Research Article |
Corresponding author: Tim M. Blackburn ( t.blackburn@ucl.ac.uk ) Academic editor: Wolfgang Nentwig
© 2017 Tim M. Blackburn, Sally L. Scrivens, Sarah Heinrich, Phillip Cassey.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Blackburn TM, Scrivens SL, Heinrich S, Cassey P (2017) Patterns of selectivity in introductions of mammal species worldwide. NeoBiota 33: 33-51. https://doi.org/10.3897/neobiota.33.10471
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Humans have an extremely long history of transporting and introducing mammal species outside their native geographic ranges. The characteristics of the species introduced (taxonomy, life-history, ecology, environment) can all influence which traits are available (and selected) for establishment, and subsequent invasive spread. Understanding the non-randomness in species introductions is therefore key to understanding invasions by alien species. Here, we test for selectivity in the identities and traits of mammal species introduced worldwide. We compiled and analysed a comprehensive database of introduced mammal species, including information on a broad range of life history, ecological, distributional and environmental variables that we predicted to differ between introduced and non-introduced mammal species. Certain mammal taxa are much more likely to have been introduced than expected, such as Artiodactyls in the families Bovidae and Cervidae. Rodents and bats were much less likely to have been introduced than expected. Introduced mammal species have significantly larger body masses, longer lifespans and larger litter sizes than a random sample of all mammal species. They also have much larger native geographic ranges than expected, originate from significantly further north, from cooler areas, and from areas with higher human population densities, than mammal species with no recorded introductions. The traits and distributions of species help determine which have been introduced, and reflect how the evolutionary history of mammals has resulted in certain species with certain traits being located in the way of human histories of movement and demands for goods and services. The large amount of unexplained variation is likely to relate to the intrinsically stochastic nature of this human-driven process.
Acclimatisation Societies, alien species, geographic range, introduced mammals, phylogenetic logistic regression models, taxonomic bias
Humans have deliberately (and accidentally) transported a large number of species beyond the limits of their native distributions, to areas where they have subsequently escaped, or been released, into environments where they do not naturally occur (here termed introductions or introduced). Yet, these species are only a small fraction of those that could potentially be introduced. Given that introductions occur during the earliest stages of a process that leads, in some cases, to alien invasions (
Many studies have examined what proportion of the species in a taxon have been introduced, largely as a result of the influential Tens Rule proposed by Mark Williamson (
Introduced species tend not to be a random subset of the species in a taxon. This has been studied most extensively for birds (
Similar patterns of selectivity have been shown in other taxa. For example, introduced fishes show a strong taxonomic bias towards game or forage fishes, or other species of human interest. They are also often piscivorous (Garcia-Berthou 2007). At the global scale, introduced amphibians tend to originate from the Northern hemisphere, to have broad geographic ranges, and to be sympatric with high densities of humans (
Here, we build on these previous studies, exploring the number and characteristics of introduced species, using a global database of mammal introductions. First, we quantified and characterised the taxonomic distribution of introduced mammal species, to reveal which orders and families of mammals have more (or fewer) introduced species than expected by chance. As far as we are aware, this is the first study to identify non-randomness in the taxonomic distribution of introduced mammal species worldwide. We then tested for non-randomness in a range of characteristics that previous studies have shown to be associated with introduction selectivity, and which may help explain why certain taxa are over or under-represented in the list of introduced mammals. Specifically, we tested whether mammal species that have been introduced somewhere in the world differed in measures of (1) body size, (2) fecundity, (3) lifespan, (4) ecological generalism, (5) herbivory, (6) geographic extent, (7) human population density across their geographic ranges, and (8) location of their native geographic range, compared to mammal species that have not been introduced. The specific hypotheses tested are given in Table
The characteristics of species that we expected to influence whether or not mammal species have been introduced, based on patterns of selectivity shown in other taxa (see Introduction for more details), the specific hypotheses associated with those characteristics, the specific variables analysed (with sample size) and a description of that variable (see Methods and
Characteristic | Hypotheses | Variable (sample size) | Description |
---|---|---|---|
Body size | We expect utilitarian species (e.g., food and pack animals) to be more likely to have been transported and introduced, and therefore that introduced species will be larger than expected by chance. | Adult body mass (3,542 species) | Grams (log transformed) |
Fecundity | Species with relatively slow life histories may be more likely to be utilitarian species (and so also have large body size) and better able to survive the introduction process. Alternatively, species with faster life histories may be more likely to maintain populations through the stresses of transport and introduction. | Litter size (2,502 species) | Number of offspring born per litter (log transformed) |
Lifespan | Species with relatively slow life histories may be more likely to be utilitarian species (and so also have large body size and low fecundity) and better able to survive the introduction process. | Maximum Longevity (1,013 species) | Months (log transformed) |
Ecological generalism | Generalist species may be more widespread and abundant, more easily kept in captivity, and more flexible in their ability to cope with the demands of transport and introduction. Thus, introduced species are more likely to have generalist diets. | Diet breadth (2,161 species) | Number of dietary categories used by a species |
Generalist species may be more widespread and abundant, more easily kept in captivity, and more flexible in their ability to cope with the demands of transport and introduction. Thus, introduced species are more likely to be habitat generalists. | Habitat breadth (2,724 species) |
Number of habitat layers used by a species | |
Herbivory | We expect utilitarian species (e.g., food and pack animals) to be more likely to have been transported and introduced, and therefore that introduced species are more likely to be herbivores. | Trophic level (2,161 species) |
1: herbivore (not vertebrate and/or invertebrate prey): 2: omnivore (vertebrate and/or invertebrate prey plus any of the other categories); 3: carnivore (vertebrate and/or invertebrate prey only) |
Geographic extent | Species with a greater native distribution (which tend also to be abundant) will be more available for deliberate or accidental transport and introduction. | Geographic range size (4,668 species) | Area of the native range in km2 (log transformed) |
Human population density | Introduced species tend to be those affiliated with humans. Such species may be more likely to be found in areas with greater concentrations of humans and human activities, and will be more likely to be deliberately or accidentally transported and introduced as a result. | Human population density (4,668 species) | Average number of persons per km2 within the native geographic range (log +1 transformed) |
Location of the native geographic range | Many introductions have been associated with colonial expansion of European countries, primarily to Neo-European colonies at similarly high latitudes. We therefore expect introduced species to be more likely than expected by chance to derive from higher latitudes. | Latitudinal mid-point of the geographic range (4,668 species) |
Degrees of latitude, with negative values indicating mid-points south of the equator |
Many introductions have been associated with colonial expansion of European countries. We therefore expect introduced species to be more likely than expected by chance to derive from European longitudes. | Longitudinal mid-point of the geographic range (4,668 species) | Degrees of longitude, with negative values indicating mid-points west of the Greenwich Meridian | |
Rainfall tends to be higher in tropical areas that have been less associated with European colonial expansion. We therefore expect introduced species to be less likely than expected by chance to derive from high rainfall regions. | Mean precipitation (4,533 species) | Mean monthly precipitation (mm) within the geographic range (log transformed) | |
For the same reasons as latitude, we expect introduced species to be more likely than expected by chance to derive from areas with lower mean temperatures. | Mean temperature (4,533 species) | Mean monthly temperature (°C) within the geographic range |
We compiled a comprehensive database of mammal species introduced to areas beyond the limits of their historically recognised native geographic ranges. The starting point for our database was the compilation of mammal introductions by
Species were considered to be introduced when there was evidence that individuals arrived into an environment via human mediation, except when there was evidence that the liberated or escaped populations were to sites within the historic range of the species (i.e., re-introductions). Native ranges were determined from a combination of IUCN distribution maps (
We obtained data on a range of life history and geographic variables for a large sample of mammal species from the PanTheria database (
We analysed introduction as a binary trait. We did not address variation in the number of introductions because it is difficult to get good data on the number of introductions, especially for species that have been accidentally translocated. We adopted both taxonomic and phylogenetic approaches to assess non-randomness in the characteristics of introduced mammal species. All analyses were conducted in R v. 3.1.1 (
We used the permutation approach described in
We used phylogenetic logistic regression (
We identified a total of 306 mammal species that have been recorded as having been introduced to areas beyond the limits of their normal geographic distributions (Suppl. material
Six mammalian orders have had more species introduced outside their native range limits than expected by chance (Table
The distribution, across mammal orders, of all mammal species (No. species), introduced mammal species (No. introduced), and the expected number of introduced species per order (median and range, based on 100,000 iterations of the permutation test) assuming that mammal species were selected for introduction at random (Expectation). Species numbers are based on the taxonomy in
Order | No. Species | No. Introduced | Expectation |
---|---|---|---|
Afrosoricida | 51 | 1 | 3 (0–12) |
Artiodactyla | 239 | 83*** | 13 (2–32) |
Carnivora | 286 | 41*** | 16 (3–34) |
Cetacea | 84 | 0* | 5 (0–17) |
Chiroptera | 1116 | 3*** | 63 (33–98) |
Cingulata | 21 | 2 | 1 (0–9) |
Dasyuromorphia | 71 | 1 | 4 (0–14) |
Dermoptera | 2 | 0 | 0 (0–2) |
Didelphimorphia | 87 | 3 | 5 (0–15) |
Diprotodontia | 143 | 28*** | 8 (0–22) |
Erinaceomorpha | 24 | 2 | 1 (0–8) |
Hyracoidea | 4 | 0 | 0 (0–4) |
Lagomorpha | 92 | 12* | 5 (0–17) |
Macroscelidea | 15 | 0 | 1 (0–6) |
Microbiotheria | 1 | 0 | 0 (0–1) |
Monotremata | 5 | 2 | 0 (0–4) |
Notoryctemorphia | 2 | 0 | 0 (0–2) |
Paucituberculata | 6 | 0 | 0 (0–4) |
Peramelemorphia | 21 | 2 | 1 (0–8) |
Perissodactyla | 16 | 6** | 1 (0–7) |
Pholidota | 8 | 0 | 0 (0–5) |
Pilosa | 10 | 1 | 0 (0–5) |
Primates | 376 | 30 | 21 (6–41) |
Proboscidea | 3 | 2* | 0 (0–3) |
Rodentia | 2277 | 75*** | 129 (89–168) |
Scandentia | 20 | 0 | 1 (0–9) |
Sirenia | 5 | 0 | 0 (0–4) |
Soricomorpha | 428 | 12** | 24 (7–46) |
Tubulidentata | 1 | 0 | 0 (0–1) |
The distribution, across mammal families, of all mammal species (No. species), introduced mammal species (No. introduced), and the expected number of introduced species per family (median and range, based on 100,000 iterations of the permutation test) assuming that mammal species were selected for introduction at random (Expectation). Species numbers are based on the taxonomy in
Order | Family | No. species | No. Introduced | Expectation |
---|---|---|---|---|
Artiodactyla | Bovidae | 143 | 49*** | 8 (0–21) |
Camelidae | 4 | 4*** | 0 (0–4) | |
Cervidae | 50 | 19*** | 3 (0–13) | |
Suidae | 19 | 5** | 1 (0–7) | |
Tayassuidae | 3 | 2* | 0 (0–3) | |
Carnivora | Canidae | 35 | 8** | 2 (0–10) |
Mustelidae | 59 | 14*** | 3 (0–12) | |
Viverridae | 35 | 7** | 2 (0–10) | |
Chiroptera | Hipposideridae | 81 | 0* | 4 (0–16) |
Molossidae | 100 | 1* | 6 (0–19) | |
Phyllostomidae | 160 | 0*** | 9 (0–23) | |
Pteropodidae | 186 | 1** | 10 (0–28) | |
Vespertilionidae | 407 | 0*** | 23 (6–45) | |
Diprotodontia | Macropodidae | 65 | 16*** | 4 (0–13) |
Potoroidae | 10 | 3* | 0 (0–5) | |
Vombatidae | 3 | 2* | 0 (0–3) | |
Lagomorpha | Leporidae | 61 | 12** | 3 (0–13) |
Perissodactyla | Equidae | 7 | 5*** | 0 (0–4) |
Primates | Cercopithecidae | 132 | 14* | 7 (0–20) |
Lemuridae | 19 | 6** | 1 (0–8) | |
Proboscidea | Elephantidae | 3 | 2* | 0 (0–3) |
Rodentia | Castoridae | 2 | 2** | 0 (0–2) |
Cricetidae | 681 | 12*** | 38 (16–66) | |
Hystricidae | 11 | 3* | 0 (0–6) | |
Muridae | 730 | 17*** | 41 (20–69) | |
Sciuridae | 278 | 25* | 16 (2–33) | |
Soricomorpha | Soricidae | 376 | 10** | 21 (5–42) |
The mammalian order with second highest number of introduced species is the Rodentia, with 75 (Table
Introduced species are distributed across the mammal phylogeny with D = 0.51. This was significantly different from both phylogenetic randomness (P < 0.0001) and a strict Brownian motion model of evolution (P < 0.0001). Univariate phylogenetic logistic regressions show that introduced species have significantly larger body masses and litter sizes, longer lifespans and broader diet breadths than mammal species not introduced (Table
Univariate phylogenetic generalised logistic models of the relationship between mammal species introduction and the variables in the second column. Ch. = characteristic of interest with which each variable is associated (see Introduction, Methods, and Table
Ch. | Variable | Estimate ± s.e. | t | N | P | λ |
---|---|---|---|---|---|---|
1 | Log. Adult Body Mass | 0.029 ± 0.004 | 7.44 | 3435 | < 0.0001 | 0.44 |
2 | Log. Litter Size | 0.092 ± 0.016 | 5.62 | 2460 | < 0.0001 | 0.43 |
3 | Log. Maximum longevity | 0.152 ± 0.023 | 6.63 | 1000 | < 0.0001 | 0.53 |
4 | Diet Breadth | 0.013 ± 0.004 | 2.95 | 2114 | 0.003 | 0.46 |
4 | Habitat Breadth | 0.013 ± 0.012 | 1.12 | 2664 | 0.26 | 0.52 |
5 | Trophic Level | –0.025 ± 0.013 | –1.86 | 2114 | 0.06 | 0.43 |
6 | Log. Geographic range size | 0.014 ± 0.001 | 11.19 | 4457 | < 0.0001 | 0.43 |
7 | Log. (1+Human Pop. Density) | 0.008 ± 0.003 | 2.80 | 4457 | 0.005 | 0.43 |
8 | Lat. range mid-point | 0.0017 ± 0.0002 | 7.70 | 4457 | < 0.0001 | 0.42 |
8 | Long. range mid-point | –0.0001 ± 0.00007 | –1.47 | 4457 | 0.14 | 0.43 |
8 | Log. Precipitation | –0.028 ± 0.005 | –5.25 | 4336 | < 0.0001 | 0.44 |
8 | Temperature | –0.0005 ± 0.00006 | –8.73 | 4336 | < 0.0001 | 0.43 |
The full phylogenetic logistic regression model, for the subset of 704 (of which 178 were introduced) species for which data on all nine significant variables in Table
The full phylogenetic generalised logistic model based on the significant variables in Table
Variable | Estimate | Std. Error | t | P |
---|---|---|---|---|
Intercept | –1.08 | 0.238 | –4.52 | <0.0001 |
Log adult body mass | 0.046 | 0.010 | 4.58 | <0.0001 |
Log. Litter Size | 0.140 | 0.040 | 3.50 | 0.0005 |
Log maximum longevity | 0.099 | 0.031 | 3.21 | 0.0014 |
Diet Breadth | 0.009 | 0.009 | 0.95 | 0.34 |
Log geographic range size | 0.049 | 0.008 | 5.74 | <0.0001 |
Log. (1+Human Pop. Density) | 0.046 | 0.015 | 3.13 | 0.002 |
Lat. range mid-point | 0.0009 | 0.001 | 1.01 | 0.31 |
Precipitation | –0.029 | 0.025 | –1.16 | 0.24 |
Temperature (0.1°C) | –0.001 | 0.0003 | –4.38 | <0.0001 |
The geographic distributions of species have always been dynamic, but in recent centuries the processes underlying these changes in distribution have been greatly accelerated. In particular, natural dispersal, which for most of the history of life has been the only way in which species expand their ranges, has been massively augmented by the global movement of organisms by human activities. The first recorded human-introduction relates to a mammal–the grey cuscus Phalanger orientalis introduced to New Ireland around 20,000 years ago (
Our database includes 306 species that we considered to have been introduced somewhere in the world, which is just under 6% of all mammal species. Mammals therefore sit between birds (c.10%;
For example, there is little doubt that the Barbary ape (Macaca sylvanus) population on Gibraltar derives from individuals liberated by humans (other individuals were released in Germany;
The mammalian order with the most introduced species globally in our database is the Artiodactyla: this order includes less than 5% of all mammal species, but 27% of all introduced species (Table
The mammalian order with the second highest number of introduced species globally is the Rodentia (75 species, 24.5%; Table
Other mammalian orders well represented on the global list of alien species include Carnivora (41 species, 13%) and Diprotodontia (28 species, 9%) (Table
As well as exhibiting significant selectivity in terms of identity, introduced mammals are a non-random set in terms of their traits (Table
Species traits help determine which mammals have been introduced, but so too do the characteristics of their geographic range: widespread species inhabiting cooler locations and areas with denser human populations are more likely to have been introduced (Tables
Phylogenetic analysis revealed that there is significant phylogenetic signal in which mammal species have been introduced, albeit less than expected under a Brownian motion model of evolution. This reflects the clear non-randomness of introduction with respect to taxonomic affiliation, but that selection is not simply based around phylogenetic clumping of mammals. These models demonstrate that several variables explained independent variation in introduction (large-bodied, long-lived, widespread, temperate species), in line with findings from other taxa at the global or regional scale (
Introduction is an early step on the invasion pathway (
We thank the referees for comments that greatly improved this manuscript. PC was an ARC Future Fellow (FT0914420), and this work was supported by the Invasive Animals CRC (Project No. 1.L.4), and by the ARC Discovery Grant (DP140102319).
A list of introduced mammal species
Data type: Text
References from which the database of introduced mammals was constructed
Data type: Text