Three reasons why expanded use of natural enemy solutions may offer sustainable control of human infections

Abstract

1. Many infectious pathogens spend a significant portion of their life cycles in the environment or in animal hosts, where ecological interactions with natural enemies may influence pathogen transmission to people. Yet, our understanding of natural enemy opportunities for human disease control is lacking, despite widespread uptake and success of natural enemy solutions for pest and parasite management in agriculture. 2. Here we explore three reasons why conserving, restoring, or augmenting specific natural enemies in the environment could offer a promising complement to conventional clinical strategies to fight environmentally mediated pathogens and parasites. (1) Natural enemies of human infections abound in nature, largely understudied and undiscovered. (2) Natural enemy solutions could provide ecological options for infectious disease control where conventional interventions are lacking. And, (3) Many natural enemy solutions could provide important co-benefits for conservation and human well-being. 3. We illustrate these three arguments with a broad set of examples whereby natural enemies of human infections have been used or proposed to curb human disease burden, with some clear successes. However, the evidence base for most proposed solutions is sparse, and many opportunities likely remain undiscovered, highlighting opportunities for future research.

Keywords: biological control; disease control; disease ecology; infectious disease; natural enemies; sustainability; sustainable development.

Figure 1.

Natural enemies (outlined in green) of human infections in the environment (outlined in orange). (A) Larvivorous fish predators of mosquito vectors. (B) Macrobrachium spp. crustacean predators of schistosomiasis intermediate host snails. (C) Daphnia spp. crustacean predators of aquatic bacteria, including Escheria coli and Campylobacter jejuni. (D) Phage predation on V. cholerae. (E) Vulture consumers of disease-carrying carcasses, and competitors of wild dogs that can carry rabies. (F) Copepod predators of larval Aedes mosquito vectors of dengue virus. (G) Fungal pathogen, Beauveria bassiana, of tick disease vectors.

Figure 2.

General categories of natural enemy interactions with disease-causing organisms: (A) predation; (B) parasitism; and, (C) competition, including intraguild predation, a special case of competition when an organism is both a competitor and a predator of another organism.

Figure 3.

The number of countries reporting mosquito vector resistance to one or more major classes of insecticide used globally in the fight against mosquito-borne diseases. Data was obtained from the Vectorbase database (Giraldo-Calderón et al., 2015); resistance data was filtered to include resistance reported as percent mortality, and resistance was conservatively defined as mosquito mortality less than 95%.

Figure 4.

Natural predators (green) of adult and larval mosquitoes are widespread, and include various species of bats, arthropods, birds, amphibians, fish, and crustaceans. Naturally occurring strains of Wolbachia bacteria may (i) inhibit development of arboviruses in Aedes spp. and, potentially, malaria in Anopheles spp., or (ii) lead to sterility when artificially infected male mosquitoes mate with wild, uninfected females.