Invasive predators and global biodiversity loss Tim S. Dohertya,b,1, Alistair S. Glenc, Dale G. Nimmod, Euan G. Ritchiea, and Chris R. Dickmane a Centre for Integrative Ecology, School of Life and Environmental Sciences, Deakin University, Geelong, VIC 3216, Australia; bCentre for Ecosystem Management, School of Natural Sciences, Edith Cowan University, Joondalup, WA 6027, Australia; cLandcare Research, Auckland 1072, New Zealand; d Institute for Land, Water and Society, School of Environmental Science, Charles Sturt University, Albury, NSW 2640, Australia; and eDesert Ecology Research Group, School of Life and Environmental Sciences, University of Sydney, Sydney, NSW 2006, Australia
Invasive species threaten biodiversity globally, and invasive mammalian predators are particularly damaging, having contributed to considerable species decline and extinction. We provide a global metaanalysis of these impacts and reveal their full extent. Invasive predators are implicated in 87 bird, 45 mammal, and 10 reptile species extinctions—58% of these groups’ contemporary extinctions worldwide. These figures are likely underestimated because 23 critically endangered species that we assessed are classed as “possibly extinct.” Invasive mammalian predators endanger a further 596 species at risk of extinction, with cats, rodents, dogs, and pigs threatening the most species overall. Species most at risk from predators have high evolutionary distinctiveness and inhabit insular environments. Invasive mammalian predators are therefore important drivers of irreversible loss of phylogenetic diversity worldwide. That most impacted species are insular indicates that management of invasive predators on islands should be a global conservation priority. Understanding and mitigating the impact of invasive mammalian predators is essential for reducing the rate of global biodiversity loss. extinction
| feral cat | island | invasive mammal | trophic cascade
I
nvasive mammalian predators (“invasive predators” hereafter) are arguably the most damaging group of alien animal species for global biodiversity (1–3). Species such as cats (Felis catus), rats (Rattus rattus), mongoose (Herpestes auropunctatus), and stoats (Mustela erminea) threaten biodiversity through predation (4, 5), competition (6), disease transmission (7), and facilitation with other invasive species (8). The decline and extinction of native species due to invasive predators can have impacts that cascade throughout entire ecosystems (9). For example, predation by feral cats and red foxes (Vulpes vulpes) has led to the decline or extinction of two thirds of Australia’s digging mammal species over the past 200 y (10, 11). Reduced disturbance to topsoil in the absence of digging mammals has led to impoverished landscapes where little organic matter accumulates and rates of seed germination are low (10). In the Aleutian archipelago, predation of seabirds by introduced Arctic foxes (Alopex lagopus) has lowered nutrient input and soil fertility, ultimately causing vegetation to transform from grasslands to dwarf shrub/forb-dominated systems (12). Mitigating the negative impacts of invasive mammalian predators is a primary goal of conservation agencies worldwide (1, 13, 14). Regardless, there remains no global synthesis of the role of invasive predators in species declines and extinctions (but see refs. 3 and 15). Here, we quantify the number of bird, mammal, and reptile species threatened by, or thought to have become extinct (since AD 1500) due to, invasive mammalian predators. We use metaanalysis to examine taxonomic and geographic trends in these impacts and show how the severity of predator impacts varies according to species endemicity and evolutionary distinctiveness.
include three canids, seven mustelids, five rodents, two procyonids, three viverrids, two primates, two marsupials, two mongooses, and single representatives from four other families, with 60% from the order Carnivora (Table S1). The 738 impacted species consist of 400 bird species from 78 families, 189 mammal species from 45 families, and 149 reptile species from 26 families (Dataset S1). Invasive mammalian predators emerge as causal factors in the extinction of 87 bird, 45 mammal, and 10 reptile species, which equates to 58% of modern bird, mammal, and reptile species extinctions globally (including those species classed as “extinct in the wild”). Invasive predators also threaten 596 species classed as “vulnerable” (217 species), “endangered” (223), or “critically endangered” (156), of which 23 are classed as “possibly extinct.” To assess the comparative severity of predator impacts, we assigned each of 1,439 predator-threatened species cases a value of either 0.25 (secondary cause of species decline), 0.75 (primary cause of species decline), or 1.0 (species extinction attributed to the predator), and we weighted these values by the strength of evidence available, drawing on a total of 996 supporting references (Methods). The severity of predator impacts and the strength of evidence supporting them [the inverse of the width of confidence intervals (CIs)] was higher for bird and mammal species compared with reptile species (Fig. 1). Rodents are linked to the extinction of 75 species (52 bird, 21 mammal, and 2 reptile species; 30% of all extinctions) and cats to 63 extinctions (40, 21, and 2 species, respectively; 26%) whereas red foxes, dogs (Canis familiaris), pigs (Sus scrofa), and small Indian mongoose (H. auropunctatus) are implicated in 9–11 extinctions each (Fig. 2). For all threatened and extinct species combined, cats and rodents threaten similar numbers of species (430 and 420 species, respectively), followed by dogs (156 species), pigs (140 species), mongoose (83 species), red foxes (48 species), stoats (30 species) (Fig. 2), and the remaining predators Significance Invasive mammalian predators are arguably the most damaging group of alien animal species for global biodiversity. Thirty species of invasive predator are implicated in the extinction or endangerment of 738 vertebrate species—collectively contributing to 58% of all bird, mammal, and reptile extinctions. Cats, rodents, dogs, and pigs have the most pervasive impacts, and endemic island faunas are most vulnerable to invasive predators. That most impacted species are insular indicates that management of invasive predators on islands should be a global conservation priority. Understanding and mitigating the impact of invasive mammalian predators is essential for reducing the rate of global biodiversity loss. Author contributions: T.S.D., A.S.G., D.G.N., E.G.R., and C.R.D. designed research; T.S.D. and A.S.G. performed research; T.S.D. analyzed data; and T.S.D., A.S.G., D.G.N., E.G.R., and C.R.D. wrote the paper. The authors declare no conflict of interest.
Results and Discussion In total, 596 threatened and 142 extinct species (total 738) have suffered negative impacts from 30 species of invasive mammalian predators from 13 families and eight orders. These species www.pnas.org/cgi/doi/10.1073/pnas.1602480113
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ECOLOGY
Edited by Daniel S. Simberloff, The University of Tennessee, Knoxville, TN, and approved July 20, 2016 (received for review February 12, 2016)
Model-estimated impact
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Fig. 1. Model-estimated severity of impact of invasive predators on birds, mammals, and reptiles for all species combined (Total), insular endemics (Insular), and species found on continents (Continental). Error bars are 90% confidence intervals. Model estimates and confidence intervals are weighted by the strength of evidence available. See Table S5 for model estimates.
Number of extinct and threatened species
(range 1–14 species). The lower number of species impacted by some predators, such as red foxes and stoats, reflects the limited number of locations in which these predators have established alien populations (16). The frequency of impacted species in each taxonomic class differed among predators (χ2 = 112.27, P < 0.001). Cats, rodents, and stoats threaten more bird than mammal or reptile species whereas red foxes threaten more mammal species (Fig. 2). Dogs threaten fewer reptile species, and pigs and mongoose threaten fewer mammal species, compared with other taxonomic classes (Fig. 2). Although cats and rodents negatively affect the most bird species, birds experience similar impact across predator species (Fig. 3). Mammals experience lower, but more variable, impacts from pigs and stoats compared with the other predators (Fig. 3). The greatest impact on reptile species is from stoats, and the lowest from foxes (no impact) and pigs (Fig. 3). The “significance” of differing relationships between invasive predators and impacted species classes is uncertain, however, because confidence intervals overlapped in most cases. Central America (including the Caribbean) has experienced the most extinctions (33 species), followed by Micro-/Mela-/ Polynesia (25), Australia (21), the Madagascar region (20), New Zealand (15), and Hawaii (11), with the remaining regions having 0–7 species extinctions each (Fig. 4). The taxonomy of impacted species varied among regions, with the highest numbers of impacted mammal species occurring in Australia and Central America, and most of the impacted reptile species occurring in Micro-/Mela-/Polynesia and Central America (Fig. 4). Most impacted bird species are in Micro-/Mela-/Polynesia, New Zealand, the Madagascar region, Central America, and Hawaii (Fig. 4). Insular endemics accounted for 87% of extinct species (124 species) and 81% of the sum of all threatened/extinct species (601 species). The proportions of total threatened/extinct species that were insular endemics varied between taxonomic classes
(χ2 = 117.29, P < 0.001; birds 90%, mammals 55%, reptiles 91%). Insular endemic reptile species were more negatively affected by invasive mammalian predators than continental species, whereas mammal and bird species experienced similar impacts between the two groups (Fig. 1). If Australia is reclassified as an island, insular endemic mammals experience more severe predator impacts than continental species (Fig. S1). We sourced evolutionary distinctiveness scores from published databases (Methods) to show that species negatively affected by invasive predators were more evolutionarily distinct than “nonimpacted” species for both bird (t = 3.32, P = 0.001) and mammal species (t = 3.31, P = 0.001) (Fig. S2). Although it is often stated that invasive predators have contributed to many modern extinctions (1, 2, 11, 17), our findings reveal the magnitude and pervasiveness of their impacts and link them to the majority (58%) of modern bird, mammal, and reptile species extinctions. This figure is likely an underestimate because 23 critically endangered species negatively affected by invasive predators are currently classed as possibly extinct. Evolutionarily distinct species are most affected, meaning that invasive predators are drivers of irreversible loss of global phylogenetic diversity, affecting both mainland and island-endemic species. Introduced rodents and cats are major agents of extinction, collectively being listed as causal factors in 44% of modern bird, mammal, and reptile species extinctions. We pooled the impacts of rodents across five species, but previous studies indicate that R. rattus has negatively affected the most species, followed by Rattus norvegicus and Rattus exulans (18–20). The role of the house mouse (Mus musculus) is less well understood, but there is emerging evidence of severe predatory impacts on insular seabird (21) and lizard species (22). We found that cats, rodents, dogs, and pigs have had the most pervasive effects across regions and taxonomic classes, supporting recent work by Bellard et al. (3), who identified these four taxa as the invasive species affecting the greatest number of threatened vertebrates globally, after chytrid fungus (Batrachochytrium dendrobatidis). However, other predators have had large impacts in particular regions; stoats remain a major threat to New Zealand bird and reptile species (23), and the red fox, along with the feral cat, is an important driver of Australian mammal species extinctions (11). Fewer reptile species were negatively affected by invasive mammalian predators, compared with bird and mammal species. Reptiles also had a lower average impact score, which may be because reptiles are less studied than birds and mammals (9), with only 40% of the world’s reptiles having been assessed for the Red List thus far (compared with ∼99% for birds and mammals) (24). Further insights will likely emerge once the conservation status of most reptiles has been determined. Detailed studies from individual regions nonetheless demonstrate that invasive predators can have severe impacts on local reptile assemblages
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Fig. 2. Numbers of threatened and extinct bird (B), mammal (M), and reptile (R) species negatively affected by invasive mammalian predators. Gray bars are the total number of extinct and threatened species, and red bars are extinct species (including those classed as extinct in the wild). Predators affecting
