Alien species as a driver of recent extinctions

Abstract

We assessed the prevalence of alien species as a driver of recent extinctions in five major taxa (plants, amphibians, reptiles, birds and mammals), using data from the IUCN Red List. Our results show that alien species are the second most common threat associated with species that have gone completely extinct from these taxa since AD 1500. Aliens are the most common threat associated with extinctions in three of the five taxa analysed, and for vertebrate extinctions overall. © 2016 The Author(s) Published by the Royal Society. All rights reserved.

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Research
Cite this article: Bellard C, Cassey P,
Blackburn TM. 2016 Alien species as a driver of
recent extinctions. Biol. Lett. 12: 20150623.
http://dx.doi.org/10.1098/rsbl.2015.0623
Received: 16 July 2015
Accepted: 18 December 2015
Subject Areas:
ecology
Keywords:
non-native species, amphibian, bird,
mammal, plant, reptile
Author for correspondence:
Tim M. Blackburn
e-mail: t.blackburn@ucl.ac.uk
An invited contribution to the special feature
‘Biology of extinction: inferring events, patterns
and processes’ edited by Barry Brook and
John Alroy.
Electronic supplementary material is available
at http://dx.doi.org/10.1098/rsbl.2015.0623 or
via http://rsbl.royalsocietypublishing.org.
Conservation biology
Alien species as a driver of recent
extinctions
Ce
´line Bellard1, Phillip Cassey2and Tim M. Blackburn1,2,3, 4
1
Department of Genetics, Evolution and Environment, Centre for Biodiversity and Environment Research,
Darwin Building, UCL, Gower Street, London WC1E 6BT, UK
2
School of Biological Sciences and the Environment Institute, The University of Adelaide, Adelaide,
South Australia 5005, Australia
3
Institute of Zoology, Zoological Society of London, Regent’s Park, London NW1 4RY, UK
4
Distinguished Scientist Fellowship Program, King Saud University, Riyadh 1145, Saudi Arabia
TMB, 0000-0003-0152-2663
We assessed the prevalence of alien species as a driver of recent extinctions
in five major taxa (plants, amphibians, reptiles, birds and mammals), using
data from the IUCN Red List. Our results show that alien species are the
second most common threat associated with species that have gone com-
pletely extinct from these taxa since AD 1500. Aliens are the most
common threat associated with extinctions in three of the five taxa analysed,
and for vertebrate extinctions overall.
1. Introduction
Biological diversity naturally varies substantially over space and time, but this vari-
ation is ultimately the product of just four key processes: speciation, immigration,
emigration and extinction [1]. These processes are increasingly being perturbed,
and subsequently shaped, by the actions of humans [2]. Human exploitation of
species and appropriation of land and water have greatly increased extinction
rates in recent centuries relative to the background levels in the fossil record [3,4].
Human activities have also greatly increased the rates of immigration [5,6], by delib-
erately or accidentally transporting and introducing large numbers of species to
areas beyond normal biogeographic barriers to their spread, where they may estab-
lish viable populations (here termed alien) [7]. Alien species have had a range of
impacts documented in their new environments [8], and there are well-documented
examples of native species that have been driven extinct by aliens [9,10]. Indeed,
alien species are often cited as the second most common cause of recent and ongoing
extinctions (since AD 1500) after habitat destruction (i.e. for the USA, see [11]).
Human activities are clearly elevating extinction rates, but it is contentious how
much of that elevation is due to direct effects of exploitation and appropriation,
and how much arises indirectly as a consequence of our elevation of species’ immi-
gration. As a consequence, the role of aliens as important drivers of past extinctions
and/or current extinction risk has been disputed [12–14], the evidence underpin-
ning the ‘second commonest cause’ claim has been questioned [15], and indeed,
speciation by aliens has even been argued to lead to a net increase in diversity
in some taxa in some regions [16]. These arguments form part of a narrative that
the detrimental effects of alien species have been overemphasized [14–18].
Some of the arguments about the impacts of alien species [12,19] have been
based on data on extinction, and extinction risk, from the IUCN (International
Union for Conservation of Nature) Red List. This is a dynamic resource, for which
regular updates add ever greater and more accurate information on the conservation
status of increasing numbers of species. Here, we revisit this resource to assess the
current state of knowledge on associated causes of extinction in five of the best-
studied taxa worldwide. Specifically, we assess the frequency with which alien
species are cited under the causes of loss of plant, amphibian, reptile, bird and
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mammal species considered to be extinct (category EX) and
extinct in the wild (category EW).
2. Methods
The Red-Listing process identifies and classifies 12 major threats
to the persistence of species (IUCN threat classification scheme
v. 3.0) [20]. We compiled data on the total numbers of described,
extinct and possibly extinct (category EX), and extinct in the wild
(category EW) plant, amphibian, reptile, bird and mammal
species from the 2015 IUCN Red List with threat information
(n¼247) [21]. We maintained the same classification scheme as
IUCN except for threat category number 8 (‘Invasive and other
problematic species, genes & diseases’), which we subdivided
into alien species (i.e. invasive non-native (alien) species and dis-
eases) and other problematic species (i.e. native species or species
of unknown origin).
We ascribed threats to each EX and EW species according to
the information in the IUCN Red list. For instance, if a species is
recorded as threatened by biological resource use according to
IUCN, it was given a ‘1’ in the data matrix; otherwise, it received
a value of ‘0’. We repeated this process for the 12 external threats
listed. This allows that species may have been affected by mul-
tiple threats. For each taxonomic group, we calculated the
number of EX þEW species for which alien species are cited as
a threat among species with known threats. This allowed us to
calculate the proportion of all threats that relate to alien species.
We classified EX and EW species either as an island endemic
or mainland species using the IUCN Red List database (www.
iucnredlist.org; accessed June 2015). Geographical range distri-
butions were also used to assign each EX and EW species to
one of 12 biogeographic regions (figure 1).
All analyses were conducted in R v. R 3.2.0 [22].
3. Results
A total of 215 species from the five taxa considered here are
recorded as extinct in the IUCN Red List, and a further 32
are extinct in the wild (table 1). Alien species are listed as a
cause for 58% of all EX, and 31% of all EW species for
which a cause is given (see electronic supplementary
material, table S1, for the species list). These percentages
vary across taxa (table 1). Aliens are less important as an
extinction (EX þEW) driver for plants (27%, 15/55 species)
than for vertebrates (62%, 119/192), and indeed, they are
listed as a driver for more than half of the extinctions in
each of the vertebrate taxa analysed (table 1). Extinct species
commonly have more than one threat identified (mean ¼
1.90), but aliens compose from 14% (plants) to 45%
(mammals) of all listed threats for a given taxon, and
28.51% of all threats listed (table 1). For those species with
just a single extinction (EX þEW) driver listed, this driver
is alien species for 17% of plants, no amphibians, 25% of
reptiles, 27% of birds and 47% of mammals.
For all four vertebrate taxa, the top three threats ranked
by the percentage of extinct (EX) species impacted are agri-
culture and aquaculture, alien species and biological
resource use (overexploitation; table 2). Alien species is the
top-ranked threat for extinct amphibians, reptiles and mam-
mals. For plants, residential and commercial development is
one of the top three threats, displacing alien species down
to fourth (table 2). In total, 58% of EX species (125/215) in
the five taxa analysed were listed as impacted by biological
resource use, which is the highest ranked overall. Alien
species comes in a close second, with 58% of extinct species
(124/215) impacted, whereas agriculture and aquaculture
ranks a distant third (61/215; 28%).
Most recorded extinctions (EX þEW) in the taxa analysed
for which alien species are a listed driver have concerned
island endemic species (86%, 115/134 species; electronic
supplementary material, figure S1). All EX þEW plants and
reptiles were island endemic species, whereas 27% of amphi-
bians, 93% of birds and 80% of mammals were island
endemics. Nevertheless, there are eight amphibian, five bird
and six mammal species with continental mainland popu-
lations for which alien species are listed as an extinction
driver (electronic supplementary material, figure S1). Most
of the species that aliens have helped to drive extinct have
been lost from Australia, New Zealand and other locations
in the Pacific (figure 1). However, most amphibian losses
have been from the Americas (figure 1).
4. Discussion
Our results confirm that, for the five major taxa analysed
here, alien species are the second most common threat
taxon
amphibian
bird
mammal
plant
reptile
no. of species
0
10
20
30
Central America
eastern Africa
western Africa
eastern Asia
northern America
South America
Polynesia
Melanesia
Micronesia
Australia and New Zealand
Caribbean
Figure 1. The locations of the (now lost) native ranges of the 134 extinct (EX þEW) species for which alien species are listed as a driver.
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associated with species that have gone completely extinct
since AD 1500. They are relegated into second place by bio-
logical resource use, by the smallest possible margin (125
versus 124 species affected). In fact, alien species are the
most common threat associated with extinctions in three of
the five taxa analysed, and for vertebrate extinctions overall.
Alien species are listed as having contributed to the extinction
of more than half of all the species in our analyses (EX þEW),
and to almost two-thirds of the vertebrates. Around 30
alien taxa are implicated, including ‘bees’, rainbow trout
Oncorhynchus mykiss, ‘tortoises’, great horned owls Bubo virgi-
nianus and guinea pigs Cavia porcellus, but especially rats
Rattus spp. and cats Felis catus for extinct birds and mammals,
diseases (especially chytridiomycosis and avian malaria) for
extinct amphibians and birds, and herbivores (especially
goats Capra hircus, sheep Ovis aries and European rabbits
Oryctolagus cuniculus) and alien plants for extinct plant
species [21]. Extinctions since AD 1500 are only a small pro-
portion of the vertebrate species lost in the period following
human expansion out of Africa [23,24]. However, well-
typified fossil assemblages reveal a number of extinctions
that are most likely to have been caused by alien species
[25]. Thus, alien-driven extinctions are unlikely to be just a
modern phenomenon.
The IUCN Red List represents probably the best available
data on the factors associated with recent extinctions, and on
current extinction risk, and we have taken the causes of
extinction it records at face value. It remains possible that
the Red List may systematically overestimate the impact of
alien species, if these are not the causal agents of extinction,
but symptoms of the real causes (e.g. habitat destruction)
[13]. We doubt that any such overestimation is substantial.
Alien species may often act in synergy with other extinction
drivers—and indeed, most extinctions are associated with
more than one—but the impacts of alien species have been
well documented in multiple contexts [9,26]. Further, habitat
loss, harvesting and human disturbance co-occur randomly
with impact from aliens as threats to vertebrates on the
IUCN Red List [27]. One could argue equally convincingly
that the impacts of alien species may in many cases be
Table 1. The total number of species either extinct (EX) or extinct in the wild (EW) according to the IUCN Red List (2015) in each of five major taxa, and the
total number (S
alien
) and percentage (%S
alien
) for which alien species are listed as a causal threat, the mean number of threats recorded per species (+s.d.),
and the percentage of all listed threat categories that relate to aliens (%T).
taxon status species S
alien
%S
alien
threats %T
plants EX 32 9 28 2 (+1) 14
EW 23 6 26 2 (+1) 15
amphibians EX 15 10 67 4 (+2) 19
EW 2 1 50 4 (+1) 13
reptiles EX 6 4 67 2 (+1) 29
EW 1 0 0 1 0
birds EX 119 71 60 2 (+1) 35
EW 4 3 75 3 (+2) 27
mammals EX 43 30 70 2 (+1) 45
EW 2 0 0 3 (+1) 0
total 247 134 54 2 (+1) 29
Table 2. The top four threats associated with extinct (EX) species in each taxon, and the percentage and (in parentheses) numbers of extinct species for which
each threat was listed. Only three threats are listed for reptiles, because the percentages for the fourth- to seventh-ranked threats were all equal (17%). Alien
species (AS) is highlighted in italics. Other threats are: AG, agriculture and aquaculture; CC, climate change and severe weather; BR, biological resource use
(overexploitation); PO, pollution; SM, natural system modifications; UR, residential and commercial development (urbanization).
taxon status rank 1 rank 2 rank 3 rank 4
plants threat AG BR UR AS
% (number) 59 (19) 44 (14) 34 (11) 28 (9)
amphibians threat AS AG BR PO
% (number) 67 (10) 60 (9) 53 (8) 47 (7)
reptiles threat AS BR AG
% (number) 67 (4) 50 (3) 33 (2)
birds threat BR AS AG SM
% (number) 70 (83) 60 (71) 17 (20) 8 (10)
mammals threat AS BR AG SM
% (number) 70 (30) 40 (17) 26 (11) 7 (3)
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underestimated, as many interactions (especially between
alien parasites and native hosts) [28] are very hard to
detect. Nevertheless, in many cases, the true contribution of
alien species versus other extinction drivers will never be
known, given that the impacted species concerned are now
extinct.
Alien species are not just a problem forisland species. While
most of the recent extinctions associated with alien species
relate to island endemics (figure 1), 14% of alien-related extinc-
tions have concerned species with mainland populations. Alien
species are a significant concern for mainland species currently
threatened with extinction. In particular, the highest absolute
number of species threatened by alien species are located in
South American countries [29]. In summary, our results do
not support arguments that the detrimental effects of alien
species have been overemphasized [14–18].
Data accessibility. The data on which this paper is based are freely avail-
able on the IUCN Red List website (www.redlist.org). A list of extinct
species is given in the electronic supplementary material.
Authors’ contributions. C.B., P.C. and T.M.B. conceived the study; C.B.
compiled and analysed the data; C.B., P.C. and T.M.B. wrote the
paper. The authors agree to be accountable for all aspects of the
work reported.
Competing interests. The authors have no competing interests.
Funding. C.B. was supported by an AXA Fellowship. P.C. was supported
by an ARC Future Fellowship (FT0914420) and by an ARC Discovery
grant (DP140102319). T.M.B. had no funding for this work.
Acknowledgements. Wethank Barry Brookand John Alroy for inviting us to
write this paper, and three anonymous referees for helpful comments.
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