Effects of climate change and human activities on vector-borne diseases

Effects of climate change and human activities on vector-borne diseases | Nature Reviews Microbiology

Abstract

Vector-borne diseases are transmitted by haematophagous arthropods (for example, mosquitoes, ticks and sandflies) to humans and wild and domestic animals, with the largest burden on global public health disproportionately affecting people in tropical and subtropical areas. Because vectors are ectothermic, climate and weather alterations (for example, temperature, rainfall and humidity) can affect their reproduction, survival, geographic distribution and, consequently, ability to transmit pathogens. However, the effects of climate change on vector-borne diseases can be multifaceted and complex, sometimes with ambiguous consequences. In this Review, we discuss the potential effects of climate change, weather and other anthropogenic factors, including land use, human mobility and behaviour, as possible contributors to the redistribution of vectors and spread of vector-borne diseases worldwide.

Introduction

Vector-borne diseases involve parasites, bacteria or viruses that are transmitted to humans and other vertebrates by the bite of infected haematophagous arthropods, including mosquitoes, ticks, sandflies, midges, triatomine bugs and blackflies. Approximately 6.3 billion people live at risk of vector-borne diseases, which cause more than 300 million disease cases and more than 700,000 deaths annually 1. Currently, malaria and dengue fever cause the highest disease burdens. Malaria is caused by Plasmodium spp. parasites that are transmitted by Anopheline mosquitoes. Globally, 219 million cases and more than 500,000 deaths occur annually, disproportionally affecting children in Africa 2. Other prominent vector-borne human diseases include yellow fever, chikungunya, Zika virus (ZIKV) diseases, West Nile virus (WNV) infections, Japanese encephalitis virus (JEV) infections, Rift Valley fever, leishmaniasis, plague, typhus, tick-borne encephalitis, Lyme disease, Chagas disease, lymphatic filariasis, onchocerciasis and human African trypanosomiasis. The most important vector-borne diseases of domesticated animals are African swine fever, Rift Valley fever, bluetongue disease, African animal trypanosomiasis (also known as nagana), African horse sickness, epizootic haemorrhagic disease and vesicular stomatitis.

The transmission cycle of vector-borne diseases involves infection and replication of pathogens in both the vectors and vertebrate hosts. Cycles can be limited to a small number of competent vectors and a single vertebrate host (that is, human-amplified cycles) as described for some Plasmodium spp., Wuchereria bancrofti (lymphatic filariasis) and most DENV genotypes 3. However, most vector-borne diseases are zoonotic and use various wild animals as enzootic hosts, with spillover infections to humans (from enzootic host to vector to human). Examples include WNV and its avian enzootic hosts, and Borrelia burgdorferi, which causes Lyme disease and infects rodents and other mammalian enzootic hosts 3. Some pathogens undergo secondary amplification involving domesticated animals (that is, epizootic cycles), which increases spillover to humans (often dead-end hosts) in certain settings

Multiple factors that directly or indirectly affect both vectors and vertebrate hosts can drive vector-borne disease dynamics. For example, vectors are ectothermic (cold-blooded and unable to regulate their body temperature) and particularly affected by weather patterns (especially temperature but also humidity) and climate (long-term weather patterns), which can also influence vertebrate hosts (Box 1). In this way, climate change, a multi-scale phenomenon that is characterized by an alteration in weather patterns over decades or longer, can affect vector-borne disease transmission 4. Global warming is a component of climate change that, without major reductions in CO2 and other greenhouse gas emissions, is likely to increase the global temperature to 4 °C above pre-industrial temperatures by 2100. However, the current ~1.1 °C increase already lies within some ‘ tipping points’, conditions beyond which changes in components of the climate system become self-perpetuating and amplified 5. Consequently, climate change may lead to weather patterns that are less stable and predictable, with globally widespread adverse impacts on nature and humans well beyond natural climate variability (Box 2). For example, climate change may lead to abrupt, irreversible and dangerous impacts on the entire planet, such as ecosystem collapse, species extinctions, and more frequent and intense extreme weather events, including heat, flooding, drought and tropical cyclones or hurricanes 4.

In this Review, we discuss the potential effects of weather patterns and climate projections on vectors, hosts and pathogens. We also explore the possible effects of climate change drivers such as deforestation, agriculture, urbanization and exploitation of natural resources on transmission dynamics and disease spread. Finally, we consider the consequences of altered human mobility and behaviour, including the roles of travel and trade routes in the spread of vectors, hosts and their pathogens, as well as trends in migration and ageing, individual and collective behaviours, and socioeconomic burdens. We do not discuss the potential evolutionary adaptation of vectors and hosts to altered climate; however, adaptation — especially of RNA arboviruses with potentially high rates of evolution, but also of vectors and hosts — may be crucial drivers of population size changes in climate-projected scenarios and anthropogenically altered environments. For example, climate is thought to have had a major role in the evolution of domestication of A. aegypti about 5,000 years ago in Africa, probably driven by human water storage in arid regions 6. Although our focus is limited to vector-borne pathogens that affect humans and other animals, there are numerous vector-borne plant pathogens that we do not discuss in this Review, such as Begomovirus, tomato spotted wilt virus, bacteria such as Phytoplasma spp. and Liberibacter spp., and fungi that belong to the Ascomycota and Basidiomycota taxa 7. These pathogens are prevalent in both managed and natural ecosystems, and many pose substantial economic threats to agriculture and forestry. Climate change can also influence the predictability and risk associated with these vector-borne pathogens 8. Additionally, our scope does not include pathogens that are mechanically transmitted by arthropods, such as Treponema pallidum subsp. pertenue (endemic treponematoses), Vibrio cholerae, Salmonella spp. and Shigella spp. transmitted by the housefly (Musca domestica).

Effects of climate

Effects of climate on vector development and life cycles

Weather (that is, short-term atmospheric conditions) and climate (that is, long-term, prevailing weather patterns) directly influence vector biology. Examples include rates of development, longevity and survival, fecundity, biting, and pathogen replication and development in the vector required for transmission 9, 10, 11, 12. However, weather and climate may have very different impacts on vectors with varying life spans 13(Fig. 1). Dipteran vectors such as mosquitoes usually have a short life cycle with full development from egg to adult from 1 week to months, and development of each stage within days. Consequently, their population sizes can be greatly affected by extreme, short-term weather events that bring heavy rains, floods, wind or temperature changes. By contrast, the life cycle of ticks can take months to years, and development between stages takes months. Therefore, short-term weather changes may have less immediate impacts on tick populations compared with dipterans such as mosquitoes that respond faster to weather events 13, 14. Additionally, adult dipteran females may blood-feed more than once on multiple hosts, whereas ticks blood-feed in all stages, but usually only once on a single animal for each life stage. This difference can directly affect pathogen transmission (Fig. 1).

a, Mosquitoes, with a rapid life cycle (weeks to months) that encompasses both terrestrial and aquatic stages, examples of vectors with short development periods and their associated pathogen transmission cycle. The mosquito-borne pathogen cycle starts with an uninfected mosquito biting an infected vertebrate (humans or other animals). The feeding mosquito ingests pathogens during a blood meal from an infected host, and the pathogen then undergoes replication and/or development within the vector (including trans-stadial transmission) and may become infectious when refeeding. Next, the mosquito transmits the pathogen to a new host through biting, completing the cycle. Some mosquito-borne pathogens such as Venezuelan equine encephalitis virus (VEEV) and Japanese encephalitis virus (JEV) have cycles involving multiple wild and domestic animals (that is, enzootic and epizootic cycles), and others such as Plasmodium falciparum and dengue virus (DENV) are maintained in a single vertebrate host (human-amplified cycles). Temperature affects the extrinsic incubation period (EIP) (light blue arrow), or the minimum time after vector infection when transmission can occur, of the pathogen within the mosquito. Temperature, humidity and precipitation affect fecundity, reproduction and inter-stadial developmental rates of the vector (grey arrow). Vector activity, biting rate and transmission probability all respond to temperature variations (red arrows), whereas temperature also has an impact on the development between stages (yellow arrow). b, Ticks, with longer development periods (months to years) and predominantly terrestrial or host-attached life cycles, exemplify vectors with extended development times. Arrows depict how temperature influences their life cycle and pathogen transmission dynamics. The tick-borne pathogen cycle starts with uninfected larva hatching and seeking a blood meal, typically from small mammals or birds (primary host). At the nymph stage, the tick needs another blood meal to develop, which can be from the same type of animal as the primary host, another small mammal or even a larger animal. This is where horizontal transmission can occur: an uninfected larval tick can bite an infected vertebrate and become infected, followed by transmission by the nymph. This requires transfer of the pathogen between these two life stages (trans-stadial transmission). A trans-stadially infected adult tick can transmit the pathogen to a third blood meal host, typically larger animals such as deer (which may be incompetent reservoirs for some pathogens such as Borrelia burgdorferi) or humans (incidental or dead-end hosts). Additionally, some pathogens can be transmitted from an infected female tick to its eggs, infecting the hatching larvae (transovarial transmission). The life cycle and transmission mechanisms of tick-borne disease vary depending on the pathogen and the tick species involved. c, Thermal response of mosquito vectors (Aedes aegypti, Aedes albopictus and Culex pipiens) on key biological traits. Optimal, minimum and maximum temperatures are indicated in degrees Celsius (°C) for the biting rate, fecundity, development rate and immature survival 32. d, Effects of thermal response of tick vectors (Ixodes scapulatis, Amblyomma americanum and Dermacentor variabilis) on key biological traits: lower and upper lethal temperature, greatest activity and thermal preference 185.

Extreme weather has major effects on human society and natural ecosystems. For instance, the frequency and intensity of El Niño and La Niña events, which are natural cyclical weather patterns that affect Pacific Ocean temperatures, are expected to increase under anthropogenic impacts 15, 16, and may also be modulated by climate change 17 although the precise nature of this interaction remains unclear. El Niño, the warm phase of the El Niño Southern Oscillation (ENSO), affects global weather systems, and predictably disrupts temperature, rainfall and winds. By contrast, La Niña, part of the broader ENSO pattern, triggers a cooling phase with opposite effects to El Niño 15. The ENSO has been correlated with a dual impact on vector activity and risk of vector-borne diseases (Fig. 2). Fortunately, the periodicity and relative predictability of ENSO cycles enables the anticipation of increased vector-borne disease risks and the development of mitigation strategies. For example, Rift Valley fever virus (RVFV) epizootics in East Africa follow a cyclical pattern, typically recurring at intervals of 5–15 years linked to the ENSO 18. This connection stems from the direct influence of precipitation on vegetation growth, which enhances the survival of Aedes mosquitoes infected with RVFV, increasing the risk of outbreaks 19. Therefore, RVFV outbreaks in East Africa can be anticipated to some extent by combining climate indicators, such as the ENSO, with observations of vegetation development, rainfall and land surface temperatures, which can be monitored remotely. Additionally, ENSO cycles may also reduce the risk of vector-borne diseases, such as the 1997–1998 El Niño event in Tanzania that decreased malaria cases despite the increased rainfall 20. The very heavy rainfall associated with El Niño may have washed away immature aquatic mosquitoes, leading to a reduction in malaria transmission.

Floods and droughts have been linked to changes in the transmission of vector-borne diseases with different delays, locations and environments (Fig. 2). Intense precipitation may create more suitable aquatic environments for oviposition, larval development and survival of some vectors owing to the formation of stagnant water pools, the high humidity and surface moisture. These favourable conditions for some vectors can raise the risk of malaria, dengue fever and chikungunya 21, 22, 23. Interestingly, some mosquito species have reproductive cycles strongly associated with flooding (often called floodwater mosquitoes), such as Aedes vexans and Aedes ochraceus, which are both responsible for transmitting both Dirofilaria immitis (dog heartworm) and RVFV. Floodwater mosquitoes such as Aedes and Psorophora spp. lay their eggs, which can remain viable for many years, individually on moist soil above the water line to await flooding, leading to explosive populations following heavy rainfall or tidal flooding 24. However, strong winds associated with flooding storms may kill many adult mosquitoes if safe resting locations are not abundant. Also, because people spend more time outdoors cleaning up after a hurricane or flood, they may be more exposed to mosquito bites 25. For example, early-season hurricanes in the northern Gulf of Mexico can increase total annual WNV-positive mosquito numbers by 7.8% and human neuro-invasive disease incidence by 94.3% across all areas with hurricane damage 26. Moreover, drought is also a primary climatic driver of increased WNV epidemics in the United States. It is hypothesized that drought alters WNV transmission not by reducing mosquito abundance but by increasing the infection prevalence if lower avian reproduction increases the vector–host ratio, or if patterns of host–vector contact are altered due to avian congregation or stress 27. Drought can also be associated with increased dengue risk in highly urbanized areas (that is, a human-amplified cycle) with unstable water supplies that can lead to water shortages 28(Fig. 2). The increased dengue risk can be explained by water storage in improvised, open containers around the house, which could provide larval habitats for A. aegypti. In contrast to mosquitoes, extensive and prolonged flooding events have a more limited effect on ticks, but have been shown to reduce populations 29, 30. Droughts can also decrease tick populations due to desiccation 31. Finally, many ticks can survive colder temperatures than dipteran vectors, and can be active at lower temperatures, down to 7 °C for ticks compared with typically ≥15 °C for dipterans 14, 32.

Effects of climate on vector-borne pathogen transmission

Although the impacts of climate change on the distributions of vectors are somewhat predictable, the relationship between temperature and vector-borne pathogen transmission efficiency is complex, sometimes with apparently contradictory inferences. Vector competence is the intrinsic ability of an arthropod to become infected and transmit a pathogen after oral ingestion, whereas vectorial capacity (V) is more complex and describes secondary infections arising from each vector, including the parasite’s extrinsic incubation period (EIP; n days), the mosquito to human ratio (m), daily mosquito survival (p) and the human biting rate (a): V = ma2pn/−ln(p) (ref. 33). Climate and weather can directly or indirectly influence all four components of vectorial capacity. The temperature of extrinsic incubation (the time between the infectious blood meal and transmission) in mosquito vectors of arboviruses has been studied extensively; it can greatly affect the transmission efficiency because mosquitoes undergo high daily mortality rates and, thus, may not survive the minimum EIP. Conversely, ticks generally survive longer, so the EIP may be less important. However, even for mosquito vectors, results of temperature experiments have differed greatly among virus–vector pairs, with some showing more efficient infection and transmission at lower temperatures and others at higher temperatures 34. For example, efficient enzootic WNV amplification, which leads to increased human spillover infections in the United States and Canadian prairies, are associated with above-average summer temperatures 35. Bluetongue virus (BTV) seems to be limited geographically by the temperature requirement (>15 °C) for efficient extrinsic incubation in the Culicoides vector 36. Projected increased summer temperatures seem to be expanding both the geographic range of WNV and BTV circulation and the length of the transmission seasons 37. Extrinsic incubation of western equine encephalitis (WEEV) and St. Louis encephalitis viruses in Culex tarsalis show progressively reduced extrinsic incubation times upon incubation from 10 to 30 °C 38. However, another study with WEEV showed reduced C. tarsalis competence with incubation at 32 °C compared with 18 °C or 25 °C 39. Extrinsic incubation in nature occurs in microclimates where vectors rest during blood digestion, arbovirus replication and dissemination, and ambient temperatures generally used experimentally may not reflect these conditions. Also, diurnal fluctuations in the temperature of extrinsic incubation, which are seldom reproduced in experimental studies, can also affect transmission efficiency. Furthermore, laboratory findings coupled with modelling suggest that the intensity of DENV transmission by A. aegypti mosquitoes and malaria transmission by Anopheles mosquitoes can be influenced by the specific combination of mean and range of temperature fluctuations. This is attributed to the negative impact of the diurnal temperature range on vector competence and survival, both of which are critical components of vectorial capacity 12, 40. Thus, larger fluctuations in temperate regions with lower overall temperatures may also increase the potential for dengue epidemics, which suggests greater risk for outbreaks in temperate regions than typically recognized 41. In addition to the extrinsic incubation temperature, the temperature at which larval and pupal development occurs also affects vector competence. This temperature, which inversely affects the development time, adult body size and other characteristics of both immature and adult vectors, variably affects vector competence of mosquitoes and Culicoides spp., as well as rates of transovarial virus transmission 34.

The mechanisms whereby temperature affects vector competence have begun to be elucidated. Although arthropod vectors do not possess adaptive immune responses analogous to those of vertebrates, they do have innate mechanisms that control the replication and development of the pathogens they transmit. In the case of arboviruses, RNA interference (RNAi) suppresses viral replication, presumably to limit pathogenic effects on the vector that would be counterproductive for survival and transmission 34, 42. Conversely, arboviruses have mechanisms to counteract RNAi to achieve adequate replication for maintaining fitness, and a balance between these pathogen and host effects is required for efficient transmission. Examples include subgenomic flavivirus RNAs that function as decoys to inhibit Dicer, a key component of RNAi 43. Other conserved pathways, including the Janus kinase-signal transducer and activator of transcription (JAK–STAT) and Toll pathways, combined with an immune deficiency in the vectors, also limit pathogen replication and development in vectors 42.

Temperature can affect the efficiency of RNAi, and thus the transmission of arboviruses; global warming will thus impact vector competence in many regions. Transgenic ‘sensor’ mosquitoes that indirectly measure RNAi revealed that A. aegypti reared at 18 °C have lower RNAi efficiency than those reared at 28 °C 44. These results may explain the consensus findings that higher temperatures of the EIP, to a point, favour more efficient arbovirus transmission by mosquitoes and other vectors. Although vector competence is critical for pathogen transmission, vectorial capacity may respond in a more complex manner to climate change 45. For example, although high temperatures may increase vector competence, they may also reduce survival of adult females, a more important factor in the vectorial capacity formula.

The release of Wolbachia-infected mosquitoes into wild populations has emerged as an effective strategy to control A. aegypti 46, 47. This approach relies on the ability of Wolbachia bacteria to suppress vector competence, rendering them less capable of transmitting pathogens. Nevertheless, the success of Wolbachia introgression depends on local characteristics (for example, climate, environmental factors and a genetic match between native and released mosquitoes); fortunately, this technology is projected to remain resilient to near-term climate change 48. Additionally, interactions between insect-specific viruses, which cannot infect vertebrates, and arboviruses in mosquitoes can interfere with replication of the latter. For example, the presence of two insect-specific viruses, Phasi Charoen-like and Humaita Tubiacanga virus, increase the ability of A. aegypti mosquitoes to transmit DENV and ZIKV using an experimental mouse model 49, but the effect of climate on these interactions remains poorly understood.

Impacts of climate change on the distribution of vector-borne pathogens

Several vector-borne pathogens have emerged, re-emerged or expanded their geographic distributions in recent years. For example, DENV has spread throughout tropical and subtropical regions over the past 60 years and now threatens more than half of the world’s population 2. In recent decades, many studies have associated the effects of climate change with the risk of vector-borne diseases on different geographic and temporal scales 50. Most have focused on mosquitoes such as A. aegypti and A. albopictus, which are the key vectors for the transmission of DENV, yellow fever virus (YFV), chikungunya virus (CHIKV) and/or ZIKV 2, 51, 52, 53, 54. The main parameter used to model climate change related to vector-borne diseases is temperature 52, 54, 55, but others, such as precipitation and humidity, are also frequently incorporated because they affect the reproduction and survival of vectors 54, 56, 57. Additionally, some studies have incorporated thermal performance curves for mosquitoes, arboviral transmission and scenarios of projected global socioeconomic change 2, 51, 58, 59, 60. These studies suggest that climate change will promote a redistribution of vectors and vector-borne diseases, initially increasing the environmental suitability in currently endemic areas, particularly in tropical and subtropical regions. Vectors and their pathogens will then likely expand latitudinally (pole-ward) into historically temperate regions. For example, warming of winters will permit A. aegypti to survive without the need for embryonic diapause, which is dissimilar to A. albopictus 2, 51, 52, 54, 61(Fig. 3). Paradoxically, substantial long-term reductions in climate suitability are projected for these Aedes mosquitoes in tropical regions including Southeast Asia and West Africa, because severe warming could exceed the optimal temperature ranges for their survival 53, 55. Similarly, climate change is likely to lead to temperature increases in altitudinal clines (Fig. 3); thus, highly elevated regions (upslope) and those with temperate climates are likely to become more suitable for vectors and pathogen transmission 58, 62. The pole-ward and upslope redistribution due to projected warming temperatures that surpass the current physiological limits of vector survival is also predicted for other important mosquito and tick vectors, such as Culex quinquefasciatus, Culex annulirostris, Ixodes scapularis, Ixodes ricinus, Ixodes cookei and Dermacentor variabilis 63, 64, 65.

a, Some vectors (for example, Aedes aegypti, Aedes albopictus, Culex quinquefasciatus and Dermacentor variabilis) and vector-borne pathogens (for example, dengue virus (DENV), Zika virus (ZIKV) and chikungunya virus (CHIKV)) that are currently circulating predominantly in tropical and subtropical climate zones may expand latitudinally into previously temperate zones (towards poles). This shift may be driven by climate change, which is creating suitable temperature conditions for transmission beyond current limits 52, 55, 63, 64, 65. b, The altitudinal gradient vector-borne pathogen range (for example, malaria 58 and Lyme disease 186) may extend to higher elevations due to warming temperatures in the current altitudinal range owing to climate change. This upslope expansion may occur as the current temperature range at higher elevations becomes more favourable for vector survival and pathogen transmission 14, 58, 63.

Some studies suggest that climate change can promote a shift among vector-borne diseases. For example, warming temperatures projected in many regions will likely transfer the malaria disease burden to A. aegypti-borne viruses (DENV, ZIKV, YFV and CHIKV) in sub-Saharan Africa through 2080. This prediction is based on thermal performance curves of malaria transmission by Anopheles gambiae, which peak at 25 °C, whereas DENV transmission by A. aegypti peaks at 29 °C 66. Thus, warming temperatures could favour DENV transmission while reducing malaria. This hypothesis is also supported by an empirical study showing that increasing temperatures generate opposing effects on malaria dynamics for lowland and highland regions 67. A shift in the malaria burden to A. aegypti-borne arboviruses has already been observed in Latin America 68, 69. However, the mechanisms involved may not be exclusively climate, and may also involve socioeconomic and ecological factors. Although mosquitoes transmit both malaria and DENV, a shift towards DENV dominance may necessitate substantial modifications to control strategies. This is because insecticide-treated bed nets, used in combination with the drug artemisinin for malaria control, are less effective against DENV vectors, which unlike most anophelines bite during the daytime. Additionally, unlike malaria, arboviral diseases including infections with DENV generally lack specific treatments or immunization programmes. Nevertheless, immunization programmes against yellow fever are partially available, and are being developed against chikungunya and dengue 70, 71.

Currently, there is no strong consensus on exactly how climate change will affect vector-borne diseases overall. Differing views may reflect the choice of climatic parameters, modelling approach, exclusion of abiotic and biotic drivers, and spatial or temporal scales 50. Nonetheless, most studies suggest that climate change will lead to geographic redistribution and expanded ranges of many vector-borne diseases worldwide. This will likely result in the emergence of vector-borne diseases in previously unaffected regions with immunologically naive populations and unprepared public health systems, leading to major outbreaks as observed recently for WNV, CHIKV and ZIKV 72, 73, 74.

Land use and land cover changes

Land use change is often characterized by human activities such as agriculture (for example, cropland and livestock), exploitation of natural resources (for example, logging, mining and dams) and manmade constructions on the land’s surface, such as urban expansion. These activities can contribute substantially to climate change through biodiversity loss, and reducing natural carbon capture and storage 4. Furthermore, anthropogenic land use and cover changes have been described as a major driver of zoonotic pathogen spillover from wildlife to human populations 75, 76, 77. Vector-borne diseases are susceptible to land use and cover change because these activities affect both host and vector communities as well as vector predators, vector larval and adult habitats, microclimate suitability for vectors and pathogens, vector–host contact rates or a combination thereof (Fig. 4).

Circular pairs of upward and downward arrows indicate the potential for either an increase or decrease due to anthropogenic changes such as deforestation, livestock production, agriculture, urbanization, mining and dams. Vertical arrows indicate a more consistent change anticipated.

Deforestation

The impact of deforestation on the overall prevalence of diverse vector-borne pathogens and their vectors is likely to be heterogeneous. In certain situations, deforestation has been linked to disruption of the transmission cycles of vector-borne diseases by several mechanisms that may increase human or domestic animal exposure to vectors. For example, resource extraction, early stages of settlement and forest edge habitats may enhance the risk of some zoonotic vector-borne diseases by increasing vector abundance and human–vector contact. This mechanism could explain the effects of deforestation on the occurrence of leishmaniasis and malaria in Latin America 78, 79. Similarly, during the 1940s, Trinidad experienced a severe malaria outbreak triggered by extensive deforestation for cocoa (Theobroma cacao) plantations under nurse trees of the genus Erythrina. The introduction of Erythrina spp. nurse trees created ideal habitats for 34 epiphytic bromeliad species, with an average of 66 bromeliads per tree. Notably, 20 of these bromeliad species provided preferred larval habitats for Anopheline mosquitoes, including Anopheles bellator, the region’s primary malaria vector. Consequently, the A. bellator population surged, which led to a malaria epidemic that was only controlled when nurse tree use was reduced and plantation practices were modified 80. In addition, deforestation can reduce biodiversity and host communities through a chain of events initiated by wildlife death or migration. These events can disturb interactions between vector predators (for example, dragonfly larvae, fish and birds) and their prey (vectors) (predator–prey interactions) by reducing the predator population. Consequently, disease transmission can be impacted by both vector survival and population size 81. For instance, increases in human WNV cases during droughts are associated with improved predator avoidance during mosquito oviposition

Deforestation can also contribute to the reduction of some vector-borne diseases. For example, tsetse flies (Glossina morsitans morsitans) are endemic to sub-Saharan Africa and transmit trypanosomes, which cause trypanosomiasis in humans and livestock. The progressive deforestation for crop and livestock production, combined with the near elimination of large game animals, has resulted in a substantial decline in tsetse fly distribution and trypanosomiasis prevalence 82, 83. This pattern suggests a clear connection between habitat fragmentation and tsetse fly abundance, which now is largely limited to undisturbed, protected areas. Interestingly, heavily fragmented habitats harbour lower tsetse fly populations, but as natural vegetation fragmentation decreases, tsetse fly abundance increases following a sigmoidal-like curve 82.

Deforestation, due to anthropogenic transformation of natural landscapes into agricultural or urban environments, can alter haematophagous arthropod populations, potentially affecting the dynamics of vector-borne diseases. Vectors such as ticks are more common in natural and rural areas compared with urban settings. This is explained by their host preferences and attachment behaviour, which are influenced by a combination of host presence, behaviour and chemical cues, as well as environmental factors such as climate and microhabitat availability 84. These preferences and attachment patterns can also vary among tick species and life stages. For instance, immature I. scapularis, vectors of B. burgdorferi, Anaplasma phagocytophilum and Powassan virus, typically exhibit generalist feeding habits, parasitizing small and medium-sized mammals, birds and reptiles. Then, when they became adult ticks, although also feeding on medium-sized mammals, they exhibit a strong preference for white-tailed deer (Odocoileus virginianus). Notably, not all mammalian hosts are equally competent in maintaining and transmitting pathogens. For example, the white-footed mouse (Peromyscus leucopus) is competent for B. burgdorferi, whereas other mammals such as white-tailed deer are not 85. Based on this differential competence, increased biodiversity could lead to a ‘dilution effect’ on pathogen transmission. This concept is based on the hypothesis that higher biodiversity reduces pathogen transmission in multi-host–multi-vector systems due to the presence of hosts and vectors with varying degrees of competence 86, 87. However, simulations suggest that both amplification and dilution effects can occur, with outcomes dependent on specific factors such as competition dynamics, host–tick contact rates and acquired host resistance to ticks 88.

Forest disturbance and fragmentation can also lead to vector habitat loss and changes in blood meal availability. For example, YFV remains endemic in South America due to the enzootic cycle involving non-human primates and transmission by sylvatic mosquitoes (Haemagogus and Sabethes spp.) in tree canopies. These sylvatic vector mosquitoes occasionally descend to ground level to transmit spillover infections to humans, which may be enhanced by deforestation and biodiversity loss 89. The descending behaviour of vectors from forest canopies is critical for YFV epidemiology, where the most affected hosts are non-human primates, including those that remain near ground level, which can also suffer fatal infections, and unvaccinated people exposed to forest mosquitoes 90. Thus, the sylvatic YFV cycle, the result of human transport from Africa, precludes eradication by human vaccination and causes ecological imbalances due to non-human primate mortality. Furthermore, increasing anthropogenic intersections of forests and urban areas combined with limited vaccination coverage may increase the risk of re-emergent urban yellow fever in Latin America.

Abiotic environmental conditions can also have a heterogeneous effect on vector ecology, depending on vector species and specific microclimates created by deforestation. Hence, understanding the broad relationships between deforestation and vectors is critical to mitigating the emergence or re-emergence of vector-borne diseases. For example, Ixodes pacificus ticks are strongly associated with dense forests and cool, moist microclimates. By contrast, Dermacentor occidentalis and D. variabilis are more tolerant of higher average temperatures and more open habitats 91. Thus, I. pacificus, a vector of B. burgdorferi, is expected to experience reductions in geographic distribution and seasonal activity caused by deforestation and climate change compared with D. occidentalis and D. variabilis, which are vectors for Rickettsia rickettsia. Dipteran vectors can also be affected by abiotic changes because deforestation can alter water quality, increase temperatures, decrease humidity and eliminate natural larval habitats, such as bamboo stumps, tree holes, leaf axils and bromeliads 92, 93.

Overall, deforestation will favour vectors with greater tolerance of anthropogenic changes, including some capable of transmitting pathogens from wildlife to humans and domestic animals (zoonotic spillover). However, several factors need to be aligned in this scenario, such as ecological, epidemiological, immunological and behavioural determinants 94. Conversely, human–wildlife interactions can result in transmission of pathogens from humans to wild animals ( spillback or reverse zoonosis), which results in novel enzootic cycles such as enzootic, sylvatic, neotropical YFV initiated hundreds of years ago 95.

Agriculture and livestock production

Approximately one third of the global land surface has been affected by crops and livestock production 96. Although agriculture has many benefits for society, this ecological disruption can also affect vector-borne disease risk 97. For instance, irrigation systems for rice cultivation are linked to changes in the risk of malaria 98, dengue 99 and Japanese encephalitis 100. The impact of agricultural change depends on the specific ecology of the vector species and can have negative or positive effects on the distribution and abundance of vectors and diseases. However, overall, agricultural development frequently leads to an increased risk of vector-borne diseases 101, 102. For example, in sub-Saharan Africa, the main malaria vectors undergo larval development in irrigated rice fields, whereas in parts of southeast Asia they are found in small puddles and stream pools in the forest fringe 103. Thus, the expansion of rice production through deforestation in southeast Asia has reduced malaria prevalence 104, whereas in Africa, rice cultivation has increased populations of malaria vectors (A. gambiae) 98. Moreover, the decline of rice cultivation in the western Mediterranean region has been associated with the decline of Anopheles labranchiae, the primary malaria vector in France and Italy 105. In addition, oil palm expansion in Malaysian Borneo increases by 1.5-fold the abundance and, thus, vectorial capacity of A. albopictus (DENV vector), compared with forest habitats 106.

Livestock production can modify vector-borne disease dynamics by increasing blood meal availability and providing competent reservoir hosts to maintain and amplify zoonotic pathogens, which is referred to as zoopotentiation. For example, some studies suggest that domestic pigs are major rural amplifying hosts of JEV in Asia and Oceania, whereas cattle are a major feeding source for RVFV vectors in Africa 107, 108. Indeed, the proximity between humans and swine farming is proposed as a leading risk factor for human JEV infection in many countries with the largest swine industries 109, 110. This association may explain the rising incidence of JEV infection in Australia, where approximately 800,000 people may be vulnerable due to its recent geographical expansion combined with piggery locations near human populations 111. Likewise, RVFV is an arboviral zoonosis that affects both humans and domestic animals, causing harm to public health and the local economy in sub-Saharan Africa, Madagascar and, recently, the Middle East.

In specific contexts, livestock production can be employed for zooprophylaxis to divert host-seeking mosquitoes away from humans by exploiting the host preferences of certain vectors that preferentially feed on animals (zoophilic) rather than on humans (anthropophilic). This approach has produced mixed results, as observed in studies investigating the impact of livestock ownership on malaria. For instance, in the Democratic Republic of Congo, cattle ownership within household compounds is associated with reduced exposure to Plasmodium falciparum infection, whereas chicken ownership has been linked to an increased risk 112. A modelling study of malaria trends in Britain between 1840 and 1910 suggests that at least 20% of the observed decline could be attributed to the combined effects of an expanding cattle population and a decrease in wetland habitats 113. Overall, technical solutions for vector and disease control in agricultural settings are critical to resolving conflicts between agricultural and public health policies in the era of rapid global changes 97, 114.

Urbanization

The global population living in urban areas continues to climb from 29.6% (0.8 billion) in 1950 to 56.2% (4.4 billion) in 2020, and is projected to reach 68.4% (6.7 billion) by 2050 (ref. 115). Similarly, mosquito-borne diseases are rising worldwide linked to dramatic urbanization, which particularly favours the proliferation of certain Aedes (A. aegypti and A. albopictus) 52, 61, 116, Culex 117 and Anopheles 118 mosquitoes. Mosquito dominance in urban areas partially reflects vector evolution to specialize in biting humans and to live in anthropogenic settings. For example, A. aegypti was likely among the first species to specifically adapt to live among humans 119. The anthropophilic subspecies (A. aegypti aegypti) has genetic changes in a few chromosomal regions, compared with its African sylvatic ancestor (A. aegypti formosus), that enhance preference for human odours over those of other animals 120. This preference is explained by human odour enrichment in long-chain aldehydes, which generate strong and prolonged attraction regulated by a selectively tuned olfactory glomerulus within the mosquito brain 121. This activity drives host-seeking and may explain why mosquitoes prefer human over animal odour at long range. Also, A. aegypti aegypti prefers to oviposit in artificial containers with pure water and high oxygen levels rather than forest tree holes used by their ancestors, a heritable characteristic 119. Additionally, inadequate waste management in urban settings can exacerbate arthropod-borne diseases by creating suitable larval habitats for vectors. For instance, plastic debris that retains water can provide ideal habitats for immature stages of certain vectors and shelter for anthropophilic species, particularly mosquitoes such as A. aegypti 122.

The urban ecosystem has biophysical, socioeconomic, cultural and institutional properties that determine the risk of vector-borne diseases, human exposure to infected vectors and disease vulnerability 116. Some factors that explain the success of mosquitoes in urban areas include a broad range of aquatic habitats that facilitate reproduction 123 and diminished predation pressure 124. Also, urban surface temperatures are higher than those in surrounding rural areas, resulting in ‘urban heat islands’ 125. Based on greenhouse gas emissions, temperatures could rise by more than 4 °C in cities by 2100 (ref. 126). This could profoundly affect urban residents because warmer temperatures may directly cause health complications that could affect the transmission dynamics of vector-borne diseases 127, 128.

Urban green spaces characterized by partly or completely vegetated land (for example, grass, trees or shrubs) can help mitigate the rise in temperatures, heat island effects and the impact of global warming 129. Although several studies have linked urban green spaces to various health benefits, their effect on vector-borne diseases varies. Some studies have shown that mosquito diversity and composition in urban green spaces exhibit species–area relationships, whereby larger green spaces harbour more species, and a nested distribution, whereby species-poor sites exhibit greater similarity 130, 131. This suggests a non-random process of species loss or gain. Notably, species loss in urban green spaces may increase the risk of pathogen transmission, as most remaining mosquito species such as A. aegypti tend to transmit human pathogens 130. Furthermore, a study in China suggested that the increase in green space could raise malaria risk based on providing more Anopheles vector habitat 132. Finally, urban populations may have greater access to healthcare compared with those in rural locations 133.

Exploitation of natural resources

Exploiting natural resources (for example, dam construction, mining and logging) can promote economic growth and develop resources for the population’s well-being. However, it can also lead to deforestation (see above), higher greenhouse gas emissions, biodiversity loss, desertification and social disruption caused by construction and involuntary resettlement, thereby increasing risk of zoonotic spillover and vector-borne diseases 134. For instance, dams have been identified as hotspots for malaria in sub-Saharan Africa 135. The most important predictor of malaria around these dams is lower slopes at the shoreline that result in poor drainage, promoting the persistence of surface water and stable pools suitable for Anopheles larvae 136. Considering the hundreds of large dams under construction or planned in Africa, and the approximately 25 million people expected to live in these areas by 2050, additional malaria control measures are needed, such as planning higher slopes at the shoreline to facilitate drainage 137.

Mining disrupts ecosystems and can increase pathogens crossing inter-species barriers, especially in areas of high biodiversity. This association has been observed throughout South America 138, 139, 140. For example, mining was likely to be the main driver of increased malaria incidence in Guyana and Venezuela, whereas climate may have contributed synergistically 138, 139. Also, gold-mining villages in inland neotropical forests have 65-fold higher risk for infection by Leishmania guyanensis compared with other regions of French Guiana 140. Mechanistically, the link between vector-borne diseases and mining is increased vector exposure and reduced healthcare seeking. Also, the high mobility of mining workers can be a source of introductions and dissemination of pathogens in both rural and urban environments, as seen in an unusual case of human anaplasmosis (Anaplasma sparouinense) in gold miners in French Guiana 141. Therefore, effective and timely surveillance and vector control in mining areas should be prioritized in Latin America. Combining better mining oversight, epidemiological surveillance and medical care will mitigate the risk of spillover and vector-borne diseases.

Railway and road construction offer economic benefits for communities, including enhanced access to healthcare 133. But these constructions can have both positive and negative impacts on vector-borne disease transmission. Road construction may limit tick expansion by restricting the movement of infested large mammals 142. By contrast, the construction phase itself can increase exposure to vectors and vector-borne diseases for individuals residing in those areas. For instance, road construction in the Amazon region has been linked to an increase in malaria transmission 143, and malaria and yellow fever caused the deaths of approximately 20,000 workers during the construction of the Panama Canal 144.

Human mobility and behaviour

Human mobility and trade routes

Human mobility and trade have critical roles in burning fossil fuels, the main contributor to climate change 4. Human mobility is also essential for access to healthcare, and infectious disease patterns locally and globally 145. Travel and trade among countries have been repeatedly accompanied by the spread of vectors and their pathogens into regions with suitable environmental conditions 61, 146(Fig. 5). For example, YFV and A. aegypti were probably introduced into the Americas from Africa during the slave trade in the sixteenth and seventeenth centuries 147, 148. For ticks, their introduction is often associated with vertebrate hosts utilized in agriculture, including species such as Amblyomma variegatum, Haemaphysalis longicornis and Rhipicephalus microplus, with their introductions into the Americas likely to have occurred between the eighteenth and nineteenth centuries 73, ZIKV 74 and new lineages and genotypes of DENV 149, 150 nearly worldwide in the tropics and subtropics. The most likely mechanism of these introductions is infected travellers exposed to native or introduced vector populations to initiate local transmission at their destination, as the probability of infected vectors surviving a flight is lower 151. Thus, considerable increases in air and terrestrial travel facilitate vector-borne disease and vector spread, and enable pathogens to travel further and faster than ever before. Furthermore, most introductions of haematophagous arthropods have continued to occur through intensive transportation by sea and sometimes via roads. For example, used tyres and plants such as ‘lucky bamboo’ have been implicated in the introduction of A. albopictus into the United States and Europe 148. Also, there are unconventional routes of introduction of vector-borne diseases, such as the first outbreak of African swine fever outside Africa that occurred in Portugal in 1957 as a result of airline waste being fed to pigs near the Lisbon airport 152. Similarly, an epizootic of African horse sickness in Spain in 1987 was caused by an importation of subclinically infected zebras from Namibia 153.

The introduction of vectors or pathogens can be a result of trade and travel routes from multiple sources. The newly established transmission cycle usually occurs with the introduction of an invasive vector species, such as a mosquito or tick, from location A to location C through trade routes. Next, the pathogen itself arrives in location C, carried by infected humans (travel routes) or infected livestock (trade routes) from location B. If both the introduced vector and a suitable host (humans or animals) are present in location C, the pathogen can establish a transmission cycle, leading to disease outbreaks and endemicity. The intensity of this transmission can be influenced by various socioeconomic factors and human behaviours in location C, including vector control efforts, healthcare access and individual behaviours such as exposure avoidance (for example, repellent use). Also, native vector species in location C could play a role in transmitting the introduced pathogen instead of or in addition to the invasive species. Likewise, invasive vectors may become vectors of native pathogens in location C.

Appropriate environmental conditions, competent vectors and susceptible vertebrate hosts are the main requirements for establishing transmission of vector-borne diseases after their introduction. The global cost for the largely unsuccessful management of A. aegypti and A. albopictus was estimated at approximately US $149 billion between 1970 and 2017 (ref. 154), and the number of invasive vector species continues to increase 155, 156. Most invasive vectors thrive in anthropogenically modified habitats, feed on humans or domestic animals and survive across a broad range of climatic conditions. These characteristics facilitate survival in diverse habitats, and thus the introduction of new diseases in anthropogenically altered habitats.

In 2019, the airline industry estimated that there were more than 4.5 billion passengers worldwide 157, and approximately 281 million international migrants were predicted in 2020 (ref. 158). Climate change is enhancing migration and population displacement worldwide due to rising sea levels, extreme weather and disrupted livelihoods, particularly in low-income regions disproportionally affected by vector-borne diseases 4, 159, 160. Therefore, migration, planned relocation or forced displacement by climate or socio-political events (for example, war, conflict and persecution) are likely to reshape the transmission of vector-borne diseases by introducing and re-introducing them into countries with immunologically naive populations. Interactions among climate change, migration and vector-borne diseases, as well as the magnitude of these impacts, remain important areas for research.

Human behaviour and socioeconomic consequences

Human behaviour is a critical determinant of infectious disease outbreak trajectories 161. For vector-borne diseases, avoiding exposure can prevent new infections and is strongly affected by underlying socioeconomic factors (Fig. 5). For example, studies incorporating predictions of vector expansion, population density and vectorial capacity suggest that arboviruses transmitted by Aedes mosquitoes (for example, DENV, ZIKV and CHIKV) will become endemic in the United States 2, 51, 52, 61, 162. Although these projections are useful for anticipating vector control needs, they do not incorporate other factors such as higher rates of air-conditioning (~90% of homes in the United States) 163, 164, avoidance of outdoor areas with mosquitoes 165, use of long-sleeved clothing in outdoor environments 166 and insecticides 167, which reduce the risk of efficient human-amplified arbovirus transmission in the United States more than in many parts of the world 168.

Households are incriminated as the main locations of infection by many vector-borne pathogens 169, 170. Thus, eliminating mosquito oviposition sites and reducing peridomestic tick habitats and wildlife hosts can suppress vector populations and the risk of peridomestic transmission (Fig. 5). However, these mitigations require effective engagement and mobilization of communities for optimal, integrated vector control 171, 172. Other sociologic factors that affect the risk of vector-borne diseases include gender differences in roles. For example, in many countries, women spend more time at home than men, which probably explains why CHIKV disproportionally infects women 169, 173. However, this pattern has not been described for other A. aegypti-borne diseases, such as DENV and YFV, possibly reflecting a greater peridomestic risk association of CHIKV because it is usually highly debilitating and immobilizing, reducing spread. Additionally, other groups particularly susceptible to Aedes mosquito bites are children, because they typically play outside, and outdoor workers. Both groups may adopt different play and work hours in response to increasing temperatures, potentially exposing them to vectors with crepuscular biting periodicity. In the United States, outdoor worker populations are projected to increase substantially up to 2080 (ref. 174). Moreover, the global ageing of human populations may reshape the risk of vector-borne diseases with age-dependent pathogenicity (for example, WNV, CHIKV and DENV) 173, 175, 176, 177, particularly in low and middle-income countries where two thirds of the world’s population older than 60 years of age will live by 2050.

Lower socioeconomic status can also increase the risk of vector-borne diseases, particularly mosquito-borne infections; however, there is major heterogeneity in conclusions across studies 178. Poverty has long been considered a key determinant of mosquito-borne infections (for example, DENV and CHIKV). However, the scarcity of studies with consistent measures of income and social vulnerability leaves this correlation disputed 50, which refers to the seemingly lower risk of malaria infection in communities near irrigated rice fields, even those with larger populations of malaria vectors 98. Although rice fields are considered a risk factor for malaria, the economic benefits of rice production for communities living in these areas counteract this risk and lead to reduced malaria transmission.

Finally, most vector-borne diseases disproportionally affect low and middle-income countries and cause an economic burden for national governments, which are the largest source of financing for prevention, surveillance and healthcare. For example, the annual global cost estimated for DENV and malaria control is US $8.9 billion and US $6.6 billion, respectively 179, 180. Associations between vector-borne disease burden and poverty can have downstream effects on education and employment and lead to ‘poverty traps’, a self-reinforcing mechanism that enables poverty and diseases to persist 181.

Conclusions

Climate and anthropogenic changes will undoubtedly reshape the risk and burden of vector-borne disease worldwide in the coming years and decades. Recent advances in disease surveillance networks and public health capacity in some locations developed during the COVID-19 pandemic could be extended to mitigate the increasing threat of emerging vector-borne infections. However, many other actions are needed to reduce the burden of vector-borne diseases in the era of climate change, such as the Lancet Countdown 182. First, we must reduce inequities in healthcare access and improve vector-borne disease surveillance, particularly in low and middle-income countries. Traditional passive surveillance needs to be supplemented by low-cost molecular, serology and genomic approaches to better understand pathogen spread and identify susceptible populations. Second, developing and implementing cost-effective methods for vector control are needed to interrupt transmission of vector-borne diseases at national scales. For example, deployments of A. aegypti mosquitoes infected with Wolbachia are cost-effective interventions to reduce dengue 47, 183. Third, digital and technological innovations can be powerful allies to prevent and/or reduce the burden of arboviral diseases through monitoring importation risk, evaluating (or modelling) climate suitability and mapping potential hotspot locations for focused surveillance and mitigations. Fourth, developing affordable and broadly effective vaccines (that protect against multiple diseases) could have a crucial impact on addressing present and future vector-borne diseases. However, these vaccines must be affordable and available to the affected populations, as limited supply and implementation can leave regions vulnerable to disease re-emergence, as exemplified recently by YFV 184. Fifth, enhanced funding of interdisciplinary research to better understand the mechanisms that drive vector-borne disease transmission in the climate change era will inform interventions and safeguard global health. Last, all these steps need to be aligned with a global view of vector-borne disease risk, and should be prioritized to prevent their continued or accelerated emergence and spread.
World Health Organization. Global vector control response 2017–2030. WHO
https://www.who.int/publications/i/item/9789241512978(2017).
Messina, J. P. et al. The current and future global distribution and population at risk of dengue. Nat. Microbiol. 4, 1508–1515 (2019).
Weaver, S. C., Charlier, C., Vasilakis, N. & Lecuit, M. Zika, chikungunya, and other emerging vector-borne viral diseases. Annu. Rev. Med. 69, 395–408 (2018).
The Intergovernmental Panel on Climate Change. Climate change 2022: impacts, adaptation and vulnerability. IPCC Sixth Assessment. IPCC
https://www.ipcc.ch/report/ar6/wg2/(2022).
Armstrong McKay, D. I. et al. Exceeding 1.5 °C global warming could trigger multiple climate tipping points. Science 377, eabn7950 (2022).
Rose, N. H. et al. Dating the origin and spread of specialization on human hosts in. eLife 12, e83524 (2023).
Eigenbrode, S. D., Bosque-Pérez, N. A. & Davis, T. S. Insect-borne plant pathogens and their vectors: ecology, evolution, and complex interactions. Annu. Rev. Entomol. 63, 169–191 (2018).
Singh, B. K. et al. Climate change impacts on plant pathogens, food security and paths forward. Nat. Rev. Microbiol. 21, 640–656 (2023).
Delatte, H., Gimonneau, G., Triboire, A. & Fontenille, D. Influence of temperature on immature development, survival, longevity, fecundity, and gonotrophic cycles of Aedes albopictus, vector of chikungunya and dengue in the Indian Ocean. J. Med. Entomol. 46, 33–41 (2009).
Shocket, M. S. et al. Transmission of West Nile and five other temperate mosquito-borne viruses peaks at temperatures between 23 °C and 26 °C. eLife 9, e58511 (2020).
Shapiro, L. L. M., Whitehead, S. A. & Thomas, M. B. Quantifying the effects of temperature on mosquito and parasite traits that determine the transmission potential of human malaria. PLoS Biol. 15, e2003489 (2017).
Lambrechts, L. et al. Impact of daily temperature fluctuations on dengue virus transmission by Aedes aegypti. Proc. Natl Acad. Sci. USA 108, 7460–7465 (2011).
Ogden, N. H. & Lindsay, L. R. Effects of climate and climate change on vectors and vector-borne diseases: ticks are different. Trends Parasitol. 32, 646–656 (2016).
Ogden, N. H., Ben Beard, C., Ginsberg, H. S. & Tsao, J. I. Possible effects of climate change on ixodid ticks and the pathogens they transmit: predictions and observations. J. Med. Entomol. 58, 1536–1545 (2020).
Wang, B. et al. Historical change of El Niño properties sheds light on future changes of extreme El Niño. Proc. Natl Acad. Sci. USA 116, 22512–22517 (2019).
Lawman, A. E. et al. Unraveling forced responses of extreme El Niño variability over the Holocene. Sci. Adv. 8, eabm4313 (2022).
Wengel, C. et al. Future high-resolution El Niño/Southern Oscillation dynamics. Nat. Clim. Change 11, 758–765 (2021).
Linthicum, K. J. et al. Climate and satellite indicators to forecast Rift Valley fever epidemics in Kenya. Science 285, 397–400 (1999).
Linthicum, K. J., Britch, S. C. & Anyamba, A. Rift valley fever: an emerging mosquito-borne disease. Annu. Rev. Entomol. 61, 395–415 (2016).
Lindsay, S. W., Bødker, R., Malima, R., Msangeni, H. A. & Kisinza, W. Effect of 1997–98 El Niño on highland malaria in Tanzania. Lancet 355, 989–990 (2000).
Boyce, R. M. et al. Dihydroartemisinin–piperaquine chemoprevention and malaria incidence after severe flooding: evaluation of a pragmatic intervention in rural Uganda. Clin. Infect. Dis. 74, 2191–2199 (2022).
Roiz, D., Boussès, P., Simard, F., Paupy, C. & Fontenille, D. Autochthonous chikungunya transmission and extreme climate events in southern France. PLoS Negl. Trop. Dis. 9, e0003854 (2015).
Grossi-Soyster, E. N. et al. Serological and spatial analysis of alphavirus and flavivirus prevalence and risk factors in a rural community in western Kenya. PLoS Negl. Trop. Dis. 11, e0005998 (2017).
Diniz, D. F. A., de Albuquerque, C. M. R., Oliva, L. O., de Melo-Santos, M. A. V. & Ayres, C. F. J. Diapause and quiescence: dormancy mechanisms that contribute to the geographical expansion of mosquitoes and their evolutionary success. Parasit. Vectors 10, 310 (2017).
Barrera, R. et al. Impacts of hurricanes Irma and Maria on. Am. J. Trop. Med. Hyg. 100, 1413–1420 (2019).
Caillouët, K. A. & Robertson, S. L. Temporal and spatial impacts of hurricane damage on West Nile virus transmission and human risk. J. Am. Mosq. Control. Assoc. 36, 106–119 (2020).
Paull, S. H. et al. Drought and immunity determine the intensity of West Nile virus epidemics and climate change impacts. Proc. Biol. Sci. 284, 20162078 (2017).
Lowe, R. et al. Combined effects of hydrometeorological hazards and urbanisation on dengue risk in Brazil: a spatiotemporal modelling study. Lancet Planet. Health 5, e209–e219 (2021).
Forero-Becerra, E., Acosta, A., Benavides, E., Martínez-Díaz, H. C. & Hidalgo, M. Amblyomma mixtum free-living stages: inferences on dry and wet seasons use, preference, and niche width in an agroecosystem (Yopal, Casanare, Colombia). PLoS ONE 17, e0245109 (2022).
Weiler, M., Duscher, G. G., Wetscher, M. & Walochnik, J. Tick abundance: a one year study on the impact of flood events along the banks of the River Danube, Austria. Exp. Appl. Acarol. 71, 151–157 (2017).
Stafford, K. C. Survival of immature Ixodes scapularis (Acari: Ixodidae) at different relative humidities. J. Med. Entomol. 31, 310–314 (1994).
Mordecai, E. A. et al. Thermal biology of mosquito-borne disease. Ecol. Lett. 22, 1690–1708 (2019).
Brady, O. J. et al. Vectorial capacity and vector control: reconsidering sensitivity to parameters for malaria elimination. Trans. R. Soc. Trop. Med. Hyg. 110, 107–117 (2016).
Samuel, G. H., Adelman, Z. N. & Myles, K. M. Temperature-dependent effects on the replication and transmission of arthropod-borne viruses in their insect hosts. Curr. Opin. Insect Sci. 16, 108–113 (2016).
Reisen, W. K., Fang, Y. & Martinez, V. M. Effects of temperature on the transmission of west nile virus by Culex tarsalis (Diptera: Culicidae). J. Med. Entomol. 43, 309–317 (2006).
Mullens, B. A., Tabachnick, W. J., Holbrook, F. R. & Thompson, L. H. Effects of temperature on virogenesis of bluetongue virus serotype 11 in Culicoides variipennis sonorensis. Med. Vet. Entomol. 9, 71–76 (1995).
Jacquot, M., Nomikou, K., Palmarini, M., Mertens, P. & Biek, R. Bluetongue virus spread in Europe is a consequence of climatic, landscape and vertebrate host factors as revealed by phylogeographic inference. Proc. Biol. Sci. 284, 20170919 (2017).
Reisen, W. K., Meyer, R. P., Presser, S. B. & Hardy, J. L. Effect of temperature on the transmission of western equine encephalomyelitis and St. Louis encephalitis viruses by Culex tarsalis (Diptera: Culicidae). J. Med. Entomol. 30, 151–160 (1993).
Kramer, L. D., Hardy, J. L. & Presser, S. B. Effect of temperature of extrinsic incubation on the vector competence of Culex tarsalis for western equine encephalomyelitis virus. Am. J. Trop. Med. Hyg. 32, 1130–1139 (1983).
Paaijmans, K. P. et al. Influence of climate on malaria transmission depends on daily temperature variation. Proc. Natl Acad. Sci. USA 107, 15135–15139 (2010).
Liu-Helmersson, J., Stenlund, H., Wilder-Smith, A. & Rocklov, J. Vectorial capacity of Aedes aegypti: effects of temperature and implications for global dengue epidemic potential. PLoS ONE 9, e89783 (2014).
Samuel, G. H., Adelman, Z. N. & Myles, K. M. Antiviral immunity and virus-mediated antagonism in disease vector mosquitoes. Trends Microbiol. 26, 447–461 (2018).
Schnettler, E. et al. Noncoding flavivirus RNA displays RNA interference suppressor activity in insect and mammalian cells. J. Virol. 86, 13486–13500 (2012).
Adelman, Z. N. et al. Cooler temperatures destabilize RNA interference and increase susceptibility of disease vector mosquitoes to viral infection. PLoS Negl. Trop. Dis. 7, e2239 (2013).
Macdonald, G. The Epidemiology and Control of Malaria (Oxford Univ. Press, 1957).
Ribeiro Dos Santos, G. et al. Estimating the effect of the wMel release programme on the incidence of dengue and chikungunya in Rio de Janeiro, Brazil: a spatiotemporal modelling study. Lancet Infect. Dis. 22, 1587–1595 (2022).
Utarini, A. et al. Efficacy of Wolbachia-infected mosquito deployments for the control of dengue. N. Engl. J. Med. 384, 2177–2186 (2021).
Vásquez, V. N., Kueppers, L. M., Rašić, G. & Marshall, J. M. Mel replacement of dengue-competent mosquitoes is robust to near-term change. Nat. Clim. Change 13, 848–855 (2023).
Olmo, R. P. et al. Mosquito vector competence for dengue is modulated by insect-specific viruses. Nat. Microbiol. 8, 135–149 (2023).
Franklinos, L. H. V., Jones, K. E., Redding, D. W. & Abubakar, I. The effect of global change on mosquito-borne disease. Lancet Infect. Dis. 19, e302–e312 (2019).
Messina, J. P. et al. Mapping global environmental suitability for Zika virus. eLife 5, e15272 (2016).
Kraemer, M. U. G. et al. Past and future spread of the arbovirus vectors Aedes aegypti and Aedes albopictus. Nat. Microbiol. 4, 854–863 (2019).
Mordecai, E. A. et al. Detecting the impact of temperature on transmission of Zika, dengue, and chikungunya using mechanistic models. PloS Negl. Trop. Dis. 11, e0005568 (2017).
Iwamura, T., Guzman-Holst, A. & Murray, K. A. Accelerating invasion potential of disease vector Aedes aegypti under climate change. Nat. Commun. 11, 2130 (2020).
Ryan, S. J., Carlson, C. J., Mordecai, E. A. & Johnson, L. R. Global expansion and redistribution of Aedes-borne virus transmission risk with climate change. PLoS Negl. Trop. Dis. 13, e0007213 (2019).
Santos-Vega, M. et al. The neglected role of relative humidity in the interannual variability of urban malaria in Indian cities. Nat. Commun. 13, 533 (2022).
Smith, M. W. et al. Incorporating hydrology into climate suitability models changes projections of malaria transmission in Africa. Nat. Commun. 11, 4353 (2020).
Colón-González, F. J. et al. Projecting the risk of mosquito-borne diseases in a warmer and more populated world: a multi-model, multi-scenario intercomparison modelling study. Lancet Planet. Health 5, e404–e414 (2021).
Tjaden, N. B. et al. Modelling the effects of global climate change on Chikungunya transmission in the 21st century. Sci. Rep. 7, 3813 (2017).
Gaythorpe, K. A., Hamlet, A., Cibrelus, L., Garske, T. & Ferguson, N. M. The effect of climate change on yellow fever disease burden in Africa. eLife 9, e55619 (2020).
Kraemer, M. U. et al. The global distribution of the arbovirus vectors Aedes aegypti and Ae. albopictus. eLife 4, e08347 (2015).
Estrada-Peña, A. & Fernández-Ruiz, N. A retrospective assessment of temperature trends in Northern Europe reveals a deep impact on the life cycle of Ixodes ricinus (Acari: Ixodidae). Pathogens 9, 345 (2020).
Minigan, J. N., Hager, H. A., Peregrine, A. S. & Newman, J. A. Current and potential future distribution of the American dog tick (Dermacentor variabilis, Say) in North America. Ticks Tick. Borne Dis. 9, 354–362 (2018).
Shocket, M. S., Ryan, S. J. & Mordecai, E. A. Temperature explains broad patterns of Ross River virus transmission. eLife 7, e37762 (2018).
Samy, A. M. et al. Climate change influences on the global potential distribution of the mosquito Culex quinquefasciatus, vector of West Nile virus and lymphatic filariasis. PLoS ONE 11, e0163863 (2016).
Mordecai, E. A., Ryan, S. J., Caldwell, J. M., Shah, M. M. & LaBeaud, A. D. Climate change could shift disease burden from malaria to arboviruses in Africa. Lancet Planet. Health 4, e416–e423 (2020).
Wang, Z. et al. The relationship between rising temperatures and malaria incidence in Hainan, China, from 1984 to 2010: a longitudinal cohort study. Lancet Planet. Health 6, e350–e358 (2022).
Recht, J. et al. Malaria in Brazil, Colombia, Peru and Venezuela: current challenges in malaria control and elimination. Malar. J. 16, 273 (2017).
Wilder-Smith, A. et al. Epidemic arboviral diseases: priorities for research and public health. Lancet Infect. Dis. 17, e101–e106 (2017).
Cohen, J. A chikungunya vaccine is likely to get approved. Who will get it? Science 382, 503–504 (2023).
Thomas, S. J. Is new dengue vaccine efficacy data a relief or cause for concern? NPJ Vaccines 8, 55 (2023).
Nash, D. et al. The outbreak of West Nile virus infection in the New York City area in 1999. N. Engl. J. Med. 344, 1807–1814 (2001).
Nunes, M. R. et al. Emergence and potential for spread of Chikungunya virus in Brazil. BMC Med. 13, 102 (2015).
Faria, N. R. et al. Zika virus in the Americas: early epidemiological and genetic findings. Science 352, 345–349 (2016).
Jones, K. E. et al. Global trends in emerging infectious diseases. Nature 451, 990–993 (2008).
Gibb, R. et al. Zoonotic host diversity increases in human-dominated ecosystems. Nature 584, 398–402 (2020).
Song, X. P. et al. Global land change from 1982 to 2016. Nature 560, 639–643 (2018).
Santos, C. V. B. D., Sevá, A. D. P. & Werneck, G. L. Does deforestation drive visceral leishmaniasis transmission? A causal analysis. Proc. Biol. Sci. 288, 20211537 (2021).
MacDonald, A. J. & Mordecai, E. A. Amazon deforestation drives malaria transmission, and malaria burden reduces forest clearing. Proc. Natl Acad. Sci. USA 116, 22212–22218 (2019).
Walsh, J. F., Molyneux, D. H. & Birley, M. H. Deforestation: effects on vector-borne disease. Parasitology 106, S55–S75 (1993).
Russell, M. C. et al. Both consumptive and non-consumptive effects of predators impact mosquito populations and have implications for disease transmission. eLife 11, e71503 (2022).
Ducheyne, E. et al. The impact of habitat fragmentation on tsetse abundance on the plateau of eastern Zambia. Prev. Vet. Med. 91, 11–18 (2009).
Van den Bossche, P., Shumba, W. & Makhambera, P. The distribution and epidemiology of bovine trypanosomosis in Malawi. Vet. Parasitol. 88, 163–176 (2000).
Estrada-Peña, A. & Jongejan, F. Ticks feeding on humans: a review of records on human-biting Ixodoidea with special reference to pathogen transmission. Exp. Appl. Acarol. 23, 685–715 (1999).
Kurokawa, C. et al. Interactions between Borrelia burgdorferi and ticks. Nat. Rev. Microbiol. 18, 587–600 (2020).
Levi, T., Keesing, F., Holt, R. D., Barfield, M. & Ostfeld, R. S. Quantifying dilution and amplification in a community of hosts for tick-borne pathogens. Ecol. Appl. 26, 484–498 (2016).
Occhibove, F., Kenobi, K., Swain, M. & Risley, C. An eco-epidemiological modeling approach to investigate dilution effect in two different tick-borne pathosystems. Ecol. Appl. 32, e2550 (2022).
Ogden, N. H. & Tsao, J. I. Biodiversity and Lyme disease: dilution or amplification? Epidemics 1, 196–206 (2009).
Li, S. L. et al. Mapping environmental suitability of Haemagogus and Sabethes spp.mosquitoes to understand sylvatic transmission risk of yellow fever virus in Brazil. PLoS Negl. Trop. Dis. 16, e0010019 (2022).
Faria, N. R. et al. Genomic and epidemiological monitoring of yellow fever virus transmission potential. Science 361, 894–899 (2018).
MacDonald, A. J. Abiotic and habitat drivers of tick vector abundance, diversity, phenology and human encounter risk in southern California. PLoS ONE 13, e0201665 (2018).
Kweka, E. J., Kimaro, E. E. & Munga, S. Effect of deforestation and land use changes on mosquito productivity and development in western Kenya highlands: implication for malaria risk. Front. Public Health 4, 238 (2016).
Burkett-Cadena, N. D. & Vittor, A. Y. Deforestation and vector-borne disease: forest conversion favors important mosquito vectors of human pathogens. Basic. Appl. Ecol. 26, 101–110 (2018).
Plowright, R. K. et al. Pathways to zoonotic spillover. Nat. Rev. Microbiol. 15, 502–510 (2017).
Weaver, S. C. Urbanization and geographic expansion of zoonotic arboviral diseases: mechanisms and potential strategies for prevention. Trends Microbiol. 21, 360–363 (2013).
Hurtt, G. C. et al. Harmonization of land-use scenarios for the period 1500–2100: 600 years of global gridded annual land-use transitions, wood harvest, and resulting secondary lands. Clim. Change 109, 117 (2011).
Waage, J. et al. Changing food systems and infectious disease risks in low-income and middle-income countries. Lancet Planet. Health 6, e760–e768 (2022).
Chan, K. et al. Malaria transmission and prevalence in rice-growing versus non-rice-growing villages in Africa: a systematic review and meta-analysis. Lancet Planet. Health 6, e257–e269 (2022).
Sarfraz, M. S. et al. Analyzing the spatio-temporal relationship between dengue vector larval density and land-use using factor analysis and spatial ring mapping. BMC Public Health 12, 853 (2012).
Franklinos, L. H. V. et al. Joint spatiotemporal modelling reveals seasonally dynamic patterns of Japanese encephalitis vector abundance across India. PLoS Negl. Trop. Dis. 16, e0010218 (2022).
Jones, B. A. et al. Zoonosis emergence linked to agricultural intensification and environmental change. Proc. Natl Acad. Sci. USA 110, 8399–8404 (2013).
Shah, H. A., Huxley, P., Elmes, J. & Murray, K. A. Agricultural land-uses consistently exacerbate infectious disease risks in Southeast Asia. Nat. Commun. 10, 4299 (2019).
Sinka, M. E. et al. The dominant Anopheles vectors of human malaria in the Asia–Pacific region: occurrence data, distribution maps and bionomic précis. Parasit. Vectors 4, 89 (2011).
Trung, H. D. et al. Malaria transmission and major malaria vectors in different geographical areas of Southeast Asia. Trop. Med. Int. Health 9, 230–237 (2004).
Boccolini, D. et al. Impact of environmental changes and human-related factors on the potential malaria vector, Anopheles labranchiae (Diptera: Culicidae), in Maremma, Central Italy. J. Med. Entomol. 49, 833–842 (2012).
Gregory, N., Ewers, R. M., Chung, A. Y. C. & Cator, L. J. Oil palm expansion increases the vectorial capacity of dengue vectors in Malaysian Borneo. PLoS Negl. Trop. Dis. 16, e0009525 (2022).
Le Flohic, G., Porphyre, V., Barbazan, P. & Gonzalez, J. P. Review of climate, landscape, and viral genetics as drivers of the Japanese encephalitis virus ecology. PLoS Negl. Trop. Dis. 7, e2208 (2013).
Tchouassi, D. P. et al. Mosquito host choices on livestock amplifiers of Rift Valley fever virus in Kenya. Parasit. Vectors 9, 184 (2016).
Kumar Pant, D., Tenzin, T., Chand, R., Kumar Sharma, B. & Raj Bist, P. Spatio-temporal epidemiology of Japanese encephalitis in Nepal, 2007–2015. PLoS ONE 12, e0180591 (2017).
Yakob, L. et al. Japanese encephalitis emergence in Australia: the potential population at risk. Clin. Infect. Dis. 76, 335–337 (2022).
Lord, J. S., Gurley, E. S. & Pulliam, J. R. Rethinking Japanese encephalitis virus transmission: a framework for implicating host and vector species. PLoS Negl. Trop. Dis. 9, e0004074 (2015).
Morgan, C. E. et al. Association between domesticated animal ownership and Plasmodium falciparum parasite prevalence in the Democratic Republic of the Congo: a national cross-sectional study. Lancet Microbe 4, e516–e523 (2023).
Kuhn, K. G., Campbell-Lendrum, D. H., Armstrong, B. & Davies, C. R. Malaria in Britain: past, present, and future. Proc. Natl Acad. Sci. USA 100, 9997–10001 (2003).
Hayek, M. N. The infectious disease trap of animal agriculture. Sci. Adv. 8, eadd6681 (2022).
He, C. et al. Future global urban water scarcity and potential solutions. Nat. Commun. 12, 4667 (2021).
Kache, P. A. et al. Bridging landscape ecology and urban science to respond to the rising threat of mosquito-borne diseases. Nat. Ecol. Evol. 6, 1601–1616 (2022).
Wilke, A. B. B. et al. Urbanization favors the proliferation of Aedes aegypti and Culex quinquefasciatus in urban areas of Miami-Dade County, Florida. Sci. Rep. 11, 22989 (2021).
Allan, R., Budge, S. & Sauskojus, H. What sounds like Aedes, acts like Aedes, but is not Aedes? Lessons from dengue virus control for the management of invasive Anopheles. Lancet Glob. Health 11, e165–e169 (2023).
Metz, H. C. et al. Evolution of a mosquito’s hatching behavior to match its human-provided habitat. Am. Nat. 201, 200–214 (2023).
Rose, N. H. et al. Climate and urbanization drive mosquito preference for humans. Curr. Biol. 30, 3570–3579.e6 (2020).
Zhao, Z. et al. Mosquito brains encode unique features of human odour to drive host seeking. Nature 605, 706–712 (2022).
Maquart, P. O., Froehlich, Y. & Boyer, S. Plastic pollution and infectious diseases. Lancet Planet. Health 6, e842–e845 (2022).
Wilke, A. B. B. et al. Urbanization creates diverse aquatic habitats for immature mosquitoes in urban areas. Sci. Rep. 9, 15335 (2019).
Carlson, J., Keating, J., Mbogo, C. M., Kahindi, S. & Beier, J. C. Ecological limitations on aquatic mosquito predator colonization in the urban environment. J. Vector Ecol. 29, 331–339 (2004).
Zhao, L., Lee, X., Smith, R. B. & Oleson, K. Strong contributions of local background climate to urban heat islands. Nature 511, 216–219 (2014).
Zhao, L. et al. Global multi-model projections of local urban climates. Nat. Clim. Change 11, 152–157 (2021).
Patz, J. A., Campbell-Lendrum, D., Holloway, T. & Foley, J. A. Impact of regional climate change on human health. Nature 438, 310–317 (2005).
Caminade, C., McIntyre, K. M. & Jones, A. E. Impact of recent and future climate change on vector-borne diseases. Ann. N. Y. Acad. Sci. 1436, 157–173 (2019).
Nieuwenhuijsen, M. J. Green infrastructure and health. Annu. Rev. Public Health 42, 317–328 (2021).
Medeiros-Sousa, A. R., Fernandes, A., Ceretti-Junior, W., Wilke, A. B. B. & Marrelli, M. T. Mosquitoes in urban green spaces: using an island biogeographic approach to identify drivers of species richness and composition. Sci. Rep. 7, 17826 (2017).
Obame-Nkoghe, J. et al. Urban green spaces and vector-borne disease risk in Africa: the case of an unclean forested park in libreville (Gabon, Central Africa). Int. J. Environ. Res. Public Health 20, 5774 (2023).
Liu, L., Zhong, Y., Ao, S. & Wu, H. Exploring the relevance of green space and epidemic diseases based on panel data in China from 2007 to 2016. Int. J. Environ. Res. Public Health 16, 2551 (2019).
Weiss, D. J. et al. Global maps of travel time to healthcare facilities. Nat. Med. 26, 1835–1838 (2020).
Plowright, R. K. et al. Land use-induced spillover: a call to action to safeguard environmental, animal, and human health. Lancet Planet. Health 5, e237–e245 (2021).
Kibret, S., McCartney, M., Lautze, J., Nhamo, L. & Yan, G. The impact of large and small dams on malaria transmission in four basins in Africa. Sci. Rep. 11, 13355 (2021).
Kibret, S., Lautze, J., McCartney, M., Nhamo, L. & Yan, G. Malaria around large dams in Africa: effect of environmental and transmission endemicity factors. Malar. J. 18, 303 (2019).
Kibret, S. Time to revisit how dams are affecting malaria transmission. Lancet Planet. Health 2, e378–e379 (2018).
De Salazar, P. M., Cox, H., Imhoff, H., Alexandre, J. S. F. & Buckee, C. O. The association between gold mining and malaria in Guyana: a statistical inference and time-series analysis. Lancet Planet. Health 5, e731–e738 (2021).
Fletcher, I. K. et al. Synergies between environmental degradation and climate variation on malaria re-emergence in southern Venezuela: a spatiotemporal modelling study. Lancet Planet. Health 6, e739–e748 (2022).
Rotureau, B., Joubert, M., Clyti, E., Djossou, F. & Carme, B. Leishmaniasis among gold miners, French Guiana. Emerg. Infect. Dis. 12, 1169–1170 (2006).
Duron, O. et al. Novel chronic anaplasmosis in splenectomized patient, Amazon rainforest. Emerg. Infect. Dis. 28, 1673–1676 (2022).
VanAcker, M. C., Little, E. A. H., Molaei, G., Bajwa, W. I. & Diuk-Wasser, M. A. Enhancement of risk for Lyme disease by landscape connectivity, New York, New York, USA. Emerg. Infect. Dis. 25, 1136–1143 (2019).
Yasuoka, J. & Levins, R. Impact of deforestation and agricultural development on anopheline ecology and malaria epidemiology. Am. J. Trop. Med. Hyg. 76, 450–460 (2007).
Stern, A. M. The public health service in the Panama Canal: a forgotten chapter of U.S. public health. Public. Health Rep. 120, 675–679 (2005).
Kraemer, M. U. G. et al. Mapping global variation in human mobility. Nat. Hum. Behav. 4, 800–810 (2020).
Tatem, A. J., Hay, S. I. & Rogers, D. J. Global traffic and disease vector dispersal. Proc. Natl Acad. Sci. USA 103, 6242–6247 (2006).
Chippaux, J. P. & Chippaux, A. Yellow fever in Africa and the Americas: a historical and epidemiological perspective. J. Venom. Anim. Toxins Incl. Trop. Dis. 24, 20 (2018).
Cuthbert, R. N. et al. Invasive hematophagous arthropods and associated diseases in a changing world. Parasit. Vectors 16, 291 (2023).
Tian, H. et al. Increasing airline travel may facilitate co-circulation of multiple dengue virus serotypes in Asia. PLoS Negl. Trop. Dis. 11, e0005694 (2017).
Nunes, M. R. et al. Air travel is associated with intracontinental spread of dengue virus serotypes 1–3 in Brazil. PLoS Negl. Trop. Dis. 8, e2769 (2014).
Baker, R. E. et al. Infectious disease in an era of global change. Nat. Rev. Microbiol. 20, 193–205 (2022).
Costard, S. et al. African swine fever: how can global spread be prevented? Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 2683–2696 (2009).
Rodriguez, M., Hooghuis, H. & Castaño, M. African horse sickness in Spain. Vet. Microbiol. 33, 129–142 (1992).
Diagne, C. et al. High and rising economic costs of biological invasions worldwide. Nature 592, 571–576 (2021).
Juliano, S. A. & Lounibos, L. P. Ecology of invasive mosquitoes: effects on resident species and on human health. Ecol. Lett. 8, 558–574 (2005).
Backus, L. H., Pascoe, E. L. & Foley, J. Will new ticks invade North America? How to identify future invaders. Trends Parasitol. 38, 805–814 (2022).
The Bureau of Transportation Statistics, part of the U.S. Department of Transportation. Air transport, passengers carried. BTS
https://www.bts.gov/newsroom/full-year-2022-us-airline-traffic-data(202….
International Organization for Migration. World Migration Report 2022
https://publications.iom.int/books/world-migration-report-2022(2021).
McMichael, C. Human mobility, climate change, and health: unpacking the connections. Lancet Planet. Health 4, e217–e218 (2020).
Schütte, S., Gemenne, F., Zaman, M., Flahault, A. & Depoux, A. Connecting planetary health, climate change, and migration. Lancet Planet. Health 2, e58–e59 (2018).
Bharti, N. Linking human behaviors and infectious diseases. Proc. Natl Acad. Sci. USA 118, e2101345118 (2021).
Nsoesie, E. O. et al. Global distribution and environmental suitability for chikungunya virus, 1952 to 2015. Euro Surveill.
https://doi.org/10.2807/1560-7917.ES.2016.21.20.30234(2016).
Reiter, P. et al. Texas lifestyle limits transmission of dengue virus. Emerg. Infect. Dis. 9, 86–89 (2003).
Davis, L. W. & Gertler, P. J. Contribution of air conditioning adoption to future energy use under global warming. Proc. Natl Acad. Sci. USA 112, 5962–5967 (2015).
Centers for Disase Control and Prevention (CDC). Knowledge, attitudes, and behaviors about West Nile virus — Connecticut, 2002. MMWR Morb. Mortal. Wkly. Rep. 52, 886–888 (2003).
McCarthy, T. A. et al. West Nile virus serosurvey and assessment of personal prevention efforts in an area with intense epizootic activity: Connecticut, 2000. Ann. N. Y. Acad. Sci. 951, 307–316 (2001).
Haenchen, S. D. et al. Mosquito avoidance practices and knowledge of arboviral diseases in cities with differing recent history of disease. Am. J. Trop. Med. Hyg. 95, 945–953 (2016).
Adams, L. E. et al. Epidemiology of dengue, chikungunya, and Zika virus disease in U.S. states and territories, 2017. Am. J. Trop. Med. Hyg. 101, 884–890 (2019).
Salje, H. et al. How social structures, space, and behaviors shape the spread of infectious diseases using chikungunya as a case study. Proc. Natl Acad. Sci. USA 113, 13420–13425 (2016).
Slatculescu, A. M. et al. Rurality, socioeconomic status, and residence in environmental risk areas associated with increased lyme disease incidence in Ontario, Canada: a case–control study. Vector Borne Zoonotic Dis. 22, 572–581 (2022).
Aenishaenslin, C. et al. Behavioral risk factors associated with reported tick exposure in a Lyme disease high incidence region in Canada. BMC Public Health 22, 807 (2022).
Costa, G. B., Smithyman, R., O’Neill, S. L. & Moreira, L. A. How to engage communities on a large scale? Lessons from World Mosquito Program in Rio de Janeiro, Brazil. Gates Open. Res. 4, 109 (2020).
de Souza, W. M. et al. Spatiotemporal dynamics and recurrence of chikungunya virus in Brazil: an epidemiological study. Lancet Microbe 4, e319–e329 (2023).
Rohat, G. et al. Intersecting vulnerabilities: climatic and demographic contributions to future population exposure to Aedes-borne viruses in the United States. Environ. Res. Lett. 15, 084046 (2020).
McDonald, E. et al. Surveillance for West Nile virus disease — United States, 2009–2018. MMWR Surveill. Summ. 70, 1–15 (2021).
de Lima, S. T. S. et al. Fatal outcome of chikungunya virus infection in Brazil. Clin. Infect. Dis. 73, e2436–e2443 (2021).
Rowe, E. K. et al. Challenges in dengue fever in the elderly: a typical presentation and risk of severe dengue and hospital-acquired infection [corrected]. PLoS Negl. Trop. Dis. 8, e2777 (2014).
Power, G. M. et al. Socioeconomic risk markers of arthropod-borne virus (arbovirus) infections: a systematic literature review and meta-analysis. BMJ Glob. Health 7, e007735 (2022).
Haakenstad, A. et al. Tracking spending on malaria by source in 106 countries, 2000–16: an economic modelling study. Lancet Infect. Dis. 19, 703–716 (2019).
Shepard, D. S., Undurraga, E. A., Halasa, Y. A. & Stanaway, J. D. The global economic burden of dengue: a systematic analysis. Lancet Infect. Dis. 16, 935–941 (2016).
Ngonghala, C. N. et al. Poverty, disease, and the ecology of complex systems. PloS Biol. 12, e1001827 (2014).
Romanello, M. et al. The 2023 report of the Lancet Countdown on health and climate change: the imperative for a health-centred response in a world facing irreversible harms. Lancet 402, 2346–2394 (2023).
Brady, O. J. et al. The cost-effectiveness of controlling dengue in Indonesia using wMel Wolbachia released at scale: a modelling study. BMC Med. 18, 186 (2020).
Nwaiwu, A. U., Musekiwa, A., Tamuzi, J. L., Sambala, E. Z. & Nyasulu, P. S. The incidence and mortality of yellow fever in Africa: a systematic review and meta-analysis. BMC Infect. Dis. 21, 1089 (2021).
Fieler, A. M. et al. Larval thermal characteristics of multiple ixodid ticks. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 257, 110939 (2021).
Li, S. et al. Lyme disease risks in Europe under multiple uncertain drivers of change. Env. Health Perspect. 127, 67010 (2019).

Acknowledgements

W.M.d.S. is supported by a Global Virus Network fellowship, Burroughs Wellcome Fund — Climate Change and Human Health Seed Grants (no. 1022448) and Wellcome Trust — Digital Technology Development Award in Climate Sensitive Infectious Disease Modelling (no. 226075/Z/22/Z). S.C.W. is supported by National Institutes of Health (NIH) grant AI120942.

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Glossary
Anthropogenic
Resulting from the influence of humans on nature.
Enzootic
Ancestral, often continuous cycles of zoonotic arboviruses involving wild animals serving as amplification and/or reservoir hosts.
Epizootic
An outbreak of disease in non-human animal populations.
Global warming
Long-term heating of the Earth’s surface observed since the pre-industrial period.
Spillback
Transmission of pathogens from humans to wild animals, sometimes resulting in stable enzootic cycles.
Spillover
Pathogen transmission from zoonotic wildlife hosts to humans, sometimes resulting in stable human-amplified transmission.
Thermal performance curves
Effects of ambient temperature on biological rate processes of organisms, including vectors, from behaviour to biological processes, that can be used to predict the potential effects of global warming on ecological systems.
Tipping points
Critical thresholds in a climate system that, when exceeded, can lead to a significant change in the climate state, often with predicted irreversible changes.
Trans-stadial transmission
Sequential passage of pathogens acquired during one life stage, or stadium, through the moult to the next stage or stages, or stadium.
Vector competence
The intrinsic ability of an arthropod to become infected and transmit a pathogen.
Zoonotic
Infections that spill over from non-human animals to humans.

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de Souza, W.M., Weaver, S.C. Effects of climate change and human activities on vector-borne diseases. Nat Rev Microbiol (2024). https://doi.org/10.1038/s41579-024-01026-0
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DOI: https://doi.org/10.1038/s41579-024-01026-0