ECOGRAPHY 23: 687 – 692. Copenhagen 2000
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 , Uni
6
.
de Barcelona , A
6 da Diagonal
E 08028 Barcelona , Spain .
645 ,
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
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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.
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
New Zealand
Australia
Hawaiian islands
USA
41
16
45
13
149
48
103
98
No. native extant species Area (km
2
)
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.
The percentage of species introduced successfully was similar in NZ (27.5%) and AUS (33.3%, x 2 = 0.32,
DF = 1, p
B
0.57), but higher in HA (43.7%) than in the US (13.3%, x 2 = 13.8, DF = 1, p B 0.0002) (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 x 2
Yates 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 ( x 2
Yates correction
= 0.86, DF = 1, p = 0.35), and in only seven cases the result was in the 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).
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
ECOGRAPHY 23:6 (2000)
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.
Atkinson, I. 1989. Introduced animals and extinctions. – In:
Western, D. and Pear, M. (eds), Conservation for the twenty-first century. Oxford Univ. Press, pp. 54 – 69.
Case, T. J. 1996. Global patterns in the establishment and distribution of exotic birds. – Biol. Conserv. 78: 69 – 96.
Case, T. J. and Bolger, D. T. 1991. The role of introduced species in shaping the abundance and distribution of island reptiles. – Evol. Ecol. 5: 272 – 290.
Diamond, J. M. and Veitch, C. R. 1981. Extinctions and introductions in the New Zealand avifauna: cause and effect? – Science 211: 499 – 501.
Ebenhard, T. 1988. Introduced birds and mammals and their ecological effects. – Viltrevy 13: 1 – 106.
Elton, C. S. 1958. The ecology of invasions by animals and plants. – Methuen.
Green, R. E. 1997. The influence of numbers released on the outcome of attempts to introduce exotic bird species to
New Zealand. – J. Anim. Ecol. 66: 25 – 35.
Harvey, P. H. and Pagel, M. D. 1991. The comparative method in evolutionary biology. – Oxford Univ. Press.
Huston, M. A. 1994. Biological diversity. – Cambridge Univ.
Press.
Levine, J. M. and D’Antonio, C. M. 1999. Elton revisited: a review of evidence linking diversity and invasibility. –
Oikos 87: 15 – 26.
Lodge, D. M. 1993. Biological invasions: lessons for ecology.
– Trends Ecol. Evol. 8: 133 – 137.
Long, J. L. 1981. Introduced birds of the world. – David and
Charles.
Lonsdale, W. M. 1999. Global patterns of plant invasions and the concept of invasibility. – Ecology 80: 1522 – 1536.
Mayr, E. 1965. The nature of colonization in birds. – In:
Naker, H. G. and Stebbins, G. L. (eds), The genetics of colonizing species. Academic Press, pp. 29 – 47.
McLain, D. K., Moulton, M. P. and Readfearn, T. P. 1995.
Sexual selection and the risk of extinction of introduced birds on oceanic islands. – Oikos 74: 27 – 34.
Møller, A. P. and Birkhead, T. R. 1992. A pairwise comparative method as illustrated by copulation frequency in birds.
– Am. Nat. 139: 644 – 656.
Moulton, M. P. and Pimm, S. L. 1983. The introduced Hawaiian avifauna: biogeographic evidence for competition. –
Am. Nat. 121: 669 – 690.
Moulton, M. P. and Sanderson, J. 1996. Predicting the fates of
Passeriform introductions on oceanic islands. – Conserv.
Biol. 11: 552 – 558.
Newsome, A. E. and Noble, I. R. 1986. Ecological and physiological characters of invading species. – In: Groves,
R. H. and Burdon, J. J. (eds), Ecology of biological invasions. Cambridge Univ. Press.
Pimm, S. L. 1991. The balance of nature? – Univ. of Chicago
Press.
Sibley, C. and Monroe, B. 1990. Distribution and taxonomy of birds of the world. – Yale Univ. Press.
Simberloff, D. 1986. Introduced insects: a biogeographic and systematic perspective. – In: Mooney, H. A. and Drake, J.
A. (eds), Ecology of biological invasions of North America and Hawaii. Ecol. Stud. 58, Springer, pp. 3 – 26.
Simberloff, D. 1992. Extinction, survival, and effects of birds introduced to the Mascarenes. – Acta Oecol. 13: 663 – 678.
Simberloff, D. 1995. Why do introduced species appear to devastate islands more than mainland areas? – Pac. Sci. 49:
87 – 97.
Sol, D. 2000. Introduced species: a significant component of the global environmental change. – Ph.D. thesis, Univ. of
Barcelona.
Sol, D. and Lefebvre L. 2000. Behavioural flexibility predicts invasion success in birds introduced to New Zealand. –
Oikos 90: 599 – 605.
Sorci, G., Møller, A. P. and Clobert, J. 1998. Plumage dichromatism of birds predicts introduction success in New
Zealand. – J. Anim. Ecol. 67: 263 – 269.
Veltman, C. J., Nee, S. and Crawley, M. J. 1996. Correlates of introduction success in exotic New Zealand birds. – Am.
Nat. 147: 542 – 557.
Williamson, M. 1996. Biological invasions. Chapman and
Hall.
690
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 USA Hawaiian islands
Anseriformes
Anseriformes
Anseriformes
Anseriformes
Ciconiiformes
Ciconiiformes
Columbiformes
Columbiformes
Anatidae
Anatidae
Anatidae
Anatidae
Pteroclidae
Pteroclidae
Columbidae
Columbidae
Columbiformes Columbidae
Columbiformes Columbidae
Craciformes Cracidae
Galliformes
Galliformes
Galliformes
Numididae
Odontophoridae
S
S
.
.
senegalensis turtur
Crax rubra
Numida meleagris
Lophortyx californicus
Odontophoridae L .
gambelii
Galliformes
Galliformes
Galliformes
Galliformes
Phasianidae
Phasianidae
Phasianidae
Phasianidae
Alectoris chukar
Alectoris rufa
Ammoperdix griseogularis
Callipepla squamata
Coturnix coturnix Galliformes
Galliformes
Galliformes
Galliformes
Phasianidae
Phasianidae
Phasianidae
Phasianidae
C .
chinensis
Chrysolophus pictus
Francolinus erckelli
Galliformes
Galliformes
Galliformes
Phasianidae
Phasianidae
Phasianidae
Alopochen aegyptiacus
Anas platyrrhynchos
Branta canadiensis
Cygnus olor
Pterocles alchata
P .
exustus
Columba li 6 ia
Streptopelia decaocto
Galliformes
Galliformes
Galliformes
Galliformes
Galliformes
Galliformes
Galliformes
Galliformes
Galliformes
Phasianidae
Phasianidae
Phasianidae
Phasianidae
Phasianidae
Phasianidae
Phasianidae
Phasianidae
Phasianidae
F .
francolinus
Gallus gallus
Lophura leucomelana
L .
nycthemera
Oreortyx pictus
Pa 6 o cristatus
Perdix perdix
Phasianus colchicus
Syrmaticus ree
6 esii
S .
soemmerringii
Tympanuchus cupido
Tympanuchus phasianellus
0 (4)
1 (136)
0 (6)
1 (20)
0 (10)
0
1
0
1
0
0
1 (2500)
0 (20)
0
0
1
0
1
0
0 (200)
1 (1500)
0 (8)
1 (1539)
1 (60)
1 (29)
0 (8)
0
1
1
1
0
0
1 (1420)
0 (8)
0
0
0
0
0
1
0 (676)
1 (244)
1
1
1
1
0
0
1
0
0
1
0
0
0
1
0
1
1
1
0
0
0
1
1
0
1
0
0
1
1
1
0
0
0
0
1
1
1
1
0
1
0
0
0
0
ECOGRAPHY 23:6 (2000)
691

Appendix. (Continued)
Order Family
Passeriformes
Passeriformes
Passeriformes
Passeriformes
Passeriformes
Passeriformes
Passeriformes
Passeriformes
Passeriformes
Passeriformes
Passeriformes
Passeriformes
Passeriformes
Passeriformes
Passeriformes
Passeriformes
Passeriformes
Passeriformes
Passeriformes
Passeriformes
Passeriformes
Passeriformes
Passeriformes
Passeriformes
Passeriformes
Passeriformes
Psitaciformes
Psitaciformes
Psitaciformes
Psitaciformes
Sturnidae
Sturnidae
Sturnidae
Sturnidae
Sylviidae
Sylviidae
Psittacidae
Psittacidae
Psittacidae
Psittacidae
Alaudidae
Fringillidae
Fringillidae
Fringillidae
Fringillidae
Fringillidae
Fringillidae
Fringillidae
Fringillidae
Fringillidae
Fringillidae
Fringillidae
Fringillidae
Muscicapidae
Muscicapidae
Muscicapidae
Passeridae
Passeridae
Passeridae
Pycnonotidae
Species Australia New Zealand USA
0
Hawaiian islands
1 Alauda ar
6 ensis
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 oryzi 6 ora
Passer domesticus
P .
montanus
Pycnonotus jocosus
Acridotheres tristis
Gracula religiosa
Mymus polyglottos
Sturnus 6 ulgaris
Cettia diphone
Leiothrix lutea
Cacatua galerita
Myiopsitta monachus
Nandayus nenday
Platycercus eximius
1 (700)
0 (50)
1 (500)
1 (150)
0 (80)
1 (350)
1 (450)
1
1
0
0
0 (15)
0 (16)
0 (200)
0 (80)
0 (47)
1 (70)
1 (70)
0 (100)
1 (100)
1 (70)
1 (391)
0 (209)
1 (626)
1 (65)
0 (54)
0
0
1 (656)
0 (6)
1 (449)
0 (121)
0 (123)
1 (596)
1 (343)
0 (6)
1 (416)
0 (14)
1 (88)
1 (653)
1
1
1
0
1
1
1
1
1
1
1
0
1
1
1
1
1
1
1
1
1
1
1
1
0
1
692
ECOGRAPHY 23:6 (2000)