Download Are islands more susceptible to be invaded than continents? Birds

ECOGRAPHY 23: 687–692. Copenhagen 2000
Are islands more susceptible to be invaded than continents? Birds
say no
Daniel Sol
Sol, D. 2000. Are islands more susceptible to be invaded than continents? Birds say
no. – Ecography 23: 687 – 692.
Island communities are generally viewed as being more susceptible to invasion than
those of mainland areas, yet empirical evidence is almost lacking. A species-by-species examination of introduced birds in two independent island-mainland comparisons is not consistent with this hypothesis. In the New Zealand-mainland Australia
comparison, 16 species were successful in both regions, 19 always failed and only
eight had mixed outcomes. Mixed results were observed less often than expected by
chance, and in only 5 cases was the relationship in the predicted direction. This result
is not biased by differences in introduction effort because, within species, the number
of individuals released in New Zealand did not differ significantly from those released
in mainland Australia. A similar result emerged in the Hawaiian islands-mainland
USA comparison: among the 35 species considered, 15 were successful in both
regions, seven always failed and 13 had mixed outcomes. In this occasion, the results
fit well to those expected by chance, and in only seven cases was the relationship in
the direction predicted. I therefore conclude that, if true, the view that islands are less
resistant than continents to invasions is far from universal.
D. Sol, Dept de Biologia Animal-Vertebrats, Uni6. de Barcelona, A6da Diagonal 645,
E-08028 Barcelona, Spain.
The invasion of natural communities by introduced
plants and animals constitutes one of the most serious
threats to biodiversity (Williamson 1996, Lonsdale
1999). One of the concepts that has received more
attention of ecologists is invasibility of communities
(Pimm 1991, Lodge 1993, Williamson 1996, Levine and
D’Antonio 1999). Invasions literature is full of hypotheses regarding whether communities vary in their
resistance to invasions (e.g. Simberloff 1995, Levine
and D’Antonio 1999, Lonsdale 1999). One of these
hypotheses is that islands are more easily invaded than
mainland areas, as island biotas are species-poor and
the species are thought to be less competitive than those
of mainland (Elton 1958, Mayr 1965). Some recent
theoretical elaborations have lended some credence to
this hypothesis, although others have shown that the
question is not so simple (Pimm 1991, Lonsdale 1999,
Levine and D’Antonio 1999 and references therein).
However, apart from theoretical arguments the hypothesis remains to be tested.
An ideal test of the ‘‘island susceptibility hypothesis’’
would consist of introducing, under identical conditions, the same species in both islands and continents
(Case 1996). Unfortunately, the ecological problems
often associated to exotic species, as well as several
methodological inconvenient (Pimm 1991), preclude
this type of experiment and so we must resort to
historical introductions to test the hypothesis. A consistent pattern that emerges from the study of past introductions is that the number of exotic species in islands
is generally higher than in continents. Atkinson (1989),
for example, noted that about three times as many bird
species have been successfully introduced to islands
than to mainland areas. Yet, this result cannot be taken
as evidence for reduced invasibility of islands, because
it can be simply the result of a higher number of
Accepted 3 February 2000
Copyright © ECOGRAPHY 2000
ISSN 0906-7590
Printed in Ireland – all rights reserved
ECOGRAPHY 23:6 (2000)
687
introductions to islands than to continents (Huston
1994, Lonsdale 1999). Looking for real differences in
invasibility requires data on the failure and success of a
vast number of introductions performed to islands and
continents. Two such tests have been carried out. Simberloff (1986) tabulated successes and failures of insect
introductions from mainland to island, mainland to
mainland, island to mainland and island to island, and
found little support for a higher success in mainland-toisland introductions. Newsome and Noble (1986) reported a high failure rate of avian species introduced to
Australia mainland when compared with islands off
Australia, although no differences were found between
Australia and the near-by Kangaroo island. Yet, the
success of a given introduction depends not only on the
properties of the target ecosystem, but also on the
biological attributes of the invader and the effort of
introduction (Lodge 1993, Williamson 1996, Lonsdale
1999). One therefore must control for these potential
biases in order to perform a valid test of the ‘‘island
susceptibility’’ hypothesis.
In this contribution, I test the ‘‘island susceptibility’’
hypothesis using avian introductions as a model of
study. The approach adopted here to overcome the
problem of differences among the biological properties
of invaders consists of comparing the outcome of species introduced to both an island and a continent. I
have used two island-continent data sets to test the
hypothesis: species introduced to mainland Australia vs
New Zealand, on the one hand, and species introduced
to mainland USA vs the Hawaiian islands, on the
other. These data sets were chosen because they provide
a sufficient number of species for comparison and they
have been previously used in other comparative studies
(e.g. Simberloff 1986, Case 1996, Veltman et al. 1996).
Most introductions in Australia, New Zealand and
USA were carried out by acclimatisation societies,
hence ensuring that success or failure have been accurately measured. In addition, data on number of individuals introduced is available for many species
introduced to Australia and New Zealand, which made
it possible to test for the potential bias of differential
introduction effort.
Methods
Data on species introduced to New Zealand (NZ),
mainland Australia (AUS), Hawaiian islands (HA) and
mainland USA (US) were gathered from Long (1981),
Moulton and Pimm (1983), Newsome and Noble
(1986), Moulton and Sanderson (1996) and Veltman et
al. (1996). Table 1 shows that, as the hypothesis assumes, species richness is much more higher in the
mainland areas than in the islands. These differences
also holds at lower spatial scale. For example, the
number of native species in both Florida and California
are 10 times higher than the number of natives in the
Hawaiian islands. The four regions share a similar
history of human occupation (Case 1996), which makes
comparisons more meaningful. In the HA-US comparison, however, there is a potential problem of comparing
tropical with temperate regions. The justifications of
using these data are twofold. First, at present there is
no robust evidence supporting the view that temperate
ecosystems are more invasible than tropical ones
(Londsdale 1999). Second, in both islands and mainland areas, exotic birds occur primarily in habitats
disturbed by humans, which are far from pristine and
more similar to one another (Case 1996).
Both intentionally (mostly) and accidentally introduced species were considered, but not natural colonisations and re-introductions. Species that were
intentionally introduced in one region and accidentally
introduced in the other were excluded. A total of 42
species for NZ-AUS comparison and 35 for HA-US
were used in the analyses (see Appendix). These comprise a wide array of taxonomic orders (n= 7), although most species are Galliformes and Passeriformes.
For 30 species intentionally introduced to both NZ and
AUS, the minimum number of released individuals was
recorded by acclimatisation societies; these species were
used to test for a potential bias in the results due to
differences in introduction effort. The number of released individuals has been used as estimator of introduction effort in several previous studies (e.g. Veltman
et al. 1996, Green 1997).
To test the ‘‘island susceptibility’’ hypothesis, I examined species-by-species differences in introduction outcome using a Wilcoxon paired-matching test. In this
way, I controlled for differences in biological attributes
of species. Differences in introduction effort were
analysed in a similar way. Species can generally not be
considered independent data points because closely-related ones tend to share many characters through common descent rather than independent evolution
(Harvey and Pagel 1991). However, this problem is
avoided here by performing the comparisons within
Table 1. Statistics on introduced and native species for the four studied regions.
Island/mainland
No. successfully introduced species
No. introduced species
No. native extant species
Area (km2)
New Zealand
Australia
Hawaiian islands
USA
41
16
45
13
149
48
103
98
52
466
27
553
266 800
7 680 000
12 136
7 827 622
688
ECOGRAPHY 23:6 (2000)
species instead of among species (see Møller and Birkhead 1992). In addition, a recent study (Sol 2000)
shows that most variance (72.4%) in invasion success is
accounted for species within genera, which also justifies
the use of species as independent data points.
Results
The percentage of species introduced successfully was
similar in NZ (27.5%) and AUS (33.3%, x2 = 0.32,
DF=1, p B0.57), but higher in HA (43.7%) than in
the US (13.3%, x2 =13.8, DF =1, p B0.0002) (Table
1). Although these results can be interpreted as giving
partial support to the hypothesis, they are of limited
value because they do not take into account the potential effect of differences in invading capacities between
species. When such potential bias is controlled by pairwise comparisons of species introduced to both an
island and a continent, a quite different picture
emerges.
In the NZ-AUS comparison, the differences in invasion success still remain non-significant (z =0.63, p =
0.528). Among the 42 species considered, 16 were
successful in both places, 18 failed in both and only 8
had mixed outcomes. The frequency of each possible
outcome differed from that expected by chance
(x2Yates correction =13.84, DF =1, p =0.0002), with mixed
results being observed less often than expected. In only
five cases the relationship was in the predicted direction
(success in NZ and failure in AUS), whereas the value
expect by chance is 11.7. No differences in the effort of
introduction was found between NZ and AUS (n =30,
z=1.24, p =0.21), even when comparing only species
that succeed (n=12, z=0.31, p= 0.75) or failed in
both places (n =13, z =0.86, p = 0.39). Differences in
introduction effort may, however, partially explain the
mixed results; hence, in all the cases where information
on introduction effort was available (n =4), the effort
was lower for the site where the species failed to
become established (see Appendix) and in three the
effort of introduction was extremely small (Branta
canadensis and Emberiza citrinella for AUS and Passer
montanus for NZ). A re-analysis of the data with a
subset of species for which a minimum of 10 individuals
were known to have been introduced still supports the
conclusion that species did not invade the islands more
easily than the continent (n =22, z=0.53, p =0.59).
In the HA-US comparison, differences in invasion
success became non-significant when the comparison
was performed within species instead of across-species
(z =0.24, p =0.807). Among the 35 species considered,
15 were successful in both sites, 7 always failed and 13
had mixed outcomes. In this case, results fit well to
those expected by chance (x2Yates correction =0.86, DF = 1,
p =0.35), and in only seven cases the result was in the
ECOGRAPHY 23:6 (2000)
predicted direction (i.e. success in HA and failure in
US).
To maximise sample size and hence reduce a type-II
error, I also performed a test with all data pooled. Note
that despite some species appeared twice in the analysis,
the assumption of independence of data was not violated as comparisons were within species and each
introduction is independent of the others. The only
problem with such an analysis is that the predominance
of data from a few species can bias the results whether,
for example, these species are generally successful invaders. This is not the case here, since each species
appeared as a maximum twice in the analysis. Once
again, the result does not support the hypothesis, as no
differences in invasion success were detected between
islands and continents (n =78, z=0.57, p = 0.57).
Discussion
The examination of past introduction shows that islands are much more invaded than mainland areas,
which have lead to the conventional wisdom that island
communities are more invasible than those of mainland
areas. However, my analysis of birds introduced to
both islands and mainlands does not support this view,
suggesting that, if true, the hypothesis is far from
universal.
The discrepancies between my results and those of
Newsome and Noble (1986) could come from considering or not the nature of species in the analyses. Recent
studies suggest that, in birds, biological traits of species
are key determinants of invasion success (Newsome and
Noble 1986, McLain et al. 1995, Veltman et al. 1996,
Green 1997, Sorci et al. 1998, Sol and Lefebvre 2000).
Testing the ‘‘island invasibility’’ hypothesis without taking into account these differences could lead to incorrect conclusions. My results show that when the species
nature is controlled for, the hypothesis that islands are
more invasible is not supported.
A limitation of the approach used here is that, as
focus on large spatial scales, it does not take into
account the processes that determine the success or
failure of species at lower spatial scales. However, the
conclusion that birds do not invade islands more easily
than mainland agrees with observations at ecosystem
scale. Ebenhard (1988) noted that introduced birds are
rarely reported as having negative impact on ecosystems (Ebenhard 1988). Case (1996) showed that in
birds, invasion success does not decline significantly
with the richness of the native avifauna nor the variety
of potential mammalian predators, but probably with
the extent of human perturbations. These observations
largely contrast with those reported for other vertebrates. Ebenhard (1988), for example, also noted that a
much larger percentage of introduced mammals than
689
birds impact on the target ecosystems. In reptiles, on the
other hand, native species number seems to play an
important role in limiting the success of exotics (Case and
Bolger 1991). It seems that recipient community plays a
lower role in birds than in other vertebrates in preventing
exotic success and this could be related to the fact that
exotic and native birds tend to share habitats, and
therefore interact, less frequently than do exotic and
native reptiles or mammals (Diamond and Veitch 1981,
Simberloff 1992, Case 1996). In both islands and mainland areas, exotic birds occur primarily in disturbed
habitats, which are far from pristine and more similar to
one another, whether on island or mainland areas
(Diamond and Veitch 1981, Simberloff 1992, Case 1996).
The results reported in this study are therefore not totally
unexpected.
Recent progress in community ecology shows that the
reasons why certain communities are more easily invaded
than others are far from being as simple as one suspected.
In addition to species richness, the nature of the species
present, the structure of the food-web and the process of
community assembly also seems to play an important
role (Pimm 1991, Simberloff 1995, Williamson 1996,
Levine and D’Antonio 1999). On the other hand, the idea
that island species evolve to be less competitive than
species from continents has received little empirical
support (Simberloff 1995 and references therein). Perhaps, as Simberloff (1995) points out, generic statements
of the fragility of islands are not useful and we should
speak on specific islands and mainlands.
Acknowledgements – I thank Louis Lefebvre for helpful discussions, and Carme Pujol for her constant help and support.
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ECOGRAPHY 23:6 (2000)
Appendix. List of species used in the within species-comparison of introduction success in islands vs continents
(0=unsuccessful introduction, 1 =successful introduction; the minimum number of individuals introduced
appears between brackets). Taxonomy follows Sibley and Monroe (1990).
Order
Family
Species
Australia
New Zealand
Anseriformes
Anatidae
0 (4)
0 (8)
Anseriformes
Anatidae
1 (136)
1 (1539)
Anseriformes
Anatidae
0 (6)
1 (60)
Anseriformes
Ciconiiformes
Ciconiiformes
Columbiformes
Columbiformes
Anatidae
Pteroclidae
Pteroclidae
Columbidae
Columbidae
1 (20)
0 (10)
0
1
0
1 (29)
0 (8)
0
1
1
Columbiformes
Columbiformes
Craciformes
Galliformes
Galliformes
Columbidae
Columbidae
Cracidae
Numididae
Odontophoridae
1
0
1
0
0
1 (2500)
0
1 (1420)
Galliformes
Galliformes
Galliformes
Galliformes
Odontophoridae
Phasianidae
Phasianidae
Phasianidae
0 (20)
0
0 (8)
0
Galliformes
Phasianidae
Galliformes
Galliformes
Galliformes
Phasianidae
Phasianidae
Phasianidae
Galliformes
Phasianidae
Galliformes
Galliformes
Galliformes
Phasianidae
Phasianidae
Phasianidae
Galliformes
Galliformes
Galliformes
Galliformes
Galliformes
Phasianidae
Phasianidae
Phasianidae
Phasianidae
Phasianidae
Galliformes
Phasianidae
Galliformes
Galliformes
Phasianidae
Phasianidae
Galliformes
Phasianidae
Alopochen
aegyptiacus
Anas
platyrrhynchos
Branta
canadiensis
Cygnus olor
Pterocles alchata
P. exustus
Columba li6ia
Streptopelia
decaocto
S. senegalensis
S. turtur
Crax rubra
Numida meleagris
Lophortyx
californicus
L. gambelii
Alectoris chukar
Alectoris rufa
Ammoperdix
griseogularis
Callipepla
squamata
Coturnix coturnix
C. chinensis
Chrysolophus
pictus
Francolinus
erckelli
F. francolinus
Gallus gallus
Lophura
leucomelana
L. nycthemera
Oreortyx pictus
Pa6o cristatus
Perdix perdix
Phasianus
colchicus
Syrmaticus
ree6esii
S. soemmerringii
Tympanuchus
cupido
Tympanuchus
phasianellus
ECOGRAPHY 23:6 (2000)
0
1
0
0
0
USA
Hawaiian
islands
1
1
1
0
1
1
1
0
0
0
1
0
1
1
0
1
0
0
1
0
0
0
0
0
0
1
1
1
0
1
1
1
1
1
0
1
0
0
0
0
0
0
1
0
0
1
0
0
0 (200)
1 (1500)
1
0 (676)
1 (244)
691
Appendix. (Continued)
Order
Family
Species
Australia
New Zealand
USA
Hawaiian
islands
Passeriformes
Passeriformes
Alaudidae
Fringillidae
1 (700)
0 (50)
1 (391)
0 (209)
0
1
Passeriformes
Passeriformes
Passeriformes
Passeriformes
Fringillidae
Fringillidae
Fringillidae
Fringillidae
1 (500)
1 (150)
0 (80)
1 (626)
1 (65)
0 (54)
1
1
Passeriformes
Passeriformes
Passeriformes
Fringillidae
Fringillidae
Fringillidae
0
1
Passeriformes
Passeriformes
Passeriformes
Passeriformes
Passeriformes
Passeriformes
Passeriformes
Passeriformes
Passeriformes
Passeriformes
Passeriformes
Fringillidae
Fringillidae
Fringillidae
Fringillidae
Muscicapidae
Muscicapidae
Muscicapidae
Passeridae
Passeridae
Passeridae
Pycnonotidae
1
1
1
1
1
1
1
1
Passeriformes
Sturnidae
Passeriformes
Passeriformes
Sturnidae
Sturnidae
1
1
1
1
Passeriformes
Passeriformes
Passeriformes
Psitaciformes
Psitaciformes
Sturnidae
Sylviidae
Sylviidae
Psittacidae
Psittacidae
1
0
1
1
1
0
Psitaciformes
Psitaciformes
Psittacidae
Psittacidae
Alauda ar6ensis
Carduelis
cannabina
C. carduelis
C. chloris
C. spinus
Carpodacus
mexicanus
Pyrrhula pyrrhula
Serinus canaria
Emberiza
citrinella
E. hortulana
Fringilla coelebs
F. montifringilla
Paroaria coronata
Erithacus rubecula
Turdus merula
T. philomelos
Padda oryzi6ora
Passer domesticus
P. montanus
Pycnonotus
jocosus
Acridotheres
tristis
Gracula religiosa
Mymus
polyglottos
Sturnus 6ulgaris
Cettia diphone
Leiothrix lutea
Cacatua galerita
Myiopsitta
monachus
Nandayus nenday
Platycercus
eximius
1
1
692
0
0
0 (15)
0
0
1 (656)
0 (16)
0 (200)
0 (80)
0 (6)
1 (449)
0 (121)
0
1
1
0
1
1
0
1
1
0
1
0
(47)
(70)
(70)
(100)
(100)
(70)
1 (350)
1 (450)
1
1
(123)
(596)
(343)
(6)
(416)
(14)
1 (88)
1 (653)
1
1
ECOGRAPHY 23:6 (2000)