Invasive predators and global biodiversity loss Tim S. Dohertya,b,1, Alistair S. Glenc, Dale G. Nimmod, Euan G. Ritchiea, and Chris R. Dickmane aCentre 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; dInstitute 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 Edited by Daniel S. Simberloff, The University of Tennessee, Knoxville, TN, and approved July 20, 2016 (received for review February 12, 2016) Invasive species threaten biodiversity globally, and invasive mam- include three canids, seven mustelids, five rodents, two procyo- malian predators are particularly damaging, having contributed to nids, three viverrids, two primates, two marsupials, two mon- considerable species decline and extinction. We provide a global gooses, and single representatives from four other families, with metaanalysis of these impacts and reveal their full extent. Invasive 60% from the order Carnivora (Table S1). The 738 impacted predators are implicated in 87 bird, 45 mammal, and 10 reptile species consist of 400 bird species from 78 families, 189 mammal species extinctions—58% of these groups’ contemporary extinc- species from 45 families, and 149 reptile species from 26 families tions worldwide. These figures are likely underestimated because (Dataset S1). Invasive mammalian predators emerge as causal 23 critically endangered species that we assessed are classed as factors in the extinction of 87 bird, 45 mammal, and 10 reptile “possibly extinct.” Invasive mammalian predators endanger a fur- species, which equates to 58% of modern bird, mammal, and reptile ther 596 species at risk of extinction, with cats, rodents, dogs, species extinctions globally (including those species classed as “ex- and pigs threatening the most species overall. Species most at risk tinct in the wild”). Invasive predators also threaten 596 species from predators have high evolutionary distinctiveness and inhabit classed as “vulnerable” (217 species), “endangered” (223), or “criti- insular environments. Invasive mammalian predators are therefore cally endangered” (156), of which 23 are classed as “possibly extinct.” important drivers of irreversible loss of phylogenetic diversity To assess the comparative severity of predator impacts, we worldwide. That most impacted species are insular indicates that assigned each of 1,439 predator-threatened species cases a value management of invasive predators on islands should be a global of either 0.25 (secondary cause of species decline), 0.75 (primary conservation priority. Understanding and mitigating the impact of cause of species decline), or 1.0 (species extinction attributed to invasive mammalian predators is essential for reducing the rate of the predator), and we weighted these values by the strength of global biodiversity loss. evidence available, drawing on a total of 996 supporting references (Methods). The severity of predator impacts and the strength of extinction | feral cat | island | invasive mammal | trophic cascade evidence supporting them [the inverse of the width of confidence intervals (CIs)] was higher for bird and mammal species compared nvasive mammalian predators (“invasive predators” hereafter) with reptile species (Fig. 1). Iare arguably the most damaging group of alien animal species Rodents are linked to the extinction of 75 species (52 bird, 21 ECOLOGY for global biodiversity (1–3). Species such as cats (Felis catus), mammal, and 2 reptile species; 30% of all extinctions) and cats rats (Rattus rattus), mongoose (Herpestes auropunctatus), and to 63 extinctions (40, 21, and 2 species, respectively; 26%) stoats (Mustela erminea) threaten biodiversity through predation whereas red foxes, dogs (Canis familiaris), pigs (Sus scrofa), and (4, 5), competition (6), disease transmission (7), and facilitation small Indian mongoose (H. auropunctatus) are implicated in 9–11 with other invasive species (8). The decline and extinction of extinctions each (Fig. 2). For all threatened and extinct species native species due to invasive predators can have impacts that combined, cats and rodents threaten similar numbers of species cascade throughout entire ecosystems (9). For example, pre- (430 and 420 species, respectively), followed by dogs (156 spe- dation by feral cats and red foxes (Vulpes vulpes) has led to the cies), pigs (140 species), mongoose (83 species), red foxes (48 decline or extinction of two thirds of Australia’s digging mammal species), stoats (30 species) (Fig. 2), and the remaining predators species over the past 200 y (10, 11). Reduced disturbance to topsoil in the absence of digging mammals has led to impoverished Significance landscapes where little organic matter accumulates and rates of seed germination are low (10). In the Aleutian archipelago, pre- Invasive mammalian predators are arguably the most damag- dation of seabirds by introduced Arctic foxes (Alopex lagopus)has ing group of alien animal species for global biodiversity. Thirty lowered nutrient input and soil fertility, ultimately causing vege- species of invasive predator are implicated in the extinction or tation to transform from grasslands to dwarf shrub/forb-dominated endangerment of 738 vertebrate species—collectively contrib- systems (12). uting to 58% of all bird, mammal, and reptile extinctions. Cats, Mitigating the negative impacts of invasive mammalian pred- rodents, dogs, and pigs have the most pervasive impacts, and ators is a primary goal of conservation agencies worldwide (1, 13, endemic island faunas are most vulnerable to invasive preda- 14). Regardless, there remains no global synthesis of the role of tors. That most impacted species are insular indicates that invasive predators in species declines and extinctions (but see management of invasive predators on islands should be a refs. 3 and 15). Here, we quantify the number of bird, mammal, global conservation priority. Understanding and mitigating the and reptile species threatened by, or thought to have become impact of invasive mammalian predators is essential for re- extinct (since AD 1500) due to, invasive mammalian predators. ducing the rate of global biodiversity loss. We use metaanalysis to examine taxonomic and geographic trends in these impacts and show how the severity of predator Author contributions: T.S.D., A.S.G., D.G.N., E.G.R., and C.R.D. designed research; T.S.D. impacts varies according to species endemicity and evolutionary 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 distinctiveness. C.R.D. wrote the paper. The authors declare no conflict of interest. Results and Discussion This article is a PNAS Direct Submission. In total, 596 threatened and 142 extinct species (total 738) have 1To whom correspondence should be addressed. Email: [email protected]. suffered negative impacts from 30 species of invasive mammalian This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. predators from 13 families and eight orders. These species 1073/pnas.1602480113/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1602480113 PNAS | October 4, 2016 | vol. 113 | no. 40 | 11261–11265 Downloaded by guest on September 30, 2021 Birds Mammals Reptiles (χ2 = 117.29, P < 0.001; birds 90%, mammals 55%, reptiles 1.00 91%). Insular endemic reptile species were more negatively af- 0.75 fected by invasive mammalian predators than continental species, whereas mammal and bird species experienced similar impacts 0.50 between the two groups (Fig. 1). If Australia is reclassified as an impact 0.25 island, insular endemic mammals experience more severe predator impacts than continental species (Fig. S1). We sourced evolu- Model-estimated 0.00 tionary distinctiveness scores from published databases (Methods) Total Insular Total Insular Total Insular to show that species negatively affected by invasive predators were Continental Continental Continental 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. 1. Model-estimated severity of impact of invasive predators on birds, (Fig. S2). mammals, and reptiles for all species combined (Total), insular endemics (Insular), and species found on continents (Continental). Error bars are 90% Although it is often stated that invasive predators have con- confidence intervals. Model estimates and confidence intervals are weighted tributed to many modern extinctions (1, 2, 11, 17), our findings by the strength of evidence available. See Table S5 for model estimates. 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 (range 1–14 species). The lower number of species impacted by 23 critically endangered species negatively affected by invasive some predators, such as red foxes and stoats, reflects the limited predators are currently classed as possibly extinct. Evolutionarily number of locations in which these predators have established distinct species are most affected, meaning that invasive preda- alien populations