UC Santa Cruz

Human health and ecosystem health are intricately linked through ecosystem services and through common threats. For example, deforestation, resource overexploitation, pollution, and introduction of invasive species are the four main threats to biodiversity (Dirzo and Raven 2003, Dirzo et al. 2014), and these have also been linked to the emergence of pathogens of public health concern and overall human health issues (e.g. (Daszak et al. 2001, Patz et al. 2004, Wolfe et al. 2005, Epstein et al. 2006)). Non-native species, which often become invasive in ecosystems that have been anthropogenically disturbed and that have been depleted of or lack native competitors or predators (Allendorf and Lundquist 2003, Doherty et al. 2016), are also reservoirs of several pathogens that affect humans. Because they can reach large population sizes and displace other host species, invasive species can modify and potentially amplify disease transmission dynamics through the introduction of novel pathogens or through changes in community structure (Young et al. 2017). Invasive species are often found in close association to humans, usually as human commensals (e.g. peri-domestic rodents, cats, mosquitos), which can increase the risk of human exposure to pathogens transmitted or carried by these species. Thus, management of invasive species through population control, eradication (in the case of islands) or ecosystem management, which are frequently implemented as biodiversity conservation tools (Doherty et al. 2015, Jones et al. 2016a, Sokolow et al. 2016, Spatz et al. 2017), have the potential to also benefit human health. Although the relationship between ecosystem and human health has just recently emerged as an important area of study, there are few concrete examples of the potential for synergistic interventions benefiting both (Wolfe et al. 2005, Ostfeld et al. 2006, Herrera et al. 2017). Here I focus on the public health impacts of invasive cats (Felis catus) and through three case studies, I provide evidence of the potential for combined public health and conservation benefits of eradicating invasive cat populations from islands and controlling free-roaming colonies on continental areas.

Cats have been introduced to approximately 179,000 islands, and co-occur with people in approximately 560 of them (Medina et al. 2011, Threatened Island Biodiversity Database Partners 2014). Cats are the second most widespread invasive predator on islands and are responsible at least in part for 14% of all bird, mammal and reptile extinctions on islands (Doherty et al. 2016, Jones et al. 2016b). Free-roaming cats on the mainland are also opportunistic predators and in many cases are additionally subsidized directly with supplemental food or indirectly with peri-domestic rodents (Lepczyk et al. 2004, Baker et al. 2005). Management schemes for free-roaming populations range from complete elimination of the population (i.e. eradication) to varying degrees of population control (e.g. trap-neuter-release (TNR), trap-neuter-adopt or trap-euthanize). Most countries and many states in the USA have few, if any, regulations concerning cat ownership and cat owner responsibilities, making free-roaming cat population control inconsistent and difficult to enforce (LaCroix 2006). Programs such as TNR adhere more closely to the demands of cat advocates, resulting in negligible benefits to wildlife, high long-term management costs, and usually uncontrolled free-roaming cat colonies (Andersen et al. 2004, Foley et al. 2005). In theory, these forms of management can significantly reduce cat population sizes if they cover a large proportion of the population and are done consistently (Andersen et al. 2004). However, supplementary feeding, pet abandonment, and persistence of fertile females may attract cats from nearby colonies and increase local cat densities (Bengsen et al. 2015), eventually making trapping efforts a waste of resources. On the other hand, eradications are only implemented when the goal is to permanently eliminate cat populations and are thus only conducted in closed systems such as islands, requiring considerable financial investment, capacity building, and ongoing biosecurity measures to prevent reintroduction (Donlan and Wilcox 2007). Eradications on human-inhabited islands represent additional logistical, social and economic constrains because some invasive species have a social and/or economic value for island inhabitants (Oppel et al. 2011). As a result, successful eradication of domestic cat populations on human-inhabited islands have been limited to islands with no more than 1,000 people (Jones et al. 2016b).

Cats and other wild felids are the only known definitive hosts of Toxoplasma gondii, and infected cats can shed up to one billion or hundreds of million oocysts in their feces (Hill and Dubey 2002). Infection with T. gondii can cause miscarriage or severe ocular and neurological lesions in newborns, systemic disease in immunocompromised individuals, and has been associated with neurological disorders such as Alzheimer’s and schizophrenia (Brown et al. 2005, Mortensen et al. 2007, Torrey et al. 2007, Maenz et al. 2014, Ngô et al. 2017). Exposure to T. gondii oocysts (the environmental stage of the parasite) through contact with contaminated soil is one of the most common routes of T. gondii infection (Cook et al. 2000a, Spalding et al. 2005, Jones et al. 2009, Egorov et al. 2018). Soil-related activities such as gardening or having an occupation involving soil exposure are associated with high risk of T. gondii infection (Jones et al. 2001). There is currently no vaccine against T. gondii, and treatment is often limited to reducing the risk of congenital transmission in women who become infected during pregnancy, or severe illness in people with a compromised immune system (SYROCOT (Systematic Review of Congenital Toxoplasmosis) study group 2007, Robert-Gangneux and Dardé 2012). Following proper food handling and hygiene practices can reduce exposure to T. gondii (Bahia-Oliveira et al. 2017). However, because free-roaming cats contribute significantly to the environmental load of T. gondii (VanWormer et al. 2013a), implementing management strategies that effectively control cat populations can be a more effective approach for reducing environmental contamination at its source. Likewise, on the majority of islands that do not harbor native felids, the local environmental source of T. gondii can be eliminated through cat eradications.

To examine whether cat eradication or population control on islands could benefit human health by reducing the burden of T. gondii infection, I compared the seroprevalence and risk factors associated with T. gondii exposure in people on seven islands with variation in cat density, including one island in which cats were eradicated in the year 2000, and another island in which cats had never been present. I found that eradication of introduced cats on islands could significantly reduce human risk of exposure to T. gondii. Exposure to T. gondii was completely absent on the island that never had cats and near zero on the island where cats were eradicated. Furthermore, all island resident children born after cats were eradicated showed no evidence of exposure to the parasite. The odds of T. gondii infection were nearly five-fold higher in people that had cats near their homes. On islands with cats, we found no association between local cat density and T. gondii seroprevalence, suggesting that complete eradication rather than control of cat population densities is necessary to reduce public health impacts of T. gondii infection.

Understanding the burden of T. gondii infection is required to assess whether cat eradication can benefit human health while also reducing one of the main threats to native species. The burden of T. gondii infection can be further integrated into cost-benefit analyses of cat eradications to determine if the costs of T. gondii infection and biodiversity threats outweigh the socioeconomic costs of eradication. However, epidemiological information on T. gondii infection in people is only known for a small number of islands (N=18) where invasive cats co-occur with people and threatened island native species. This paucity of epidemiological information may be due to lack of reporting and/or limitations in public health services. To estimate the burden of T. gondii infection on islands where this epidemiological information was missing, I used T. gondii prevalence as a proxy for disease burden, and readily available ecological and socioeconomic variables as predictors. I found prevalence of T. gondii to be significantly and negatively correlated with human population size and with the per capita gross domestic product of islands. I used the results of the predictive model to estimate seroprevalence of T. gondii infection for the remaining islands where epidemiological information was missing. This predictive model can be used as a tool for identifying islands where T. gondii prevalence is high and where cat eradication has potential for benefiting human health. These models should be used with caution as further on-the-ground measurement is required before cost-benefit analyses are implemented.

Shedding and persistence of T. gondii oocysts in soil can change through time and can also be influenced by environmental factors, such as temperature and humidity as well as by cat demographic factors, such as cat density, juvenile abundance and supplemental feeding. To examine the spatial and temporal patterns of T. gondii prevalence, I sampled soil at free-roaming cat colonies present in community gardens, playgrounds and parks associated during three seasons (Spring, Summer and Fall) and in areas located along the coast and inland Central California, USA. I used seasons as proxies for temporal variation in both environmental and cat demographic variables, and geographic location of sites to examine spatial differences in prevalence of T. gondii in soil. I detected T. gondii only during Fall and in coastal sites. Results from this study suggest that environmental conditions play an important role in T. gondii presence, or at least persistence in soil, and cat abundance (or juvenile abundance) may be influencing T. gondii transmission dynamics. These results indicate that free-roaming cat colonies in spaces where people (including children) recreate is an important source of T. gondii.