climate change and invasive species double jeopardy
TRANSCRIPT
102 © 2010 ISZS, Blackwell Publishing and IOZ/CAS
REVIEW
Climate change and invasive species: double jeopardy
Susan A. MAINKA1 and Geoffrey W. HOWARD2
1Science and Learning Unit, International Union for Conservation of Nature, Gland, Switzerland and 2Regional Office for Eastern and
Southern Africa, International Union for Conservation of Nature, Nairobi, Kenya
Abstract
Two of the key drivers of biodiversity loss today are climate change and invasive species. Climate change is already
having a measurable impact on species distributions, reproduction and behavior, and all evidence suggests that
things will get worse even if we act tomorrow to mitigate any future increases in greenhouse gas emissions:
temperature will increase, precipitation will change, sea level will rise and ocean chemistry will change. At the same
time, biological invasions remain an important threat to biodiversity, causing species loss, changes in distribution
and habitat degradation. Acting together, the impacts of each of these drivers of change are compounded and
interactions between these two threats present even greater challenges to field conservationists as well as policy-
makers. Similarly, the social and economic impacts of climate change and invasive species, already substantial, will
be magnified. Awareness of the links between the two should underpin all biodiversity management planning and
policy.
Key words: climate change, ecosystem management, invasive species.
Correspondence: Susan A. Mainka, International Union for
Conservation of Nature, rue Mauverney 28, CH1196 Gland,
Switzerland.
Email: [email protected]
CLIMATE CHANGE IMPACTS ON
BIODIVERSITY
Climate is changing nature before our eyes. Species
distributions, demography, and even their life histories
are changing as previously reliable seasons are no longer
so predictable. A review was carried out of 1700 species
range shifts, showing an average 6.1 km movement per
decade towards the poles, and spring events advancing
by 2.3 days per decade (Parmesan et al. 2003). This con-
firmed the growing evidence that climate is already chang-
ing our natural world. Similarly, the Climatic Atlas of Eu-
ropean Breeding Birds (Huntley et al. 2007) reports that
the potential breeding distribution of most of Europe’s
breeding birds will shift several hundred kilometers north.
In addition, extirpations (local extinctions) and extinctions
of amphibians have been linked with climate change (Ron
et al. 2003; Burrowes et al. 2004; Pounds et al. 2006). Cold-
blooded species such as reptiles are also projected to fare
poorly in a warming world (Kearney et al. 2009).
Marine fishes are predicted to be affected by rising
water temperatures, which will change oxygen levels in
the world’s oceans (Poertner & Knust 2007). Vaquer-
Sunyer and Duarte (2008) report on impacts of decreasing
oxygen in marine environments, concluding that thresh-
olds of vulnerability to hypoxia vary greatly across ma-
rine species. In addition, increasing carbon dioxide is rais-
ing the acidity of the oceans, with severe impacts on some
marine communities, especially those taxa with skeletons
based on calcium carbonate.
In short, climate change will affect the distribution of
species, their demography and their life histories. These
changes will have consequences for human livelihoods,
Integrative Zoology 2010; 5: 102-111 doi: 10.1111/j.1749-4877.2010.00193.x
103© 2010 ISZS, Blackwell Publishing and IOZ/CAS
including changing the distribution patterns of human
disease and the spread of pest and weed infestations.
Climate change impacts on species are not distributed
equally across the spectrum of life, either taxonomically or
geographically. Foden et al. (2008) propose a set of char-
acteristics that would make a species more vulnerable to
climate change. These include species with:
specialized habitat and/or microhabitat requirements
narrow environmental tolerances or thresholds that are
likely to be exceeded due to climate change at any stage
in the life cycle
dependence on specific environmental triggers or cues
that are likely to be disrupted by climate change
dependence on interspecific interactions which are likely
to be disrupted by climate change
poor ability or limited opportunity to disperse to, or
colonize, a new or more suitable range
This list shows that those species with the highest spe-
cializations in terms of lifestyle or location are typically
most at risk. Using these characteristics, the International
Union for Conservation of Nature (IUCN) Species Sur-
vival Commission, a global network of species conserva-
tion experts, assessed selected taxa (birds, amphibians
and corals) for their vulnerability to climate change and,
therefore, potential increased risk of extinction (IUCN 2009).
They report that:
35, 52 and 71% of birds, amphibians and corals,
respectively, have traits that render them particularly
susceptible to climate change impacts
70–80% of birds, amphibians and corals that are already
threatened are also “climate-change-susceptible.”
IMPACTS OF BIOLOGICAL INVASIONS
ON BIODIVERSITY
Biological invasions occur when a species is introduced
to a habitat or ecosystem where it is not native and then
becomes established, spreads and causes damage to
biodiversity, human development or human health. Spe-
cies that bring about these biological invasions and the
associated changes in the habitat are termed “invasive
species.” The Invasive Species Specialist Group of IUCN
has developed the Global Invasive Species Database and
has also identified a list of 100 of the world’s worst inva-
sive alien species (IUCN 2010).
Invasive species can cause biodiversity loss, changes
in water chemistry, altered biogeochemical processes,
hydrological modifications and altered food webs
(Ehrenfeld 2003; Dukes & Mooney 2004) as well as changes
in availability of light, air, food, shelter and breeding sites
or of services such as pollination (Moroñ et al. 2009). For
birds, Butchart (2008) notes that biological invasions
threaten birds in many ways, including predation on adults,
reproductive stress through predation on eggs or chicks,
and habitat degradation (particularly by invasive herbi-
vores or invasive plants). As a result of these impacts,
biological invasions are an important threat to biodiversity
and ecosystem services; they are considered 1 of the 5
major threats to ecosystem integrity by Millennium Eco-
system Assessment (2005).
Baillie et al. (2004) report biological invasions as a ma-
jor threat faced by 11% of threatened amphibian species
and 8% of threatened mammals for which data are
available. They also note that island species are particu-
larly susceptible, noting that 67% of threatened birds on
oceanic islands are affected by invasives, compared to
8% of continental birds. Darwall et al. (2008) report that
85% of threatened fish in southern Africa, 55% of threat-
ened freshwater fish in Europe and just under 45% of threat-
ened freshwater fish in Madagascar are affected by inva-
sive species, the latter largely as a result of implementing
a plan to re-establish local fisheries by introducing 24 non-
native fish species (Benstead et al. 2003). Butchart (2008)
reports that the one-third of threatened bird species threat-
ened by invasive species are at risk largely through pre-
dation by carnivores and rodents.
Characteristics that define invasive potential include
both factors intrinsic to the invading species as well as
the habitat to be invaded. Howard and Ziller (2008) list
factors for invading plants, and we have added those for
animals, such as:
rapid growth rate
ability to grow well and reproduce in dry or otherwise
adverse conditions (have broad environmental
tolerance)
having many and well-protected fruits and seeds (high
yielding plant species)
having high rates of reproductive success and rearing
young or independent larval (and other immature stage)
survival (vertebrates and invertebrates)
producing fruit and seeds (or other plant propagules)
early in their growth and development for plants, and
breeding early in development for animals
ability to disperse widely through wind or water or by
animals that feed on them or carry their propagules (for
plants)
effective competition with other plants and animals.
Predicting potential invasiveness of any individual spe-
Climate change and invasive species
104 © 2010 ISZS, Blackwell Publishing and IOZ/CAS
S. A. Mainka and G. Howard
cies can be an uncertain process because invasions can
be confounded by issues of timing and change (Baskin
2002). In fact, the biological invasion process is always a
combination of the characteristic of the introduced spe-
cies and the “reactions” of the invaded ecosystem.
Nevertheless, numerous decision-support tools have been
developed to help assess potential invasiveness of species,
including Pheloung et al. (1999), Jefferson et al. (2004)
and Gordon et al. (2008).
Acting together, climate and invasions
The traits of species that make them invasive (i.e. abil-
ity to survive in adverse conditions, rapid growth rates
and wide dispersal) will often help them succeed in com-
petition with native species under climate change. Condi-
tions that facilitate invasion that might be created by cli-
mate change can be viewed from several perspectives.
Hellman et al. (2008) consider the stages of the invasion
pathway and identify the following mechanisms: (i) altered
transport and introduction mechanisms; (ii) establishment
of new invasive species; (iii) altered impact of existing
invasive species; (iv) altered distribution of existing inva-
sive species; and (v) altered effectiveness of control
strategies. Another perspective, as discussed in the
present paper, is to consider the changes in the environ-
ment that would have an impact on species survival. These
include changes in temperature (terrestrial and marine),
precipitation, chemistry (terrestrial and marine), ocean cir-
culation and sea levels (see examples in Table 1). Climate
change also tests the adaptive capacity of native species
through these changes to their environment, making it
difficult for native species to survive, allowing invaders
to take over empty niches, or compromising the native
species’ ability to compete against hardy generalist
invaders. From a Darwinian perspective, the characteris-
tics of many invasive species promote their survival and,
thereby, natural selection for these characteristics in fu-
ture generations. However, in some cases, the interaction
between climate change and invasive species might not
be in favor of the invader, as in the case of some invasive
coldwater species (Rahel & Olden 2008). Nevertheless,
acting together, climate change and invasive species can
put many native species in situations beyond their ability
to successfully compete.
As early as 1993, climate/invasive species interactions
were noted by Binggeli and Hamilton (1993), who specu-
lated that climate change played a role in the spread of the
alien tree Maesopsis eminii Engl. in the East Usumbara
mountain forests, Tanzania. They cite temperature changes,
extremes of precipitation and decreased mist as potential
factors promoting Maesopsis invasion. The impacts can
be both direct, on survival of a species in question, and/or
indirect in terms of influence on other factors such as pest
or prey species. For example, one of the impacts of cli-
mate/invasives interaction noted recently was decreased
numbers of grizzly bears (Peacook 2009), hypothesized to
be a result of decreasing availability of the nuts of whitebark
pine which provide an important autumn food source for
the bears (Perkins & Roberts 2003). Similarly, Dukes et al.
(2009) note that climate change will directly affect trees in
northeastern North America, as well as influence the im-
pact of associated pest and pathogen species in those
forests. Currently, most examples of species’ range ex-
pansions in response to climate change are terrestrial (see
Root et al. 2003; Roura-Pascual et al. 2004; Parmesan &
Yohe 2006; Sugiura 2009) or from freshwater, as in the
northward movement of water hyacinth (Eichhornia
crassipes (Mart.) Solms) in Europe (S. Brunel, pers. comm.).
Some invasive species do not require climate change to
damage ecosystems, yet climate change might exacerbate
the damage they do cause. Two examples of invasive spe-
cies that alter the invaded ecosystem even without cli-
mate change are the common carp (Cyprinus carpio L.,
1758) and salt cedar (Tamarix ramosissima Ledeb). The
common carp, native to Asia, decreases water quality (by
increasing turbidity) and destroys viable nesting and feed-
ing habitat for other desirable species of fish in other parts
of the world, while the drought tolerant and deep-rooted
salt cedar, native to Eurasia, dominates riparian forests
that were once dominated by cottonwoods and willows in
North America (Kolar & Lodge 2000; Lite & Stromberg
2005; Charles & Dukes 2007). Climate change might have
positive feedbacks for both of these invading species if
waters warm in the mid-western and northern USA and if
south-western USA experiences more frequent droughts,
leading to an increase in the amount of suitable habitat to
invade (Seager et al. 2007). This interaction between cli-
mate change and invasive species may intensify ecosys-
tem effects and possibly increase the spatial extent of these
effects. A potential positive effect from increased inva-
sive species is, in some cases, promotion of carbon se-
questration by those species (Wardle et al. 2007).
In addition to highlighting the interaction across cli-
mate change and invasive species, these examples also
illustrate that:
Climate change can turn a native species into an in-
vader (Mueller & Hellmann 2008) in its native habitat
by altering that habitat such that it is exotic to its origi-
nal ecosystem situation,
Climate change can affect many aspects of an invading
105© 2010 ISZS, Blackwell Publishing and IOZ/CAS
species including distribution, speed of dispersal, and
life history.
Climate change, invasive species and human
well-being
Both climate change and invasive species are economi-
cally important threats. In a report on the economics of
climate change (Stern 2006), the costs of climate change
were estimated to be 5% of global GDP per year. In terms
of human impact, the Global Humanitarian Forum estimates
that 90% of these losses will be mainly in South and South-
Table 1 Examples of climate change influences on invasiveness of species
Climate change and invasive species
106 © 2010 ISZS, Blackwell Publishing and IOZ/CAS
East Asia and Africa plus the Middle East (Global Hu-
manitarian Forum 2009).
The estimated annual damage from invasive species
worldwide totals more than $1.4tn: 5% of the global
economy (Pimentel et al. 2001). The cost to African na-
tions of the control of invasions is an estimated $US60m
per year (Chenje & Mohammed-Katerere 2002). Costs in-
clude not only direct management costs like prevention,
eradication and mitigation of invasive species, but also
indirect costs of loss of ecosystem services, such as clean
water, plant products and decreased ecotourism revenues.
Strategic and prioritized management of invasive species
is essential and urgent, especially given the limited re-
sources available.
Loss of habitat and biodiversity resulting from the in-
teraction of climate change and invasive species will add
to these costs while also contributing to increased vul-
nerability of rural communities whose livelihoods and
household incomes are derived, either directly or indirectly,
from natural products. For example, climate change, and
the associated temperature and ozone changes, can alter
the invasive capabilities of pests of common agricultural
and horticultural crops (Kiritani 2007; Booker et al. 2009;
Jaramillo et al. 2009). Loss of habitat and biodiversity also
poses a threat to wildlife-based tourism, therefore affect-
ing income to national economies depending on tourism.
Climate change and biological invasions also have so-
cial/cultural implications, both in terms of impacts and
potential solutions. With respect to climate change, the
most vulnerable will be those people engaged in subsis-
tence agriculture because of the many constraints that
limit their capacity to adapt to change (Morton 2007). The
2007/2008 Human Development Report (UNDP 2007, 2)
highlights the potential impact of climate change on pov-
erty reduction strategies and development planning and
notes that failure to fully address the impacts of climate
change will “consign the poorest 40 percent of the world’s
population to a future of diminished opportunity.”
However, local and traditional knowledge about natural
resource management can form an important basis for cli-
mate change adaptation planning and implementation, as
has already been demonstrated in the Arctic (Ford et al.
2006) and Sahel (Nyong et al. 2007).
Pfeiffer and Ortiz (2007) report that the spread of intro-
duced tamarisks (Tamarix spp.) in south-western USA has
caused significant losses of native plants, including cot-
tonwoods (Populus fremontii S. Wats.) and willows (Salix
spp.), which are used in traditional basketry. In contrast,
some traditional resource management practices in Ha-
waii have actually enhanced the spread of invasive spe-
cies while also providing the potential to control invasive
species through support of expert cultural practitioners
who incorporate weeding of invasive species into day-to-
day resource management activity (Ticktin et al. 2006).
However, implementing an invasive species management
program can also disrupt traditional management practices
(Hanson 2004). Clearly, any program to manage impacts
of climate change and invasive species will need to be
developed in consideration of not only environmental
needs, but also social and economic needs.
Measures that need to be taken
Biodiversity can play a role in mitigating the impacts of
climate change and supporting adaptation. However, in-
vasive species have the potential to compound the im-
pacts of climate change on biodiversity and adversely af-
fect biodiversity’s potential to play this role. Conversely,
taking measures to prevent or control invasive species
can enhance an ecosystem’s resilience to climate change.
Therefore, actions should be taken to ensure that the com-
bined impacts of climate change and invasives are elimi-
nated or minimized while enhancing the resilience of eco-
systems to support mitigation and adaptation.
Improved understanding of invasiveness and links with
climate change
Although scientists are already identifying many of the
linkages, continuing research is needed, especially with
respect to the ability to accurately predict the spread of
biological invasions in the context of global change. A
critical resource for developing or adapting invasive spe-
cies management plans will be tools that provide an as-
sessment of the invasion threat posed by each potentially
invasive species and tools that allow effective manage-
ment of invasive species at the community level. Ap-
proaches that have been proposed to help refine such
assessments include use of models combining local and
global, biotic and abiotic factors (Ficetola et al. 2007) and
use of variants of niche through BIOCLIM, DOMAIN and
MAXENT modeling (Ward 2007). In addition, modeling
approaches being developed to understand species’ re-
sponses to climate change more generally (e.g. Anderson
et al. 2009; Brook et al. 2009) should be useful for applica-
tion more specifically to potentially invasive species.
Although risk management for biological invasions re-
sulting from global change will always be a challenge, there
are already several assessment frameworks now available
or in development. Examples include the weed risk assess-
ment system in use in Australia, which has been very ac-
curate in assessing species of unknown invasive poten-
S. A. Mainka and G. Howard
107© 2010 ISZS, Blackwell Publishing and IOZ/CAS
tial (Gordon et al. 2008). Such tools need to be refined, as
new knowledge about invasiveness becomes available,
and used as regular components of risk management strat-
egies for all sectors, especially agriculture and energy.
These can also be applied to climate change situations to
use in the prevention of biological invasions.
The Invasive Species Specialist Group of the Species
Survival Commission of IUCN has produced “Guidelines
for the prevention of biodiversity loss caused by alien
invasive species” (IUCN 2000), which provide direction
on preventing and managing invasive species across 4
areas; namely,
improving understanding and awareness
strengthening the management response
providing appropriate legal and institutional mecha-
nisms
enhancing knowledge and research efforts.
Eradication and control within adaptive management
strategies, including disaster recovery planning
The impact of either climate change or biological inva-
sion is a dynamic process and highly dependent on the
characteristics of the invading species as well as those in
the habitat being invaded. Any strategy to eradicate or
control an invasion will have to include the principles of
adaptive management. In undertaking eradication, ecosys-
tem managers should also be aware of potential second-
ary impacts of that eradication (Zavaleta et al. 2001;
Bergstrom et al. 2009). In some cases, removing one in-
vader has simply provided space for another to move in.
Control and eradication plans should be developed with a
landscape scale approach to take into consideration, as
much as possible, these secondary effects.
Successful eradication cases have 3 key factors in
common: particular biological features of the target
species; sufficient economic resources devoted for a long
time; and widespread support from the relevant agencies
and the public (Mack et al. 2000). When eradication is not
possible, or if it is not desired, as in the case of native
species invading through range expansion, some measures
of “maintenance control” aimed at maintaining popula-
tions of the invading species at acceptably low levels have
been attempted, usually through biological control.
However, the quicker-acting chemical and mechanical con-
trols sometimes used pose many problems, including their
high cost and the low public acceptance of some prac-
tices (Mack et al. 2000).
Climate change is already demonstrably increasing the
number of extreme natural events (e.g. floods and
hurricanes) and many countries are developing longer-
term (mitigation) strategies to manage the potential im-
pact of such disasters. This recovery planning should also
incorporate measures to prevent invasions. For example,
invasive species were also a critical concern in the recov-
ery plans for Hurricane Katrina, which hit New Orleans in
2006. The Formosan subterranean termite (Coptotermes
formosanus Shiraki, 1909) is native to China but was acci-
dentally introduced into the USA, and has since invaded
at least 9 southern states. Prior to hurricane Katrina, the
Formosan termite was responsible for an estimated
$US100m annually in damage to homes and businesses in
the New Orleans area (US EPA 2005). Following Hurricane
Katrina, the Louisiana Department of Agriculture and For-
estry passed the Formosan Termite Initiative Act, effec-
tively quarantining debris from the disaster (Louisiana
Department of Agriculture 2005). The act notes that, “The
hurricane has left millions of tons of wood debris, includ-
ing debris infested with Formosan Termites,” and that “Im-
position of this quarantine is required to prevent the spread
of Formosan termites and infestation of areas, homes and
structures that are not currently infested, or which are to
be built or reconstructed.”
Invasive-aware energy choices
Interestingly, many characteristics of crops being con-
sidered for cultivation as biofuels are shared by invasive
species, such as being fast growing and having high
productivity, adaptability to a range of soil and climatic
conditions and resistance to pests and diseases (Howard
& Ziller 2008). Nipa palm (Nypa fruticans Wumb), for
example, has invaded and colonized over 200 km2 of the
Atlantic coast of Nigeria and can produce far greater
biofuel per hectare than sugar cane, according to some
experts. All introduced crops for biofuel production
should, therefore, be treated as suspect or potentially in-
vasive until proven otherwise. While simply harvesting
existing problem invasives species such as water hyacinth,
lantana (Lantana camara L.) and nipa palm might present
an attractive option for biofuel feedstocks, it will not con-
trol them and there is perverse risk that markets are cre-
ated for such invasives species, thereby encouraging their
spread and so further damaging biodiversity.
Continuing on a fossil-fuel based economy path will
not support the action needed to mitigate climate change,
and some energy choices, specifically biofuels, have added
additional environmental stress through the introduction
of invasive species. Buddenhagen et al. (2009), in review-
ing potential biofuel crops for Hawaii through application
of a weed risk assessment system, determine that those
crops were 2–4 times more likely to become invasive.
Climate change and invasive species
108 © 2010 ISZS, Blackwell Publishing and IOZ/CAS
Enabling policy environment
Climate mitigation and adaptation policy frameworks
should include consideration of biological invasions
(assessment, monitoring and management), both as indi-
cators of change and in their own right. Climate change
can facilitate invasions leading to impacts and costs, and
invasions can increase the magnitude of climate impacts
on people. Therefore, it is vital that policy decisions taken
with respect to climate change include consideration of
invasive species. A recent review of the vulnerability of
Australia’s biodiversity to climate change recognizes the
potential of compounding threats to biodiversity and con-
cludes that: “Significant changes are required in policy
and management for biodiversity conservation to meet
these types of challenges” (Steffen et al. 2009, 1).
In practical terms, this can mean that production of re-
newable energy sources such as biofuels should only be
undertaken in a manner that does not introduce invasives.
The Roundtable on Sustainable Biofuels has drafted a set
of guidelines for sustainability that incorporate consider-
ation of the potential invasiveness of biofuel feedstocks
(RSB 2008).
Given that it is expected that climate change will result
in an increased number of extreme events, and that evi-
dence from the ecological aftermath of such events, in-
cluding that from Hurricane Katrina noted above as well
as the 2004 Indian Ocean tsunami (UNEP 2005) includes
impacts from invading species, it is imperative to consider
the potential of combined impacts when planning and
implementing policy for disaster risk management.
Setting policy frameworks for invasive species that fail
to consider climate change can mean missing out on vital
issues that are required to prevent and control invasion.
Geographic frameworks that do not build in flexibility might
bring biological disaster in the future. For example, with
decreasing ice in the Arctic as a result of climate change,
far northern waters might soon become a major shipping
lane. Although the Arctic is currently among the least in-
vaded of the marine realms, increased shipping has been
implicated in the spread of invasions and, therefore, man-
agement policies should be implemented in these waters
to reduce the ever-present risk of invasions through trans-
ported ballast water and through hull fouling (Molnar et
al. 2008). Adapting invasive species management strate-
gies to cope with the effects of climate change will be
required at a range of scales, including continental,
regional, national and local. Bierwagen et al. (2008) note
that an adaptive management approach will facilitate this
integration and that climate change monitoring activities
should be fundamental elements of such approaches. As
noted above, they will need to be developed within the
context of local cultures and traditional practices.
Pyke et al. (2008) propose that for optimum synergy
across climate change and invasive species policy, the
following 3 principles should be followed:
ensure that climate change mitigation does not exacer-
bate invasive species problems
invasive species management should take climate
change into account
climate change adaptation activities should contribute
to invasive species management.
CONCLUSIONS
1. Climate change and invasive species are two drivers of
biodiversity loss that, acting together, can compound
impacts on the environment in general and biodiversity
in particular.
2. Taking action to address one or the other threat alone
may not lead to desired results either for biodiversity
or human well being.
3. Tools for addressing this situation are currently avail-
able or being further refined for better predictability.
4. Raising awareness of the climate change/biological in-
vasion interaction and the consequent increase in
threats to biodiversity, development and human liveli-
hoods is a critical element for successful prevention
and/or management of the resulting impacts.
ACKNOWLEDGEMENTS
The authors wish to thank two anonymous reviewers
for their helpful comments and additional references to
improve the manuscript. We would also like to thank the
ISZS international research program Biological Conse-
quences of Global Change (BCGC) sponsored by Bureau
of International Cooperation, Chinese Academy of Sci-
ences (GJHZ200810).
REFERENCES
Anderson BJ, Akçakaya HR, Araújo MB et al. (2009). Dy-
namics of range margins for metapopulations under cli-
mate change. Proceedings of the Royal Society B 276,
1415–20.
Baillie J, Hilton-Taylor C, Stuart SN (2004). 2004 IUCN Red
List of Threatened Species: A Global Species
Assessment. IUCN - World Conservation Union, Spe-
cies Survival Commission. Gland, Switzerland.
Barnes DKA (2002). Invasions by marine life on plastic
S. A. Mainka and G. Howard
109© 2010 ISZS, Blackwell Publishing and IOZ/CAS
debris. Nature 416, 808–9.
Baskin Y (2002). A Plague of Rats and Rubber Vines: The
Growing Threat of Species Invasions. Island Press,
Washington, DC.
Benstead JP, De Rham PH, Gattoliat JL et al. (2003). Con-
serving Madagascar’s freshwater biodiversity. Bio-
science 53, 1101–11.
Bergstrom D, Lucieer A, Kiefer K et al. (2009). Indirect ef-
fects of invasive species removal devastate World Heri-
tage Island. Journal of Applied Ecology 46, 73–81.
Bierwagen BG, Thomas R, Kane A (2008). Capacity of man-
agement plans for aquatic invasive species to integrate
climate change. Conservation Biology 22, 568–74.
Binggeli P, Hamilton AC (1993). Biological invasion by
Maesopsis eminii in the East Usambara forests,
Tanzania. Opera Botanica 121, 229–35.
Booker F, Muntifering R, McGrath M et al (2009). The ozone
component of global change: Potential effects on agri-
cultural and horticultural plant yield, product quality
and interactions with invasive species. Journal of Inte-
grative Plant Biology 51, 337–51.
Braby CE, Somero GN (2006). Ecological gradients and rela-
tive abundance of native (Mytilus trossulus) and inva-
sive (Mytilus galloprovincialis) blue mussels in the Cali-
fornia hybrid zone. Marine Biology 148, 1249–62.
Brook BW, Akçakaya HR, Keith DA, Mace GM, Pearson
RG, Araújo MB (2009). Integrating bioclimate with popu-
lation models to improve forecasts of species extinc-
tions under climate change. Biology Letters 5, 723–5.
Buddenhagen CE, Chimera C, Clifford P (2009). Assessing
biofuel crop invasiveness: A case study. PLoS ONE 4,
e5261.
Burrowes PA, Joglar RL, Green DE (2004). Potential causes
for amphibian declines in Puerto Rico. Herpetologica
60, 141–54.
Butchart S (2008). Red List Indices to measure the
sustainability of species use and impacts of invasive
alien species. Bird Conservation International 18,
S245–62.
Charles H, Dukes JS (2007). Impacts of invasive species on
ecosystem services. In: Nentwig W, ed. Biological
invasions, Ecological Studies Vol. 193. Springer, New
York, pp. 217–37.
Chen DX, Coughenour MB, Eberts D et al. (1994). Interac-
tive effects of CO2 enrichment and temperature on the
growth of dioecious Hydrilla verticillata. Environmen-
tal and Experimental Botany 34, 345–53.
Chenje M, Mohammed-Katerere J (2002). Invasive alien
species. In: Africa Environment Outlook. UNEP, Nairobi,
Kenya, pp. 331–49.
Darwall W, Smith K, Allen D et al. (2008). Freshwater
biodiversity – A hidden resource under threat. In: Vié
JC, Hilton-Taylor C, Stuart SN, eds. Wildlife in a Chang-
ing World: An Analysis of the 2008 IUCN Red List of
Threatened Species. IUCN, Gland, Switzerland pp. 43–
54.
Dukes JS, Mooney HA (2004). Disruption of ecosystem
processes in western North America by invasive species.
Revista chilena de historia natural 77, 411–37.
Dukes JS, Pontius J, Orwig D et al. (2009). Responses of
insect pests, pathogens, and invasive plant species to
climate change in the forests of northeastern North
America: What can we predict? Canadian Journal of
Forest Research 39, 231–48.
Ehrenfeld JG (2003). Effects of exotic plant invasions on
soil nutrient cycling processes. Ecosystems 6, 503–23.
Ficetola GF, Thuiller W, Miaud C (2007). Prediction and
validation of the potential global distribution of a prob-
lematic alien invasive species – The American bullfrog.
Diversity and Distributions 13, 476–85.
Foden W, Mace G, Vié JC et al. (2008). Species susceptibil-
ity to climate change impacts. In: Vié JC, Hilton-Taylor
C, Stuart SN, eds. Wildlife in a Changing World: An
Analysis of the 2008 IUCN Red List of Threatened
Species. IUCN, Gland, Switzerland, pp. 77–88.
Ford JD, Smit B, Wandel J (2006). Vulnerability to climate
change in the Arctic: A case study from Arctic Bay,
Canada. Global Environmental Change 16, 145–60.
Global Humanitarian Forum (2009). Human Impact Report:
Climate change – The Anatomy of a Silent Crisis.
Geneva, Switzerland. [Cited 19 Feb 2010.] Available at
URL: www.ghf-ge.org
Gordon DR, Onderdonk DA, Fox AM, Stocker RK (2008).
Consistent accuracy of the Australian weed risk assess-
ment system across varied geographies. Diversity and
Distributions 14, 234–42.
Hanson DE (2004). ASSIST: Development of the American
Samoa Selected Invasive Species Task Force. Weed Tech-
nology 18, 1334–7.
Hellmann JJ, Byers JE, Bierwagen BG, Dukes JS (2008).
Five potential consequences of climate change for in-
vasive species. Conservation Biology 22, 534–43.
Howard G, Ziller S (2008). Alien alert – Plants for biofuel
may be invasive. Bioenergy Business July/August, 14–
6.
Huntley B, Green RE, Collingham YC, Willis SG (2007). A
Climate change and invasive species
110 © 2010 ISZS, Blackwell Publishing and IOZ/CAS
Climatic Atlas of European Breeding Birds. Lynx
Edicions, Barcelona, Spain.
IUCN (2000). IUCN Guidelines for the Prevention Of
Biodiversity Loss Caused By Alien Invasive Species.
[Cited 19 Feb 2010.] Available at URL: http://www.issg.
org/infpaper_invasive.pdf
IUCN Species Survival Commission (SSC) (2009). Wildlife
in a changing world: An analysis of the 2008 IUCN
Red List of Threatened Species. IUCN, Gland,
Switzerland.
IUCN (2010). 100 of the world’s worst invasive alien species.
[Cited 19 Feb 2010.] Available at URL: http://www.issg.
org/database/species/search.asp?st=100ss
Jaramillo J, Chabi-Olaye A, Kamonjo C et al. (2009). Ther-
mal tolerance of the Coffee Berry Borer Hypothenemus
hampei: Predictions of climate change impact on a tropi-
cal insect pest. PLoS ONE 4, e6487.
Jefferson LA, Havens K, Ault J (2004). Implementing inva-
sive screening procedures: The Chicago botanic model.
Weed Technology 18, 1434–40.
Kearney M, Shine R, Porter WP (2009). The potential for
behavioral thermoregulation to buffer “cold-blooded”
animals against climate warming. PNAS 106, 3835–40.
Kiritani K (2007). The impact of global warming and land-
use change on the pest status of rice and fruit bugs
(Heteroptera) in Japan. Global Change Biology 13,
1586–95.
Kolar CS, Lodge DM (2000). Freshwater nonindigenous
species: Interactions with other global changes. In:
Mooney HA, Hobbs RJ, eds. Invasive species in a
changing world. Island Press, Washington, DC, pp. 3–
30.
Kurz KA, Dymond CC, Stinson G et al. (2008). Mountain
pine beetle and forest carbon feedback to climate change.
Nature 452, 987–90.
Lambert CC, Lambert G (2003). Persistence and differential
distribution of nonindigenous ascidians in harbors of
the Southern California Bight. Marine Ecology Progress
Series 259, 145–61.
Lite SJ, Stromberg JC (2005). Ground-water and surface
water thresholds for maintaining Populus-Salix forests,
San Pedro River, Arizona. Biological Conservation 125,
153–67.
Logan JA, Powell JA (2001). Ghost forests, global warming,
and the mountain pine beetle (Coleoptera: Scolytidae).
American Entomologist 47, 160–73.
Lonsdale WM (1993). Rates of Spread of an Invading
Species: Mimosa Pigra in Northern Australia. Journal
of Ecology 81, 513–21.
Louisiana Department of Agriculture and Forestry, Office
of Agricultural and Environmental Sciences (2005). Im-
position of Quarantine. [Cited 19 Feb 2010.] Available
from URL: http://www.ldaf.state.la.us/portal/Portals/0/
AES/Horticulture/katrinaquarantine.pdf
Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M,
Bazzaz FA (2000). Biotic invasions: Causes,
epidemiology, global consequences, and control. Eco-
logical Applications 10, 689–710.
Millennium Ecosystem Assessment (2005). Synthesis 2005.
[Cited 19 Feb2010.] Available at URL: http://www.
millenniumassessment.org/documents/document.356.
aspx.pdf
Molnar JM, Gamboa RL, Revenga C, Spalding MD (2008).
Assessing the global threat of invasive species to ma-
rine biodiversity. Frontiers in Ecology and Environ-
ment 6, 485–92.
Moroñ D, Lenda M, Skórka P, Szentgyörgyi H, Settele J,
Woyciechowski M (2009). Wild pollinator communities
are negatively affected by invasion of alien goldenrods
in grassland landscapes. Biological Conservation 142,
1322–32.
Morton JF (2007). The impact of climate change on small-
holder and subsistence agriculture. PNAS 104, 19680–
85.
Nyong A, Adesina F, Osman EB (2007). The value of indig-
enous knowledge in climate change mitigation and ad-
aptation strategies in the African Sahel. Mitigation and
Adaptation Strategies for Global Change 12, 787–97.
Parmesan C (2006). Ecological and evolutionary responses
to climate change. Annual Review of Ecology, Evolu-
tion and Systematics 37, 637–69.
Parmesan C, Yohe G (2003). A globally coherent fingerprint
of climate change impacts across natural systems. Na-
ture 421, 37–42.
Peacook D (2009). Yellowstone’s grizzly bears face threats
on two fronts. Yale Environment 360 14 May [Cited 10
Feb 2010.] Available from URL: http://e360.yale.edu/con-
tent/feature.msp?id=2152
Perkins DL, Roberts DW (2003). Predictive models of
whitebark pine mortality from mountain pine beetle. For-
est Ecology and Management 174, 495–510.
Pfeiffer JM, Ortiz EH (2007). Invasive plants impact Califor-
nia Native plants used in traditional basketry. Fremontia
35, 7–13.
Pheloung PC, Williams PA, Halloy SR (1999). A weed risk
assessment model for use as a biosecurity tool evaluat-
S. A. Mainka and G. Howard
111© 2010 ISZS, Blackwell Publishing and IOZ/CAS
ing plant introductions. Journal of Environmental Man-
agement 57, 239–51.
Pimentel D, McNair S, Janecka J et al. (2001). Economic
and environmental threats of alien plant, animal, and
microbe invasions. Agriculture, Ecosystems and Envi-
ronment 84, 1–20.
Poertner HO, Knust R (2007). Climate change affects ma-
rine fishes through the oxygen limitation of thermal
tolerance. Science 315, 95–7.
Poloczanska ES, Babcock RA, Butler A et al. (2007). Cli-
mate change and Australian marine life. In: Gibson RN,
Atkinson RJA, Gordon JDM, eds. Oceanography and
Marine Biology: An Annual Review, Vol. 45. CRC Press,
Boca Raton, Florida, USA, pp. 407–78.
Pounds JA, Bustamante MR, Coloma LA et al. (2006). Wide-
spread amphibian extinctions from epidemic disease
driven by global warming. Nature 469, 161–7.
Pyke CR, Thomas R, Porter RD et al. (2008). Current prac-
tices and future opportunities for policy on climate
change and invasive species. Conservation Biology 22,
585–92.
Rahel FJ, Olden JD (2008). Assessing the effects of climate
change on aquatic invasive species. Conservation Bi-
ology 22, 521–33.
Renner C (2004). Plant dispersal across the tropical Atlan-
tic by wind and sea currents. International Journal of
Plant Science 165 (4 Suppl.), S23–33.
Ron SR, Duellman WE, Coloma LA, Bustamante MR (2003).
Population decline of the Jambato Toad Atelopus
ignescens (Anura: Bufonidae) in the Andes of Ecuador.
Journal of Herpetology 37, 116–26.
Root TL, Price JT, Hall KR, et al. (2003) Fingerprints of
global warming on wild animals and plants. Nature 421,
57–60.
Roundtable for Sustainable Biofuels (RSB) (2008). Global
principles and criteria for sustainable biofuels
production, Version Zero. [Cited 19 Feb 2010.] Available
from URL: http://cgse.epfl.ch/webdav/site/cgse/shared/
Biofuels/VersionZero/Version%20Zero_RSB_Std_en.
Roura-Pascual N, Suarez AV, Gómez C, Pons P et al. (2004).
Geographical potential of Argentine ants (Linepithema
humile Mayr) in the face of global climate change. Pro-
ceedings of the Royal Society of London B 271, 2527–34.
Seager R, Ting M, Held I et al. (2007). Model projections of
an imminent transition to a more arid climate in south-
western North America. Science 316, 1181–4.
Steffen W, Burbidge A, Hughes L et al. (2009). Australia’s
biodiversity and climate change: Summary for policy
makers 2009. Summary of a report to the Natural Re-
source Management Ministerial Council commissioned
by the Australian Government, pp. 1. [Cited 19 Feb 2010.]
Available from URL: http://www.climatechange.gov.au/
~/media/publications/biodiversity/biodiversity-sum-
mary-policy-makers.ashx
Stern N (2006). Stern Review on the Economics of Climate
Change. [Cited 19 Feb 2010.] Available from URL: http:/
/www.hm-treasury.gov.uk/independent_reviews/
s t e rn_rev iew_economics_c l ima te_change /
sternreview_index.cfm
Sugiura S (2009). Seasonal fluctuation of invasive flatworm
predation pressure on land snails: Implications for the
range expansion and impacts of invasive species. Bio-
logical Conservation 142, 3013–9.
Ticktin T, Whitehead AN, Fraiola H (2006). Traditional gath-
ering of native hula plants in alien-invaded Hawaiian
forests: Adaptive practices, impacts on alien invasive
species and conservation implications. Environmental
Conservation 33, 185–94.
UNDP (United Nations Development Programme) (2007).
UNDP 2007/2008 Human Development Report: Fighting
climate change: Human solidarity in a divided world, pp.
2. [Cited 19 Feb 2010.] Available from URL: http://hdr.
undp.org/en/reports/global/hdr2007-2008/
UNEP (United Nations Environment Programme) (2005).
After the Tsunami: Rapid Environmental Assessment.
UNEP, Nairobi, Kenya.
US EPA (Environmental Protection Agency) (2005). The
Formosan Subterranean Termite in Georgia. [Cited 19
Feb 2010.] Available from URL: http://www.caes.uga.edu/
departments/ent/upmp/termites.html
Vaquer-Sunyer R, Duarte CM (2008). Thresholds of hy-
poxia for marine biodiversity. PNAS 105, 15452–7.
Ward DF (2007). Modelling the potential geographic distri-
bution of invasive ant species in New Zealand. Biologi-
cal Invasions 9, 723–35.
Wardle DA, Bellingham PJ, Fukami T, Mulder CPH (2007).
Promotion of ecosystem carbon sequestration by inva-
sive predators. Biology Letters 3, 479–82.
Zavaleta ES, Hobbs RJ, Mooney HA (2001). Viewing inva-
sive species removal in a whole-ecosystem context.
Trends in Ecology and Evolution 16, 454–9.
Climate change and invasive species