Biological invasions: Much progress plus several controversies

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DISTINGUISHED LECTURES

OPEN A ACCESS

CONTRIBUTIONS to SCIENCE 9 (2013) 7-16 Institut d’Estudis Catalans, Barcelona, Catalonia

doi: 10.2436/20.7010.01.158 ISSN: 1575-6343 www.cat-science.cat

CONTRIBUTIONS to SCIENCE 9 (2013) 7-16

Summary. Invasion biology has allowed to progress in our understanding of invasions

and our ability to manage them. Recent research has largely focused on invasions that

impact entire ecosystems. Molecular genetics has revealed the relative commonality of

hybridizations between introduced and native species and between genetically differ-

ent populations introduced into the same region. Controversies surrounding the find-

ings of invasion biology and management include: i) The claim that most invasions are

inconsequential, even if they have been scarcely studied. ii) The argument that inva-

sions can increase local biodiversity, without recognizing that they decrease global bio-

diversity. iii) The statement that invasion biology is a form of xenophobia, downplay-

ing evidence that fighting invasive species is motivated by their negative impacts. iv)

The belief that there is little we can do to prevent or control invasions, ignoring suc-

cessful eradication and management projects and promising novel approaches. iv) Ani-

mal rights objections to the management of invasive vertebrates, particularly mammals,

which reflects different philosophical stances and will not be easily resolved.

Keywords: biological control · biological invasion · ecosystem impact · eradication ·

hybridization · lag time · maintenance management

Resum. La biologia de les invasions ha permès avançar en la comprensió de les invasi-

ons i de la capacitat per gestionar-les. La recerca recent s’ha centrat sobretot en les inva-

sions que afecten ecosistemes sencers. La genètica molecular ha revelat la generalització

relativa d’hibridacions entre espècies introduïdes i natives, i entre poblacions genètica-

ment diferents introduïdes en una mateixa regió. Les controvèrsies sobre els resultats

de la biologia de les invasions i de la seva gestió són: i) L’afirmació que la majoria d’in-

vasions causen poc impacte, encara que hagin estat poc estudiades. ii) L’argument que

les invasions poden augmentar la biodiversitat local, sense reconèixer que disminuei-

xen la biodiversitat global. iii) L’afirmació que la biologia de les invasions és una forma

de xenofòbia, restant importància al fet que la lluita contra les espècies invasores està

motivada pels seus impactes negatius. iv) La creença que hi ha poc que puguem fer per

prevenir o controlar les invasions, fent cas omís de l’éxit dels projectes d’eradicació i

gestió i de nous enfocaments prometedors. iv) Les objeccions dels defensors dels drets

dels animals a la gestió dels vertebrats, particularment mamífers, sent aquest un proble-

ma que no es resoldrà fàcilment.

Paraules clau: control biològic · invasió biològica · impacte a l’ecosistema · eradicació ·

hibridació · desfasament temporal · gestió del manteniment

Based on the lecture given by the author at

the Aula Magna of the Faculty of Biology of

the University of Barcelona on 31 October

2012. Daniel Simberloff received the Ramon

Margalef Award for Ecology 2012.

Correspondence:

Dept. of Ecology and Evolutionary Biology

University of Tennessee

Knoxville, TN 37996, USA

Tel. +1-8659740849

Fax +1-8659743067

E-mail: dsimberloff@utk.edu

Ramon Margalef Award for Ecology 2012

Biological invasions: Much progress

plus several controversies

Daniel Simberloff

Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, TN, USA

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while others are relatively unscathed? (iii) How can the

knowledge developed in response to these two questions be

used to improve the management of invasive species? In fact,

these questions (i) and (ii) dominated the SCOPE workshops

and publications, whereas management was a lesser concern.

The SCOPE project as well as much of the research it in-

spired over the next decade greatly expanded our under-

standing of how particular invaders affect native species. The

majority of cases could be placed in a few well-understood

categories. The phenomenon receiving the most attention

was predation by an introduced predator on native prey,

with the most dramatic outcome being the complete loss of

the native species. Striking examples include the extinction

of more than 200 native cichlid fish species in Lake Victoria

in response to predation by the introduced Nile perch, Lates

niloticus [57], and the extinction of 15 species and subspecies

of forest birds on Guam after the introduction of the brown

tree snake Bioga irregularis [45]. Herbivory by invaders, both

vertebrates and invertebrates, is also common. For instance,

the South American nutria (Myocastor coypus), introduced

into North America and Europe, has caused both the local

extirpation of several aquatic plants and important crop loss-

es [69]. In the 19th century, an insect from North America,

the phylloxera Daktulosphaira vitifoliae, devastated European

vineyards [56]. Invaders can carry diseases to which they are

resistant such as the crayfish plague (Aphanomyces astaci)

transmitted by North American to European crayfish [46].

Similarly, squirrel pox (Parapox virus), which arrived in Eu-

rope with the North American gray squirrel (Sciurus carolin

ensis), is currently devastating the native red squirrel (S. vul

garis) population in Great Britain and Italy [7,68]. Invaders

can also compete with native species. In Spain, the African

ice plant (Carpobrotus spp.) outcompetes native plants for

light and water, while a North American turtle, the red-eared

slider (Trachemys scripta elegans), excludes native turtle spe-

cies from their optimal habitats [69].

During and in the wake of the SCOPE project it was de-

termined that introduced species often hybridize with close-

ly related native species [61]. Indeed, when native popula-

tions are small relative to the size of the invasive population,

as was the case for the native white-head duck Oxyura leuco

cephala in Spain, which hybridized with the North American

ruddy duck O. jamaicensis [51], this phenomenon can even

lead to a sort of “genetic extinction,” as the original native

genotypes become lost in a hybrid swarm. Moreover, hybrid-

ization can generate new species, as occurred in Great Britain

when North American smooth cordgrass (Spartina alterni

flora) hybridized with native small cordgrass S. maritima to

produce the polyploid hybrid common cordgrass, S. anglica

[93]. In this case, although the native parent S. maritima is

never invasive [92], the new hybrid species is listed among a

selection of 100 of the world’s worst invaders [48].

THE RECOGNITION THAT BIOLOGICAL INVASIONS constitute a

global change of the first order—along with changes in cli-

mate, nutrient cycles, and land use—came slowly. As early as

the 18th century, the Swedish Finn Pehr Kalm noted fifteen

European plant species and several European insects during

his travels in North America [13]. Early phytogeographers,

such as the Augustin Pyrame de Candolle, from Switzerland,

greatly expanded the records of species believed to be intro-

duced, deliberately or inadvertently, by humans to various

locations around the world [13]. Victorian naturalist-explor-

ers continued this tradition of documentation during the

19th century. Among them, Charles Darwin lamented the

replacement of native plants by two invaders from the Old

World into the Patagonian pampas [19], while Alfred Russel

Wallace deplored the devastation wrought by some invasive

species on various islands [107]. However, except for Dar-

win and Wallace, the focus of all these investigators was

squarely on the geography of life—which species are

where—and not on the impacts of non-native species.

In the early 20th century, George M. Thomson [94]

wrote entirely about introduced plants and animals and

their impacts in New Zealand, and James Ritchie [64] de-

tailed the impacts of animal invaders in Scotland. Neither

book led to new research efforts to study the effects of the

entire gamut of biological invaders, although Thomson’s

work was rediscovered almost a century later and his data

were used in analyses of bird introductions in New Zealand

[23,24,99]. Through the mid-20th century, scientists would

occasionally point to the impacts of particular species as

meriting greater consideration [e.g., 52], but still no broad-

based movement arose to study invasions. In 1958, Charles

Elton published his famous monograph, The ecology of inva

sion by animals and plants [26], which is often cited as the

founding document of modern invasion biology [62,63].

Although this book addressed the ecological impacts of in-

vasive plants, animals, and microbes worldwide, it had little

contemporary influence and did not inspire a wave of re-

search on invasions [77]. Rather, modern invasion biology

largely arose from a project of the Scientific Committee on

Problems of the Environment (SCOPE) in the 1980s that en-

gaged over 100 prominent ecologists and evolutionists in a

series of workshops held in various countries and which re-

sulted in several widely read books [77]. Thus, given the

long history of the problem of invasive species, the modern

field of invasion biology is remarkably young.

The first fifteen years

The SCOPE mandate was to determine: (i) Why are certain

species particularly invasive once introduced, while others

either disappear or remain restricted and innocuous? (ii)

What makes certain habitats particularly prone to invasions

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Expanded and new research directions

The SCOPE contributions and the immediately ensuing re-

search were largely focused on one-on-one ecological interac-

tions—how does a single particular invader affect one native

or a particular group of them? However, even in the initial

SCOPE project, Peter Vitousek [104,105] called attention to

the fact that certain invasive species can fundamentally alter

an entire ecosystem, involving a large number of species that

play various roles in the biotic community. In Vitousek’s ex-

ample, the particular invader was the Atlantic shrub Morella

faya (or Myrica faya), introduced to the Hawaiian Islands. As

a nitrogen-fixer in mid- and upper-elevation areas character-

ized by nutrient-poor volcanic soils—to which native plants

were adapted—and in the absence of native nitrogen-fixers,

M. faya effectively fertilized the soil, making it more hospita-

ble to other non-native plants previously excluded by the low

nitrogen levels. It also entrained a number of other changes in

the ecosystem [4]. Further, this ecosystem change was exac-

erbated by “invasional meltdown” [87], in which the com-

bined impact of two or more invaders is greater than their

summed impact. The major seed-disperser of M. faya is the

Japanese white-eye, Zosterops japonicus [111]; by clustering

under M. faya, introduced earthworms increase the rate at

which nitrogen is added to the soil [3].

Another ecosystem-wide impact of a single invader

was described by Fukami et al. [31], who found that both

the above-ground and below-ground communities differ

profoundly on small New Zealand islands invaded by rats

(either Rattus rattus or R. norvegicus) compared to rat-free

islands. This type of research is distinct from many previ-

ous studies of the impact of introduced rats on islands

[5,96]. Ecosystem-level research has now become a leading

edge of invasion biology and it has shown that many eco-

system impacts are caused by changes in nutrient and fire

regimes and in physical structure [25,78].

The other major new thrust of invasion biology research

is the role of evolution in invasions. It is puzzling that, de-

spite the participation of several prominent evolutionists in

the SCOPE program and the obvious possible relevance of

invasion events to evolutionary questions (e.g., the relative

importance of founder effects and natural selection in small,

newly established populations), evolutionary biologists did

not join the rapidly growing biological invasions research

program in great numbers for over a decade after SCOPE

[77]. Spurred by the rapid increase in the development and

availability of molecular genetic technologies, evolution has

since become an integral part of the invasion biology re-

search program. Yet, the first monograph on evolution and

biological invasions was published only in 2004 [16].

Nowadays, molecular tools, particularly the study of

microsatellite and mitochondrial DNA sequences, are used

The achievements by great scientists can be usually

found in the articles and books they have published

throughout their careers. Many of their ideas and

thoughts, however, are not always left in print, unless

they write memoirs or books of essays.

Ramon Margalef used to say, in a tone half-humorous

and half-sarcastic, that he felt suspicious—and had had

good reasons for it—of the traditional systems of educa-

tion, especially higher (i.e., university) education. On one

occasion, when we were discussing an emergent and sig-

nificant issue in the young science of microbial ecology,

he told me: “This is so important, Ricard, that in twenty

years it will already be included in textbooks”. R. Guerrero.

Professor Ramon Margalef. (Images courtesy of Gallery of

Catalan Scientists, Institute for Catalan Studies).

Not in print

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to trace the origins of particular invasive species. An exam-

ple is the demonstration that the Cuban anole (Anolis sagrei)

in Florida must have undergone multiple introductions be-

cause many locations in Florida have a greater diversity of

mtDNA haplotypes than does any one location in Cuba

[38]. The same study was able to show that invasions by

this lizard of Hawaii and Taiwan must have arrived from

Florida rather than Cuba. This particular study did not

demonstrate that the multiple origins had consequences for

the invasion. However, for reed canary grass (Phalaris arun

dinacea) in North America [40] and the multicolored lady

beetle (Harmonia axyridis) in North America and Europe

[47], similar genetic analyses show that, as noted above,

hybridization between individuals introduced separately

from different regions can produce more invasive geno-

types. Hybridization between a native and an introduced

oomycete is responsible for alder blight (Phytophthora alni),

a new pathogen that is killing alders (Alnus spp.) through-

out Europe [113].

In general, the plethora of genetic studies on invaders has

detected far more multiple introductions than had been sus-

pected as well as frequent hybridizations between popula-

tions introduced from different regions. These studies also

revealed that hybridizations between introduced and related

native species occur more often than previously assumed

based on simple morphological analyses. The frequency of

multiple introductions at least partly resolves the “paradox of

invasion genetics.” That is, it has long been noted that al-

though very small populations are frequently presumed to be

endangered by genetic deterioration, engendered by genetic

drift and inbreeding-induced genetic depression [2,28],

many strikingly successful invasions have originated from

very small propagules, which greatly reduced genetic varia-

tion by virtue of the “bottleneck effect” [75]. However, we

now know that some introduced populations, such as the

Florida populations of the Cuban anole, have greater genetic

variation than any one native population, thereby hindering

the expected genetic deterioration [66].

Many introduced populations have evolved morpholog-

ically in their new homes. A remarkable example is the Old

World fruit fly Drosophila subobscura, introduced into west-

ern North and South America. Old World populations have

a pronounced latitudinal cline in wing length whereas in

North American populations no wing length cline was de-

tected ten years after introduction of the species; but after

20 years a cline had evolved that largely converged with the

Old World cline [35]. However, different sections of the

wing are responsible for the cline in North American vs. Old

World populations. Thus, the evolution of geographic varia-

tion in wing length was predictable, but expression of the

genes by which the cline was achieved depended on other

factors. Introduced South American populations also rapid-

ly evolved a cline of increased wing length with increased

latitude, but a different section of the wing is responsible for

the cline in South American than in either North American

or Old World fruit flies. Furthermore, many traits other

than morphology have evolved in introduced populations,

including changes in life history, physiology, and behavior

[16]. Perhaps best known to the public are the many cases

in which insects have evolved resistance to insecticides, ei-

ther physiological changes to tolerate or detoxify the chemi-

cal or behavioral changes to avoid it [67,108]. Native spe-

cies sometimes also evolve very quickly in response to

invasions [91]. For instance, after introduction of the preda-

tory green crab (Carcinus maenas) to the Atlantic coast of

North America, the dog whelk (Nucella lapillus), a native

prey species, evolved thicker shells [100].

The explosion of research publications on invasions has

led to a proliferation of formal meta-analyses of that litera-

ture—as the method became known outside the field of

medicine [11]—particularly regarding the first two ques-

tions of the SCOPE agenda: what determines the invasive-

ness of species and the invasibility of sites or habitats (e.g.,

[43,44,102]). However, it seems unlikely that such efforts

will advance our understanding of invasions substantially for

two reasons. First, particular invasions are highly idiosyn-

cratic such that a fundamental requirement of meta-analysis

is violated: the different studies can by no means truly be

viewed as replicate tests of the same hypothesis. Second, this

same idiosyncrasy implies that an effect size in an analysis in

one case will have limited predictive value for an invasion by

the same species or type of species in another. This is most

clearly shown by the fact that a single species can be highly

invasive at one site and either fail utterly or have minor im-

pact at another [114]. What is needed most to advance our

understanding of invasions is not the study of effect sizes but

of actual effects, on the ground and in a multitude of cases

[74]. Unfortunately, this sort of research is largely in the tra-

dition of detailed natural history at the community level,

which has fallen from academic favor precisely because com-

munity dynamics are too variable and idiosyncratic [41]. Yet,

even though community studies are highly idiographic, they

are precisely what is needed if we are to understand and suc-

cessfully address many environmental and conservation is-

sues, including invasions [73].

Controversies surrounding invasions and

invasion biology

Aspects of invasion management and policy have been con-

troversial since well before the advent of modern invasion

biology [72], but for the most part criticism arose from the

humanities and social sciences. More recently, these con-

troversies have become more visible as the field of invasion

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cies; in this light, the instances in which non-native species

confer conservation benefits are highly questionable [106].

(ii) Introduced species increase biodiversity. It has been

frequently noted that introduced species increase local bio-

diversity in certain circumstances or even maintain local

biodiversity in the face of extinctions (e.g., [70]). However,

invasions cause a sharp decrease in global biodiversity. Con-

sider the birds of the Hawaiian Islands [85]. Of 114 known

bird species present at the time of human colonization of the

archipelago, at least 56 are globally extinct [9]. Introduced

bird species contributed to this hecatomb through disease

transmission [112] and possibly through competition [29].

Remarkably, 53 non-native bird species are now established

on the islands [65], approximately “balancing” the extinc-

tions. However, almost all of the introduced birds are com-

mon in their native ranges, and many have been introduced

to other sites. They can hardly be said to “compensate” for

the global extinction of the native birds.

Certain introduced species in specific circumstances in-

crease biodiversity very locally by providing a resource for

native species that would otherwise be more sparsely dis-

tributed in the region. For instance, in Argentina the kelp

Undaria pinnatifida, native to cold temperate regions of the

Pacific northwest, constitutes a new structural habitat that

increases the local richness of native animal species [36]. As

with the introduced species claimed to aid conservation,

discussed above, it is important in each case to tally the

long-term net benefits and debits to regional ecosystems.

(iii) Are actions against introduced species xenophobic?

A persistent claim, originally from scholars in the social sci-

ences and humanities (references in [72]), is that antipathy

towards introduced species is simply displaced xenophobia.

This suggestion is rarely expressed by scientists working on

invasions, but the burst of recent criticism at least hints at

this charge: consider the title of Davis et al. [20]: “Don’t

judge species on their origins.” A full examination of this al-

legation is beyond the scope of this article; I have treated it

fully elsewhere [72,79]. This view of invasion biology

amounts to a classic social construction of science [10], in

which the development of a field is ascribed to the psycho-

logical states and power relationships among the participants

rather than to increasing knowledge of the subject of study.

An excellent example is the work of the American histo-

rian Philip J. Pauly [54], who saw the approximate syn-

chrony of the first American laws restricting human immi-

gration and the earliest statutes attempting to prevent

harmful biological invasions as proof of his thesis. The in-

creasingly strict immigration laws are widely acknowledged

to have reflected a growing nativism in early 20th century

America [33,95]; so, in Pauly’s view, the anti-invasion regu-

biology itself expands and matures. Matters came to a head

with a Comment in Nature [20] signed by 19 ecologists and

an immediate rebuttal [84] signed by 141 ecologists. Popu-

lar science writers, sensing a hot topic, have also entered

the fray (e.g., [49,103]). In fact, there are several distinct

criticisms, with different critics focusing on different ones

[80,82]. These boil down to five main areas of contention.

(i) Which invasive species are harmful? It is widely ac-

knowledged that a minority of biological invaders have harm-

ful impacts, and critics of invasion biology (e.g., [20]) take

that finding as evidence that the entire invasion problem is

overblown. In fact, for three reasons the statistics on known

invasion impacts should be interpreted with caution. First,

the great majority of introduced populations have not been

studied in any detail, so that their true impact is as yet un-

known. For instance, of the over 10,000 non-native plants in

Europe, the ecological effects have been studied in fewer than

11 % [101]. Second, in a number of instances invasions are

substantial and even affect entire ecosystems, but their im-

pacts are nonetheless subtle and not readily apparent. A good

example is the fertili zation of Hawaiian Islands by the nitro-

gen-fixing M. faya [104,105], discussed above. The gradual

change was not obvious, but since the reporting of this phe-

nomenon many similar examples have been uncovered [25].

Third, many introduced populations remain more or less re-

stricted and innocuous for long periods, often several de-

cades, before abruptly exploding across the landscape with

broad-ranging consequences [17]. Thus, even if we were

aware of the current effects of all introduced populations,

their future impacts would be severely underestimated, even

if no further invasions occurred. This phenomenon—that fu-

ture impacts will arise because of populations already intro-

duced—has been called the “invasion debt” [27].

The charge that most invasions are not known to be

harmful is occasionally buttressed by either or both of two

observations. First, some native species have ecologically or

economically harmful impacts that are analogous to those

caused by invasive non-natives. This is true, but the likeli-

hood of such impacts is far less than for non-natives

[53,86]. For instance, plant species introduced to the Unit-

ed States are 40× more likely than native plant species to

generate harmful effects. In the relatively few instances in

which this indeed occurs, it is almost always in the wake of

an anthropogenic environmental modification, such as

changed fire regime or overgrazing by livestock [86]. A sec-

ond occasional observation is that sometimes non-native

species actually aid conservation in some way (e.g., [71]).

Of course, this is true; any time a species, including an in-

troduced one, becomes common, some other species will

use it as a resource. However, one must always consider the

full panoply of impacts on the ecosystem and all of its spe-

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would otherwise have become devastating invasions [81,82].

It is often argued that eradication of a long-established,

widespread invader is impossible (e.g., [18,60]), and there

is little doubt that is far more difficult than eliminating a

limited, narrowly distributed population. However, several

very widely established invaders have nevertheless been

eliminated, such as the pasture weed Kochia scoparia in

Western Australia [58] and the melon fly Bactrocera cucur

bitae in the entire Ryukyu Archipelago [37,39]. Recently,

the viral pathogen of ungulates, rinderpest, which devas-

tated Africa in the 20th century, was eradicated from the

face of the Earth [50]. These successes are not to say that

eradication is straightforward, only that it is often techno-

logically feasible and that recent advances (see, e.g.,

[12,98]) have made possible many eradication efforts that

would have seemed hopeless only one or two decades ago.

If eradication fails, there are several technologies that can

maintain invasive populations at levels that are not problem-

atic. Traditional maintenance management approaches are

physical control, mechanical control, chemical control, and

biological control. Each has achieved major success, and

each has failed in other circumstances [76,83]. The impor-

tant point is that the technologies associated with all of these

methods have evolved (e.g., [14,21,55,97,109]).

In addition, novel approaches to maintenance manage-

ment (and in some cases possibly eradication) of particular

invaders arise occasionally. The essence of creativity is that

we cannot predict exactly when it will arise and from what

direction, only that new ideas will occur with some fre-

quency. This is certainly proving true for the management

of invasive species, as interest in and publicity about the

problem increase. For instance, invasive sea lampreys

(Petromyzon marinus) in the North American Laurentian

Great Lakes—long controlled somewhat successfully with

lampricides and dams but at great expense and with some

non-target impacts—can now be managed in many circum-

stances by exploiting a pheromone emitted by larval lam-

preys to attract adult lampreys to particular streams to

breed [88,89]. Invasive zebra mussels (Dreissena polymor

pha), long intractable to chemical control because they are

acutely sensitive to the presence of toxins in the water and

shut their valves in response to them, can now be managed

at municipal and industrial water facilities where non-tar-

get native mollusks are not a concern. This is achieved by

“BioBullets,” minute beads of toxic potassium chloride that

the mussels cannot sense because they are coated with a

masking fatty substance that dissolves after they have been

filtered out of the water by the mussels [1]. Autocidal meth-

ods that manipulate an invasive species’ genetics in such a

way as to lower its population size were proposed in the

1960s and 1970s (e.g., [32]), but the necessary technolo-

gies were lacking. Today, in an era of transgenes and ge-

lations could only reflect the same xenophobic sentiment:

“attitudes towards foreign pests merged with ethnic preju-

dices: the gypsy moth and the oriental chestnut blight both

took on and contributed to characteristics ascribed to their

presumed human compatriots” [54]. In fact, the invasions of

both the gypsy moth Lymantria dispar [90] and the chestnut

blight Cryphonectria parasitica [30] were devastating and

widely lamented by the contemporary public and politicians.

The discussions in Congress and the federal agencies that led

to early regulations of species introductions referred heavily

to these impacts [72]. This is not to say that nativists of the

period did not occasionally deplore non-native species, but

the scientists of that era and modern invasion biologists fo-

cused, in fact, on impacts, not origins [15]. Absent from

analyses such as Pauly’s is a consideration of the impacts of

introduced species, much less sophisticated insights such as

those of Aldo Leopold, who recognized that the absence of

co-evolution with native species led to far greater risks of

damage from introduced species than from native ones [42].

(iv) Whatever their impacts, is it futile to fight invaders?

Several critics of the effort to stem invasions concede that at

least some of them do wreak substantial damage, but they

argue that, in the face of growing trade and travel, the effort

is largely hopeless and we should not waste precious re-

sources trying to stop them. This sentiment was captured

vividly by Mark Gardener (in [103]), a signatory to the

Comment by Davis et al. [20], as he neared the end of his

tenure as director of the Charles Darwin Research Station in

the Galapagos: “It’s time to embrace the aliens. Blackberries

now cover more than 30,000 ha here, and our studies show

that island biodioversity is reduced by at least 50 % when

it’s present. But as far as I’m concerned, it’s now a Galapa-

gos native, and it’s time we accepted it as such.”

In fact, such pessimism is not warranted, particularly in

light of the relative youth of modern invasion biology and the

tremendous recent strides in management technologies [76].

Of course, the best approach is to have sufficiently stringent

regulations and inspection such that few invaders enter in

the first place; as in medicine, an ounce of prevention is

worth a pound of cure. The experience of New Zealand in

the wake of its Biosecurity Act of 1993 shows that such mea-

sures are both feasible and effective [85]. The impediments

to putting such measures in place are mostly political, al-

though the expense of establishing adequate inspection has

played a role [81]. If an introduced population nevertheless

becomes established, the next step would be to find it quick-

ly and try to eradicate it. Nowhere in the world are there ad-

equate monitoring programs to find such incipient invasions,

even though engaging citizen scientists is a cost-effective way

to greatly improve monitoring and it has led to several re-

markable eradications of populations that almost certainly

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www.cat-science.cat

favor humane ways of killing invasive sentient individuals if

such individuals are to be killed, but even if a completely

painless management or eradication method were to be de-

vised, certain advocates of animal rights would object to it.

Discussion

Controversies over the urgency and scope of the problems

posed by invasions, the real impact of invasions on biodiver-

sity, the charge of xenophobia, and the argument that op-

posing invasions is largely futile are not likely to ever go

away, but they will be less divisive with continued research

and especially education of the public about the results of

that research. As more people learn more about the impacts

of invasions and the developing technologies for managing

them, they will be increasingly inclined to support manage-

ment activities. Policymakers, reflecting the will of the pub-

lic, will follow suit. However, the controversy revolving

around animal rights is of a different type. It reflects deep-

seated differences in worldview and an almost religious zeal

in certain individuals on either side of the issue. Such pro-

found underlying differences will not quickly yield to better

education about the negative impacts and the promising

management possibilities. In such cases, society as a whole

will have to reach a decision, as scientists are simply citizens

among many others in society. Perhaps the early engage-

ment of social scientists in attempting to understand the dif-

fering viewpoints and to adjudicate among them would aid

in generating good outcomes. The ability of a segment of the

Italian population to determine the fate of a species and,

consequently, various ecosystems throughout Europe sug-

gests that better methods are needed to allow all stakehold-

ers to have input into decisions that are urgent, irrevocable,

and of great consequence.

netic modification, such methods are again being re-

searched and have reached the testing state in both fishes

(e.g., [6]) and dipterans (e.g., [59]).

(v) Animal rights objections to the management and

eradication of vertebrates. Attempts to eradicate or

even simply to manage mammals and birds often generate

heated opposition from animal rights and animal welfare

organizations, such as People for the Ethical Treatment of

Animals and The Fund for Animals (PETA) [80,83]. Per-

haps the best known example is the spread of the North

American gray squirrel in Italy. As noted above, in Great

Britain the gray squirrel has greatly reduced native European

red squirrel populations, by spreading squirrel pox and by

competition [110]. An escaped population in central Italy

led to a well-planned eradication campaign, because of the

feared threat to mainland European red squirrels [8]. How-

ever, a lawsuit by animal rights advocates, sustained by Ital-

ian courts, stopped the campaign in its tracks [7] and the

gray squirrel has, accordingly, continued to spread; it is

currently nearing France [22]. Even rats threatening sea-

bird populations have elicited enough sympathy to inspire

attempts to impede eradication campaigns [34,80].

This issue usually boils down to whether one considers

collective entities, such as species or populations, to be wor-

thy of moral consideration, if that moral consideration con-

fers rights on such entities (say, a population of an endan-

gered seabird), and whether such rights trump the rights to

continued life of individuals of some other species, intro-

duced by humans, that may threaten them (e.g., introduced

rats) [80]. Philosophers are divided on this issue, so it is not

surprising that so is the public. Animal rights advocates gen-

erally come down on the side of the rights of individual sen-

tient animals to continued life. Clearly, all sides of this debate

Daniel Simberloff is the Nancy Gore Hunger Professor of Environmental Studies at the University of

Tennessee at Knoxville. At Harvard University, he received his A.B in mathematics (1964) and obtained

his doctoral thesis under Prof. E.O. Wilson (1969). He worked at Florida State University from 1968 to

1997, when he became the Nancy Gore Hunger Professor of Environmental Studies at the University of

Tennessee, where he directs the Institute for Biological Invasions. His research focuses on ecology,

evolution, conservation biology, biogeography, and statistical ecology, with specific topics including in-

vasion biology, community composition and structure, and community morphological structure; he is

considered to be a world leader in the study of invasive species. In 1971 he shared with E.O. Wilson the

Mercer Award of the Ecological Society of America. Other awards include the 2006 Eminent Ecologist

Award of the Ecological Society of America, and the 2012 Ramon Margalef Award for Ecology. He is a

fellow of several academies including the American Academy of Arts and Sciences, and the US National

Academy of Sciences. (Image courtesy of Generalitat de Catalunya).

Professor Daniel Simberloff, recipient of the Ramon Margalef Award for Ecology 2012, deliv-

ered the lecture entitled “Biological invasions: much progress, plus several controversies”

on 31 October 2012 at the University of Barcelona.

Page 8

Biological invasions: Much progress plus several controversies

CONTRIBUTIONS to SCIENCE 9 (2013) 7-16

www.cat-science.cat

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Scientists awarded the Ramon Margalef Prize for Ecology (2005–2012)

Year

Winner

Main topic of research

Country

2005

Paul Dayton

Population and community ecology, mostly in benthic environments.

USA

2006

John Lawton

Dynamics of populations and communities, impact of global changes in

organism populations and communities.

2007

Harold A. Mooney

Plant physiological ecology and phenomena affecting global changes,

such as ecological invasions, the loss of diversity and the degradation of

ecosystems.

USA

2008

Daniel Pauly

Study of the decline of fish stocks and the ecosystems’ response to

human pressure.

France

2009

Paul R. Ehrlich

Population and human over-population.

USA

2010

Simon A. Levin

Mathematical modelling and empirical studies in the understanding of

macroscopic patterns of ecosystems and biological diversities.

USA

2011

Juan Carlos Castilla

Marine ecology, mostly rocky ecosystems and theur sustainability.

Chile

2012

Daniel Simberloff

Invasive species and their impact in the loss of diversity.

USA

The Autonomous Government of Catalonia created the Ramon Margalef Award for Ecology to honor the memory of the Cata-

lan scientist Ramon Margalef (1919−2004), one of the main thinkers and scholars of ecology as a holistic science. His contri-

butions were decisive to the creation of modern ecology. This international award recognizes those people around the world

who have also made outstanding contributions to the development of the science of ecology. More information can be ob-

tained at: www.gencat.cat/premiramonmargalef.