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Mapping geographic and demographic shifts for container breeding mosquito-borne disease transmission suitability in Central and South America in a warming world [1]

['Sadie J. Ryan', 'Department Of Geography', 'The Emerging Pathogens Institute', 'Quantitative Disease Ecology', 'Conservation', 'Qdec', 'Lab', 'University Of Florida', 'Gainesville', 'Florida']

Date: 2024-06 

Abstract The recent Intergovernmental Panel on Climate Change Sixth Assessment Report (IPCC-AR6) brought into sharp relief the potential health impacts of a changing climate across large geographic regions. It also highlighted the gaps in available evidence to support detailed quantitative assessments of health impacts for many regions. In an increasingly urbanizing world, there is a need for additional information about the risk of mosquito-borne diseases from vectors adapted to human water storage behavior. Specifically, a better understanding of the geographic distribution of disease risk under different climate warming scenarios and human population shifts. We present novel geospatial descriptions of risk for transmission for five mosquito-borne disease systems under future projected climate and demographic scenarios, including the potential risk for malaria in the event of the introduction and establishment of a vector of high global concern, Anopheles stephensi. We then present country-level and IPCC geospatial sub-regional risk descriptions under baseline and future projected scenarios. By including demographic projections using the shared socioeconomic pathway (SSP) scenarios, we capture potential future risk in a way that is transparent and straightforward to compare and replicate. The goal of this paper is to report on these model output data and their availability. From a sub-regional perspective, the largest proportional gains in risk will be seen in the Southwestern South America (SWS) sub-region, comprising much of the southwestern coastline, for which the suitability for Aedes aegypti-transmitted dengue and Zika will see massive increases with warming, putting a large number of people at risk under future scenarios. In contrast, at the country level, the largest projected population impacts will be seen in Brazil for both arboviral and potential introduced malaria risk, despite some risks projected to decrease as parts of the country are too hot to sustain transmission. This paper provides modeled outputs for future use, in addition to broad summary descriptions at regional and country levels.

Citation: Ryan SJ, Lippi CA, Stewart-Ibarra AM (2024) Mapping geographic and demographic shifts for container breeding mosquito-borne disease transmission suitability in Central and South America in a warming world. PLOS Clim 3(5): e0000312. https://doi.org/10.1371/journal.pclm.0000312 Editor: Shlomit Paz, University of Haifa, ISRAEL Received: October 2, 2023; Accepted: April 9, 2024; Published: May 6, 2024 Copyright: © 2024 Ryan et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability: All population product data used within are freely available online, all climate layers comprising the ensemble are freely available online, as described in methods. The model input and output layers are available at linked repositories within the manuscript. Funding: The authors received no specific funding for this work. Competing interests: The authors have declared that no competing interests exist.

Introduction Ongoing and future climate change is expected to continue to have profound impacts on the global distribution and burden of many mosquito-borne diseases (MBDs) [1–5]. Nearly every link in the transmission chain of vector-borne pathogens is mediated by environmental influences, notably on vector reproduction and behavior, and pathogen replication [1,4]. The ideal conditions that drive vector-borne transmission systems vary with different vector-pathogen combinations. Still, many MBDs of public health importance, including malaria, yellow fever, dengue fever, and Zika, are typically associated with the tropics [1]. Increasing global temperatures are projected to expand the suitable transmission range of MBDs. However, these changes are not expected to result in uniformly elevated transmission risk throughout all regions. Rather, we expect that there will be shifts in the geographic expanse of MBD thermal transmission suitability [5]. As subtropical and temperate areas warm, becoming more suitable for transmitting historically tropical diseases, other locations currently associated with high MBD incidence may become too hot, exceeding the physiological thermal limits of pathogens and vectors. While decreasing MBD suitability may seem advantageous at face value, any decrease in risk may be grossly outweighed by cumulative gains in the geographic area of suitability, the extension of transmission season length in locations that currently experience low MBD burden, or the expansion of the geographic range of transmission suitability into high population centers. It is also vital for public health planners to understand the shifting risk of MBDs against the backdrop of not only a changing climate but also the movement of people on the landscape. As the world experiences climate warming, we are simultaneously experiencing changes to the global human population, such as increasing urbanization, population densities, contact rates, and movements of people, goods, pathogens, and vectors. These changes directly affect MBD risk, particularly in urban and periurban environments. The spread of novel mosquito vectors has, in many instances, been linked to international trade networks and the movement of goods. For example, the expansion of Aedes albopictus via maritime transport, the used tire trade and ground transportation networks [6], and recent detections of Anopheles stephensi near seaports [7] and in a livestock quarantine station [8]. Human water storage practices and behaviors can create reservoirs of suitable habitat for mosquito oviposition on landscapes with otherwise inadequate precipitation. Water use and storage practices have consistently been identified as a major risk factor for urban dengue throughout Latin America, influencing household risk of infection [9–11], mosquito presence [12–17], and driving vector activity in arid cities [18]. Because of the profound influence that human activity has on vector distributions and MBD risk, it is therefore prudent to consider the intersection of thermal suitability and socioeconomic factors when estimating overall future vector suitability and population-level risk to humans. Previous studies have made efforts to delineate potential shifts in the geography of MBD transmission risk driven by climate change [2,4,19,20]. Much of this work has focused on the transmission of Plasmodium falciparum malaria in Africa, given its considerable global health burden. Although malaria remains a public health concern in the Americas, outbreaks of arboviral diseases currently place larger resource strains on many public health systems throughout Latin America. Dengue fever is a major public health issue throughout the tropics and subtropics worldwide, including Central and South America. In 2019, the Pan American Health Organization (PAHO) reported more than 3.1 million cases in the Americas, a record breaking total which included 28,176 severe cases and 1,535 deaths [21,22]. Following the unprecedented 2019 outbreak, dengue fever outbreaks continue to burden public health systems and communities, which also had to contend with the devastating effects of the SARS-CoV-2 pandemic [22]. Zika virus, which swept through the region in 2016, imposed a high burden throughout Latin America and the Caribbean as an emerging pathogen. While cases have dropped precipitously in many countries following the pandemic, Zika is still circulating in the Americas (over 40,000 cases reported in 2022 [23]), and has the potential to trigger future outbreaks as population-level immunity wanes. Malaria incidence has declined greatly throughout Central and South America in recent decades, where cases have dropped by 70% between 2000 and 2021 [24]. Historically, P. falciparum accounted for the bulk of regional cases in Latin America, though following eradication efforts, most malaria burden is currently attributable to Plasmodium vivax [24,25]. Several regions in Central and South America have successfully achieved local malaria elimination through concerted vector control efforts, including Belize [26], El Salvador [27], Argentina, Paraguay [28], and the Ecuadorian-Peruvian border [29]. Nevertheless, localized hotspots of malaria activity persist and have even increased throughout the region. The reemergence of malaria remains a concern for public health officials [30], particularly in the Amazon region [25], where outbreaks have occurred in portions of southern Venezuela and Brazil [31,32]. In addition to the current threat of reemergence, the invasive mosquito An. stephensi would further complicate the landscape of malaria transmission in the Americas should this vector become established. Global projections of thermal suitability already indicate that the Americas are suitable for establishment and transmission should the vector be introduced [33]. Adept at transmitting both P. falciparum and P. vivax, An. stephensi has aggressively expanded its range in recent years and is associated with increased malaria outbreaks in the Horn of Africa [34]. Perhaps most troublesome, this vector has life history characteristics that mirror container-breeding Aedes spp., presenting the unprecedented risk of urban malaria transmission in its introduced range [34]. Studies focusing on exposure risk solely by geographic region or landscape suitability may not communicate the most useful information for public health planning. Expressing risk in terms of estimated population exposure, or population at risk (PAR), clearly demonstrates to stakeholders the potential impact of shifting MBD transmission suitability on health infrastructure. This is a salient point for informing policy in Latin America, where public health authorities grapple with limited resources in the face of large MBD outbreaks. Further to this point, many of Latin America’s major population centers are located in coastal areas, and uneven population distributions mean that assessing potential exposure to risk purely in terms of geographic area does not capture the nuance of projected health burdens. This study aims to generate model-based descriptions of container breeding MBD risk for IPCC-designated sub-regions in Central and South America and country-level summary information under baseline and future climate projections and using corresponding population projections from the Global Population of the World (GPW4) and Shared Socioeconomic Pathways (SSPs) products. This work is the first effort to bring mapped temperature suitability models for currently circulating arboviral vector and disease risks and malaria transmission under the scenario of a potential novel vector (An. stephensi) together in one framework, facilitating comparisons of risk across diseases, climate change scenarios, and countries in these regions. To make these results available and useful for decision-making and planning, the resulting rasterized model outputs and both IPPC sub-regional and country-level data are freely and openly available via the Harvard Dataverse (https://dataverse.harvard.edu/dataverse/CSAM_PAR_2024; https://dataverse.harvard.edu/dataverse/Aedesmaps, https://dataverse.harvard.edu/dataverse/stephensimaps).

Discussion This study documents the current and projected potential exposure risk for five container breeding mosquito-pathogen pairings, encompassing three mosquito species (Ae. aegypti, Ae. albopictus, An. stephensi), and four pathogens (DENV, ZIKV, P. falciparum, and P. vivax) in Central and South America. These findings expand on the IPCC AR6 Working Group II chapter for Central and South America, which describes the present-day and future thermal suitability risk of DENV and ZIKV transmission [47] by including potential risk from two malaria transmission scenarios in the event of introduction and invasion of the novel vector An. stephensi. This study also disaggregates all scenarios to the country level to allow more comprehensive examinations of baseline and future projections. We show here that a combination of projected human population changes and climate change scenarios drive vastly different responses in the number of people exposed to mosquito-borne disease transmission suitability at different time horizons. These patterns depend on the underlying physiology and temperature responses of mosquito-pathogen pairings. In an increasingly urbanizing world, the capacity of mosquitoes to use artificially generated breeding habitats—containers for water storage, puddling on non-porous surfaces, ditches, garbage able to capture even small volumes of standing water—is amplified and complicates the effects of seasonal precipitation. Using the population projections generated under the SSP framing, the redistribution of human population density on the globe as a function of responses to a moderate (SSP2, RCP 4.5) and the worst case (SSP5, RCP 8.5) scenario, reflect assumptions about both fertility differences between higher and lower income countries, and climate-induced migrations [48]. Importantly, an increase in urban population density due to these projections will promote and amplify the availability of containers for breeding. Thus, understanding risk as the intersection of thermal transmission suitability and human population characteristics provides us with a means to anticipate and target vector control activity—even at a broad scale. In addition, these findings provide evidentiary support to develop health sector responses to climate change, e.g., including robust vector surveillance and control actions in Health National Adaptation Plans (HNAPs). As an illustration, even when the geographic range of thermal suitability appears to be fairly consistent across most scenarios, as with dengue transmitted by Ae. aegypti or P. falciparum malaria spread by An. stephensi, we still found dramatic changes in both the magnitude and geographic distribution of population at risk (PAR). As the socioeconomic pathway projections (SSPs) include spatially implicit population shifts in response to climate, these changes will be additionally driven by the movement of people in response to climate change [41,48]. Incorporating the movement of people into projections captures shifting human population densities, thus increasing container potential where humans are increasing. Dengue virus transmitted by Ae. aegypti currently imposes major public health burdens throughout Central and South America, as evidenced by historically large outbreaks in 2019 and 2023 [49]. As shown here and elsewhere, dengue will continue to be a public health threat as overall transmission suitability increases and shifts in the future, placing new populations at risk of disease. In contrast, Ae. albopictus, though a competent dengue vector, is currently not as widely distributed throughout Central and South America [50], but shows patterns of ongoing invasion and establishment. If this species were to become broadly established due to its lower tolerance for high temperatures and preference for more temperate habitats, it is predicted to experience greatly diminished areas of suitability in the future. This would result in massive reductions in PAR of dengue exposure from this species. Nonetheless, in the absence of Ae. aegypti, it is probable that Ae. albopictus would become the primary vector of arboviruses [51,52]. Thus, Ae. albopictus presents a persistent risk for dengue transmission despite fragmented future suitability, particularly in cooler climates that would otherwise suppress transmission from Ae. aegypti, such as high elevations in mountainous regions [53] and currently temperate areas, such as the southern cone of South America. Emerging precision and targeted vector control methods are becoming more prevalent and tailored to specific species, such as Ae. aegypti (e.g., improved sterile insect techniques [54,55], gene drive approaches [56,57], and transgenics [58]). However, these findings highlight the importance of remaining vigilant to non-target species such as Ae. albopictus. Anopheles stephensi presents the spectre of a novel potential invader and malaria vector in the Americas. This mosquito has left its native range of the Indian subcontinent and parts of the Middle East. It has become established in urban and periurban settings across the African continent, where it has caused unprecedented urban malaria outbreaks in its introduced range [34]. In light of this global public health threat, the World Health Organization has released vector alerts concerning the spread of An. stephensi in 2019 [59] and in 2023 [60], underscoring the importance of preparing vector control agencies for the potential arrival of this new malaria vector. The potential invasion of An. stephensi threatens malaria elimination efforts throughout much of the Americas. Anopheles stephensi is a competent vector for P. falciparum and P. vivax malaria. Introductions and establishments in novel African locations have been attributed to possible port introductions, as well as possible land transportation route paths for goods [7]. This is equally feasible in Latin America via connections to the global trade network and multiple international ports. Much of Latin America already experiences suitable temperatures for this vector, and the region is projected to experience additional months of suitability and increases in PAR. This is an interesting observation, particularly in light of future reductions in malaria transmission predicted for sub-Saharan Africa. However, the primary African malaria vectors (e.g., Anopheles gambiae, An. funestus, An. arabiensis, An. coluzzi) and current malaria vectors in the Americas are, to date, not described as urban container breeders. Anopheles stephensi has a much higher optimal transmission temperature for malaria than the African malaria vectors in our previous work comparing malaria and dengue suitability. Thus, the projections to the Americas will follow the hotter temperature expansions—more similarly to dengue in Ae. aegypti. This contrasts with the reduction in Ae. albopictus projected suitability, as it has a cooler optimum temperature, which underlies the comparably restricted range prediction. Clinical interventions and surveillance programs for malaria have been scaled back in some areas following elimination due to many social and ecological factors, including antimalarial drug resistance, changing climate conditions, agricultural expansion, waning international and national political will, and declines in external funding [29]. However, as an urban container breeding mosquito, the control of An. stephensi would, in many ways, align with existing vector control operations for Aedes spp. mosquitoes, requiring minimal additional investments for capacity building and resource allocation [34]. Thus, strengthening surveillance efforts for novel Anopheles spp mosquitoes, added training in entomological identification, and clear communication for reporting findings of An. stephensi, introduced or newly established, will be essential to preparing for this potential novel vector. To facilitate the utility of the mapping approach adopted in this study, it is essential that model outputs are available. For this work, we strive to present summary information within this study to describe the broad findings and evidence supporting the IPCC report and beyond, to extend this work to a novel potential malaria threat in a changing world. All raster data layers are openly accessible (https://dataverse.harvard.edu/dataverse/Aedesmaps, https://dataverse.harvard.edu/dataverse/stephensimaps), as are all tabular model output (https://dataverse.harvard.edu/dataverse/CSAM_PAR_2024), generated at regional and country levels for all scenarios described. While maps provide one means of communication, we hope that model output reuse can contribute to decision-making processes in other ways (e.g., see S3 Fig).

Conclusions The combined impacts of global change present major challenges to public health, including climate change, rapid population shifts, urbanization, and globalized movements of people, goods, pathogens, and vectors. Quantitative estimates of shifting disease transmission risks are urgently needed to target climate change adaptation planning in the health sector. In this study, we present a framework for understanding the potential shifting risk for mosquito-borne diseases transmitted by container breeders in Central and South America, for both currently present vectors and pathogens, and a potential invader, Anopheles stephensi. There is an overall trend of increased risk and geographic shifts into novel spaces. Investment in existing best practices in vector surveillance and control strategies for container-breeders, as well as novel control strategies, will be needed to support climate change adaptation actions and improve human health.

Supporting information S1 Fig. Total Population at Risk (PAR) for one or more months of thermal suitability for transmission (i.e. dengue virus transmitted by Ae. aegypti or Ae. albopictus, and Zika virus transmitted by Ae. aegypti) in Central and South America, and potential (PAR) for thermal suitability of malaria transmission (i.e. P. falciparum or P. vivax transmitted by An. stephensi), at baseline climate (BAS), and under two representative concentration pathways (RCP 4.5 and RCP 8.5) paired with a shared socioeconomic pathway projection of population growth (RCP 4.5 × SSP2 (A); RCP 8.5 × SSP5 (B)). https://doi.org/10.1371/journal.pclm.0000312.s001 (TIF) S2 Fig. Total Population at Risk (PAR) for year-round thermal suitability for transmission (i.e. dengue virus transmitted by Ae. aegypti or Ae. albopictus, and Zika virus transmitted by Ae. aegypti) in Central and South America, and potential (PAR) for thermal suitability of malaria transmission (i.e. P. falciparum or P. vivax transmitted by An. stephensi), at baseline climate (BAS), and under two representative concentration pathways (RCP 4.5 and RCP 8.5) paired with a shared socioeconomic pathway projection of population growth (RCP 4.5 × SSP2 (A); RCP 8.5 × SSP5 (B)). https://doi.org/10.1371/journal.pclm.0000312.s002 (TIF) S3 Fig. Map depicting the overlap in the number of study vector: Pathogen pairings (1–5) suitable for endemic transmission (i.e. for 10–12 months), under current and future climate conditions (RCP 4.5 × SSP2). This figure was produced in ArcGIS 10.1 (ESRI, Redlands, CA) using shapefiles freely available from the Natural Earth dataset ver. 4.1.0 (naturalearthdata.com). https://doi.org/10.1371/journal.pclm.0000312.s003 (TIF)

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