). The most serious ways in which human activities are modifying the natural world include habitat fragmentation, greenhouse gas release, nitrogen deposition, and the spread of invasive nonindigenous species. In seeking to provide guidance on such pressing concerns, ecology must sometimes reach beyond its disciplinary boundaries, especially when social issues are involved, working together with researchers in economics, geography, sociology, and other disciplines. Understanding ecological change requires interdisciplinary work because the indirect drivers of ecological change are often economic and cultural. Furthermore, interdisciplinary work is intellectually challenging because it requires researchers to extend beyond traditional disciplinary boundaries and approaches. For ecological research to be relevant to natural resource policy and management, it must investigate and increase our understanding of the important drivers of ecological change. 1
In this dissertation, I have applied scientific principles to address important practical questions pertaining to the policy and management of invasive nonindigenous species. This work is grounded in ecology, but at times also connects to other disciplines, in an effort to enhance the potential relevance of the findings of this research. Humans interact with the natural world in multiple ways. Some human interactions with the environment involve deriving benefits (i.e., goods and services) from ecosystems (Costanza et al. 1997, Daily 1997). Other human-environment interactions are the byproducts of economic activities and can sometimes result in environmental degradation. Natural resource policy and management actions are generally intended either to maintain or enhance ecosystem services (i.e., the benefits of nature to society) or to limit environmental damage from other anthropogenic sources (Daily and Matson 2008). Scientific research in ecology is a tool to understand how human actions, including natural resource policy and management decisions, may affect the ecosystems with which humans interact (Naidoo et al. 2008). Nevertheless, understanding anthropogenic effects on ecosystems is difficult because ecological systems are complex (Levin 1999). With this complexity comes a high degree of scientific uncertainty about the functioning, and even the structure, of these systems. Some of this scientific uncertainty arises from the difficulty of connecting cause to effect in ecological dynamics. The vast complexity of ecosystems and the challenge of understanding how they operate have led to various approaches for gaining knowledge about them. In recent decades, one of the most common strategies in ecological research has been a reductionist approach, whereby ecological interactions are stripped down to their simplest form. This simplification allows controlled, replicated 2
experiments to be performed. Using experiments, researchers can investigate how one or a few variables of interest respond to the manipulation of one or a few potentially important explanatory variables (Pickett et al. 1994, Underwood 1997). In conjunction with inferential statistics, this is a powerful approach in learning how organisms interact with one another and with their physical environment (Platt 1964). Despite its usefulness in discovering the mechanisms of ecological interactions, not all important questions in ecology and environmental science can be adequately addressed using reductionist science. Logistical considerations generally constrain controlled, manipulated experiments to short time frames, small spatial scales, and questionable realism (Diamond 1986). Recent efforts have been made, however, to increase the spatial scale and realism of controlled ecological experiments. Notable among such efforts are the Free-Air Carbon dioxide Enrichment (FACE) experiments that are investigating the effects of elevated atmospheric carbon dioxide on forest ecosystems (DeLucia et al. 1999). These experiments are being conducted at the acreplus scale and will perhaps provide a more integrated understanding of ecosystem responses to elevated carbon dioxide than will data from smaller-scale experiments conducted in environmental chambers. A classic historical example of manipulating an entire ecosystem and documenting the effects of the manipulation versus an unmanipulated control are whole-lake phosphorus amendments in the northern temperate region (Schindler et al. 1978, Elser et al. 1986, Carpenter and Kitchell 1993). Though the value of these large-scale experiments is clear, it is also clear that as system complexity increases, so does the difficulty of tracking the causal linkages from manipulated features of an ecosystem to the components hypothesized to respond to 3
manipulation. Moreover, the more complex (i.e., realistic) a system is, the greater the uncertainty that the same system or a highly similar one would respond in the same way to nearly the same manipulation, if repeated. Even the comparatively simple dynamics of insect populations, for example, can exhibit extreme sensitivity to initial conditions, or chaos, making the outcome of manipulations uncertain in the absence of complete knowledge of the initial conditions (May 1974). Nevertheless, most ecological studies are conducted on plots that are less than 3 square meters and for periods of time less than 5 years, and are not repeated by independent investigators (Levin 1992, Lodge et al. 1998). If one of the goals of ecological research is to provide knowledge to manage ecosystems according to scientific principles, there are many instances where short, small-scale experiments may have limited utility in providing such guidance. One reason for such limitations is that the data and inferences from such investigations may not match well with critical policy and management questions in the real world. Furthermore, other interactions in an ecosystem may be more important drivers of the system’s dynamics than the interactions that have been studied. Thus, well-studied mechanisms may be swamped in importance by relatively unknown interactions that operate on a higher organizational level. Such higher-level interactions may remain unstudied because of their limited tractability under traditional reductionist methods. One approach that has been used to address higher-order ecological phenomena that operate at large spatial scales has been to take advantage of naturally occurring manipulations to ecosystems (i.e., perturbations), observing how variables in the ecosystem respond to natural events or conditions. For example, hurricanes have been 4
used to study the role of disturbance and the process of secondary succession (Turner et al. 1998); bird communities on islands of different sizes have been used to study colonization, niche breadth, and community assembly rules (Diamond 1970, Diamond 1973); other cases of the biogeography of islands have been used to learn more about dispersal, colonization, extinction, and community dynamics (MacArthur and Wilson 1967), and volcanic eruptions allow for the study of primary succession (Wood and Delmoral 1987). These types of opportunities have been called natural experiments (Diamond 1986). In natural experiments, differences in conditions among locations because of varying degrees of perturbation (i.e., across space) are employed to make inferences about how ecosystems develop through time with respect to their structure and functioning. The space-for-time swap is a common approach in ecology that allows conclusions to be drawn about temporal processes in a much shorter timeframe, months or years versus centuries or millennia, than would be possible by actually observing the processes over time. In other words, because we can observe what happens given varying ecological conditions across space, we can make predictions about what will occur as ecological conditions vary through time. Biological invasions provide an opportunity to reverse the typical space-for-time swap in ecological research to a time-for-space swap. By retrospectively assessing the process and consequences of previous biological invasions, many of which have occurred in the recent past, and for which some degree of historical data are available, we can make predictions about patterns and processes of biological invasions of the same or similar species that are likely to occur in other locations (i.e., elsewhere in space). This
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kind of analysis may prove to be highly informative for natural resource policy and management of biological invasions.
1.2 Nonindigenous Species Harmful nonindigenous species are an environmental problem of global concern. Invasive species have been implicated in declines of native biodiversity (Nalepa et al. 1996, Wilcove 1998, Gurevitch and Padilla 2004), with many of their greatest impacts expected to occur in freshwater ecosystems (Sala et al. 2000). Economic losses from invasive species are also substantial, over $100 billion per year in the United States (Pimentel et al. 2005). Because biological invasions are linked with trade, invasions are expected to increase in the coming decades as trade also increases (Levine and D’Antonio 2003). Thus, there is a critical need for science to help improve policy and management related to biological invasions. Biological invasions result from a multi-stage process (Figure 1.1A) that begins with species being transported beyond their native range via some transportation pathway or vector. There are two major categories of anthropogenic transportation of live organisms. The first is the intentional movement of organisms for commercial purposes (e.g., live food trade, pet trade) and the second is the inadvertent transport of live organisms that is incidental to commerce and travel (e.g., planktonic species in ballast water in ships, wood-boring beetles in packaging materials). Via a wide array of transportation vectors in these two categories, species are introduced to areas outside their native range. A percentage of introduced species (typically 10-50%) become established in a new area when they form one or more self-sustaining 6
A)
Invasion Process Species in pathway
B)
General Policy and Management Options
C)
Selected Research Questions
Prevention Transported and released alive
Population established
Spread
Ecological, human health, or economic impact
Early detection, rapid response, and eradication
Is there a relationship between introduction pathway and origin of nonindigenous species established in a particular region? (Chapter 2) What species does a particular pathway spread? (Chapter 4) What strategies and tactics most effectively limit the spread of species by particular transportation pathways? (Chapters 4 and 5) How accurately can models predict the spread of invasions? (Chapter 5)
Control and slow the spread
Are species’ impacts related to introduction pathway? (Chapter 2)
Human adaptation (change behavior and bear the costs)
Have NIS introduced by a particular pathway to a particular region modified ecosystem goods and services, and what have been the economic impacts of changes? (Chapter 3) What is the importance of nonindigenous species’ impacts relative to other drivers of change in determining how humans interact with the environment? (Chapter 6)
Figure 1.1. The multi-stage process of biological invasions (Panel A), general policy and management options for dealing with each stage of an invasions (Panel B), and selected research questions for which scientific inquiry can improve the policy and management of invasive species (Panel C). Each of these questions is addressed for specific cases in this dissertation. See the text in the Dissertation Outline section of this chapter for how each of these questions is addressed in the chapters specified above. Panels A and B are redrawn with permission from Lodge et al. (2006).
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populations there (Williamson 1996, Jeschke and Strayer 2005). When this occurs, species become part of the nonindigenous flora or fauna of the region. A nonindigenous species is classified as invasive if it spreads throughout the new range and has net negative impacts on ecosystems, human health, or economic interests (Lodge et al. 2006). Of course, assessments of whether the impacts from a nonindigenous species are on the net positive or negative depend on society’s perceptions. It is, therefore, not the role of ecologists alone to specify whether a species is invasive or not. In the chapters that follow, I focus on nonindigenous aquatic species that are currently established in the Laurentian Great Lakes (GL) and the surrounding region. Some of these species are widely acknowledged as being invasive, including, for example, Eurasian watermilfoil Myriophyllum spicatum and zebra mussel Dreissena polymorpha. Others, however, are not, including many of the species on the list of 95 aquatic species established in the GL that I consider in Chapter Two (see Appendix A). Thus, depending on the chapter and its focus and on the species involved, I refer to some species as aquatic invasive species (AIS) and to others as freshwater nonindigenous species (NIS). Biological invasions have important ecological and evolutionary implications (Sax et al. 2005). When a species joins a biological community beyond its native range, it interacts with species that may be very different from those with which it has interacted through evolutionary time. These interactions may include predation, competition, and parasitism, but may also occur through more indirect means, for example by changing abiotic environmental conditions. These novel interactions can affect the evolutionary trajectory of the nonindigenous and native species in a community (Wares et al. 2005). 8
Potentially novel abiotic conditions can also place new selective pressures on NIS, at times resulting in rapid evolution (Huey et al. 2005). On shorter time scales, the establishment of NIS in a community can have substantial effects at the population, community, and ecosystem levels (Sakai et al. 2001, D'Antonio and Hobbie 2005, Blackburn and Gaston 2005). Human societies deem some of these ecological effects to be undesirable. Negative impacts include population declines of native species, nuisance-level abundance of NIS, increased disease of humans and organisms important to humans, and alterations to ecosystem functioning (e.g., nutrient cycling; Hall et al. 2003). As previously mentioned, aquatic NIS with these types of ecological effects are often considered to be AIS. Although the invasion process is relatively well understood (Figure 1.1A) and general recommendations for dealing with invasions are available (Figure 1.1B), many biological invasions have not been studied in sufficient detail to use this understanding to support informed natural resource policy and management decisions (Figure 1.1C). More in-depth scientific study regarding specific stages of specific invasions, such as presented in this dissertation, will help to identify aspects of NIS policy and management that could be improved through scientific research. Similar efforts could also reveal areas where additional scientific developments are most needed before valid scientific advice can be offered.
1.3 Human Influence on the Ecology of the Laurentian Great Lakes Region The geographic focus of this dissertation is on the GL and the states that surround the lakes. The history of GL is an instructive study in the interactions between humans 9
and natural resources. Beginning in the early 1800s, humans have extracted fishery resources from the GL at a sometimes unsustainable pace (Bogue 2000). These resources contributed to rapid regional population growth and prosperity. Larger populations demanded more resource extraction, more intensive agriculture, and the development of industries. Erosion and water pollution, byproducts of agriculture and industry, further modified the GL environment, often to the detriment of populations of native species, especially fisheries. In an effort to conserve these valuable natural resources, a variety of management actions were taken. Early management actions generally aimed to maintain or enhance utilitarian production of fishery resources, but later actions sought to rehabilitate and restore native ecological structure and function (Brown et al. 1999). Anthropogenic changes to the surrounding landscape also affected the ecology of the GL. Dams placed on GL tributaries for irrigation and power generation limited reproductive opportunities for potadromous fish species. For example, Atlantic salmon (Salmo salar), once abundant in L. Ontario, had nearly disappeared by 1850, a casualty of overfishing and spawning habitat loss (Coon 1999). Shipping canals provided new hydrological connections among the lakes and to the lakes from other waterways, facilitating species introductions, which in some cases significantly altered GL foodwebs. The Welland Canal, first completed in 1829, circumvented the barrier of Niagara Falls, which until then had prevented species (and ship) movement upstream from L. Ontario to L. Erie and the upper GL. Via the Welland Canal, sea lamprey (Petromyzon marinus) invaded L. Erie and the upper GL early in the 20th century, exerting massive predation pressure on lake trout (Salvelinus namaycush).
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Victim to overfishing, spawning habitat loss, and sea lamprey predation, lake trout populations crashed across the GL from 1940 to 1950 (Eshenroder and Amatangelo 2002). Lake trout had historically been an abundant top piscivore in the lakes and its dramatic decline prompted mitigation efforts: commercial fisheries were heavily regulated, some spawning habitat was restored, and lamprey control was initiated. Despite these efforts, lake trout had already been essentially extirpated from all GL except for L. Superior. The loss of the lakes’ top predator led to substantial foodweb alterations. The most striking of these changes was the invasion of alewife (Alosa pseudoharengus), a North Atlantic planktivore, via the Erie Canal, which connects the Hudson-Mohawk Rivers to L. Erie. In the absence of large piscivores and with abundant plankton, a byproduct of cultural eutrophication, to consume alewife populations exploded (O’Gorman and Stewart 1999). Alewife reached nuisance levels in the GL, especially L. Michigan, in the early to mid-1960s. Through egg and larval predation and competition with juveniles and adults, alewife further changed native fish assemblages, causing declines in yellow perch (Perca flavescens) and deepwater ciscoes (Coregonus spp.) (Crowder 1980). Humans also experienced the negative effects of the alewife outbreak directly when particularly cold overwinter temperatures led to a massive alewife die-off in the spring of 1967. Tons of dead, rotting alewife fouled beaches near major population centers, prompting public outcry. In response, fishery managers in the US began stocking piscivorous Pacific salmonines, including chinook (Oncorhynchus tshawytscha), coho (Oncorhynchus kisutch), and steelhead salmon (Oncorhynchus mykiss), as biocontrol against alewife and in hopes of enhancing sport fishing opportunities. The 11
voracious and fast-growing exotic salmonines consumed vast quantities of alewife (Stewart and Ibarra 1991) and supported an extremely economically valuable put-growtake sport fishery (Gale 1987, Talhelm 1988), shifting the emphasis from commercial to sport fisheries in the US waters of the GL. The Pacific salmonine-alewife predator-prey system, however, proved unstable, experiencing fluctuations due to stressors such as climatic factors (e.g., cold water temperatures) and disease (e.g., bacterial kidney disease in salmonines). In the late 1980s, around the same time sport fisheries were booming, new nonnative species began appearing in the GL. These species, including zebra and quagga mussels (Dreissena polymorpha and D. bugensis, respectively), spiny and fishhook waterfleas (Bythotrephes longimanus and Cercopagis pengoi, respectively), Eurasian ruffe (Gymnocephalus cernuus), and round goby (Neogobius melanostomus), became predominantly integrated near the base of GL food webs, sometimes making their ecological impacts on fisheries difficult to isolate. These species and over 50 others, many of them from the Ponto-Caspian and Baltic regions of Europe (Grigorovich et al. 2003), were unintentionally introduced to the GL via the release of ballast water and sediments by interoceanic shipping vessels (Ricciardi 2006). A consequence of the increasing rate and scale of human commerce associated with globalization, access to the GL by interoceanic shipping vessels, and hence these NIS, was made possible by the opening of the St. Lawrence Seaway in 1959. Since its opening, concern for the effects of unintentionally introduced NIS on the ecology of the GL has greatly increased (Mills et al. 1993).
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Since the earliest use of the GL fishery by European colonizers, society’s emphasis has shifted from investment in natural resource extraction to investment in natural resource conservation in the highly modified GL ecosystem. The GL have been and continue to be affected by multiple anthropogenic stressors. Current threats include Asian carp moving north up the Mississippi River toward Lake Michigan, emerging fish pathogens such as viral hemorrhagic septicemia virus (VHSv), the establishment and range expansion of additional ballast water NIS (particularly those native to regions of new trading partners, e.g., Asia), changes in lake levels, hypoxic conditions in portions of Lake Erie, and regional climate change. On the horizon for human influence on the ecology of the GL is a sizeable restoration effort that will seek to reverse some of the anthropogenic damage previously done to the lakes. This impending effort, known as the Great Lakes Restoration Initiative, will involve numerous state and federal natural resource management agencies, all of whom will require scientific guidance to achieve their goals and mandates effectively (http://www.glrc.us/). It is expected that this GL restoration endeavor will be similar in scale to the massive Everglades restoration project (DeAngelis et al. 1998, http://www.evergladesplan.org/). The ecology of the GL region has been and will continue to be heavily influenced by society’s choices about natural resource policy and management. In particular, the GL region has become a laboratory for the science and policy of NIS (Kelly et al. 2009). As described above, numerous NIS are established in the GL, some of which have had large ecological and economic impacts (Mills et al. 1993). This has led to substantial foment
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and energy for research and policy work on NIS in the region. The research that follows in this dissertation seeks to build upon and contribute to this body of work.
1.4 Matching Scientific Inquiries on Ecological Topics to Pertinent Policy and Management Questions In 2006, the Ecological Society of America issued a document titled “Biological Invasions: Recommendations for US Policy and Management” that stated, “The Ecological Society of America is committed to assist all levels of government and provide scientific advice to improve all aspects of invasive-species management” (Lodge et al. 2006, italics added). This statement recognizes the essential role for ecologists in guiding natural resource policy and management pertaining to biological invasions. There remain numerous open questions regarding biological invasions. Additional, and focused, scientific inquiry is required to find solutions and discover options that are available for dealing with invasions (Figure 1.1C). Thus, to keep this commitment, some ecologists must engage in research suited to providing scientific guidance on specific policy and management issues. This dissertation is an effort to apply ecological understanding, as well as to develop the necessary intellectual tools for connecting ecological and economic analysis, to conduct this sort of novel and highly relevant research. This type of effort is needed because there is often a mismatch between critical questions regarding biological invasions and the scientific data that are available to address these questions. If oriented properly and conducted at the appropriate level of detail, ecological research can provide relevant information for addressing policy and 14
management questions. One of the intellectual challenges of this type of research is to seek out and apply the scientific tools appropriate for addressing relevant questions.
1.5 Dissertation Outline One of the principal goals of scientific inquiries regarding invasive species is to predict the identity of species that are likely to become invasive if introduced (Kolar and Lodge 2002, Lodge et al. 2006, Keller et al. 2007). Retrospective historical analysis of past invasions is an information-rich way to make predictions about the identity and impacts of future invasive species (Kolar and Lodge 2001, Kolar and Lodge 2002, Leung et al. 2002). In Chapter Two, I perform a retrospective analysis on the introduction pathways of freshwater NIS in the GL. My analysis shows that ballast water release is highly likely to introduce new freshwater NIS to North America, whereas a separate pathway---commerce in living organisms---tends to introduce NIS already established elsewhere in North America. Moreover, it is primarily a matter of time before novel NIS established in the GL appear in other North American waterways. I also investigate whether the ecological impacts of these species are related to their pathway of introduction. I find that there is an apparent relationship between pathways and impacts, but that further study of species-specific impacts is needed to verify this preliminary conclusion. This research provides a better understanding of which pathways bring which species to the GL and the impacts that often result from NIS introduced by particular pathways. This understanding could inform policies to limit future introductions.
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Given the importance of ballast water release in bringing novel species to the GL, in Chapter Three I use an established technique, structured expert judgment (SEJ), in a novel application to estimate the economic impacts of ecological changes caused by ballast water NIS. Well-known direct impacts of these species include invasive zebra and quagga mussels clogging the pipes of power plant cooling systems in the GL region, necessitating costly maintenance and retrofitting (O’neill 1996). These additional operating costs are passed on to energy consumers, affecting nearly every business and household in the GL region. The zebra and quagga mussel invasion has also had indirect impacts on the GL as the filter-feeding bivalves consume large quantities of photoplankton. This has significantly increased the proportion of primary production in the GL that is drawn to the benthos (Vanderploeg et al. 2001). This change has in turn altered the energy flow in the pelagic food web of the lakes, reducing sport and commercial fish production in some instances (Mills et al. 2003). Such food web changes that alter sport and commercial fishing can have repercussions for the entire regional economy as revenues from these sectors decline (Lupi et al. 2003, Perrings et al. 2002). When an issue affects a large proportion of society and when policy and management decisions on the issue must be made, addressing the issue in a way that reckons the implications of alternative policies or management activities in common units that are widely understood is often an effective strategy (Daly and Farley 2004). In most cases, the common units of reckoning are monetary (e.g., dollars). The conversion of the ecological impacts of invasive species or of the environmental effects of alternative management plans into dollars is a pragmatic way to account for the value that society 16
ascribes to a wide variety of goods and services, including those affected by biological invasions, in terms that are widely understood and which can be benchmarked against other societal issues and concerns. Chapter Three takes this type of bio-economic approach, employing SEJ to estimate the current annual economic impacts of ballast water NIS in the GL. This study concludes that the economic impacts of ballast water species are large, but also uncertain. Nevertheless, policies that aim to reduce the likelihood of additional invasions via this pathway appear to be economically justifiable. Knowledge of species dispersal is crucial to understanding the distribution and abundance of biota in the environment. Species may establish populations in patches of suitable habitat, but individuals must first disperse to such suitable patches. Therefore, understanding species dispersal is necessary to understand population spread and range expansion (Kot et al. 1996, Clark et al. 2003). Thus, the study of species dispersal has long been an important topic in ecology (Skellam 1951, Huffaker 1958, Howe and Smallwood 1982). Chapters Four and Five of my dissertation contribute to this branch of research by considering how human movements of recreational boats and trailers move AIS throughout the landscape. It is necessary to study boats and trailers instead of, for example, bird droppings or other natural dispersal mechanisms because it has become clear that the most important vectors for the spread of AIS are anthropogenic (Johnson et al. 2001, Hastings et al. 2005). As AIS in the GL region spread to other waterways, they bring with them ecological and economic impacts, motivating efforts to reduce their rate of spread. Chapter Four is one of the first scientific studies to investigate what species are actually being transported via the overland movement of recreational boats on trailers. This 17
chapter describes my research intended to inform efforts to slow AIS spread. I collected data on the type and volume of aquatic species being transported by the overland movement of recreational boats and trailers. I also tested the efficacy of multiple methods for removing aquatic NIS from recreational boats and trailers. I found that visual inspection and hand removal is highly effective in removing the nuisance macrophyte Myriophyllum spicatum, but that high-pressure washing is needed to effectively remove small-bodied organisms, including the exotic predatory zooplankter Bythotrephes longimanus. In Chapter Five I go beyond the tactics of how to clean boats and consider the strategic placement of inspection and boat-cleaning stations on the landscape. My results show that a common predictive modeling approach (gravity modeling) is limited in its ability to predict which uninvaded lakes are likely to be invaded next. Therefore, the lakes that cleaning stations should protect cannot be identified. Instead, it appears that placing cleaning stations to block the transport of invasive propagules away from invaded lakes is generally more likely to reduce landscape-level spread than protecting uninvaded lakes. Aquatic NIS are only one of many environmental and cultural factors that affect ecosystems and, in turn, affect societal interactions with the natural environment. To put the importance of aquatic NIS in context with other potential drivers of change in GL fisheries over the next two decades, I report the results of interviews with experts on GL fisheries in Chapter Six. In these interviews, I asked experts to predict changes in GL fisheries and to identify the most likely drivers of the changes they predicted. This study
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reveals that changing cultural interests are the main reason for expected declines in GL fisheries, but that NIS are the predominant environmental driver of change. Thus, in this dissertation, I provide case studies of real world problems pertaining to biological invasions in the GL region. I selected cases for which scientific inquiry had strong potential to improve the policy and management of invasive species. I report on the findings of my research and its implications for these real world problems. Furthermore, I contend that the pursuit of such knowledge, in a form that is relevant to management and policy, contributes to the science of ecology by pushing its boundaries in ways that may benefit the science more broadly. For example, in seeking to assess the damage from invasive species across an entire region, my research introduces an approach that may be used to assess the effects of a variety of large-scale ecological perturbations. Similarly, by trying to predict which uninvaded lakes will be invaded in the near future, my work demonstrates the value of retrospective analyses in ecology to test our ability to predict future environmental change.
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CHAPTER 2: THE LAURENTIAN GREAT LAKES ARE A FRESHWATER INVASION BEACHHEAD: PATHWAYS OF NONINDIGENOUS SPECIES INTRODUCTION PREDICT PRIOR DISTRIBUTION, SUBSEQUENT SPREAD, AND POTENTIAL IMPACTS1
2.1 Abstract Biological invasions alter ecosystems and reduce societal welfare. Resources to manage invasions are limited, and efforts to prevent the arrival and establishment of new invaders are often the most cost-effective management approach to prevent future damage. Effective prevention, however, requires knowledge that is rare: how introduction pathways affect the process and consequences of invasions. Using the Laurentian Great Lakes (GL) as a case study, we investigated the relationships between different pathways of introduction and (a) the prior global distribution of freshwater species introduced; (b) the likelihood of freshwater species to spread beyond the GL basin once they are established first there; and (c) the ecological and economic impact of nonindigenous freshwater species. We focused on two categories of pathways: shipping and commerce in living organisms (e.g., horticulture and pet industries). Among other
1
The publication status of this chapter is: Rothlisberger, J.R. and D.M. Lodge. The Laurentian Great Lakes are a freshwater invasion beachhead: pathways of nonindigenous species introduction predict prior distribution, subsequent spread, and potential impacts. Diversity and Distributions (in review).
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ideas, we tested the hypothesis that the shipping pathway makes the GL a beachhead of invasions of freshwater organisms to North America: we predicted that ship-related introductions in the GL are often first-time introductions to North America, and that from the GL, the same species often colonize many additional North American freshwater ecosystems. Results of our analyses of data on the global distribution of species pre- and post-introduction to the GL were consistent with the beachhead hypothesis. We found that the distribution of species prior to their discovery in the GL was related to introduction pathway, with ballast water releases more likely than other pathways to introduce new freshwater species to North America (85% of ballast water introductions). In contrast, commerce in living organisms was most likely to introduce to the GL freshwater species already established in North America (90% of species introduced by commerce in living organisms). Pathway, however, was a poor predictor of current distribution. Instead, time since discovery in the GL was the best predictor of current distribution: 88% of species discovered more than 74 years ago are now dispersed beyond the GL basin. To examine the relationship between pathway and impacts, we reviewed the scientific literature on species introduced to the GL. Results suggest that species introduced via ballast water are more likely to prey on native species, while species introduced via commerce in living organisms are more likely to impair recreational opportunities. Our results indicate that once a nonindigenous freshwater species is established in the GL it is only a matter of time before it appears in North American waterways beyond the GL basin.
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2.2 Introduction The establishment of species beyond their native range is a large and growing environmental problem (Vitousek et al. 1997, Mack et al. 2000). Some nonindigenous species become invasive, threatening native species biodiversity and ecosystem services (Wilcove et al. 1998, Sala et al. 2000), and causing large economic losses (Perrings et al. 2005, Pimentel et al. 2005). Increasingly globalization of commerce is the main driver of nonindigenous species introductions (Levine and D’Antonio 2003, Ruiz and Carlton 2003). The two principal categories of pathways by which humans transport species are (1) unintentional transport of organisms while conducting other activities and (2) commerce in live organisms, where the purpose of the activity is to move specific organisms (Lodge et al. 2006). Pathways have been proposed as the appropriate target for policy and management aimed at reducing future invasions (Lodge et al. 2006, Hulme et al. 2008). Management and policy that focus on pathways can simultaneously reduce the probability of establishment of the multiple species that may be transported in a pathway currently and in the future. With pathways as the fundamental unit for policy and management intended to reduce the introduction of alien species, practical actions to implement such policies are relatively straightforward: reduce the volume of traffic or the number of viable organisms in the pathway, at least of species that are likely to be invasive. Despite recent emphasis on pathway-based policy and management and their apparent benefits, there has been little study of the possible relationships between introduction pathways and how invasions proceed, including the eventual ecological impacts of the species they introduce (Hulme 2008). In other words, do pathways, as a 22
function of the species they are responsible for introducing, differ with respect to the magnitude or type of threat they pose to ecoystems and human welfare (e.g., ecosystem goods and services, infrastructure)? Knowing how the origin, spread, and harm caused by invasive species are related to pathways of introduction may help to inform policy response to particular pathways. Here, we use biological invasions of the Laurentian Great Lakes (GL) by freshwater species that are not native to North America as a case study to investigate how the impacts and subsequent spread of nonindigenous species are related to pathways of introduction. The GL offer an excellent opportunity for such an investigation because they contain many nonindigenous freshwater species that have a range of ecological impact types and severities (Mills et al. 1993b, Kelly et al. 2009, Chapter 3). Moreover, these species have been introduced via numerous pathways, including authorized release (e.g., fish stocking), commerce in living organisms (e.g., aquarium dumping), ballast water release, and solid ballast dumping (Mills et al. 1993b, Ricciardi 2006). In recent years, ballast water release has been the most important pathway for new introductions (Ricciardi 2006). Nonindigenous freshwater species in the GL region are relatively wellstudied and pertinent policy and management efforts to limit additional damage are ongoing (Mills et al. 1993b, NRC 2008). Thus, the GL have been and will likely continue to be an important nexus for science, policy, and management of nonindigenous freshwater species. The GL may also be a beachhead for the invasion of freshwater species into the rest of North America. In other words, as the largest freshwater ecosystem on the North American continent, the lakes may the site of initial introduction for nonindigenous 23
freshwater species, from which they can spread readily to other freshwaters on the continent. The recent spread of zebra and quagga mussels, whose original colonization site in North America was the GL, to Lake Mead and other waterways as far west as Utah and California, provides anecdotal evidence of this possible phenomenon (Stokstad 2007), which we refer to here as the beachhead hypothesis. The possibility that the GL are an initial harbor for nonindigenous freshwater species that may eventually become widespread in North America bears further investigation given that 63 of the 391 nonindigenous freshwater species currently established in North America were first discovered in the GL (http://nas.er.usgs.gov/). A fraction of these 63 species have already spread beyond the GL basin and the rest could perhaps follow. We address three specific questions and associated hypotheses. First, is there a relationship between a species’ pathway of introduction to the GL and its distribution prior to being discovered in the GL? That is, are some pathways more likely than others to bring to the GL species that are novel to North America? We hypothesized that, of the four pathways we considered, ballast water release would be more likely than the others to introduce species to the GL that were not previously found in North America than would be expected by random chance. Second, for freshwater species that were first discovered in North America in the GL, we tested whether their pathway of introduction to the GL was related to their current North American distribution (i.e., contained within the GL or spread beyond the GL). We also quantified which combination of explanatory variables (i.e., years since discovery in the GL, taxonomic identity, endemic region, first GL invaded), along with introduction pathway, could most accurately classify the current distribution species. 24
Identifying a relationship between pathway of introduction to the GL and spread beyond the GL would allow for targeted efforts to prevent the spread of species most likely to expand their range beyond the GL. We hypothesized that introduction pathway alone would be insufficient to predict current North American distribution accurately, but thought that by combining introduction pathway with other variables, we would be able to reliably predict current distribution. Third, we asked whether a species’ pathway of introduction to the GL predicted the type and magnitude of impacts caused by the species in the GL or other waterways. To do this, we reviewed the scientific literature on ecological and economic impacts of species introduced to the GL via ballast water release and commerce in living organisms. Knowing how pathways are related to impacts would allow managers and policy-makers to direct their efforts at the pathways most likely to introduce damaging invaders in the future. Because many of the species introduced by ballast water release are planktonic or small benthic organisms, we hypothesized that the ecological impacts of species from ballast water would be diffuse food web alterations, in contrast to the more taxonomically diverse set of species introduced by commerce in living organisms, whose impacts we expected to be more varied.
2.3 Methods
2.3.1 Pathway and distribution prior to discovery in Great Lakes We extracted a list of 95 established nonindigenous freshwater species in the GL from the database of all 184 established nonindigenous species known from the GL 25
(http://www.glerl.noaa.gov/res/Programs/ncrais/glansis.html). From the same database, for each species, we recorded the taxonomic category, year of discovery in the GL, endemic region, and pathway of introduction to the GL. The 95 species on which we focus are entirely freshwater (i.e., wetland plants are not included), and are nonindigenous to North America (Appendix A). Species in the database are grouped into the broad taxonomic categories of plant, benthic algae, phytoplankton, zooplankton, benthic crustacean, mollusk, annelid, other invertebrate, fish, and virus. Pathways of introduction in the database are categorized as ballast water release, solid ballast dumping, deliberate release (i.e., authorized fish stocking), aquarium dumping, bait release, unintentional release, canals, and unknown. For the purposes of our study, we refer to deliberate release as authorized release and contrast it with ballast water release, solid ballast dumping, and commerce in living organisms, a composite category containing species in the aquarium dumping, bait release, and unintentional release categories. The canal pathway is irrelevant to our study because no freshwater species that are not native to North America have been introduced to the GL via canals. We added to this database whether, prior to their discovery in the GL, each species was not yet known in North America or already established as a nonindigenous species elsewhere in North America. Information on North American distribution prior to GL discovery came mainly from species-specific sources cited in Mills et al. (1993), but some information also came from sources cited in the species accounts available through the United States Geological Survey’s Nonindigenous Aquatic Species database (http://nas.er.usgs.gov/).
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2.3.2 Pathway and spread beyond the Great Lakes To investigate relationships between invasion pathway and whether an invader has spread beyond the GL, we analyzed data for the subset of NIS whose first North American occurrence was in the GL (63 of the 95 species considered above). These species were categorized based on their current distribution (i.e., confined to the GL basin versus beyond the GL basin). For this analysis, we added information to our database on the current North American distribution of each of these 63 species from the USGS NAS database (http://nas.er.usgs.gov/) (Appendix A). We used recursive partitioning (a nonparametric statistical pattern-finding technique; De’ath and Fabricius 2000) to test whether introduction pathway was consistently related to current distribution. The response categories are the two options for current North American distribution relative to the GL basin (within or outside the GL basin). Other potential explanatory variables that we included in this analysis are year of discovery in the GL, lake where originally discovered, endemic region, and taxonomic category. The decision tree created by a recursive partitioning analysis is a result of balancing accurate classification of the training dataset (i.e., a sufficiently complex tree could correctly classify 100% of the observations in the training dataset) against parsimony sufficient to make the tree robust in accurately classifying new observations (i.e., the decision tree is not overfit to the training data). Testing the predictions of a decision tree against the known response values of an independent dataset is the ideal method for assessing whether or not this balance has been achieved, but this approach is not advised when the dataset is
