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Amazonian rainforest loss and declining malaria burden in Brazil

2019; Elsevier BV; Volume: 3; Issue: 1 Linguagem: Inglês

10.1016/s2542-5196(18)30243-2

2542-5196

Gabriel Zorello Laporta,

Parasite Biology and Host Interactions

Malaria emergence and deforestation are often linked in a web of causal mechanisms.1Tucker Lima JM Vittor A Rifai S Valle D Does deforestation promote or inhibit malaria transmission in the Amazon? A systematic literature review and critical appraisal of current evidence.Philos Trans R Soc Lond B Biol Sci. 2017; 372: 20160125Crossref PubMed Scopus (61) Google Scholar Depending on the region of the world, the interconnections between deforestation and malaria are always related to the main characteristics of local malaria transmission dynamics.2Guerra CA Snow RW Hay SI A global assessment of closed forests, deforestation and malaria risk.Ann Trop Med Parasitol. 2006; 100: 189-204Crossref PubMed Scopus (125) Google Scholar Deep-forest vectors, which depend on deep forest shade for larval habitats, naturally benefit when their forest habitats are under conservation. In these conditions, they can transmit plasmodia to humans in central Africa (Anopheles nili), southeast Asia (Anopheles dirus), the western Pacific region (Anopheles balabacensis, Anopheles donaldi, Anopheles flavirostris, and Anopheles leucosphyrus),2Guerra CA Snow RW Hay SI A global assessment of closed forests, deforestation and malaria risk.Ann Trop Med Parasitol. 2006; 100: 189-204Crossref PubMed Scopus (125) Google Scholar or the Atlantic forest of Brazil (Anopheles cruzii).3Laporta GZ Spotlight on Plasmodium falciparum evolutionary system in the Southeastern Atlantic forest.Biota Neotropica. 2017; 17: e20160314Crossref Scopus (2) Google Scholar This phenomenon, recognised as forested malaria, has a negative correlation with deforestation.2Guerra CA Snow RW Hay SI A global assessment of closed forests, deforestation and malaria risk.Ann Trop Med Parasitol. 2006; 100: 189-204Crossref PubMed Scopus (125) Google Scholar On one hand, when deforestation occurrs in forested malaria regions, deep-forest vectors decline in abundance and local malaria incidence could decrease.2Guerra CA Snow RW Hay SI A global assessment of closed forests, deforestation and malaria risk.Ann Trop Med Parasitol. 2006; 100: 189-204Crossref PubMed Scopus (125) Google Scholar On the other hand, near-forest or non-forest vectors benefit from partial-shade and open landscapes for their larval habitats in Amazonia (Anopheles albitarsis, Anopheles darlingi, Anopheles pseudopunctipennis), central Africa (Anopheles funestus, Anopheles gambiae s.s.), South-east Asia (Anopheles culicifacies, Anopheles fluviatilis, and Anopheles minimus), and the western Pacific region (Anopheles farauti, Anopheles koliensis, Anopheles letifer, Anopheles maculatus, and Anopheles punctulatus).2Guerra CA Snow RW Hay SI A global assessment of closed forests, deforestation and malaria risk.Ann Trop Med Parasitol. 2006; 100: 189-204Crossref PubMed Scopus (125) Google Scholar For these vectors, deforestation can be positively correlated with an increase in their abundance, which could augment the likelihood of malaria emergence.2Guerra CA Snow RW Hay SI A global assessment of closed forests, deforestation and malaria risk.Ann Trop Med Parasitol. 2006; 100: 189-204Crossref PubMed Scopus (125) Google Scholar Therefore, deforestation and malaria emergence have a complex relationship that has generated a long and heated debate about the tropical rainforests of the Amazon.4Valle D Clark J Conservation efforts may increase malaria burden in the Brazilian Amazon.PLoS One. 2013; 8: e57519Crossref PubMed Scopus (42) Google Scholar, 5Hahn MB Olson SH Vittor AY Barcellos C Patz JA Pan W Conservation efforts and malaria in the Brazilian Amazon.Am J Trop Med Hyg. 2014; 90: 591-594Crossref PubMed Scopus (14) Google Scholar, 6Barros FS Honório NA Deforestation and malaria on the Amazon frontier: larval clustering of Anopheles darlingi (Diptera: Culicidae) determines focal distribution of malaria.Am J Trop Med Hyg. 2015; 93: 939-953Crossref PubMed Scopus (49) Google Scholar A darlingi is the main malaria vector in the Amazon.7Vittor AY Gilman RH Tielsch J et al.The effect of deforestation on the human-biting rate of Anopheles darlingi, the primary vector of falciparum malaria in the Peruvian Amazon.Am J Trop Med Hyg. 2006; 74: 3-11Crossref PubMed Scopus (358) Google Scholar Its niche requirements are partially shaded larval habitats, and human domiciles that are near to the emergent adult female mosquitoes.8Burkett-Cadena ND Vittor AY Deforestation and vector-borne disease: forest conversion favors important mosquito vectors of human pathogens.Basic Appl Ecol. 2017; 26: 101-110Crossref Scopus (71) Google Scholar Neither a continuous forest nor open land can benefit this vector population.6Barros FS Honório NA Deforestation and malaria on the Amazon frontier: larval clustering of Anopheles darlingi (Diptera: Culicidae) determines focal distribution of malaria.Am J Trop Med Hyg. 2015; 93: 939-953Crossref PubMed Scopus (49) Google Scholar Although forest vectors (figure A) and non-forest vectors (figure B) are primary examples of the relationships between deforestation and malaria emergence, A darlingi also has a distinct role in land-use change and vector-borne diseases.6Barros FS Honório NA Deforestation and malaria on the Amazon frontier: larval clustering of Anopheles darlingi (Diptera: Culicidae) determines focal distribution of malaria.Am J Trop Med Hyg. 2015; 93: 939-953Crossref PubMed Scopus (49) Google Scholar This species is associated with forest fragmentation when forest cover is roughly 30–70% (figure C). Independent research groups studied the paradigm of deforestation and malaria emergence in Amazon.4Valle D Clark J Conservation efforts may increase malaria burden in the Brazilian Amazon.PLoS One. 2013; 8: e57519Crossref PubMed Scopus (42) Google Scholar, 6Barros FS Honório NA Deforestation and malaria on the Amazon frontier: larval clustering of Anopheles darlingi (Diptera: Culicidae) determines focal distribution of malaria.Am J Trop Med Hyg. 2015; 93: 939-953Crossref PubMed Scopus (49) Google Scholar, 7Vittor AY Gilman RH Tielsch J et al.The effect of deforestation on the human-biting rate of Anopheles darlingi, the primary vector of falciparum malaria in the Peruvian Amazon.Am J Trop Med Hyg. 2006; 74: 3-11Crossref PubMed Scopus (358) Google ScholarEach group looked at different perspectives of this paradigm (figure D). The Patz group studied the continuous to mid-disturbed forest perspective and found that deforestation increases malaria.7Vittor AY Gilman RH Tielsch J et al.The effect of deforestation on the human-biting rate of Anopheles darlingi, the primary vector of falciparum malaria in the Peruvian Amazon.Am J Trop Med Hyg. 2006; 74: 3-11Crossref PubMed Scopus (358) Google Scholar The Valle group studied the open-land to mid-disturbed forest perspective, and found that conservation increases malaria.1Tucker Lima JM Vittor A Rifai S Valle D Does deforestation promote or inhibit malaria transmission in the Amazon? A systematic literature review and critical appraisal of current evidence.Philos Trans R Soc Lond B Biol Sci. 2017; 372: 20160125Crossref PubMed Scopus (61) Google Scholar, 4Valle D Clark J Conservation efforts may increase malaria burden in the Brazilian Amazon.PLoS One. 2013; 8: e57519Crossref PubMed Scopus (42) Google Scholar The Barros and Honório group studied the forest fringe hotspot, and found that the relationship between deforestation and malaria emergence is unimodal6Barros FS Honório NA Deforestation and malaria on the Amazon frontier: larval clustering of Anopheles darlingi (Diptera: Culicidae) determines focal distribution of malaria.Am J Trop Med Hyg. 2015; 93: 939-953Crossref PubMed Scopus (49) Google Scholar, 7Vittor AY Gilman RH Tielsch J et al.The effect of deforestation on the human-biting rate of Anopheles darlingi, the primary vector of falciparum malaria in the Peruvian Amazon.Am J Trop Med Hyg. 2006; 74: 3-11Crossref PubMed Scopus (358) Google Scholar, 8Burkett-Cadena ND Vittor AY Deforestation and vector-borne disease: forest conversion favors important mosquito vectors of human pathogens.Basic Appl Ecol. 2017; 26: 101-110Crossref Scopus (71) Google Scholar (figure D). A systematic review8Burkett-Cadena ND Vittor AY Deforestation and vector-borne disease: forest conversion favors important mosquito vectors of human pathogens.Basic Appl Ecol. 2017; 26: 101-110Crossref Scopus (71) Google Scholar on the link between deforestation and vector-borne diseases on a global scale concluded that most mosquito vectors of human pathogens are favoured by forest conversion. This study suggested that the link could reflect evolutionary processes, in which pathogen and vector converged in anthropic environments. The authors also showed that the association between deforestation and mosquito-borne disease can be complex and unpredictable, with the presence of forest vectors and non-forest vectors in the same region.8Burkett-Cadena ND Vittor AY Deforestation and vector-borne disease: forest conversion favors important mosquito vectors of human pathogens.Basic Appl Ecol. 2017; 26: 101-110Crossref Scopus (71) Google Scholar The same conclusions were reached in another study9Loaiza JR Dutari LC Rovira JR et al.Disturbance and mosquito diversity in the lowland tropical rainforest of central Panama.Sci Rep. 2017; 7: 7248Crossref PubMed Scopus (33) Google Scholar that tested the intermediate disturbance hypothesis in the lowland tropical rainforest in Panama. This study showed that forest disturbance is an important predictor for the emergence of arboviral and parasitic diseases. It also showed that mosquito species can respond in specific ways on the forest disturbance gradient, with four functional groups: colonist, climax, disturbance-tolerant, and rare. In the rare species group, they found a mid-disturbance species (Wyeomyia simmsi), the abundance of which peaked at the middle of the disturbance gradient.9Loaiza JR Dutari LC Rovira JR et al.Disturbance and mosquito diversity in the lowland tropical rainforest of central Panama.Sci Rep. 2017; 7: 7248Crossref PubMed Scopus (33) Google Scholar On the basis of the evidence from Barros and Honório6Barros FS Honório NA Deforestation and malaria on the Amazon frontier: larval clustering of Anopheles darlingi (Diptera: Culicidae) determines focal distribution of malaria.Am J Trop Med Hyg. 2015; 93: 939-953Crossref PubMed Scopus (49) Google Scholar and our experience of field work in the Amazon, we conclude that A darlingi is a mid-disturbance species. The complex relationship between A darlingi and deforestation has led the intense debate regarding the factors underlying malaria emergence in the Amazon. Most theories about this relationship seem plausible, but because it is non-linear these theories have been based on evidence that only partially shows what is happening. Here we propose that deforestation can increase or decrease malaria incidence depending of the amount of forest cover. Amazonian biodiversity is under threat because of the widespread depletion of the habitats for native species,10Alroy J Effects of habitat disturbance on tropical forest biodiversity.PNAS. 2017; 114: 6056-6061Crossref PubMed Scopus (150) Google Scholar including the larval habitats of A darlingi. Therefore, a win-lose scenario for planetary health is presented. We could be facing a much-wanted era of malaria elimination in Brazil, but and at the same time ruining the last remnants of tropical rainforests in the Amazon. I declare no competing interests.