Download A call for an end to calls for the end of invasion biology

Oikos 000: 001–006, 2013
doi: 10.1111/j.1600-0706.2013.01228.x
© 2013 The Authors. Oikos © 2013 Nordic Society Oikos
Subject Editor: Dries Bonte. Accepted 15 October 2013
A call for an end to calls for the end of invasion biology
Daniel Simberloff and Jean R. S. Vitule
D. Simberloff ([email protected]), Dept of Ecology and Evolutionary Biology, Univ. of Tennessee, Knoxville, TN 37996, USA.
– J. R. S. Vitule, Laboratório de Ecologia e Conservação, Depto de Engenharia Ambiental, Setor de Tecnologia, Univ. Federal do Paraná,
81531, 980, Curitiba, Paraná, Brazil.
Calls for the end of invasion biology are misguided. There is no evidence that modern invasion biology has progressed
slowly in its short life. Although some aspects of biological invasions fit comfortably in the framework of ecological
succession, many others do not. Some native species, particularly in the wake of various anthropogenic impacts, behave
like invasive non-native species, but the probability and degree of harmful impact are greater for non-native than for
native species. Neither native nor non-native species suffer lack of attention and research by virtue of the fact that
invasion biology focuses on the latter. Basing management solely on current observed impact is highly risky because
impacts may be subtle but nonetheless important, and impacts often change, as they are contingent on the physical
or biotic environment. The known harmful impacts of many non-native species suggest that recent introductions
warrant attention even if impacts are not evident. Neither is the focus of modern invasion biology on non-native
species motivated by xenophobia. Rather, it reflects the recognition of their likelihood of harmful impact. A related
call for the end of traditional restoration ecology shares many features with calls to terminate invasion biology, not
least because management of invasive non-native species is a key component of restoration ecology. Such species are a
dominant element in generating the ‘novel ecosystems’ that are said to render traditional restoration ecology obsolete.
The argument that both invasion management and traditional restoration are largely futile endeavors is contradicted by
substantial and growing successes in both fields.
What is it about invasion biology? No one calls for an end
to conservation biology or marine biology or aquatic ecology
or physiological ecology, but now Valéry et al. (2013),
following Davis (2009), call for an end to invasion biology,
at least as we currently know it. Surely it is unusual for
two authors (Davis 2009, Lefeuvre 2013 [a coauthor in
Valéry et al.]) to write monographs on a subject while simultaneously calling for its immediate demise. However, a
science wanes and disappears not because of such calls,
but rather as researchers, particularly young ones not committed to a particular perspective, cease to find the old field
exciting and progressive and find some other research
paradigm more fruitful (Kuhn 1962, Lakatos 1970). In ecology, something of this sort occurred with the decline of phytosociology by the 1960s in favor of a more general plant
ecology (Ewald 2003). By contrast, invasion biology is
vibrant and growing, with entire journals devoted to the
subject (e.g. Biological Invasions, NeoBiota, Aquatic Invasions, BioInvasions Records), numerous invasion articles in
prominent ecology journals (e.g. Ecology, Diversity and
Distributions, Ecology Letters, Molecular Ecology, Ecological
Applications, Oikos) and conservation journals (e.g. Biological
Conservation, Conservation Biology, Conservation Letters),
a rising tide of invasion biology books (Simberloff 2004),
an increasing number of regular international conferences
(e.g. NeoBiota, EMAPi, Biolief, the international conferences on aquatic nuisance species, the ICBI conferences in
China), and sessions every year at several annual society
meetings.
Is invasion biology proceeding too slowly?
As do Valéry et al. (2013), Davis et al. (2005) and Davis
(2009) lament what they see as the slow progress of invasion
biology, which they attribute to the failure of invasion
biologists to fold their discipline into the much older and, in
their view, highly productive field of succession ecology.
However, they present no evidence that modern invasion
biology has progressed slowly in its short (ca 25 years –
cf. Simberloff 2011b) existence, and the burgeoning plethora
of papers, books and conferences cited above belies the
claim. The very fact that Davis (2009) and Lefeuvre (2013)
wrote entire monographs about modern invasion biology,
with calls for its termination relegated to small sections,
suggests that the field remains interesting and progressive.
Davis (2009) even admitted that his call for its end was
surely quixotic. In fact, Davis’s call led to a response by Lövei
et al. (2012) that in turn inspired a new network (MDBI –
Megadiverse Region BioInvasion Network) composed
mostly of scientists from developing nations who aim to
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protect the biodiversity of megadiverse regions from threats
by invasive non-native species through collaboration on
research and management strategies.
If abolishing invasion biology by merging it with
succession ecology would allow scientists to progress more
rapidly in understanding and managing invasions, this
abolition will arise not by pronouncements but by workers
in the field recognizing the opportunities and progressively
working under the new paradigm rather than the old one,
as Kuhn (1962) and Lakatos (1970) describe for scientific
progress in general.
be studied if invasions were solely considered from the
perspective of plant succession. The massive invasion of the
yellow crazy ant Anoplolepis gracilipes on Christmas Island
(O’Dowd et al. 2003, Abbott 2004), facilitated by a nonnative scale insect, is a good example. Traditional successional models would also not accommodate many of the
aquatic invasions that are a leading feature of modern invasion biology (Gherardi 2007, Francis 2011). And some
aquatic invasions have major impacts on adjacent terrestrial
ecosystems, as has the introduction of mysid shrimp to
Flathead Lake, USA (Spencer et al. 1991, Ellis et al. 2011).
Are invasions just a part of ecological succession?
Why not incorporate native species in invasion
biology?
Davis (2009) seeks to end invasion biology mainly
because he feels the processes of plant succession subsume
those of plant invasion, so the latter should be studied in
the framework of the former rather than as part of a separate
discipline. This is not a new argument. For instance, Egler
(1942) suggested that the processes that led certain
introduced plants in the Hawaiian Islands to spread widely
and others to remain restricted or to die out were basically
the same as those that drove certain native plant species to
replace other native plant species during ordinary secondary
succession and that the same sort of research would be
needed to elucidate both phenomena. Unlike Davis (2009)
and Davis et al. (2011), however, Egler (1947) recognized
that the rapid impact of particular introduced plants, such
as red mangrove Rhizophora mangle and Chilean mesquite
Prosopis chilensis, was likely to surpass that of any native species. Davis (2009) and Davis et al. (2011) tend to downplay
the impact of non-native species and incorporate them
into the larger body of impacts of any kinds of species, native
or non-native. However, as will be discussed in the next
section, both the likelihood of substantial impact and the
magnitude of impact are far greater for non-native species.
In any event, the argument to incorporate invasion
biology in succession ecology was directed at plants only
(Davis et al. 2005), not at animals or microorganisms. As
Elton (1927) pointed out in one of the earliest books on
animal ecology, animal ecologists should understand plant
succession because of its influence on animal population
abundance and dynamics, but he also suggested that
plant ecologists should study animals, not least because
sometimes animal populations control plant succession. For
instance, Egler (1947) pointed to introduced grazing
livestock as “paramount” in the disintegration of the
“conventional” concept of succession back to a climax.
Research in invasion biology has provided a wealth of evidence not only on the specifics of Elton’s assertion (e.g. the
influence of introduced reindeer: Leader-Williams 1988,
goats: Cronk 1989, and rabbits: Copson and Whinam
1998, on plant succession) but also on how impacts of nonnative animal species are greatly influenced by introduced
non-native plant species (Lewandowski 1982) or vice
versa (Aplet 1990, Woodward et al. 1990). Certainly the
progress of some invasions fits comfortably in traditional
models of plant community succession, but other invasion
phenomena are very different from successional processes
(Egler 1947, Simberloff 2010). For example, many instances
of “invasional meltdown” (Simberloff 2006) would scarcely
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Similarly to Davis (2009) and Davis et al. (2011), Valéry
et al. (2013) object to the focus of invasion biology on nonnative species, claiming that it has “restricted the relevance
of the field both from theoretical and practical viewpoints.”
A close examination of Valéry et al. (2013) shows that
their title is an example of literary hyperbole, exploiting the
prominence achieved by Davis’s earlier call. Valéry et al.
(2013) do not really demand that scientists stop studying
invasions. Rather, their gripe is that some native species act,
in certain circumstances, in similar ways to some nonnative species that become invasive. This is true (see references in Simberloff et al. 2012). Valéry’s own doctoral
dissertation on the rapidly spreading European intertidal
grass Elymus athericus is an excellent example (Valéry 2006).
It is also true that the number of such situations is a small
fraction of the tally of those involving non-native species.
For instance, in the United States, non-native plant species
are 40 times more likely than native plant species to behave
in ways that would be termed invasive (Simberloff et al.
2012). In those instances where native plant species have
become troublesome and begun to replace native plants,
this has almost always been in response to some major
anthropogenic change in the environment, such as fire
suppression or grazing of livestock (Simberloff et al. 2012).
Furthermore, Paolucci et al. (2013) have shown that nonnative predators and herbivores inflict greater damage on
prey and host populations, respectively, than do native predators and herbivores; likewise, Salo et al. (2007) found that,
among terrestrial vertebrates, non-native predators are more
dangerous than native predators to prey populations. The
reason for these striking results has not been proven, but Aldo
Leopold (1939) probably guessed it correctly – native species
have coevolved with one another for eons, while introduction
of a non-native species lacking the opportunity for coadaptation is likely to disrupt parts of the native ecosystem.
Does science or society suffer because the relatively few
native species that become problematic are not generally
considered under the rubric ‘invasive species’? They are
certainly still studied; this is why Simberloff (2011a) and
Valéry et al. (2013) could easily cite a few. The nature of the
particular damage caused by any non-native or native species
and the reason some species are problematic and others
are not are difficult questions that can be answered only
by sustained study of the particular case at hand. We doubt
that this is not being done simply because some problematic
species is native. The junipers that Valéry et al. (2013) point
to, following Leopold (1924, 1944), Simberloff et al. (2012)
and many others, have been the subject of extensive research,
both as to the cause of their spread and means of controlling
it. To the extent that rapid expansions of native species
shed light on invasions by non-native ones, this information
is widely available in the ecological and management literature and is cited by invasion biologists.
Is invasion biology xenophobic?
Davis (2009) and Davis et al. (2011) level a darker charge
against invasion biology’s focus on non-native species. They
hint that it reflects or at least encourages xenophobia –
consider, for instance, the title of Davis et al. (2011):
“Don’t judge species on their origins.” This is an accusation
long raised against invasion biology by writers in other fields,
particularly the social sciences – e.g. philosophy (Sagoff
1999), history (Pauly 1996), art history (Helmreich 1997),
anthropology (Tsing 1995), sociology (Larson 2011),
geography (Warren 2011), women’s studies (Subramaniam
2001), garden architecture (Wolschke-Bulmahn 1997) –
but occasionally by ecologists (Brown 1989). It has entered
the popular media (Raffles 2011). In the United States,
some critics of non-native species a century ago doubtless
were motivated by the same nativist animus that swept
American politics during this period, but there is little evidence that such motivations have been present during the
rise of modern invasion biology (Coates 2006). Similar
statements in Europe in the first half of the 20th century
were at least partly motivated by xenophobia (Simberloff
2003). However, even during the prehistory of invasion
biology, much of the early motivation for concern about
non-native species and regulations governing them was
demonstrable, highly visible ecological damage, such as
that wrought by introduced predators and plant pathogens
(Simberloff 2003).
Does it make sense to focus on impacts, not origins?
The notion of critics of invasion biology that management
should focus on impacts rather than origins (Davis et al.
2011) is short-sighted on several grounds (cf. Simberloff
2013, Simberloff et al. 2013). First, invasion biology is a
very young field, as noted above (cf. Pyšek and Hulme 2009),
and very few non-native species have been studied in sufficient detail in their native and non-native ranges for us to
have a good sense of what their impacts really are. Second,
recent research shows that many introduced species (e.g.
those that modify soil chemistry) have consequences for
entire ecosystems that are initially subtle but ultimately as
severe as those of the predatory animals and overgrowing
plants that have attracted the most attention (Ehrenfeld
2011). Third, many non-native species persist innocuously
in restricted areas and numbers for an extended period
before suddenly exploding across the landscape (Crooks
2005). The reasons for these lag times are sometimes
apparent and other times mysterious, but the fact of their
existence is not in doubt. These lags contribute to what Essl
et al. (2011) have termed an “invasion debt” of impacts that
will occur in the future from invasions that have already
occurred. Finally, the phenomenon of invasional meltdown,
previously discussed, demonstrates that a currently harmless
invader can cause major damage in the future if particular
other species are introduced. Invasional meltdown and
lag effects show that invasion impact may change drastically.
It is contingent on presence or absence of other species
and on changes in physical conditions that may be very
slight but may greatly affect the extent and impact of an
invasion (the “invasion cliff” phenomenon described by
Davis 2009). Our limited knowledge of many invasion
impacts, their contingency, and the demonstrably greater
likelihood and size of non-native impact over native impact
(Salo et al. 2007, Simberloff et al. 2012, Paolucci et al.
2013) imply that deciding on whether to attempt to control
a non-native species based on its current perceived impact
and not on its non-native origin is a highly risky strategy.
Is it futile to fight invasions?
Davis et al. (2011) also suggest that invasion biologists are
overly focused on a futile fight to control many invasions
for which substantial impacts are not evident, thereby
wasting resources that could be better spent in the service
of conservation. Thomas (2013) echoes this concern, seeing such programs as a “waste of effort” powered by an
“irrational dislike of invading species.” These ideas are
echoed by science writers (Marris 2010, Vince 2011).
This argument is at least partly based on the faulty view
that all invasions are targeted for action, when in fact
managers and policymakers are forced by chronic lack of
funding to focus almost exclusively on a few invaders with
highly visible impacts, often associated with threats to agriculture or public health. This problem has long been
lamented by invasive species managers and is the aegis for
the broad effort among invasion biologists to produce risk
assessment tools for management triage (Skinner et al.
2000, Stohlgren and Schnase 2006).
For recent invaders that have not spread widely, the cost
of action is often relatively low and, in light of the uncertainty about future impacts described above, it would be
wise to attempt to eradicate or to contain them (Simberloff
et al. 2013). Shackelford et al. (2013), who suggest that they
are seeking a middle ground in the controversy over what to
do about invasions, agree with this view. It is often feasible
to minimize the impact of more widely distributed, longestablished invaders, and even sometimes to eradicate
them, but they have been embedded so long in a native
community that eliminating them or even reducing
their populations might negatively affect native species
(Shackelford et al. 2013, Simberloff et al. 2013). Each case
should be judged on its own merits. However, it is important
to recognize that there have been many successful management projects, even of widespread invaders, and the array of
possible tools is expanding rapidly owing to research and
increasing recognition of the importance of such projects
(Simberloff 2009, 2014).
A related call for the end of traditional restoration
ecology
It is not coincidental that, just as Davis (2009) and Valéry
et al. (2013) are calling for an end to invasion biology, at
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least as we currently know it, several restoration ecologists
are calling for the end of restoration ecology as we know it
(Hobbs et al. 2006, 2009, 2013, Seastedt et al. 2008, Hobbs
2013) as part of a “new world order” (Hobbs et al. 2006). A
large component of restoration ecology has been the control
or removal of non-native species (Jordan and Lubick
2011). The critics contend that the earth is increasingly
dominated by ‘novel ecosystems’, generated by an influx of
non-native species and shifting ranges of native species in
response to various anthropogenic forces, including climate change. Therefore, according to this line of reasoning, it is futile in many instances to try to remove
non-native species in an attempt to restore past conditions, and instead we should focus on promoting and
molding novel ecosystems to provide desired ecosystem
services. The key role of non-native species in novel ecosystems, and the overlapping authorship of manifestos
against invasion biology on the one hand and heralds of
the primacy of novel ecosystems on the other (Richard
Hobbs, Ariel Lugo, Mark Gardener, Timothy Seastedt,
Katharine Suding) suggest that these two arguments are
closely linked. For instance, Standish et al. (2013) transfer
the argument of Davis et al. (2011) that we should concentrate on impacts of species, not their origins, to the
matter of what species to target in ecological restoration.
As with some criticisms of invasion biology, a close
examination reveals that many advocates of a new restoration ecology (Standish et al. 2013) are not actually calling
for eliminating traditional restoration ecology. Rather, they
seek to broaden the field, so that the focus is not exclusively
on attempting to restore ecosystems to a semblance of some
historical reference ecosystem, or, as the field has evolved
more recently in recognition of the fact of ongoing changes
of various degrees, some historical ecosystem trajectory
(Clewell and Aronson 2013). Standish et al. (2013), for
example, emphasize that they do not favor abandoning
attempts to manage exotics, so long as the focus is on their
impacts rather than their non-nativeness – exactly an
agenda of Davis et al. (2011). Other proponents of abandoning traditional restoration ecology in favor of a new
field focusing on understanding and molding novel ecosystems are not as conciliatory. For instance, Marris (2013), a
noted skeptic of the importance of invasion impacts
(cf. Marris 2009), believes the “pristine” environments that
restoration ecologists have sought to recreate, such as oldgrowth forests, never existed in the first place, while Hobbs
(2013) sees advocates of traditional restoration ecology
as psychologically trapped in a sequence of states analogous
to those characterizing grieving for deceased loved ones.
Discussion
Calls to end invasion biology are based primarily on the
view that the field has not advanced quickly enough by virtue of not incorporating itself into succession ecology and
its focus on non-native species, but the explosion of
invasion research and literature belies that assertion. Some
invasions do fit comfortably into the succession framework,
but many others do not. Neither is it the case that similar
phenomena to those manifested in invasions, when they
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arise in native species, fail to be studied because they are
excluded from the mainstream of invasion biology. The
recent calls for the end of invasion biology come amidst a
long history of charges that the entire enterprise of studying and managing invasions is a manifestation of displaced
xenophobia. These arguments usually arise from outside
biology, and they consist of a social construction of the
science and fail to account for the evident focus of invasion biologists on impacts. There is no evidence that modern invasion biology is infected by xenophobia. In fact,
the focus of the field on non-native species is precisely
because they are far more likely than native species to
produce harmful ecological impacts. A focus solely on
current observed impacts, ignoring whether a species is
native or not, would risk delaying important measures that
could limit or, in some cases, eliminate invasion impacts.
Traditional ecological restoration has also been targeted
for termination, in favor of ‘novel ecosystems’ consisting of
introduced species and native species whose ranges have
shifted owing primarily to climate change. The dominant
motivation is a slight expansion of the argument that fighting invasive species is largely futile – including in this case
both invasive species and climate change. As with calls to
give up on invasive species and learn to appreciate what we
have (Marris 2011, Thomas 2013), the argument to give up
on traditional restoration also sees a silver lining – in this
case, the possibility that novel ecosystems can be molded to
yield ecosystem services for humankind. Yet there has been
progress in ecological restoration, and there are success stories (Rey Benayas et al. 2009, Moreno-Mateos et al. 2012),
while the science of molding novel ecosystems so that they
reliably yield a range of ecosystems services is in its earliest
infancy.
Finally, calls to end invasion biology, such as those by
Davis (2009) and Valéry et al. (2013), can influence policies
and management. They can provide carte blanche to policymakers (who often lack the time, training, or inclination to
read and analyze the details of an abstract argument or to
recognize academic hyperbole) to think and act in terms of
the short-term profit that introductions can bring or the
short-term costs that managing them would impose, rather
than potential long-term consequences, like losses of species
and ecosystems that will be remarkable and significant
for future generations (cf. Rodewald 2012). Similarly, arguments that traditional restoration ecology is inappropriate
for today’s challenges, as advanced by Hobbs et al. (2006,
2009, 2013), Seastedt et al. (2008), and Hobbs (2013),
risk jeopardizing large-scale, restoration efforts supported
by governments in mega-diverse nations and elsewhere
(J. Aronson pers. comm. 2013). The public can easily be led
to believe that a major scientific controversy exists when a
few credentialed critics repeatedly say that it does, thus
delaying important actions (Oreskes and Conway 2010). The
experience in the United States with critics of Darwinian
evolution and the notion of anthropogenic climate change
come to mind. Leaders of major conservation organizations
recently deplored the threat that the barrage of criticisms of
invasion biology outlined above pose to numerous sound
management programs for invaders worldwide (Lambertini
et al. 2011). It would be a pity if effective programs
for managing invasive species and restoring ecosystems
damaged by them were hindered by a barrage of charges
that do not stand up to scrutiny.
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