Vector species richness predicts local mortality rates from Chagas disease

Vector-borne diseases are a major public health concern, as they can have severe consequences for human well-being. The transmission of pathogens may be influenced by both evolutionary and ecological drivers, making it crucial to understand the role of biodiversity in the emergence and spread of these diseases, some of which are classified as neglected tropical diseases (Ostfeld and Keesing, 2000, Keesing et al., 2010). Studies have shown that biodiversity within ecological communities plays a significant role in the transmission of vector-borne diseases (Kocher et al., 2022). Hence, the presence of multiple host and vector species within these communities can have both direct and indirect effects on disease prevalence. Therefore, the conservation and management of biodiversity can play a key role in reducing the burden of vector-borne diseases (Ostfeld and Keesing, 2000).

Past reviews have argued that biodiversity reduces disease prevalence, via a hypothesis sometimes called the ‘dilution effect’ (DEH; e.g., Dobson et al., 2006, Ostfeld and Keesing, 2012, Civitello et al., 2015). Although there is increasing support for the DEH (Civitello et al., 2015), its predictions remain inconclusive as there is evidence of no such effect in some host-pathogen communities (Huang et al., 2016, Ferraguti et al., 2021). The amplification effect hypothesis (AEH), on the other hand, posits that increased biodiversity can result in a heightened risk of disease transmission (Keesing et al., 2006). It assumes that species-rich communities correlate with parasite-rich communities (Kamiya et al., 2014a). Specifically, the diversity of host communities upstream can contribute to the diversity of parasite communities in downstream host populations (Hechinger and Lafferty, 2005), which may be particularly relevant for vector-borne diseases where vectors act as upstream sources of infection for downstream hosts.

These two competing hypotheses (DEH and AEH) provide a valuable perspective on how changes in biodiversity may impact the transmission, maintenance, and prevalence of disease within ecosystems. Therefore, to fully comprehend the impact of biodiversity and disturbance on disease transmission, it is essential to examine the consistency and strength of the relationship between hosts and pathogens in the context of the opposite predictions made by the dilution and amplification hypotheses. One key component of biodiversity is species richness. Thus, to gain a deeper understanding of the relationship between vector diversity, disease transmission and host mortality rates, it is important to examine the factors that influence variation in vector richness among different regions.

Species richness can be positively associated with the incidence of vector-borne diseases (Johnson et al., 2015). In this context, host density across all suitable species can have a significant impact on parasite persistence, with higher host densities often leading to higher parasite diversity (Kamiya et al., 2014b). Furthermore, latitudinal and bioclimatic gradients can also affect vector diversity, as they are often linked to higher net primary productivity. Studies have shown that these gradients can be strong predictors of biodiversity, with a higher parasite and vector diversity found in regions with higher productivity. For example, latitude and climate can positively correlate with parasite and vector diversity (Lafferty, 2009). Hence, understanding these factors can help to identify areas of higher disease transmission risk and the potential impact of biodiversity conservation on transmission and mortality rates.

Most research has focused on the effects of host diversity on pathogen transmission, whereas vector diversity has seldom been examined (Johnson et al., 2013, Roche et al., 2013). Vector diversity is supposed to increase disease risk (Brooks and Zhang, 2010, Roche et al., 2013, Takimoto et al., 2022), nevertheless, some theoretical models suggest otherwise in certain conditions (Roche and Guégan, 2011). Due to species interactions within ecological communities, amplification and dilution effects may alter pathogen transmission depending on the ecological context (Keesing et al., 2006). For instance, species interactions (e.g., with predators, hosts, parasites, and competitors) can potentially hamper or facilitate pathogen transmission. In the case of parasites and vectors, the effects of vector species richness on disease prevalence and host death rates are still obscure. Some research suggests that decreasing vector species richness may consistently reduce pathogen transmission, while a greater vector species richness would amplify it (Roche and Guégan, 2011, Roche et al., 2013).

Chagas disease is a parasitic infection caused by the protozoan Trypanosoma cruzi. The primary mode of transmission is the bite and contact with faeces of infected triatomine vectors, also known as “kissing bugs”. However, but still related to the presence of vectors, the disease may also be transmitted through oral (food-borne) transmission, blood transfusion, organ transplant and congenital transmission (https://www.who.int/news-room/fact-sheets/detail/chagas-disease-(american-trypanosomiasis)). The disease is most prevalent in Latin America and can have severe consequences including death (Martinez et al., 2019). Chagas disease has been documented to have occurred in Latin America for a minimum of 9000 years (Araújo et al., 2009). In recent times, significant shifts in human populations, particularly the transition from rural to urban settings during the last century, have led to a transformation of the disease's transmission cycle from a predominantly sylvatic state to an urbanized one. This shift is primarily facilitated by vectors that have adapted to human-modified environments (Colussi et al., 2022).

The development of resistance among these vectors to insecticides has compromised the efficacy of vector control measures, necessitating a greater emphasis on investigating the ecological dynamics of Chagas disease cycles. It is crucial to focus research efforts on comprehending the ecological aspects pertaining to reservoirs, hosts, and vectors (Flores-Ferrer et al., 2018). Notably, studies have indicated possible effects of reservoir and vector diversity on disease prevalence (Gottdenker et al., 2012, Méndez-Cardona et al., 2022). Additionally, deforestation, leading to a loss of habitat and host diversity, may contribute to an increased frequency of human-vector interactions in both rural and urban fringe areas.

Chagas disease prevalence and higher mortality rates are likely linked to endemic areas of triatomines (Martins-Melo et al., 2021). In Latin America, the vectors of T. cruzi belong to different species of the genera Triatoma, Rhodnius and Panstrongylus (Coura, 2014, Mendes et al., 2016). In recent years, the threat of Chagas disease has increased as previously unknown biodiversity of triatomine vectors has been discovered (Costa et al., 2021), and new species have emerged as vectors in areas where the traditional main vector has been controlled (Cantillo-Barraza et al., 2022). Moreover, recent increases in food-borne transmission of the disease are alarming and are probably influenced by vector richness and abundance (Coura, 2014). Therefore, it is important to understand how vector species richness can directly or indirectly contribute to the transmission of Chagas disease to reduce the burden of the disease on specific populations where there is a higher risk of infection.

Here, we tested whether mortality rates due to Chagas disease could be predicted by Triatominae species richness. Furthermore, we analysed the relationship between triatomine species richness and human population density (host density), socioeconomic predictors, bioclimatic variables, and latitude. We expected that kissing bug richness would be more predictive of mortality than socioeconomic predictors (Gross domestic product, (GDP) per capita).

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