Measuring and managing invasive species threats in the Arctic

151 Pages·2014·7.67 MB·English

by  Christopher Ware

Measuring and managing invasive species threats
in the Arctic

by
Chris Ware
B. Sc (Hons)
Thesis submitted in partial fulfilment of the requirements for the degree of PhD
University of Tasmania

School of Geography and Environmental Studies
University of Tasmania
March 2014
Declaration of originality
This thesis contains no material which has been accepted for a degree or diploma by the University or any
other institution, except by way of background information and duly acknowledged in the thesis, and to the
best of my knowledge and belief no material previously published or written by another person except where
due acknowledgement is made in the text of the thesis, nor does the thesis contain any material that infringes
copyright.
Chris Ware Date 31 March 2014

Statement of authority of access
The publishers of the papers comprising Chapters 2 and 5 hold the copyright for that content, and access to
the material should be sought from the respective journals. The remaining non published content of the thesis
may be made available for loan and limited copying and communication in accordance with the Copyright Act
1968
Chris Ware Date 31 March 2014

Statement of Ethical Conduct
The research associated with this thesis abides by the international and Australian codes on human and animal
experimentation, the guidelines by the Australian Government's Office of the Gene Technology Regulator and
the rulings of the Safety, Ethics and Institutional Biosafety Committees of the University.

Chris Ware Date 31 March 2014

i
Statement of co-authorship
The following people and institutions contributed to the publication of work undertaken as part of this thesis:
Chapter 2: Ware C, Bergstrom DM, Müller E, Alsos IG (2012) Humans introduce viable seeds to the Arctic on
footwear. Biological Invasions, 14(3), 567-577.
Chris Ware, School of Geography and Environmental Studies / University Centre on Svalbard, Norway
Dana Bergstrom, Australian Antarctic Division
Eike Müller, University Centre on Svalbard, Norway
Inger Greve Alsos, Tromsø University Museum, Norway
Author contributions: IGA conceived idea, all authors contributed to project design, CW and EM carried out
sampling, laboratory work and data analysis, CW wrote the manuscript with input from all authors.
CW (candidate) (60%), IGA (20%), EM (15%), DMB (5%)
We the undersigned agree with the above stated “proportion of work undertaken” for the above published
peer-reviewed manuscripts contributing to this thesis:
Signed: __________________ ______________________
(James Kirkpatrick) (Name)
Supervisor Head of School
School Of Geography School of Geography
and Environmental Studies and Environmental Studies
University of Tasmania University of Tasmania
Date:_____________________

Chapter 3*: Alsos IGA, Ware C, Elven R (submitted manuscript) Past Arctic aliens passed away, current ones
may stay.
Author contributions: IGA conceived research questions and project design, IGA, CW, and RE conducted
sample collection, RE led the taxonomic revisions with input from IGA, IGA assembled and analysed the data
with CW, IGA wrote the manuscript with input from all authors.
CW (candidate) (30%), IGA (60%), RE (10%)
* Contributions for this work are concluded here as I was not the primary author.
ii
Chapter 5: Ware C, Kirkpatrick, JB, Sundet JH, Jelmert A, Berge J, Coutts ADM, Floerl O, Pellissier L, Wisz MS,
Alsos IG (2014). Climate change, non-indigenous species and shipping: assessing the risk of species
introduction to a high-Arctic archipelago. Diversity and Distributions, 20(1), 10-19.
Chris Ware, School of Geography and Environmental Studies / Tromsø University Museum, Norway
James Kirkpatrick, University of Tasmania, Sandy Bay, Tasmania, Australia
Jan Sundet, Institute of Marine Research, Norway
Anders Jelmert, Institute of Marine Research, Bergen, Norway
Jørgen Berge, University of Tromsø / University Centre on Svalbard, Norway
Ashley Coutts, Biofouling Solutions PTY LTD, Kingston, Tas., Australia
Oliver Floerl, SINTEF Fisheries & Aquaculture, Trondheim, Norway
Steffen Olsen, Danish Meteorological Institute, Denmark
Loïc Pellissier, Aarhus University, Denmark
Mary Wisz, Aarhus University, Denmark / Greenland Institute of Natural Resources, Greenland
Inger Greve Alsos, Tromsø University Museum, Norway

Author contributions: CW and IGA conceived research questions and project design, SMO, MW, and LP
provided environmental data, CW assembled and analysed data with advice from JBK and OF, and CW wrote
the manuscript with input from all authors.
CW (candidate) (70%), JBK (10%), IGA (10%), remaining authors together (10%)
We the undersigned agree with the above stated “proportion of work undertaken” for the above published
peer-reviewed manuscripts contributing to this thesis:
Signed: __________________ ______________________
(James Kirkpatrick) (Name)
Supervisor Head of School
School Of Geography School of Geography
and Environmental Studies and Environmental Studies
University of Tasmania University of Tasmania

Date:_____________________

iii
Abstract
Several decades of invasive species research have yielded a broad understanding of the nature of species
transfer mechanisms and associated threats globally. This is not true of the Arctic, however, a region where
increasing human activity and ongoing climate change is expected to promote species invasion. This thesis
examines the potential for both terrestrial and marine non-indigenous species (NIS) to be introduced to and
establish in the Arctic under present and future climatic conditions. Throughout, the work uses the high-Arctic
archipelago Svalbard as a model for the wider Arctic region. The research focuses on two of the most well-
described pathways of species introduction globally, human visitation and shipping, both of which are
increasing in intensity in Svalbard. Potential for species introduction and establishment is examined by
quantifiying and identifying propagule loads transferred to the Arctic; developing and testing species
identification methods; evaluating present and forecasting future habitat suitability for NIS; measuring the
spread of established non-indigenous vascular plants; and testing the efficacy of management measures
designed to prevent further species introduction.
Results demonstrate high plant propagule transport by people travelling to highly-visited Arctic regions is
occurring. Furthermore, propagule pressure associated with ship hull fouling poses immediate risks, while if
more stringent management related to ships’ ballast water discharge is not enacted this vector will pose an
increasing risk over the coming century. Improved vector screening methods were achieved through testing a
molecular species identification approach for organisms transported with ships, but the approach was found
to be inefficient in a biosecurity management context. Climate changes, and particularly temperature
increases, over the coming century are expected to increase Svalbard habitat suitability for both terrestrial and
marine species. Acknowledgment of the negative impacts NIS may have in Svalbard has led to the
implementation of preventative management measures designed to reduce species transfer by visitors and
ships; however, these were found to have limited effect. Scope for improved management is outlined.
Where species invasion risks are found to exist at the transport stage, the body of invasion ecology knowledge
suggests a precautionary approach whereby NIS introduction should be prevented. The imperative to ensure
this in polar regions has historically been lacking, owing largely to the strength of climatic barriers, and
assumed weak propagule pressure. By quantifying propagule pressure across different pathways and vectors,
and estimating changing habitat suitability under forecast climatic conditions, this research provides the basis
upon which to develop more informed biosecurity management for Svalbard. Moreover, given the similarity in
pathways of species introduction across the Arctic region, the work presented here suggests an Arctic-wide
need to address management and policy gaps.

iv
Acknowledgements
A number of people and organisations have provided advice, assistance, and support through the course of
this work. I wish to gratefully acknowledge and thank them for their contribution.
My Norwegian supervisor, Inger Greve Alsos, deserves particular acknowledgment for her continued support
in facilitating and supervising the project work that constitutes this thesis. Given the substantial amount of her
time required to organise an Australian to undertake this work in Norway, and the onerous task placed on her
of swiftly becoming a marine ecologist, her support in, and commitment to this project was absolutely
fundamental.
My gratitude is also extended to the University Centre on Svalbard, and the Tromsø University Museum where
Inger was employed during my candidature. My project evolved dynamically, and had the resultant support
granted by the Tromsø University Museum been foreseeable at the outset of my studies, more formal
recognition of this institute’s contribution to my studies would have been sought.
I wish to thank also my Australian supervisor, Jamie Kirkpatrick, for continued advice, assistance, and
perceptiveness, which greatly benefited the development of this thesis.
The funding support of the Svalbard Environmental Fund (Chapters 2-5, 7) and of the Fram Centre (Chapters 5-
7) is gratefully acknowledged.
The assistance of Store Norsk and the Svalbard Sysselmannen is gratefully acknowledged for providing air
transport and accommodation to support ballast water sampling. In addition I would like to thank the Russian
coal mining company Arktikugol and the shipping companies Norden and the Murmansk Shipping Company,
for their assistance and cooperation in ballast water sampling.
The support and assistance rendered by Ilja Lang and Frigg Jørgensen from the Association of Arctic Expedition
Cruise Operators (AECO) to the development and conduct of work undertaken for Chapter 3 is gratefully
acknowledged.
The AECO members, Quark, Oceanwide, Spitsbergen Travel, Silversea Expeditions, GAP, and their respective
expedition staff, are gratefully acknowledged for their cooperation in collecting samples and participating in
research that contributed to chapters 2, 4 and 5.
I wish to thank a number of people who offered their expertise throughout the course of this research (Georgy
Semenov, Ole Aardbakke, Oli Floerl, Ashley Coutts, Darren Kriticos, Slawek Kwasniewski, Andrey Sikorski,
Elisabeth Larson, and Dean Paini).
I would also like to thank Dean Paini for organising office space at CSIRO for the concluding months of my PhD.
Finally, I wish to thank my partner, Sarah. It wouldn’t have worked with anyone else.

v
Table of Contents

1. Measuring and managing invasive species threats in the Arctic: general
introduction ............................................................................................................................... 1
Why measure and manage invasive species? .................................................................. 1
Is it possible to predict which species will become invasive? ......................................... 3
How to organise research around identifying and managing risks of species
Introduction? .................................................................................................................... 4
Invasive species in the Arctic ........................................................................................... 6
Measuring and managing invasive species threats in the Arctic ..................................... 8
Thesis outline ................................................................................................................... 9
Study site ....................................................................................................................... 10
References ..................................................................................................................... 11
2. Humans introduce viable seeds to the Arctic on footwear .................................... 20
Abstract ......................................................................................................................... 21
Introduction .................................................................................................................... 22
Methods ........................................................................................................................ 23
Results ........................................................................................................................... 25
Discussion ...................................................................................................................... 29
References ..................................................................................................................... 31
3. Past Arctic aliens have passed away, current ones may stay ................................ 37
Abstract ......................................................................................................................... 38
Introduction .................................................................................................................... 39
Methods ........................................................................................................................ 40
Results ........................................................................................................................... 41
Discussion ....................................................................................................................... 43
Conclusion ..................................................................................................................... 45
References ..................................................................................................................... 45
4. The efficacy of footwear disinfection to prevent microbial species introduction
to the Arctic ........................................................................................................................... 50
Abstract ......................................................................................................................... 51
Introduction .................................................................................................................... 52
Methods ........................................................................................................................ 53
Results ........................................................................................................................... 54
Discussion ...................................................................................................................... 55
Conclusion ...................................................................................................................... 57
References ..................................................................................................................... 57
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5. Climate change, non-indigenous species, and shipping: assessing the risk of
species introduction to a high-Arctic archipelago ..................................................... 63
Abstract ......................................................................................................................... 64
Introduction .................................................................................................................... 65
Methods ........................................................................................................................ 66
Results ........................................................................................................................... 68
Discussion ...................................................................................................................... 72
Conclusion ...................................................................................................................... 75
References ..................................................................................................................... 76
6. Applicability of universal primers for identifying zooplankton in ship ballast
water ................................................................................................................................... 81
Abstract ......................................................................................................................... 82
Introduction .................................................................................................................... 83
Methods ........................................................................................................................ 84
Results ........................................................................................................................... 87
Discussion ...................................................................................................................... 90
Conclusion ...................................................................................................................... 93
References ..................................................................................................................... 94
7. Is marine species invasion a threat to a warming Arctic? ....................................... 98
Abstract ......................................................................................................................... 99
Introduction .................................................................................................................. 100
Methods ...................................................................................................................... 102
Results ......................................................................................................................... 105
Discussion .................................................................................................................... 111
Conclusion .................................................................................................................... 113
References ................................................................................................................... 114
8. Synthesis ............................................................................................................................... 122
Perspectives .................................................................................................................. 126
9. Appendix 1 ........................................................................................................................... 127
10. Appendix 2 ........................................................................................................................... 135
11. Appendix 3 ........................................................................................................................... 142

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Chapter 1: General introduction
Chapter 1: Measuring and managing biological invasions in the
Arctic: general introduction
Increases in the intensity and scale of international travel and trade have escalated the frequency and extent
of global species transfer (Mack et al. 2000, Tatem and Hay 2005, Hulme 2009, Pyšek et al. 2010). Most
activities associated with travel and trade have the potential to mediate the introduction of non-indigenous
species (NIS) (Hulme 2009), and as a result few regions are free of NIS (Catford et al. 2012). A proportion of
introduced species – somewhere around 10 % (Strayer 2011, Vila et al. 2010) – establish, spread, and become
invasive, often negatively impacting on indigenous biodiversity, ecosystem functioning and services,
economies, or human health (Pyšek and Richardson 2010). Understanding the processes underlying species
invasion is pivotal to forecasting where future risks of invasion and impact lie (Faacon et al. 2006). The
research effort has been biased towards later stages of invasion (stages post NIS-introduction – see Fig 1)
(Puth and Post 2005), and has neglected the important role of inadvertent species introduction (Hulme et al.
2008, Huiskes et al. 2014). We still have a poor understanding of the rate, type, and magnitude of threat posed
by species transferred inadvertently, yet introduction is the stage in the invasion process where management
interventions are most successful (Mack et al. 2000, Leung et al. 2002). Where socio-economic systems and
climates are changing so too are rates of species transfer. Refocusing research effort to address this
knowledge gap is vital.
Why measure and manage invasive species?
Critics of the fields of invasion ecology research and invasive species management often highlight the benefits
NIS may provide in calling for reduced or no efforts to study or prevent species introduction (e.g. Davis et al.
2011, Schlaepfer et al. 2011). While this view acknowledges the important role some NIS play in modern
societies (our dependence on crop species which are often NIS for example), it is ignorant of the wider picture.
Several decades’ worth of research and data collection enables meta-analyses of large and diverse data sets,
making it possible to now empirically evaluate the benefit of preventing NIS introductions. Such analyses
clearly demonstrate that the ratio of NIS that produce desirable as compared to undesirable impacts is low
(Vitule et al. 2012).
Box 1 What are biological invasions?
Biological invasion is a process whereby an organism is transferred by human agency (purposefully or
inadvertently) beyond the biogeographical range achieved naturally, and then subsequently establishes and
spreads in the novel habitat (IUCN 2000, Blackburn et al. 2011). Human agency is a key aspect to the
definition of biological invasion as it stipulates those range expansions that are not considered invasions –
that is, species naturally occurring in a given region which for one reason or another spread rapidly, and
species which are naturally transferred beyond the geographical range they otherwise achieve. This is
important as it defines the scope of biological invasion management.
Discussion has centred on whether this definition should include a measure of impact (e.g. Ricciardi and
Cohen 2007). Generally (but not strictly), impact is not implied in the ecological definition (though impact at
some level might be assumed given the spread of a non-indigenous organism), but is assumed in policy papers
and legislation (Ricciardi and Cohen 2007).
1
Chapter 1: General introduction
Box 2 Terminology
The variety of terminology and synonyms used in biological invasion research – and the often indiscriminate
mixing of terminology – has long been a source of confusion that has hindered comparisons and processes in
biological invasion, and has led to the reinvention of concepts and hypotheses (Blackburn et al. 2011).
Invasive species is a term that applies to any organism that fits the definition at the beginning of this section.
Non-native, non-indigenous, alien, and exotic are all synonyms for species that have been moved beyond
their natural geographic range through human agency, but these terms have no measure of impact associated
with them. That is, an invasive species is always a non-native species, but the reverse is not always true. The

term pest species is commonly used with reference to invasive vertebrates, while the term weed is often used
with reference to invasive plants. Similarly, harmful algae are invasive algae. Noxious and nuisance are two

further synonyms applied to non-indigenous species that cause negative impacts.

In this thesis, the term non-indigenous (NIS) or alien will be used and reserved for any introduced species that
has not yet spread. Invasive species will be used for any NIS/alien that has spread, but will not imply impact.

Vectors are the physical means by which species are transported beyond their indigenous range.

Pathway refers to the processes that result in the introduction of alien species from one location to another.

Impacts on biological diversity vary from reducing genetic variation and eroding gene pools, through to
extirpating populations of indigenous species, and irreversibly altering habitat and ecosystem functioning
(Hulme 2008, Bergstrom et al. 2009, Moles et al. 2012). Impacts may be rendered directly (e.g. through
predatory actions, Goldschmidt 1998), or indirectly, generally over longer time scales (e.g. through the use of
limiting resources, Didham et al. 2005). Some of the most severe ecological impacts caused by invasive species
include the extinction of over 150 indigenous species of fresh water fish through the introduction of one
species of NIS (Nile perch, Lates niloticus) (Goldschmidt 1998); trophic cascades on remote islands associated
with the introduction of Norway rats (Rattus norvegicus) (Kurle et al. 2008); and the destruction of tens of
thousands of hectares of wetland vegetation following the invasion of a semiaquatic mammal (nutria,
Myocastor coypus) (Pyke et al. 2008).
Biological invasions also cause economic and human health impacts that can be measured as financial costs or
human morbidity (Leung et al. 2002, Pimentel et al. 2005, Keller et al. 2007, Vila et al. 2010). For example,
costs incurred by biological invasions have been estimated to amount to 5% of the global gross domestic
product (Pintennal et al. 2005). Regional estimates of costs are also substantial. For NIS established in the US
across all taxonomic divisions, impacts were estimated to cost US$120 billion per year (Pimentel et al. 2005).
Sinden et al. (2004) estimated yearly costs to government agencies associated with monitoring, control,
management, and research on weeds were at least AUS$116.4 million. NIS impacts may affect a wide range of
ecosystem services that underpin human well-being, including provisioning of food and fibre; regulating the
spread of human diseases; and tourism benefits (Pejchar and Mooney. 2009, Pyšek and Richardson 2010).
Thus, disruption of ecosystem services as a result of biological invasions may have adverse socioeconomic, and
human health impacts, of which the financial and healthcare-associated burden can be high (Pyšek and
Richardson 2010).
2