Biological invasions facilitate zoonotic disease emergences

The dramatic increase in zoonotic diseases, those transmitted from animals to humans, poses a major threat to global health, economies, and social stability. The rise in both alien species introductions and zoonotic diseases, exemplified by outbreaks like avian influenza, SARS, and COVID-19, has raised concerns about their potential interrelationship. Alien species can contribute to zoonoses by increasing the abundance of existing pathogens or introducing novel ones. Furthermore, human activities associated with alien species introductions, such as pet trade and aquaculture, increase contact opportunities between alien hosts and humans. While individual case studies link alien species to zoonoses (e.g., invasive rats and plague), a comprehensive global synthesis across various taxa has been lacking. This research addresses this gap by examining the relationship between established alien zoonotic hosts and zoonoses worldwide, while controlling for various confounding factors such as propagule pressure, climate change, biodiversity loss, land-use change, and human population density. The study aims to isolate the unique contribution of alien hosts to zoonoses and inform strategies for mitigating future risks.

Previous research has highlighted the potential link between alien species invasions and zoonotic disease emergence. Studies have shown individual examples of invasive species facilitating the transmission of specific diseases, but a global scale analysis incorporating diverse taxa and controlling for confounding factors was lacking. The existing literature pointed towards correlations between alien species introductions and disease outbreaks, but causation remained unclear. Confounding factors such as propagule pressure (the number of individuals introduced), climate change, biodiversity loss, land-use change, human population density, and research effort (publication bias) needed to be addressed to isolate the independent effect of alien species introductions on zoonoses. This study builds upon prior work by conducting a global-scale analysis that incorporates a wide range of taxonomic groups and controls for these numerous cofactors.

This study employed a global database of 10,473 zoonosis events from 1348 to 2020, compiled with the assistance of the GIDEON database. The researchers used an intensive literature review to identify 795 established alien animal species, categorizing them as either zoonotic or non-zoonotic hosts. They then used generalized additive mixed models (GAMMs) to analyze the relationship between the richness of alien zoonotic hosts and the number of zoonosis events. The models controlled for several covariates: propagule pressure (using non-zoonotic alien host richness as a control), climate change (using temperature and precipitation changes), land-use change, biodiversity loss (using threatened species counts), native biodiversity, sampling effort (using PubMed citations and the Infectious Disease Vulnerability Index (IDVI)), and spatial autocorrelation. The analyses accounted for species, disease, and geographic sampling biases. Furthermore, the authors conducted additional analyses to assess the temporal relationship between alien species introductions and zoonosis events and to investigate the relative contributions of different taxonomic groups of alien hosts. Breakpoint regression analyses were used to identify the time points of significant changes in both zoonosis events and alien host introductions. Data on alien species introductions were compiled from various sources including the Global Avian Invasions Atlas (GAVIA), Introduced Mammals of the World database, and the Global Invasive Species Database (GISD). Climate data were obtained from the University of East Anglia Climate Research Unit (CRU). Land-use data came from the Anthromes v2 Dataset. Biodiversity data were sourced from the Biodiversity Mapping website. The models included continent, host order, and pathogen identity as random intercepts to account for the lack of independence among observations.

The study found a significant positive association between the richness of alien zoonotic hosts and the number of zoonosis events worldwide. This relationship held true even after accounting for various cofactors, demonstrating that the introduction of alien zoonotic hosts independently contributes to the emergence of zoonotic diseases. The analysis revealed an average of approximately 5.9 zoonoses per alien zoonotic host. Specific taxonomic groups showed stronger associations with zoonoses than others. Mammalian orders Carnivora, Artiodactyla, and Rodentia; avian groups Anseriformes (waterfowl), Galliformes, and Passeriformes; and the order Diptera (insects) exhibited particularly strong positive relationships. These findings are consistent with prior research indicating the importance of these taxa in zoonotic disease transmission. The study also revealed a positive correlation between the number of zoonosis events and human population density, biodiversity loss, climate change, and land-use change, highlighting the combined impact of these factors in shaping zoonotic disease emergence. The temporal analysis indicated a close temporal relationship between the increase in alien zoonotic hosts and the rise in zoonoses. A breakpoint regression analysis showed a sharp increase in zoonosis events in 1962, two years after a sharp increase in alien zoonotic host introductions in 1960. Finally, a global map illustrated the spatial distribution of the estimated contribution of alien zoonotic hosts to historical zoonosis events, identifying hotspots primarily in Europe, Oceania, and the Caribbean.

The findings of this study provide strong support for the hypothesis that established alien species significantly contribute to the emergence of zoonotic diseases globally. The positive association between alien zoonotic host richness and zoonosis events, even after controlling for numerous confounding variables, demonstrates a causal link beyond propagule pressure alone. The study highlights the importance of considering invasive species management as a crucial strategy for global health security. The identified hotspots of zoonotic disease risk associated with alien host introductions can guide targeted surveillance and control efforts. The results emphasize the interconnectedness of biodiversity loss, climate change, land-use change, and zoonotic disease emergence, underscoring the need for a holistic approach to disease prevention. The study's multi-taxonomic approach provides a comprehensive understanding of the risk posed by alien species invasions, enabling more effective strategies for preventing future zoonotic outbreaks.

This study presents the first comprehensive, global-scale analysis of the relationship between alien species invasions and zoonotic disease emergence, providing robust evidence for a significant causal link. The findings highlight the importance of managing alien species invasions as a critical component of global health security. The identified spatial and temporal patterns can inform targeted surveillance and control efforts, and the results underscore the need for a holistic, One Health approach to address the complex interplay of factors driving zoonotic disease outbreaks. Future research could focus on further refining risk assessments by incorporating more detailed data on pathogen spillover mechanisms and host-pathogen interactions.

While this study represents a significant advance in understanding the role of alien species in zoonoses, several limitations should be acknowledged. The reliance on existing databases may result in incomplete or biased data on both zoonosis events and alien species introductions. The accuracy of pathogen-host associations is dependent on the completeness and reliability of the literature reviewed. Furthermore, the study primarily focuses on established alien species and might not fully capture the impact of newly introduced species. Finally, the complexity of ecological interactions and the multitude of factors influencing disease emergence require further research to fully disentangle the intricate relationships.