Biodiversity can help prevent malaria outbreaks in tropical forests

Abstract

Background: Plasmodium vivax is a widely distributed, neglected parasite that can cause malaria and death in tropical areas. It is associated with an estimated 80-300 million cases of malaria worldwide. Brazilian tropical rain forests encompass host- and vector-rich communities, in which two hypothetical mechanisms could play a role in the dynamics of malaria transmission. The first mechanism is the dilution effect caused by presence of wild warm-blooded animals, which can act as dead-end hosts to Plasmodium parasites. The second is diffuse mosquito vector competition, in which vector and non-vector mosquito species compete for blood feeding upon a defensive host. Considering that the World Health Organization Malaria Eradication Research Agenda calls for novel strategies to eliminate malaria transmission locally, we used mathematical modeling to assess those two mechanisms in a pristine tropical rain forest, where the primary vector is present but malaria is absent.

Methodology/principal findings: The Ross-Macdonald model and a biodiversity-oriented model were parameterized using newly collected data and data from the literature. The basic reproduction number ([Formula: see text]) estimated employing Ross-Macdonald model indicated that malaria cases occur in the study location. However, no malaria cases have been reported since 1980. In contrast, the biodiversity-oriented model corroborated the absence of malaria transmission. In addition, the diffuse competition mechanism was negatively correlated with the risk of malaria transmission, which suggests a protective effect provided by the forest ecosystem. There is a non-linear, unimodal correlation between the mechanism of dead-end transmission of parasites and the risk of malaria transmission, suggesting a protective effect only under certain circumstances (e.g., a high abundance of wild warm-blooded animals).

Conclusions/significance: To achieve biological conservation and to eliminate Plasmodium parasites in human populations, the World Health Organization Malaria Eradication Research Agenda should take biodiversity issues into consideration.

Figure 1. Study area.

A: South America and Brazilian States; B: The Iguape-Cananéia-Paranaguá estuarine lagoon region, southeastern coast of Brazil; and C: Parque Estadual da Ilha do Cardoso. G, The Guarani Mbya village; and M, Marujá. Source: Bird and mammal observations ; Altitude and vegetation sampling (Figure S6).

Figure 2. Predicting hypothetical scenarios I: dilution effect and diffuse mosquito vector competition in The Guarani Mbya village.

Increase in abundance of non-vector mosquito species and in abundance of wild warm-blooded animals is correlated with decrease in the risk of malaria-parasite transmission. Reduction in abundance of wild warm-blooded animals (blue dashed arrow) and in abundance of non-vector mosquito species (red dashed arrow) can exceed the critical threshold level (). The red circle is estimate of our model (0.3; eq. 13). The black isoline represents malaria transmission threshold (). Color legend shows a range of values from 0.00 to 1.40.

Figure 3. Predicting hypothetical scenarios II: diffuse mosquito vector competition in Marujá.

Increase in abundance of non-vector mosquito species is linearly correlated with decrease in the risk of malaria-parasite transmission. Reduction in abundance of non-vector mosquito species (red dashed arrow) can exceed the critical threshold level (). The red circle is estimate of our model (0.39; eq. 13). The black isoline represents malaria transmission threshold (). Color legend shows a range of values from 0.00 to 1.50.

Figure 4. Predicting hypothetical scenarios III: dilution effect in Marujá.

Increase in abundance of wild warm-blooded animals is non-linearly correlated with decrease in the risk of malaria-parasite transmission. Reduction in abundance of wild warm-blooded animals (red dashed arrow) does not exceed the critical threshold level (). However, increase in human population size (blue dashed arrow) can exceed the critical threshold level (). The red circle is estimate of our model (0.39; eq. 13). The black isoline represents malaria transmission threshold (). Color legend shows a range of values from 0.00 to 1.40.