Review Evidence for the Role of Infectious Disease in Species Extinction and Endangerment KATHERINE F. SMITH,∗‡ DOV F. SAX,∗ AND KEVIN D. LAFFERTY† ∗University of Georgia, Institute of Ecology, Athens, GA 30602, U.S.A. †USGS Channel Islands Field Station, University of California Santa Barbara, Marine Science Institute, Santa Barbara, CA 93106, U.S.A. Abstract: Infectious disease is listed among the top five causes of global species extinctions. However, the majority of available data supporting this contention is largely anecdotal. We used the IUCN Red List of Threatened and Endangered Species and literature indexed in the ISI Web of Science to assess the role of infectious disease in global species loss. Infectious disease was listed as a contributing factor in <4% of species extinctions known to have occurred since 1500 (833 plants and animals) and as contributing to a species’ status as critically endangered in <8% of cases (2852 critically endangered plants and animals). Although infectious diseases appear to play a minor role in global species loss, our findings underscore two important limitations in the available evidence: uncertainty surrounding the threats to species survival and a temporal bias in the data. Several initiatives could help overcome these obstacles, including rigorous scientific tests to determine which infectious diseases present a significant threat at the species level, recognition of the limitations associated with the lack of baseline data for the role of infectious disease in species extinctions, combining data with theory to discern the circumstances under which infectious disease is most likely to serve as an agent of extinction, and improving surveillance programs for the detection of infectious disease. An evidence-based understanding of the role of infectious disease in species extinction and endangerment will help prioritize conservation initiatives and protect global biodiversity. Keywords: IUCN, wildlife disease Evidencia del Papel de Enfermedades Infecciosas en la Extinci´on y Puesta en Peligro de Especies Resumen: Las enfermedades infecciosas estan´ consideradas entre las cinco causas principales de la ex- tincion´ global de especies. Sin embargo, la mayor´ıa de los datos disponibles que sustentan esta afirmacion´ son anecdoticos.´ Utilizamos la Lista Roja de Especies Amenazadas y en Peligro de la IUCN y literatura indexada en la Red ISI de Ciencia para evaluar el papel de las enfermedades infecciosas en la p´erdida global de especies. Las enfermedades infecciosas fueron identificadas como un factor contribuyente a <4% de las extinciones conoci- das desde 1500 (833 especies de plantas y animales) y como un factor contribuyente al estatus de cr´ıticamente en peligro en <8% de los casos (2852 especies de plantas y animales en peligro cr´ıtico). Aunque parece que las enfermedades infecciosas juegan un papel menor en la p´erdida global de especies, nuestros hallazgos sub- rayan dos limitaciones importantes en la evidencia disponible: incertidumbre acerca de las amenazas a la supervivencia de especies y un sesgo temporal en los datos. Varias iniciativas podr´ıan ayudar a sobreponer esos obstaculos,´ incluyendo pruebas cient´ıficas rigurosas para determinar qu´e enfermedades infecciosas son una amenaza significativa al nivel de especie, reconocimiento de las limitaciones asociadas con la ausencia de datos basicos´ del papel de enfermedades infecciosas en la extincion´ de especies, combinacion´ de datos con teor´ıa para discernir las circunstancias bajo las cuales es mas´ probable que una enfermedad infecciosa funja como agente de extincion´ y mejoramiento de los programas de vigilancia para la deteccion´ de enfermedades infecciosas. El entendimiento, basado en evidencia, del papel de las enfermedades infecciosas en la extincion´ ‡email [email protected] Paper submitted August 23, 2005; revised manuscript accepted March 14, 2006. 1349 Conservation Biology Volume 20, No. 5, 1349–1357 C 2006 Society for Conservation Biology DOI: 10.1111/j.1523-1739.2006.00524.x 1350 Infectious Disease and Species Extinction Smith et al. y puesta en peligro de especies ayudara´ a priorizar iniciativas de conservacion´ y proteger la biodiversidad global. Palabras Clave: enfermedades de vida silvestre, IUCN Introduction conservation concern and those documented to have be- come extinct in the past 500 years. It has been used re- Recent studies suggest that infectious diseases in wildlife peatedly to assess the impact of individual and multiple populations are emerging at unusually high rates (Harvell threats in the global loss of biodiversity and for specific et al. 1999, 2002; Epstein 2001). Emerging infectious dis- groups (e.g., Butchart et al. 2004; Gurevitch & Padilla eases (EIDs) are those caused by parasites and pathogens 2004; Clavero & Garcia-Berthou 2005). The IUCN Red that have recently increased in incidence, occupied host List reports more than 38,000 plants and animals whose species or geographic extent; have been newly discov- status is categorized based on a defined set of criteria as ered; or are caused by a newly evolved agent (Lederberg extinct, extinct in the wild, critically endangered, endan- et al. 1992; Daszak et al. 2000). The diversity of EIDs af- gered, vulnerable, lower risk, near threatened, data defi- flicting wildlife, coupled with the fear that an increased cient, or of least concern (IUCN 2004). The database is frequency of outbreaks will occur in the future, have a searchable classification of major species threats (e.g., raised concern that infectious disease may play a strong habitat loss, overexploitation, invasive species) ordered role in species extinction (Holmes 1996; Daszak et al. in a hierarchical manner and reported as “summary doc- 2000; Harvell et al. 2002). Indeed, infectious diseases can umentation” for each species case. “Pathogens and par- extirpate local populations, mediate community dynam- asites” (referred to hereafter as infectious diseases) are ics, and shrink host ranges (McCallum & Dobson 1995; classified as threat types under “invasive alien species” Daszak et al. 1999; Lafferty 2003; Walsh et al. 2003). (threat 2.4) and “changes in native species dynamics” Given the effects of infectious diseases on wildlife, it is (threat 8.5) (IUCN 2004). Because this classification sys- not surprising that a survey of biologists listed infectious tem has only been applied to a fraction of species in disease among the top five causes of species extinctions the database (Clavero & Garcia-Berthou 2004), we in- in the United States (Wilcove et al. 1998). However, the dividually examined the “detailed documentation” of all majority of available data supporting this contention is records of extinct and critically endangered plants and largely anecdotal. Moreover, epidemiological theory pre- animals in the IUCN Red List (IUCN 2004) to deter- dicts that infectious diseases should only drive species mine those threatened by infectious disease. We included to extinction under specific circumstances—most com- the 60 species listed as extinct in the wild (those that monly when pre-epidemic population size is small, reser- exist only in captivity) in our tally of extinct species. voir hosts are available, or when the infectious agent can Given the breadth of the IUCN Red List, we focused on survive in the abiotic environment (de Castro & Bolker these threat categories because they are most informa- 2005). In response to a growing interest in global species tive to our goals and arguably of greatest conservation loss and emerging infectious diseases, it is worth inves- concern. tigating the generalization that infectious diseases play a The IUCN Red List reports only threats that trigger list- widespread role in species extinction. ing of the taxon concerned and does not rank or fully elu- We used the World Conservation Union (IUCN) Red cidate the relative importance of individual threats (IUCN List of Threatened and Endangered Species (IUCN 2004) 2004). Threats are reported as having occurred in the past and the Science Citation Index Expanded (ISI Web of Sci- and/or present and/or future, based on a time frame of ence) to compile the most comprehensive information three generations or 10 years, whichever is longer (not available on the causal role of infectious disease in species exceeding 100 years in the future) (IUCN 2004). A threat extinction. In doing so, we sought to accomplish three that occurred in the past, is occurring in the present, or goals. First, to discern what the available evidence sug- may occur in the future is cited as ongoing (IUCN 2004). gests about the causal role of infectious disease in species For each species account, we recorded the time frame extinction and critical endangerment. Second, to uncover of the threat. Based on the information reported in the limitations of the data that may influence these results. detailed documentation, we tallied a fourth category: hy- Third, to use this knowledge to suggest priority areas for pothesized threat. For example, the summary documen- future research on wildlife infectious diseases. tation often reported infectious disease as a contempo- rary or ongoing threat, whereas the detailed documenta- tion made it clear that the threat was only a hypothesis, IUCN Database and Literature Search that no evidence existed to support the claim, or that on- going research was attempting to discern the threat of Designed for global taxon assessments, the IUCN Red List infectious disease (e.g., descriptions for the critically