This spring, a pandemic made us wonder: will the new coronavirus disappear with the arrival of heat? After all, other infections that affect the respiratory tract, like flu and colds, are much less likely to occur in the warm period. This is partly because particles of respiratory viruses last longer in dry winter air without falling with drops of water – which means that people have more time to inhale them. Besides, dry and cold air damages the cells that line the respiratory tract, and warm, moist air, on the contrary, maintains a layer of mucus, which protects against harmful particles (Moriyama, Hugentobler, and Iwasaki 2020). 

The new SARS-CoV-2 coronavirus has recently been found to mostly spread through airborne transmission (Zhang et al. 2020). However, the studies do not positively say that the epidemic will attenuate in the summer. The spread of the virus, apparently, is not sufficiently affected by either short-term weather changes or long-term climate changes, as evidenced by the spread of the pandemic even in warm and humid areas.

For viruses in general, the role of climate is not only that it affects the survival of infections outside the host organism, and not only in the seasonal weakening of immunity. There is also a delayed effect of climate on the spread of viruses. For example, due to global warming and human encroachment into nature, the Ebola virus can go beyond the current foci of infection and spread across Africa, including large transport hubs. The global warming factor in this example is not the main one, but climatic conditions affect the spread of infections through mechanisms of different levels.

Let’s see what other topics in connection with the weather and climate changes are raised by epidemic researchers. For the review, we have performed a systematic search in the scientific literature database Scopus and have built a map of publications based on their reference lists (Figure 1). Proximity in this map and belonging to the same cluster mean that the papers cite the same publications, therefore the papers are likely to consider similar issues. The map is built using VOSviewer software.

Publications are split into six clusters:

• navy, upper left: tick-borne viruses,
• purple, bottom left: malaria,
• blue, at the bottom: main reviews on seasonality,
• gray, bottom right: flu,
• light blue, center: climate change,
• yellow, top right: intestinal bacteria (not covered in the review).

Navy cluster: tick-borne viruses

The cluster is focused on viruses and infections that cause vector-borne diseases. These are diseases that are transmitted to people only from insects (mainly mosquitoes, ticks, and flies). Vector-borne diseases account for more than 17% of all infectious diseases and over 700,000 deaths annually.

Cluster publications discuss tick-borne viruses. In recent decades, the number of cases of tick-borne encephalitis among people has increased, and its geographical coverage has expanded to the Americas, Africa, and several regions of Europe. Climate is one of the factors that determine what species of ticks are found in a given geographical region (Estrada-Peña and de la Fuente 2014). Therefore, there are new risks for humans to encounter a vector-borne disease.

Climate affects the spread of such infections such as the Zika virus, Dengue virus, malaria, and Lyme disease (see Rogers and Randolph 2006 for a review). For example, when the temperature rises, ticks go down for water from the upper layers of the vegetation where they usually live and infect small rodents that carry the virus further. Moreover, if there is a drought, then ticks prefer to save moisture without moving and, accordingly, without transmitting the virus to other carriers (Randolph and Storey 1999). Here, the humidity factor is more important than temperature.

The cluster also included publications that mention the spread of viruses by bats and its seasonal patterns (Olival and Hayman 2014).

Purple cluster: malaria

Malaria is the most important and dangerous of the infections that are transmitted by parasites. It causes more than a million deaths per year (Greenwood et al. 2005). It was malaria that the first models of the spread of infections were dedicated to, the provisions of them are still used in epidemiology (Smith et al. 2012). 

Environmental conditions strongly influence the transmission of malaria, and the models of its spread now take weather data into account (Hoshen and Morse 2004). The emergence and reintroduction of malaria are also more dependent on humidity than on temperature (Parham and Michael 2010) since malaria mosquitoes breed during the rainy season (Pascual et al. 2008). Nevertheless, infected people transmit the infection over long distances: where they come, mosquitoes become infected from them, even if weather conditions were not conducive (Wesolowski et al. 2012).

Blue cluster: main reviews on seasonality

In this cluster, the main publications on the influence of seasonality on the spread of viruses appear.

Altizer et al. (2006) consider the spread of infections to be affected by seasonal changes in how virus hosts behave, and the number of their contacts with susceptible populations; breeding periods of virus hosts; seasonal fluctuations in immunity.

Thus, flu and respiratory infections are common in winter, when children are constantly in contact at school, while the malaria example described above illustrates the factor of host multiplication. In the case of immunity, the production of antibodies depends on the production of melatonin, and it is lower when daylight is short (Dowell 2001). In winter, vitamin D production is also lower, which negatively affects immunity (Cannell et al. 2006).

Grassly and Fraser (2006) add to this classification the factor of virus survival outside the host organism. It depends on humidity, temperature, exposure to sunlight, acidity, and salinity.

For example, rotaviruses and noroviruses survive at low temperatures, so the peak incidence of gastroenteritis occurs in the winter months. The influenza virus lasts longer in the air during the cold period, when humidity is low, especially indoors, and aerosol particles with the virus do not fall in drops of water.

One illustrative and well-studied example of seasonal illness is measles. Its modeling has a long history, measles epidemics are simulated by stochastic models (Earn et al. 2000), which reflect frequent attenuation alternating with irregular large outbreaks (Ferrari et al. 2008). More general models also make it possible to assess how the number of people without immunity affects the consequences of the epidemic: either a new outbreak of the disease after some time, or a disease-free year – a “skip” (Stone, Olinky, and Huppert 2007).

Gray cluster: flu

This cluster unites empirical studies of influenza epidemics. As shown by Dushoff et al. (2004), even insignificant seasonal factors can explain the dynamics of influenza incidence.

One of the most famous types of flu is influenza A. The transmission of the influenza virus and its survival in the environment is influenced by the relative (Lowen et al. 2007) and absolute humidity (Shaman and Kohn 2009; Shaman et al. 2010). In regions with a temperate climate, absolute humidity has a pronounced seasonal cycle. The driest air is in winter, so in the Northern Hemisphere the flu season lasts from November to March, and in the Southern Hemisphere from May to September.

But seasonal epidemics are not always explained by humidity. Nelson and Holmes (2007) review evidence of other factors. For example, in waterfowl, influenza epidemics also occur in August-September, which is most likely due to the increasing density of flocks before migration, and the lack of immunity in fledglings. In the tropics, flu is present year-round despite a warm, humid climate, although the incidence peak sometimes occurs during the rainy season. Still, there are still little systematic data to study the flu in the tropics.

The authors also mention the factor of mobility (Balcan et al. 2009) and the fact that the spatial distribution of the virus corresponds to the working routes more than to mere geographical proximity of settlements (Viboud et al. 2006), although at the local level the flu is still mainly transmitted by pupils.

Light blue cluster: climate change

The most popular publication in this map also thematically belongs to this cluster, as it is related to the effects of regional climate change on human health (Patz et al. 2005). The authors note that many common diseases are associated with climate change, from cardiovascular diseases caused by heat waves to malnutrition due to crop failures, and infectious diseases.

Relating the occurrence or reappearance of the disease to climate change is problematic since there is almost no high-quality longitudinal data to separate the effect of climate change from the influence of other factors. However, the authors mention that global warming is already becoming the cause of greater morbidity and mortality in the foci of infections. Regions that are particularly vulnerable to the spread of infections due to climate change are temperate latitudes, where warming will be especially noticeable; regions along the shores of the Pacific and Indian Oceans that are affected by the El Niño climate anomaly; and sub-Saharan Africa, where the sprawl of cities and the urban heat islands can exacerbate the epidemiological situation.

Gubler et al. (2001) give an overview of the effects of climate change on diseases that are spread by insects and rodents. Researchers emphasize that infections are transmitted from tropical countries to temperate climates and survive in them.

Given this, other studies of the cluster on individual viruses are important. These are arboviruses that are distributed in the tropics and from arthropods through wildlife and livestock transmitted to humans (Weaver and Reisen 2010). It is also a Dengue fever virus (Lambrechts et al. 2011; Wearing and Rohani 2006), whose epidemic potential is increasing under global warming (Patz et al. 1998). Other tropical infections are being discussed: Japanese encephalitis (Misra and Kalita 2010), Zika virus (Barrera, Amador, and MacKay 2011), West Nile fever virus (Kilpatrick et al. 2006). All of them cause fever, headache, and other specific symptoms, as well as consequences of varying seriousness.

West Nile fever virus, for example, is more likely to be transmitted during the hot season (Hartley et al. 2012), partly because people wear more open clothing and prefer to spend time outside after sunset when mosquitoes are active. Especially often mosquitoes come in contact with those who do not have an air conditioner or reasons to stay at home in the evening – for example, there is no computer or TV (Reisen 2013). Thus, not only seasonal and climatic but also socio-economic factors play an important role in the spread of diseases.

Please proceed to page 2 to see general reviews on the climate influences on virus transmission and the description of our data.

Now it is time to discuss how human activities can exacerbate the new epidemics, where these epidemics are likely to emerge, and what are the action strategies against their spread.

During the past 40 years, about one-third of Southeast Asian forests have disappeared. Rainforests were cut down for wood, because of agricultural development, and the uncontrolled expansion of cities (Afelt, Frutos, and Devaux 2018). The forests were replaced by houses, barns, vegetable gardens, farms, orchards, and woods. Sometimes orchards are planted next to a livestock farm, as fruit bring extra income to farmers, and trees provide additional shade.

What remains after deforestation is called a fragmented forest, that is, divided into relatively small isolated areas. One type of fragmentation is the so-called forest perforation (Figure 1).

The forests of Upper Guinea, West Africa, have also declined by a third from 1975 to 2013, with 84% of their former area being lost before 1975. On the place of the rainforest, there appear monocultural oil palm plantations. Amazonian forests are cut down a similar way, for the oil palm and sugarcane. When the new plantations do not require cutting the forest, most likely they are relocated to the place of farms, while these farms move further in the forests.

Recall now that the Nipah henipavirus, which causes dangerous encephalitis in humans, as well as the coronaviruses SARS-CoV and SARS-CoV-2, the current pandemic virus, have jumped to humans from animals in Asia. Ebola filovirus, which causes hemorrhagic fever and is fatal in half the cases, has spread to humans in West Africa (Figure 2). And all these viruses are hosted by bats. Studies suggest that this is not just a coincidence.

When a forest is cut down, the bats’ habitat is depleted. Their immunity is weakened due to a lack of food and the need to look extensively for nutrients. As we have seen, it is in this state that bats begin to spread infections.

The zones inside and adjacent to the forest, shaped by humans, attract a variety of bats. In orchards and palm plantations, fruit-eating flying foxes get their food. Insects flock to the light of dwellings, attracting insectivorous bats, and bats that are used to sleeping in caves move to abandoned houses and barns (Plowright et al. 2015; Afelt et al. 2018).

We usually think that some animal species simply die out because of deforestation. It is not always so. Bats, devoid of habitat and food source, look for it everywhere and also near people. The diverse landscapes of the former forest territories only contribute to the multitude of viruses close to humans.

Now, imagine a farm in Southeast Asia. There, pigs are bred and mango trees grow nearby, tree branches hanging over the piggery to provide an extra shadow. At night, hungry flying foxes – hosts of the virus – fly to the farm and eat the fruit. Half-eaten fruit falls to the ground, with the infected saliva and excreta left on it. The next day, it is eaten by pigs that are not immune to the virus. After some time, an outbreak of the disease occurs in pigs, and then in farmers who contact with the swine. Before this, some infected piglets have already been sold to other regions of the country, and other people became infected from them. This is the story of the first major outbreak of the Nipah virus in Malaysia in 1998-99 (Pulliam et al. 2012).

There is another version of why it was in those years that the Nipah virus was introduced to farms. Then, due to the slash-and-burn method of deforestation, Southeast Asia was covered with haze. At the same time, there was a drought caused by the temperature anomaly El Niño. As a result, the remaining trees bore very little fruit. Therefore, in search of food, the species of flying foxes from other places migrated to Malaysia and infected the fruit trees of the farms (Chua, Chua, and Wang 2002). However, the recent evidence shows that cases of infection had been observed even before the haze and drought occurred (Pulliam et al. 2012). Thus, we can assume that the virus did not spread from migrating flying foxes, but from the local ones, and El Niño only exacerbated the emerging epidemic, caused by deforestation and lack of nutrition in bats.

Figure 3 shows the aforementioned pathways of the Nipah virus transmission:

1. Flying foxes – the natural hosts of the virus – drink the date palm sap and leave drops of biological fluids in it.
2. The palm sap is sold or left to ferment – but not subjected to disinfecting heat treatment.
3. Traditionally, the sap is drunk in the first few hours after collection. One way or another, in a sugar-rich environment, the virus survives for a long time and is transmitted to humans.
4. Flying foxes come to fruit trees located next to pig farms. They eat fruit, leaving biological fluids on them.
5. Half-eaten fruit falls to the ground, where pigs and other animals pick them up and get infected.
6. Infected pigs are slaughtered and/or sold.
7. Humans eat infected pork.
8. In close contact, the Nipah virus can be transmitted from person to person. (There is a hypothesis that not all strains of the virus can be transmitted this way. However, recent epidemics in Bangladesh and India have witnessed some infections from sick people. See Singh et al. 2019.)

The most important consequence of deforestation is the increased contact of bats with domestic animals and people.

In the case of the MERS-CoV coronavirus and the epidemic of the Middle East respiratory syndrome caused by it, the first transmission of the virus to humans did not occur in the tropical zone of a fragmented forest, but in contact with camels (and the camels probably picked the infection up from vespertilionid bats). However, the virus was also found in another species of bats, Taphozous, which lived in the ruins of houses. Other pets in contact with bats could spread the infection, too (Afelt, Frutos, and Devaux 2018).

Proceed to page 2 to see what forecasts the researchers make about the next transmission of the virus from bats to humans.

We will discuss this on the example of epidemics that have spread from bats. For the review, we ran a systematic literature search in the scientific publication database Scopus and found the publications devoted to bats as carriers of viruses. (For a description of the data and visualization of the science map, see page 3 of the review.)

The search results are split into clusters that correspond to the main groups of viruses transmitted by bats. In addition to rabies and influenza viruses, these are coronaviruses that cause acute respiratory syndromes; filoviruses, such as Ebola and Marburg, causing hemorrhagic fever; and henipaviruses, such as Hendra and Nipah, leading to dangerous encephalitis.

It appears that the impact of humans on nature and the subsequent spread of new viruses has long been discussed in the scientific literature – on the case of henipaviruses.

This is not surprising since the outbreaks of diseases caused by henipaviruses occurred earlier than the famous epidemics of coronaviruses. So, the Hendra henipavirus was first seen in Australia in 1995, while the noticeable Nipah henipavirus epidemic unfolded in Malaysia in 1998-9 (Mackenzie et al. 2001).

In terms of virus transmission, an important difference is that coronaviruses live in microbats, while henipaviruses are spread by megabats, or flying foxes (Figure 1). These are two different suborders of the bats order. They differ, in particular, in size and diet. Microbats are small and mostly insectivorous, although there are also predators and vampires among them. Flying foxes reach 1.5 m in the wingspan, and feed on fruits, nectar, pollen, and sometimes insects. (Remember the differences in diet, as food is an important infection pathway.)

In the review, we will use the conventional term “bats” for both types of mammals. When it comes to flying foxes or a certain species of microbats, we will note this explicitly.
We will mainly discuss the cases of henipaviruses spread by flying foxes. Where appropriate, we will also draw on examples of filoviruses and coronaviruses. All of them have pandemic potential (Luby 2013; Simons et al. 2014). The diseases they cause are characterized by high mortality: for encephalitis from the Nipah virus it is 40–75% (Singh et al. 2019), for Ebola fever it is 50% on average and has been up to 90% before (Ebola Virus Disease).

This review is divided into two parts. Today we will discuss whether bats are “especially” active hosts of the virus, and how environmental changes affect their activity.

Why are all eyes on bats?

There is a debate in science about whether bats are “special” as hosts of viruses. Some argue that humans most often get infected from a narrow range of animal groups, including bats (Luis et al. 2013). In other words, a bat species hosts relatively more zoonotic infections than a species of any other animals.

Opponents of this hypothesis believe that all animals spread viruses equally actively. It is the species diversity’ that differs, so the diversity of the transmitted viruses varies accordingly. The more species of an animal there are and, consequently, the more different viruses this group of the animal carries, the greater the likelihood that some of the viruses from this group of animals will spill over into humans.

This second stance is supported by the April publication by Mollentze and Streicker (2020). The paper is based on the most (to date) comprehensive dataset on the relations between viruses and hosts. According to the study, bats mostly do not differ from other animals in the frequency with which they transmit viruses to people (except for the rabies virus). The danger posed by these animal hosts follows a statistical pattern:

The more species of an animal there exist, the more different viruses this animal group hosts, and, accordingly, the more viruses are transmitted to people. Bats are no exception.

Figure 2 shows that this pattern holds for many types of animals. The most diverse species are among rodents, and they are also the most active carriers of viruses to humans. There are about half as many species of bats; therefore, they host proportionally fewer viruses, and fewer diseases spill over into humans from them.

Although bats seem to be not “special” in the sense of transmitting viruses to humans, from a physiological and environmental point of view, they are unusually predisposed to host infections.

Bats have a very strong immune system, presumably associated with their, unique among mammals, ability for sustained flight (O’Shea et al. 2014). Therefore, viruses that enter their bodies usually do not cause disease, and henipaviruses probably hardly even replicate – that is, they rarely reproduce, infecting new cells (Halpin et al. 2011). So viruses remain in the body without manifesting themselves.

Besides, bats sleep in caves, where sometimes thousands of individuals of different species gather, and if one of them is sick, then many bats can become infected. Moreover, bats live very densely in caves, hanging over each other and thus spraying each other with infected biological fluids. In such an unsafe environment, every single contact with the virus rarely leads to infection, but when many individuals spread it, the chance of getting infected increases manyfold (Plowright et al. 2015).

Viruses, in turn, in the course of evolution have adapted to the strong immune defenses of bats (see a review in Calisher et al. 2006). There is a hypothesis, although not verified experimentally, that due to this adaptation, the infections are very serious and even fatal when transmitted from bats to other hosts including humans (Luis et al. 2013).

Please proceed to page 2 to read why bats, being such good virus hosts, do not transmit it to humans too often.