Integrative Zoology 2010; 5: 102-111
doi: 10.1111/j.1749-4877.2010.00193.x
REVIEW
Climate change and invasive species: double jeopardy
Susan A. MAINKA1 and Geoffrey W. HOWARD2
1
Science 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 policymakers. 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.
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 confirmed the growing evidence that climate is already changing our natural world. Similarly, the Climatic Atlas of European Breeding Birds (Huntley et al. 2007) reports that
Correspondence: Susan A. Mainka, International Union for
Conservation of Nature, rue Mauverney 28, CH1196 Gland,
Switzerland.
Email: [email protected]
102
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). Coldblooded 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). VaquerSunyer and Duarte (2008) report on impacts of decreasing
oxygen in marine environments, concluding that thresholds of vulnerability to hypoxia vary greatly across marine species. In addition, increasing carbon dioxide is raising 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,
© 2010 ISZS, Blackwell Publishing and IOZ/CAS
Climate change and invasive species
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 characteristics 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 specializations in terms of lifestyle or location are typically
most at risk. Using these characteristics, the International
Union for Conservation of Nature (IUCN) Species Survival Commission, a global network of species conservation 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. Species 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 invasive 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
© 2010 ISZS, Blackwell Publishing and IOZ/CAS
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 herbivores 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 Ecosystem Assessment (2005).
Baillie et al. (2004) report biological invasions as a major 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 particularly 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 threatened freshwater fish in Europe and just under 45% of threatened freshwater fish in Madagascar are affected by invasive species, the latter largely as a result of implementing
a plan to re-establish local fisheries by introducing 24 nonnative fish species (Benstead et al. 2003). Butchart (2008)
reports that the one-third of threatened bird species threatened by invasive species are at risk largely through predation 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-
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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 species 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. ability to survive in adverse conditions, rapid growth rates
and wide dispersal) will often help them succeed in competition with native species under climate change. Conditions that facilitate invasion that might be created by climate 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 invasive species; and (v) altered effectiveness of control
strategies. Another perspective, as discussed in the
present paper, is to consider the changes in the environment that would have an impact on species survival. These
include changes in temperature (terrestrial and marine),
precipitation, chemistry (terrestrial and marine), ocean circulation 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 characteristics of many invasive species promote their survival and,
thereby, natural selection for these characteristics in future 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 speculated 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
104
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 climate/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 impact of associated pest and pathogen species in those
forests. Currently, most examples of species’ range expansions 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 species that alter the invaded ecosystem even without climate 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 feeding 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 climate change and invasive species may intensify ecosystem effects and possibly increase the spatial extent of these
effects. A potential positive effect from increased invasive species is, in some cases, promotion of carbon sequestration by those species (Wardle et al. 2007).
In addition to highlighting the interaction across climate change and invasive species, these examples also
illustrate that:
Climate change can turn a native species into an invader (Mueller & Hellmann 2008) in its native habitat
by altering that habitat such that it is exotic to its original ecosystem situation,
Climate change can affect many aspects of an invading
© 2010 ISZS, Blackwell Publishing and IOZ/CAS
Climate change and invasive species
species including distribution, speed of dispersal, and
life history.
Climate change, invasive species and human
well-being
Both climate change and invasive species are economically 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
© 2010 ISZS, Blackwell Publishing and IOZ/CAS
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S. A. Mainka and G. Howard
East Asia and Africa plus the Middle East (Global Humanitarian 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 nations of the control of invasions is an estimated $US60m
per year (Chenje & Mohammed-Katerere 2002). Costs include 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 resources available.
Loss of habitat and biodiversity resulting from the interaction of climate change and invasive species will add
to these costs while also contributing to increased vulnerability 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 affecting income to national economies depending on tourism.
Climate change and biological invasions also have social/cultural implications, both in terms of impacts and
potential solutions. With respect to climate change, the
most vulnerable will be those people engaged in subsistence 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 poverty 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 climate 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 introduced tamarisks (Tamarix spp.) in south-western USA has
caused significant losses of native plants, including cottonwoods (Populus fremontii S. Wats.) and willows (Salix
spp.), which are used in traditional basketry. In contrast,
some traditional resource management practices in Hawaii have actually enhanced the spread of invasive spe-
106
cies while also providing the potential to control invasive
species through support of expert cultural practitioners
who incorporate weeding of invasive species into day-today 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, invasive species have the potential to compound the impacts of climate change on biodiversity and adversely affect 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 combined impacts of climate change and invasives are eliminated or minimized while enhancing the resilience of ecosystems 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 species management plans will be tools that provide an assessment of the invasion threat posed by each potentially
invasive species and tools that allow effective management of invasive species at the community level. Approaches 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’ responses to climate change more generally (e.g. Anderson
et al. 2009; Brook et al. 2009) should be useful for application more specifically to potentially invasive species.
Although risk management for biological invasions resulting from global change will always be a challenge, there
are already several assessment frameworks now available
or in development. Examples include the weed risk assessment system in use in Australia, which has been very accurate in assessing species of unknown invasive poten-
© 2010 ISZS, Blackwell Publishing and IOZ/CAS
Climate change and invasive species
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 strategies 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 mechanisms
enhancing knowledge and research efforts.
Eradication and control within adaptive management
strategies, including disaster recovery planning
The impact of either climate change or biological invasion 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, ecosystem managers should also be aware of potential secondary impacts of that eradication (Zavaleta et al. 2001;
Bergstrom et al. 2009). In some cases, removing one invader 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 populations of the invading species at acceptably low levels have
been attempted, usually through biological control.
However, the quicker-acting chemical and mechanical controls sometimes used pose many problems, including their
high cost and the low public acceptance of some practices (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-
© 2010 ISZS, Blackwell Publishing and IOZ/CAS
term (mitigation) strategies to manage the potential impact of such disasters. This recovery planning should also
incorporate measures to prevent invasions. For example,
invasive species were also a critical concern in the recovery plans for Hurricane Katrina, which hit New Orleans in
2006. The Formosan subterranean termite (Coptotermes
formosanus Shiraki, 1909) is native to China but was accidentally 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 Forestry passed the Formosan Termite Initiative Act, effectively quarantining debris from the disaster (Louisiana
Department of Agriculture 2005). The act notes that, “The
hurricane has left millions of tons of wood debris, including debris infested with Formosan Termites,” and that “Imposition 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 considered 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 invasive 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 control them and there is perverse risk that markets are created 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 reviewing 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.
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S. A. Mainka and G. Howard
Enabling policy environment
Climate mitigation and adaptation policy frameworks
should include consideration of biological invasions
(assessment, monitoring and management), both as indicators 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 concludes 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 renewable 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 consideration 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 evidence from the ecological aftermath of such events, including 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 invaded of the marine realms, increased shipping has been
implicated in the spread of invasions and, therefore, management policies should be implemented in these waters
to reduce the ever-present risk of invasions through transported ballast water and through hull fouling (Molnar et
al. 2008). Adapting invasive species management strategies 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
108
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 exacerbate 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 available or being further refined for better predictability.
4. Raising awareness of the climate change/biological invasion interaction and the consequent increase in
threats to biodiversity, development and human livelihoods 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 Consequences of Global Change (BCGC) sponsored by Bureau
of International Cooperation, Chinese Academy of Sciences (GJHZ200810).
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