More than 60 percent of infectious diseases that affect humans are caused by pathogens that we share with wild and domestic animals. Such diseases, known as “zoonoses,” are transmitted from other vertebrate animals to humans in a process known as “spillover,” and pose a significant threat to human health. Spillover is more common in developing countries, which experience rapid environmental change as their human populations grow. Some zoonoses, such as rabies and anthrax, occur only when there is transmission directly from animals to humans. However, there is the potential for a shift from animal-to-human to human-to-human disease transmission. The result may be a localised outbreak of disease, such as the periodic emergences of Ebola virus in Zaire/ Democratic Republic of the Congo, or a global spread of epidemic proportions such as the recent outbreak of Severe Acute Respiratory Syndrome (SARS).

In order to better anticipate, contain, and even prevent such outbreaks, it is first necessary to improve our understanding of the basic epidemiology of zoonoses, including the factors that cause new diseases to emerge, and those that cause re-emergence of known diseases. The first step in this process is considering the anthropogenic activities that have been linked with the dramatic increase in incidence and frequency of zoonoses over the past 30 years.

Changes in human population size and density

Pathogens are more likely to occur in populations above a certain density; below this “threshold density,” pathogens cannot survive. Before the Second World War, most human settlements in tropical developing countries were scattered, with few large cities. This pattern has changed over the past decades: areas that previously consisted of scattered settlements are now occupied by large mega-cities surrounded by semi-urban settings, with only small areas of undisturbed forest area remaining near croplands and degraded lands. In 2006, there were 18 mega-cities in the world, cumulatively containing more than 10 million inhabitants. By 2025, Asia alone is predicted to have 10 mega-cities; by 2030, these areas may be home to as many as 2 billion people. Both the size and high density of human populations and their associated domestic animals increases the risk of new disease emergence. These conditions also allow rapidly reproducing pathogens more chances to undergo mutation and develop new traits that will promote survival and infectiousness. Even if there are no immediate outbreaks or emergences of new diseases, pathogens will adapt to conditions within the infected host. Later, under favorable circumstances such as a weakened host immune system, the resident microbes can cause an infection.

Land use and environmental changes

Another consequence of human population growth is an increase in deforestation, the conversion of forested land to non-forested areas such as cropland, plantation and urban habitats. This allows humans to settle in formerly isolated areas rich in previously unknown pathogens. This is probably what led to the spread of human immunodeficiency virus (HIV), which originated as simian immunodeficiency virus (SIV) in chimpanzees.
Deforestation is frequently associated with forest fragmentation, which reduces the number of predators that can occupy the habitat. Without predators to control their population, rodents and biting insects thrive; because these animals can act as reservoirs for human disease, their increase allows zoonoses to flourish. As the movement of humans and wildlife species between remnant forest and human habitation increases, pathogenhost interactions also increase and result in the spread of infections.

Global biosphere and climate change

Anthropogenic changes to the global biosphere include shifts in land and water use, biodiversity loss, and introduction of new chemicals. These processes alter environmental factors such as temperature, humidity levels, and water availability. Disease vectors such as ticks and mosquitoes, which carry disease from one organism to another, are sensitive to such changes in the environment. The resultant fluctuations in vector population can facilitate the emergence of vector-borne zoonoses such as West Nile virus.

Climate change, a phenomenon associated with global biosphere change, is likely to increase populations of vector-borne pathogens in cold regions, which are expected to become warmer. At the same time, it may decrease the transmission of infections in areas that become so warm that vectors are no longer able to survive in high numbers. Climate change is also predicted to change patterns of human activity. For example, continued warming of the Earth’s surface temperature could reduce the quality of pasture lands, causing a decline in livestock numbers and human-animal interactions.

This changing context presents many uncertainties. For example, droughts may decrease mosquito populations and, therefore, the incidence of mosquito-borne diseases; at the same time, the accumulation of dead vegetation might act as a reservoir for other pathogens. The effect of climate change on the spread of zoonotic disease is likely to vary according to geographic location and local habitat.

Human consumption of animals

Recent advances in the way food is produced, processed, and preserved can also play a role in the emergence of zoo-notic disease. One especially influential practice is the use of antimicrobial feeds and drugs. The latter are particularly to blame for an increase in the number of antimicrobial-resistant pathogens that can be transmitted from animals to humans through the food chain. In human Salmonella isolates collected in the United States, for example, resistance to antimicrobial agents rose from 0.4% to 1.0% between 1996 and 2001.

Among animals reared for agricultural purposes, repeated breeding of genetically similar stocks leads to weakened immune systems that leave animals less resistant to infections that may then be transmitted to humans. Further, these animals are often housed and transported in crowded conditions that increase the chances of exposure to, and transmission of, infections.

Another risk factor for cross-species spread of infection is subsistence hunting. The bush-meat trade–the tracking, capture and butchering of animals in the wild, and transportation of meat— brings humans dangerously close to potential vectors and the microbes they carry. Risk of infection is especially high during interactions with non-human primates such as chimpanzees; these close relatives of humans may transmit pathogens such as Ebola virus. The amount of annual wild meat consumption has been calculated to be around one billion kilograms for central African countries alone. In Cameroon, Central, and West Africa, bush-meat hunters and other persons who handle vertebrate pets are at a higher risk of zoonotic transmissions as a result of bites, cuts and exposure to the bodily fluids and tissues of infected animals. Bush-meat hunters are commonly infected by simian foamy virus; luckily, human-to-human transmission of this pathogen has not yet been established.

Zoonotic diseases in developing countries

Zoonoses are most likely to emerge where humans come into close contact with animals. Such encounters are most likely in tropical regions, which are characterised by increasing human population densities and rapid urbanisation. Because of the high number of low-income individuals in these countries, a significant proportion of the population is faced with poor sanitation, substandard housing, inadequate disease control and management, and rapid urbanisation. Globally, over 600 million people are dependent on livestock for their income, and up to 70% of these people live in marginalised developing regions. Two-thirds of the workforce in sub-Saharan Africa and South Asia is involved in agriculture; livestock are vital as a source of both income and food. Unfortunately, they may also be a source of pathogens and, to compound the problem, there are few incentives for farm-level management and control of infections.

Once infected, people in this socioeconomic group often lack access to proper medical care. Health centers are few and far between, and potential patients lack the time and money needed to visit them often. As a result, most zoonotic infections are chronically under-diagnosed. The burden of looking after a seriously ill family member may push the household further into poverty and illness.

Another major challenge associated with disease management in developing countries is the lack sufficient information to make decisions, both at an individual and a national level. In India, for example, around 68% of the national workforce depends on farming, yet most people are unable to tell whether they are working with infected or healthy animals. Because of ineffective data collection and poor disease management practices, there are no data on death rates associated with zoonotic infections across the country. Further, there seems to be a reluctance to recognise that the study and management of zoonoses requires the combined efforts of medical and veterinary professionals, who have, historically, worked in isolation from each other. The transmission of swine flu across the country can be used as an example: Even though many control measures were taken to prevent infections among humans, few or no measures were taken at the veterinary level to prevent infections among livestock. This lack of coordination and information is only exacerbated by widespread illiteracy, poverty and unsafe living conditions.

Learning from the ‘Nipah outbreak’ in Bangladesh

The emergence of new infections and the reemergence of known infectious diseases are both major global concerns, particularly in developing countries that lack adequate medical surveillance, disease management practices, and financial resources. Successful management of zoonoses requires collaborations between experts at the local, national, and global levels, as currently being demonstrated in Bangladesh in association with the emergence of the Nipah virus.

Nipah infections in Bangladesh are very different to the first emergence of this zoonosis in pig farms in Malaysia in 1998, when pigs were exposed to flying fox urine, faeces or saliva carrying Nipah virus. The disease quickly spread to humans throughout Malaysia and Singapore as infected pigs were transported to slaughterhouses. Since 2001, periodic outbreaks of Nipah virus, with approximately 200 human fatalities, have been reported from Bangladesh and northern regions of India; however, these occurrences of zoontoc disease resulted from increased habitat loss which placed humans in closer contact with flying foxes. In Bangladesh, the infections coincide with the date palm sap harvesting season from November to March because the most common transmission pathway for Nipah virus is human consumption of sap contaminated with flying fox saliva and urine.

Date palm sap is collected through a tap or funnel that drains into a clay pot, often left in place overnight and frequently visited by flying foxes that enjoy the sugar-rich sap.The harvester, their families and friends drink the raw sap the next morning. Shields to keep fruit bats away from the sap collection pots are known to local harvesters, but rarely used until scientists from United States Centers for Disease Control and Prevention, and International Centre for Diarrhoeal Disease Research, Bangladesh, determined that homemade skirts covering the sap-producing surface and mouth of the collecting pot prevented most flying fox and bats from contaminating the sap. Community intervention trials are underway to determine if changes in sap harvesting practices can reduce local spillover of Nipah virus from flying foxes to humans, minimising the human-to-human transmission which may occur during the care for an infected patient.

Prediction and prevention of the future zoonotic disease

As human populations grow, and our interactions with the environment change, there is a greater likelihood of emerging disease at the human-animal interface. However, greater awareness and collaboration among doctors, veterinarians, wildlife carers, biologists and communities can identify potential diseases at the source, before there is the potential for diseases to be carried to other regions and have a greater impact on human health and economies.

As shown by the case of Nipah virus in Bangladesh, minimising the risk of zoonoses is best accomplished with the involvement of local people. Global co-operation to support monitoring programs in tropical developing countries, hotspots for disease emergence, and new molecular methods of identification will help to quickly isolate potential new pathogens. Advanced communications technology allows outbreaks to be reported quickly so susceptible communities can be informed of transmission pathways and prevention strategies. Our best weapons against future zoonoses are understanding the origin and dynamics of pathogens in wildlife, reacting quickly to spillover events so that the disease has limited time to be transmitted among the human populations.

Further reading:

Khan SU, ES Gurley, MJ Hossain, N Nahar, MAY Sharker & SP Luby. 2012. A Randomized Controlled Trial of Interventions to Impede Date Palm Sap Contamination by Bats to Prevent Nipah Virus Transmission in Bangladesh. PLoS ONE 7: e42689. doi:10.1371/journal.pone.0042689.

When we think about malaria, we immediately think of human beings—people in the tropics being bitten by mosquitoes, and getting consumed by malaria afterward. We rarely make a mental connection between malaria and birds, yet malaria parasites influence virtually all aspects of their avian hosts’ lives. I have been studying the effects malarial infection can have on bird populations, in susceptible ecosystems like the Hawaii archipelago.
Although the word ‘malaria’ has previously been used to refer to any type of infection caused by a blood parasite, we now use the term commonly to indicate infections originating from the genus Plasmodium. Parasites from both this genus and Haemoproteus are cosmopolitan (except for Antarctica), and have been reported from a broad range of bird species. These parasites are transmitted between hosts through vectors; Plasmodium species use mosquito vectors, whereas Haemoproteus species prefer biting midges from the genus Culicoides (Diptera: Ceratopogonidae) and louse flies (Diptera: Hippoboscidae).

Avian malaria is closely related to human malaria, but unlike the human form, it is not strictly a tropical disease, and is found in many temperate birds. With recent advances in molecular genetics techniques, an astonishing diversity among blood parasites has been revealed–much of which was not evident from morphology alone. In addition, the majority of distinct lineages identified from mitochondrial DNA sequences have been shown to represent reproductively isolated entities–effectively, biological species. It has been suggested that there might be as many lineages of parasites as there are species of birds!

The severity of malarial infections in bird populations depends on whether the birds have encountered the parasite previously during the course of evolutionary history. In island systems like Hawaii, which have been isolated for millions of years, birds have evolved in blissful oblivion, without any exposure to the malarial parasite. However, in areas where malaria is found, like in Asia, some birds have been co-evolving with the parasite.

When malaria reaches where it’s never been before

Islands in the Hawaiian archipelago are a classic example of how biological invasions can have a profound effect on endemic species (those that are found only in one area and nowhere else in the world). These islands have been isolated from the mainland for many millions of years. Geographical isolation and colonisation from the mainland facilitated the evolution of countless unique lifeforms–including, for example, the Hawaiian honeycreepers. The absence of disease-causing agents has been suggested as one of the reasons why such a diversity of life forms is often found on isolated islands. Based on fossil evidence, the Hawaiian Islands were once home to more than 100 endemic species and subspecies of land and water birds.

However, things changed in Hawaii when the Polynesians, and later the Europeans, landed in the late 19th and early 20th centuries. Numerous birds from different continents were introduced to the islands. At least 17 bird species new to Hawaii became established in forest habitats after this initial introduction. The malarial pathogen (Plasmodium relictum capistranoae) was probably present in some of the introduced birds. For forest-dwelling native birds, the accidental introduction of mosquitoes (not to mention additional diseases such as avian pox and avian malaria), have had extremely negative consequences.

Across the mountains of Hawaii, birds, mosquitoes and avian malaria seem to be playing out a predictable drama. At lower elevations, there are many introduced bird species and almost no native Hawaiian bird species. The introduced mosquito, Culex quinquefasciatus, abounds in these areas. The introduced birds, however, are resistant to malaria. Malaria in the low elevations is only found in native Hawaiian birds that have somehow survived the infection–malaria prevalence is very low. As you go higher into the mid-elevation forests, the prevalence of malaria increases in native Hawaiian birds. Even higher up the mountain, abundances of both the mosquito and the Plasmodium decline due to the lower temperatures, and native Hawaiian birds are free to thrive and reach their peak numbers.

Some of the native birds also escape to higher elevations to escape from the parasites. Introduced birds seem to be doing rather well, with no mortality.

Introduced birds seem to be doing rather well, with no mortality. On the other hand, 50-90% of the endemic Hawaiian bird species are dying out. There could be many other factors causing extinctions of these native birds, but avian malaria is believed to be one of the key reasons behind the crash of bird populations in the otherwise very suitable lowland and mid-elevation habitats.

There is an exception to every rule, and this case is no different. In the Hawaii amakihi (Hemignathus virens), a species of Hawaiian honeycreeper, malarial infections affect the survival of adults. However, the disease does not affect reproductive success or prevent populations from growing. Most other native bird species are on the decline in the forests of Hawaii, but the amakihi appears to be evolving tolerance to infection: Lowland populations have rebounded dramatically in recent years.

When malaria gets into an arms race

The effect of malaria is quite different in locations where avian malaria parasites have been living for millions of years. If Hawaii is considered to be one end of the disease spectrum, the Asian mainland— where there is a long history of hosts and parasites co-evolving and engaging in arms races—is an example of a counterpart at the opposite end.

Even in areas like the Western Himalaya, where resident species (non-migrant species) might have been exposed to malaria before, there can be scenarios where the parasite can result in the sudden emergence of disease epidemics. This can happen because a new host (the endemic birds) is exposed to a parasite (the Plasmodium) to which it has no protective immune response; this is similar to what happened in Hawaii. Alternatively, a parasite can gain increased virulence (the power to infect) by various means, like mutations. Or, a change in the environment can affect the equilibrium that was established between the host and parasite over millions of years. For example, a change in climate may result in a longer transmission season to which birds might not be able to adapt quickly enough. New climatic conditions can also result in the spread of the parasites into new habitats where they may encounter new, susceptible hosts.

Hitching a ride with migrating birds

Some birds travel great distances on their migratory journeys, and carry their parasites with them when they head back from their warm wintering grounds. The role of migratory birds in the spread of diseases between regions has been widely documented. However, journeys between different altitudes in the same mountain range, and whether parasites also travel, have not been documented. Migrants move between altitudes or down to the plains, and thereby encounter more diverse faunas of parasites compared to their non-migratory counterparts.

In the plains, the resident birds may act as reservoirs for blood parasites, increasing the risk that migrants will become infected with new parasites on their wintering grounds. Insects are among the groups of organisms most likely to be affected by climate change, because climate has a particularly strong direct influence on their development, reproduction, and survival. Given that suitable vectors are present to transmit and maintain the infection, such migrants can form an effective bridge for parasites between wintering and breeding grounds. If the high altitude avian fauna has evolved in the absence of these blood parasites, their risk of infection is potentially increased.

Studies on human malaria have shown that climate change can alter both where Plasmodium is found, and how much of it is found in different areas. The period when the Plasmodium grows inside the mosquito is very sensitive to temperature; the development of the parasite is completely blocked below 15C. To make the situation even more complicated, the vectors that Plasmodium depends on for transmission are also affected by climate change. As the environment changes, some habitats that are currently too cool to sustain vector populations may become more favourable, while others that are drying may become less favourable for insect breeding. For instance, a small rise in in ambient temperature and rainfall can increase the breeding season of mosquitoes in a particular area. This can increase the time window of malaria transmission, resulting in a larger number of generations of parasites per year.

The Wellcome Trust-DBT India Alliance has funded a study of a possible altitudinal variation in the presence of avian blood parasites transmitted by vectors in the Western Himalayas. The main aim of the project is to study how changes in temperature, the community of insect vectors, the migration patterns of birds, and changes in habitat affect both rates of avian malaria infection, and its spread in high altitude areas that do not currently have malaria. The project focuses on the distribution of both Plasmodium and Haemoproteus blood parasites. It also studies the extent to which these parasites are exchanged between migrating and resident bird populations of Phylloscopus warblers (Leaf warblers) and Parus species (Titmice species) distributed across an altitudinal gradient, and how the vectors that carry these parasites between hosts are expanding to new areas in the Himalayas. The study is challenging because although we know the Western Himalayas are species-rich, the area is also relatively understudied, and there has been no research on the dynamics of the avian diseases and their vectors to date.

Across habitats as diverse as the tropical forests of Hawaii or the snow-capped peaks of the Himalayas, avian malaria parasites are important study systems for testing hypotheses about host-parasite evolution and ecology and the results of these studies have huge conservation implications for a variety of avian species. These findings can also be used to create models of the epidemiology of human malaria. Despite the similarity of disease susceptibility and transmission in humans and birds, birds may be easier to study because they are not subject to the complexities of human socio-economic and cultural patterns. Thus, they provide an excellent system in which to directly determine how ecological changes such as climate change, temperature, vector community, and habitat affect the prevalence and spread of diseases worldwide.

Illustrator: Priya Sebastian

Photoshop image: Gumani
 

Mention “disease” or “death” in a conversation, and the listener will typically cringe, wince, and turn away in disgust. Yet disease and death are part and parcel of life as we know it and play an important role in wildlife conservation, particularly for threatened and endangered species. Like humans, wildlife die from various causes, including infectious disease and non-communicable causes of death such as predation or poisonings.

Take the Laysan duck, for example. It is one of the most critically endangered water birds of the world, found only on the small island of Laysan in the northwestern corner of the Hawaiian archipelago. These ducks forage around a shallow hypersaline lake at the center of the island and raise their ducklings near freshwater seeps around the lake. In 1993-1994, massive duck mortality occurred in conjunction with a drought. The ducks had been killed by a parasitic worm, the quick and widespread transmission of which had been aggravated by the ducks’ dense congregations around scarce sources of fresh water.

Because Laysan was the only location where the ducks existed, this die-off introduced the possibility that a future disease outbreak, in conjunction with some other environmental fluctuation (e.g., storm surges) could wipe out the population completely. To prevent this, 42 ducks were translocated in 2004 from Laysan to Midway Island, a wildlife refuge managed mainly for seabirds, sea turtles and monk seals. In anticipation of the ducks’ arrival, numerous small wetlands were created on Midway. The translocation was a success, and the duck population increased six-fold over the next three years. Unfortunately, about half of the Midway ducks were lost over a two-month period in 2008 because of botulism, a natural toxin produced by bacteria in the newly created wetlands.

Botulism mortality in waterfowl can be effectively reduced with a combination of carcass removal and water management that alters conditions sufficiently to stop toxin production, and Midway has now implemented some of these practices to stem losses from botulism. As a result, in addition to monk seals, sea turtles and seabirds, Midway must now also be managed as a waterfowl refuge.

The forensics of animal deaths

Investigating wildlife mortality is a deductive process. Wildlife health experts and biologists must consider a range of possible causes and, using data from environmental and laboratory observations, systematically and efficiently eliminate these possibilities to arrive at the most likely cause of death. Valuable clues include which species are affected, the extent and timing of the mortality, and whether there have been any changes in behaviour or land use patterns. For example, the deaths of multiple species over a short time period in a localised area might suggest a non-selective agent, such as a toxic spill, rather than an infectious disease that usually targets a given species or group of animals.

Wildlife mortality is driven by three factors: the agent or cause of mortality, the host (animal affected) and the environment in which the agent and host interact. Understanding the interactions between agent, host, and environment is what makes the study of wildlife health so fascinating. To understand how mortality impacts wildlife, you need to know about things like physiology, anatomy, molecular biology, pathology (the study of disease), veterinary medicine, animal behaviour, and animal ecology just to name a few. Clearly, no one person has a grasp of such varying disciplines, so to address such complex issues, wildlife mortality investigations are best done by an interdisciplinary team comprising animal health experts with an appreciation for ecology, and biologists with an appreciation for animal health.

Ask a biologist how his or her wildlife populations are doing, and most will answer in terms of population levels or recruitment rates: If these are stable or increasing, then things are going well. Mortality, a major driver of animal populations, is often explained away as a natural phenomenon that we can do nothing about. Furthermore, many biologists do not have the necessary expertise to investigate animal mortalities or understand why animals die. Cultural norms also play a role –disease and death are not exactly pleasant topics of conversation. As a result, many animal populations are managed in absence of knowledge of the major drivers of mortality. This is unfortunate,because if we know what kills wildlife, we can, in some instances, do things to alleviate or reduce those causes of mortality, thereby aiding recovery of animal populations. Furthermore, an understanding of wildlife health ultimately facilitates an understanding of ecosystem health. Hawaii, for example, has one of the highest numbers of threatened and endangered animals per unit land area in the world; in places like this, it is critical to understand why species are declining.

Wildlife health expertise can sometimes aid biologists in identifying the cause of such declines and aid management to stem such declines.

Laboratory investigations typically begin with a necropsy of dead animals and examination of tissues under the microscope; this guides additional laboratory investigations. For instance, the presence of bacteria in tissues associated with cell death would prompt investigators to order laboratory cultures to identify the bacterium and potential cause of death. Once a cause of death is determined, then the really hard work begins: determining how to mitigate or eliminate this cause to aid recovery of the population. Achieving this requires one to know about how the agent, host, and environment interact and to identify appropriate critical points where an intervention can interrupt the cycle. For example, the discovery that mosquitoes transmitted malaria led to mosquito abatement and use of bed nets to reduce the contact between malaria-infected mosquitoes and humans. In rare cases, vaccines can be used to reduce wildlife diseases; the use of orally delivered rabies vaccines has successfully pushed the virus out of large geographic areas.

Islands are, of course, surrounded by water, and what happens on land will often impact the surrounding ocean. Ecosystem degradation often manifests as the presence of sick or dying wildlife. One example in Hawaii is the turtle tumour disease fibropapillomatosis that has been linked to polluted or degraded marine ecosystems. Researchers suspect that a virus is associated with the tumours, which grow on the eyes, mouth, and skin, and cause turtles to waste away and die. Unfortunately, this disease is difficult to manage at this time because researchers have not yet established an unequivocal link between the virus and tumour development. For this to happen, it will be necessary to culture the virus in a laboratory and then experimentally reproduce the disease in turtles. Unfortunately, growing the virus in the lab has proved elusive. This is one of many examples of the challenges faced by wildlife health professionals who often lack the necessary laboratory tools to investigate disease in the myriad animals they encounter, and who therefore must develop them de novo.

If we do not have the laboratory tools for charismatic megafauna such as turtles, imagine how difficult it is when investigating diseases in less loved life forms, such as molluscs and other invertebrates. For many of these species, we know little about physiology, anatomy, or behaviour. Yet the health of these organisms can often drive the health of entire ecosystems. For example, tropical marine ecosystems are underpinned by tiny animals called corals that form massive reef structures and provide habitat for myriad fish and other invertebrates. By buffeting the effects of storm surges, corals also protect human communities living along the coasts.

Corals are an extreme in wildlife disease ecology, in that the animal is, in essence, the environment. Loss of coral reefs is analogous to loss of rainforests, and in some regions of the world, such as the Caribbean, diseases have decimated coral reefs over the past 30 years. Unfortunately, because biologists and wildlife health experts did not team together to address the problem, we know little about the cause of coral diseases and their declines. In the Pacific Ocean, home to the highest diversity of corals, we are trying to avoid a repetition of this mistake by applying some of the standard biomedical tools we use for other wildlife species to figure out what is killing corals—with the hope that this knowledge will allow us to manage and mitigate the effects of disease on these populations.

As these examples show, the developing field of wildlife health is intellectually exciting, and promises to yield much new information about infectious and non-infectious causes of mortality in terrestrial and marine ecosystems. In this day and age of specialisation, there are few fields that afford the opportunities to work with such a variety of organisms, disciplines, and ecosystems in a truly integrative fashion. Biologists and wildlife health experts working in concert have much to learn and discover as they strive to maintain healthy ecosystems and conserve natural resources and species in an ever-changing world.

If you were asked to tally up all the diseases you’ve ever heard of, chances are that you would think of animal rather than plant infections. Except when they have created widespread problems—think of the potato blight that affected British and Irish farmers in the mid-19th century—plant pathogens have typically been interesting only to the farmers whose livelihoods have depended on quickly recognising, reacting to, and preventing the spread of these diseases. More recently, agriculturalists have been assisted in their efforts by plant geneticists and phytopathologists (researchers who specialise in the field of plant disease) tasked with developing disease-resistant crops and reducing the spread of infection between various plants and fields.

However, despite the efforts of these individuals—not to mention the millions of dollars that the agriculture and horticulture industries have poured into phytopathology research—we still lack a fundamental understanding of plant disease. In some cases we haven’t even identified the agents responsible for certain sicknesses; where these have been found, we don’t always know why they have suddenly become problematic, or how widespread the infection might ultimately become.

One way of predicting where, when and under what conditions plant infections will appear and spread is to examine the characteristics of emerging infectious diseases (EIDs)—those that have recently become more visible to us, either because they are newly evolved or discovered, have changed their method of infection, or are found in higher numbers or over a broader geographical area. An improved understanding of the mechanisms that allowed these pathogens to become so successful could not only have huge agricultural (and therefore economic) implications, but also inform conservation and management decisions relevant to sensitive or endangered wild species.

Emerging infectious diseases in plant
Plants, like animals, can be infected by a variety of microorganisms, such as viruses (the most common type of EID, causing nearly half of infections), fungi, bacteria and nematodes (the least common form of EID, responsible for ~1% of infections). Perhaps counterintuitively, a discussion of the factors responsible for the emergence of phytopathogens is best initiated with a summary of the mechanisms that prevent pathogens from running rampant in the first place. First and foremost among these is the evolution of tolerance or even complete resistance in potential host species. Though pathogens are likely to eventually develop new characteristics that allow them to break through these genetic defenses, mutation and recombination (a process by which DNA is broken and then re-joined in new patterns) both allow plants to adapt to these changing infectious circumstances. Thanks to this ‘arms race,’ neither host nor pathogen is generally ever able to completely gain the upper hand.

Another important characteristic of natural ecosystems is their diversity. Even though a habitat may offer an abundance of a particularly good host, it may also be home to plenty of terrible hosts that represent dead-ends for even the most infectious (transmissible) and virulent (harmful) of pathogens. Likewise, high biodiversity can negatively impact pathogens that rely on ‘vectors’, or organisms that shuttle infectious agents from a reservoir (an organism in which the pathogen is ‘stored’) to a host; where there are many alternative vectors, infectious agents may not end up at their intended destination. An abundance of natural predators and parasites may also waylay pathogens before they are able to infect any hosts. A number of abiotic factors can also keep pathogens in check.

Physical and geographical barriers—even something as simple as a few feet between an infectious host and its uninfected neighbour—can prevent or reduce the spread of disease. Further, changing weather conditions can kill off pathogens that are highly sensitive to temperature and moisture, while a lack of wind or hard rain can prove problematic for microorganisms that rely on these events to create injuries through which they can invade their hosts.

Given these natural checks on pathogen spread, it is not surprising that both habitat disturbances (including those caused by humans) and changes in vector populations have been identified as major players in the emergence of phytopathogens. Recombination can also play a role, since it can—temporarily, at least—allow either plants or pathogens to pull ahead in their evolutionary arms race. Fluctuating weather patterns are thought to be responsible for approximately one-quarter of emergences; many of these variations are likely tied to climate change facilitated by anthropogenic activities.

By far the most important factor, however, is the introduction of non-native species—of both hosts and pathogens. On average, introductions are responsible for just over one-half of all emerging diseases. However, the exact figure varies from one type of pathogen to the next; viruses seem particularly skilled at capitalising on interactions with organisms they have not previously encountered. Whether introductions are accidental or deliberate, things tend to go very badly for plants exposed to pathogens to which they have no innate defense.

The emergence of novel pathogens may also be facilitated by farming methodologies. Particularly problematic is the fact that we tend to grow monocultures comprising plants with a similar genetic makeup. This technique creates huge tracts of land covered by crops frequently lacking the resistance genes needed to combat that next big infection— whatever it might be. Modern farmers also tend to sow seeds fairly close together, thereby increasing the likelihood that infections will spread between grown plants. Recently, there has also been a move towards leaving plant remnants in the field once the harvest has been completed. While this helps enrich the soil, it also facilitates the spread of last year’s diseases to next year’s crops.

Compounding all of these problems is the fact that agricultural efforts have been intensifying in order to satisfy the demands of a growing human population. Given the flexibility of gene transfer amongst many pathogens, there is an almost endless supply of infectious agents available in the environment. Sooner or later, chances are good that we will experience the emergence of an infection that will be the next potato blight or cassava mosaic disease—two epidemics with extreme financial, social, and health repercussions.

Emerging infectious diseases in wild plant

Although the bulk of phytopathogen research to date has focused mainly on domestic species, epidemics can, of course, also occur in wild plants. Detailed studies of native organisms have generally been pursued only in species acting as a reservoir for infections impacting crops or ornamentals. There are, however, two notable exceptions: the American chestnut blight (caused by the fungus Cryphonectria parasitica) and the spread of Dutch elm disease (caused by fungi in the genus Ophiostoma), each of which has been fairly well documented. In both cases, the infectious agents appear to have been introduced into new habitats after hitchhiking on exotic products; C parasitica was hiding in Japanese chestnut trees bound for an American nursery, while the original Ophiostoma species (from which two others eventually evolved) was stowed away in a shipment of lumber.

Anthropogenic activity also appears to be responsible for infections threatening eucalyptus species in Australia and dogwood trees in the United States. In both cases, the pathogens (both fungi) were introduced and spread by humans. Origins of other known plant diseases are more mysterious. The Florida torreya, a conifer native to the northern portion of the US state of Florida, has suffered an extreme population decline likely resulting from one or more fungal infections; it is now considered critically endangered. Researchers are still searching for the pathogen responsible for the severe decline of pondberry, a rare and endangered North American species that had already been hit hard by habitat loss when it also began to succumb to an unknown—probably fungal—infection.

Other recent notable EIDs include ash dieback (caused by the fungus Chalara fraxinea) and sudden oak death (caused by Phytophthora ramorum). The latter of these is only the most recent disease resulting from the activity of a species in the Phytophthora genus; previous victims have been the New Zealand kauri (collar-rot), a variety of ornamental rhododendrons (root rot), beeches (stem and leave rot), and several domesticated species, including strawberries, soybeans, coconuts, and cocoa.

Effects of climate change on phytopathology

One of the biggest questions in contemporary plant phytology is how the spread and emergence of disease are impacted by climate change. Analyses of ancient sediment and ice samples have revealed evidence that both the distribution and prevalence of pathogens have been affected by historical fluctuations in weather and climate patterns. Thus, there is every reason to believe that the high rates at which infectious plant diseases have been emerging over the past several decades may be related, both directly and indirectly, to climate change.

One factor that affects emergence is moisture: fungi and bacteria tend to benefit from increases in humidity and precipitation, while viruses and insect-borne diseases thrive under drier conditions. As certain habitats have become wetter or drier (patterns affected by numerous factors, including topography and proximity to the Equator), local conditions have likely shifted to favor new pathogens. Such shifts are expected to continue— and perhaps become even more common—over the next several decades.

Variations in temperatures and broader weather patterns may also benefit pathogens by altering the distributions and abundances of both vectors and hosts, allowing disease agents to move into new habitats. Some pathogens are free-living, capable of surviving in water or soil for long periods before encountering a suitable host. Even slight variations in environmental conditions can extend the length of time over which these organisms can lie in wait, thus increasing the likelihood that hosts will eventually become infected. Researchers have even suggested that thawing glaciers might release frozen pathogens that could either infect hosts directly or contribute pathogenic genes to other infectious agents in the environment.

Climate also influences host physiology, affecting fundamental processes such as respiration and metabolism. These are characteristics that can impact how easy it is for a pathogen to infect a host, as well as the speed and strength with which an infected individual can mount an immune response to an infection. Animal pathologists have recently identified several systems in which physiological processes likely played an integral role in linking climate change with disease emergence; in all likelihood, an analysis of plant data would yield similar results.

What will happen in the future?

Paolo Bacigalupi’s 2009 award-winning novel The Windup Girl envisions a future where the world has been re-shaped by the activity of phytopathogens; agriculture companies race to develop disease-resistant genetically modified crops, while ‘natural’ plant resources are all but depleted. It is a chilling scene made all the more frightening by the fact that we have already experienced outbreaks and destruction similar to those the author describes. Luckily, there are many ways for us to escape such a future.

Given the influence of introductions on disease emergence, one of the most important tactics will be improving our monitoring systems—especially those associated with the import and export of plants and plant-based products. Many regions and countries have already initiated more stringent procedures in response to outbreaks. For example, flour export is often banned from regions affected by the smut fungus Tilletia indica (the cause of Karnal, or partial bunt), which is so destructive that it is considered a biological weapon.

There are also a number of ways in which farmers could adjust their agricultural practices to reduce the likelihood of disease spread. A greater emphasis might be placed on native, rather than exotic, crop species. Alternatively, crops could be rotated more frequently in order to reduce infection rates (though this tactic would not work as well against pathogens that can infect multiple domestic species). The development of new pesticides and genetically modified crops could also be helpful; however, these techniques must be used carefully, as they could have negative implications for both humans and wildlife, and are currently heavily regulated in many parts of the world.

Seedbanks—stores of seeds from both cultivated and wild species—may also prove useful in preserving biodiversity in the face of pathogenic activity. Seedbanks have two main benefits. First, they can be used to reintroduce plants that can no longer be found growing in the wild. Second, if we preserve a variety of seeds from each species, the bank stocks can be used to reintroduce specific genes—for example, those conferring resistance to a particular infection—that may have vanished from extant populations.

One of the most important weapons against plant epidemics is, of course, knowledge. Further scientific research will be critical in helping us identify, predict, and respond to the activity of phytopathogens. There is growing interest in improving our understanding of plant disease not just in agricultural crops, but also in wild plants. Because mild infections in native species may become widespread outbreaks in agricultural crops—and vice versa—it is vital that we study infections in a broad range of organisms and habitats. It will be equally important to consider what might happen as various disease strains hybridise and produce novel infectious agents.

Finally, we need to elucidate the ways in which specific human activities alter disease dynamics— and how these anthropogenic effects might act in conjunction with each other and other stressors to impact the spread and emergence of phytopathogens. It will be particularly important to model the possible effects of climate change in a variety of scenarios that differ according to level of mitigation; it is unclear how soon or how intensely we will adjust our behaviour to prevent further climatic variation, and so we need to be prepared for a range of potential pathogenic responses.

Unlike other agents of widespread ecological change, we are in the unique position of being cognizant of our own effects on the natural world. We can significantly reduce the likelihood of plant diseases emergence and spread by making informed decisions about farming and gardening practices, shipment of plant materials, travel practices, and land management (among other things). Perhaps the most important goal, however, is education. By raising awareness and fostering an improved understanding of disease dynamics, we can initiate a broader discussion about what we need to do to prevent both domestic and wild plant species from being eradicated by phytopathogens.

Photographs: International Maize and Wheat Improvement Center (CIMMYT), Ronnie Nijboer, Wikimedia
 

Dogs are almost everywhere on this planet. With the exception of Antarctica, this domesticated subspecies of the gray wolf occurs on every continent (Though dogs played an important role in the exploration of Antarctica prior to 1991, they were subsequently banned from the continent due to the potential threat of canine distemper, a dog disease, spreading to Antarctica’s seals). Widely distributed across the rest of the continents, dogs have a staggeringly large global population—estimated at one billion individuals—and have therefore achieved the distinction of being the world’s most abundant carnivore.

Some 58 million of these dogs (~6% of the global dog population) roam the Indian landscape. Dogs are very much a part of the backdrop everywhere in India, so commonplace that they barely warrant a second glance. Dogs occur in cities, towns and villages; around markets, garbage dumps, slaughterhouses and meat shops; outside restaurants and dhabas; on highways and farmlands; and even within protected areas. These dogs are mostly unowned or community owned (‘loosely owned’), and therefore unsupervised, unvaccinated, and freeranging. Such dog populations typically have a high population turnover, mainly due to high rates of both birth and mortality. Further, dog populations in any given landscape form a metapopulation, or a series of interconnected populations between which individuals move freely. These two factors—interconnected populations and high population turnover—allow the persistence and transmission of disease-causing pathogens. Most dog pathogens have a wide host range, meaning they can infect other species as well. For instance, dogs are the known reservoirs of rabies virus which causes fatal disease in all mammals, including humans. More than 50,000 humans die every year due to dog-transmitted rabies.

Threats to wildlife conservation

Dog-transmitted rabies also poses a conservation threat. Introduction of canine rabies resulted in the local extinction of African wild dog populations in the Serengeti-Mara system (Tanzania/ Kenya) in 1989; similar spillover events have resulted in dramatic population declines of the Ethiopian wolf population in the 1990s. Several other multi-host pathogens can also persist in large dog populations. Dogs have been implicated as a source of canine parvovirus (CPV), contributing to gray wolf mortality on Isle Royale, and as a potential source of canine adenovirus (CAV) transmitted to maned wolves in Bolivia.

Canine distemper virus (CDV) has also caused several well-documented epidemics in wild carnivores. The most infamous CDV epidemic occurred in the Serengeti in 1994, wiping out a third of all lions (>1,000 individuals) and many hyenas, leopards and bat-eared foxes. Several other species, including African wild dogs, Caspian sea seals and Lake Baikal seals have also experienced high mortality rates as a result of CDV introduced from dogs. Domestic dogs may be the source of CDV infections that have recently been reported to impact endangered Amur tigers living in the Russian far east. These examples indicate that multi-host pathogens can pose a serious conservation threat when reservoir dog populations occur alongside susceptible populations of wild carnivores.

Much ado about nothing?

In India, several wild carnivore species, including leopards, snow leopards, lions, tigers, wolves, hyenas, jackals and foxes, occur in human-dominated landscapes where dogs are omnipresent. Further, dogs are known to interact with wildlife in myriad ways; for instance, several studies in India have found that dogs are an important component of the diets of leopards. Dogs are also known to attack wild carnivores. Interactions such as chasing, fighting, or feeding events at carcasses are all potential opportunities for pathogen transmission between species. But so far, there has been no dramatic disease outbreak or disease related population declines in wild carnivores in India—or, at least, none has been documented.

The lack of evidence for disease-related population decline in wild carnivores may simply result from the fact that we have not yet looked for it. Unless there are extreme circumstances such as mass die-offs, diseases in free-ranging populations can go completely undetected because of the inherent difficulties of monitoring wild populations. Also, wild animals instinctively mask the symptoms of illness or disease; so a diseased wild animal will appear ‘normal’ to an observer. Further, it is difficult to find carcasses of wild animals quickly enough to assess the cause of their death.

In India, there has not been much research on infectious diseases of wildlife, nor do we have a system of obtaining and analysing surveillance data. This is also true for diseases of dogs: measures of the prevalence of important pathogens in dog populations are virtually lacking. Despite the serious public health threat of rabies in India (one person dies every 30 minutes due to dog-transmitted rabies), the epidemiology of rabies in dog populations has not been properly investigated. Neither do we have any reliable demographic data for dog populations in India.

Disease ecology study in India

The lack of epidemiological and demographic data on the free-ranging dog populations in India is a major impediment to understanding the real public health and conservation threats posed by dog pathogens, in achieving effective disease control, and even in managing dog populations. To address this data void, a pilot study was undertaken around the Great Indian Bustard Wildlife Sanctuary (GIB WLS) at Nannaj (near Solapur) in 2005. The protected grassland patches at Nannaj are surrounded by villages, agricultural fields, communal grazing lands, and forestry plantations. Dogs are ubiquitous in this region, and are free-ranging irrespective of ownership status. Abi Vanak, as a part of his dissertation research, was studying the ecology of Indian foxes in and around GIB WLS ) at Nannaj (near Solapur) in 2005. The protected grassland patches at Nannaj are surrounded by villages, agricultural fields, communal grazing lands, and forestry plantations. Dogs are ubiquitous in this region, and are free-ranging irrespective of ownership status. Abi Vanak, as a part of his dissertation research, was studying the ecology of Indian foxes in and around GIB WLS. Using radiotelemetry, he also studied the activity, movements and interactions of dogs and foxes in this region. Abi and I decided to use this opportunity to obtain baseline disease prevalence data from blood samples (called serologic data) for Indian foxes and free-ranging dogs in the region.

Serologic surveys indicated exposure to viral pathogens in both dog and fox populations. Most of the dogs we tested were exposed to CPV, CDV and CAV, indicating that the pathogens were enzootic (meaning ‘constantly present in animals of a specific region’—the animal version of ‘endemic’) in the dog populations around GIB WLS. The exposure rates in foxes were low compared to those in dogs, indicating the susceptibility of foxes to dog pathogens. The fox serological data also revealed an ongoing CDV epizootic in the fox population (meaning that new cases of CDV in foxes were being recorded). Further, foxes infected with CDV had a high rate of mortality. We tentatively hypothesised that high dog-fox contact rates facilitated the transmission of CDV from dogs to foxes, as the latter species would not have maintained CDV in isolation given its relatively low population density and the apparently high pathogenicity of CDV in foxes. These observations prompted the Maharashtra Forest Department to undertake mass vaccination of dogs in the villages surrounding the GIB WLS as an approach to protecting wild carnivores inhabiting the protected area.

The mass vaccination programs provided an excellent opportunity to further study the disease ecology of free-ranging dogs. I planned my dissertation research around the vaccination campaigns in six villages near the GIB WLS. Long-term serologic data was obtained for the dog populations, along with baseline demographic data. As virtually all the dogs in this region are free-ranging and not habituated to restraint of any sort, a non-invasive method using photographic mark-recapture approach was optimised for estimating dog abundance. Dogs occurred at high densities in the villages around GIB WLS (> 526 dogs per square kilometre); the dog populations were male-biased and comprised mostly adult dogs. The serology data confirmed the previous findings of high exposure rates to the three viral pathogens of interest. An in-depth analysis of the epidemiological data indicated that adult dogs had consistently high exposure rates to these pathogens, indicating that the viruses actively circulate in the dog populations. The high exposure rates of adult dogs also indicated survival following early natural exposure to these pathogens; lifelong immunity results from natural infection with CPV, CDV or CAV. Collectively, the findings suggest that most adult dogs in the study populations are immune to pathogens such as CPV, CDV and CAV, and play no current or future role in the maintenance or transmission of these pathogens.

The vaccination experiment

Vaccination of dog reservoir populations has been recommended as a potential measure that can be used to protect wild carnivores from dog diseases. By vaccinating dogs against pathogens of conservation concern, it is expected that the number of susceptible dogs in the population will be reduced, thereby reducing the occurrence of clinical cases and the likelihood of transmission events between infected dogs and wild carnivores. To determine the extent to which such mass vaccination programs are applicable and practicable for large, free-ranging dog populations, I undertook a village-level vaccination experiment. Dogs from three villages were vaccinated against rabies virus, CAV, CPV and CDV (treatment dogs), while those from three other villages were only vaccinated against rabies virus (control dogs). All dogs in the control and treatment villages were vaccinated against rabies because of the public health risks posed by dog-transmitted rabies in the region. For both the groups, we determined the proportion of dogs with protective antibodies on four occasions over a period of one year.

Vaccination failed to increase the proportion of dogs with protective antibodies against CAV, CPV or CDV in the treatment group compared to the control group, as much of the effort was put into vaccinating dogs that were already antibody-positive by virtue of prior natural exposure to these pathogens. Furthermore, several unvaccinated adult dogs acquired protection against these pathogens during the study. In such situations, vaccination of adult dogs against enzootic viral pathogens seems unnecessary, and would escalate the cost-benefit ratio of dog disease control programs. However, further research on such approaches is necessary. It should be noted, though, that mass vaccination programs will readily work for a pathogen like rabies, as exposure to rabies virus is always fatal and therefore an unvaccinated population consists entirely of susceptible dogs that will benefit from vaccination.

Model explorations

Another important outcome of this work was the realisation that effective management of diseases in free-ranging populations requires a better understanding of pathogen dynamics—specifically, the conditions favouring the persistence and transmission of the pathogens in the system under study. Experiments can be designed to study and unravel these mechanisms, but such an approach would necessitate repeated interventions requiring the capture and handling of a large number of animals. Unfortunately, legal, ethical, and logistic constraints make such interventions impossible when free-living or wildlife species are involved.

In such situations, computational models can be formulated to simulate disease transmission based on the current best understanding of the system. The model can then be used to play out various scenarios under different assumptions, and thereby explore potential disease control strategies. Using data from the ecological and epidemiological studies, I formulated a model of CDV transmission between dogs and foxes in and around the GIB WLS. The model simulated movements of dogs and foxes in the landscape, and the transmission of CDV between infected and susceptible individuals. There were two model outputs: the average number of new CDV cases in the dog population every year, and the number of times CDV was transmitted between dogs and foxes (number of ‘spillover’ events). I then investigated which potential disease control interventions would best mitigate the disease spillover threat in the model fox population.

My results indicated that spillover could be significantly reduced by a reduction in the size of dog populations, as well as by a limitation on the free-roaming tendencies of dogs. Vaccination of dogs against CDV in such settings, however, was ineffective.

Implications for management

Collectively, these findings have important implications for dog disease control programs, especially in settings where dog populations are large and free-ranging, and where pathogens like CPV, CDV and CAV are enzootic. This work underscores the importance of investigating the population pattern of pathogen exposure before considering mass vaccination programs for free-ranging dog populations. Vaccination of local dog populations will be an ineffective disease control strategy in settings where viruses are enzootic in large, free-ranging dog populations. This is an important point to emphasise, given that the National Tiger Conservation Authority has recently recommended vaccination of dogs around protected areas to prevent CDV transmission in tigers (https://projecttiger.nic.in/whtsnew/CVD.pdf). Based on the predictions of my model, disease control programs should also have a strong component of public outreach, emphasizing responsible dog owner-ship. For example, dog birth control programs implemented in and around areas of conservation concern, in combination with restrictions to the movements of dogs in habitats occupied by species of conservation concern, would reduce the disease threat to susceptible wildlife. It is likely that similar efforts in other domestic animal taxa would also be beneficial.

Overall, management of diseases in free-ranging populations is challenging, given the complex ecological and epidemiological interactions of multiple hosts and pathogens. Strategies for investigating and mitigating disease risks to wildlife should be based on scientific evidence obtained using a combination of ecological, epidemiological, and computational studies.

References:

Belsare AV & ME Gompper. 2013. Assessing Demographic and Epidemiologic Parameters of Rural Dog Populations in India During Mass Vaccination Campaigns. Preventive Veterinary Medicine 111, no. 1-2: 139-46.

Gompper ME (Ed.). 2014. Free-Ranging Dogs and Wildlife Conservation. Oxford University Press. New York, USA.

Vanak AT, AV Belsare & ME Gompper. 2007. Survey of disease prevalence in free-ranging domestic dogs and possible spill-over risk for wildlife: A case study from the Great Indian Bustard Sanctuary, Maharashtra,India. The Rufford Small Grants Foundation, UK, 1-13.

“I had had some very good black-buck shooting at Indore in January. Captain Norman Franks, the commissioner there, took me out one morning into the Maharajah Holkar’s preserves, and on a large plain we once saw quite a thousand buck in different herds.” Colonel Cuthbert Larking, Bandobast and Khabar, 1888.

If Colonel Cuthbert Larking were to time travel and today visit the same area around Indore he would be hard pressed to find even a few blackbuck. Indeed, he would barely recognise most of the Central Indian landscape that he, and numerous others, so eloquently wrote about in their travels. The reasons for this decline in blackbuck and of many other grassland species is intrinsically linked to the marginal position that these landscapes have occupied in the developmental and conservation debates in India.

Much has been written about the loss of forest cover in India during the pre- and post-independence era. However, the loss of non-forest habitats has received very little attention. Indeed, successive governments since independence have continued a colonial tradition of defining land use categories based on their “productivity”. Take, for instance, the definition of “wasteland”, first propounded by John Locke in 1680. According to the anthropologist Judy Whitehead, Locke’s “concept of wasteland, as opposed to value-producing land, constituted a founding binary opposition that constructed how landscapes were categorised. Associated with wildness, wilderness, and savagery in the 19th century, the category of wasteland also defined who would and who would not become most vulnerable to dispossession and/or enclosure”.

Thus, common village lands that were used for pastoralism and that were essentially untaxable, were deemed wastelands. These were appropriated by the state and divided amongst the peasantry, because it was assumed that private ownership and intensive cultivation was the only way to make land more productive.

As a result of these myopic and misguided policies, the government has classified large swathes of the country as wastelands. The Wasteland Atlas of India produced at great cost every few years by ISRO(Indian Space Research Organisation) for the Department of Land Resources (Ministry of Rural Development) has some logic-defying categories. Waterlogged areas and marshes, which are known to be essential for groundwater recharge; mountains under permanent snow, the source of our greatest rivers; savanna grasslands and pasturelands, on which depend the lives and livelihoods of millions of livestock and pastoralists; deserts, sand dunes, rocky outcrops, inselbergs, and plateaus, rich geological features that are also home to a unique set of fauna and flora; are all wastelands! According to this atlas, approximately 15% of the country is currently lying waste (that’s 46,000 square kilometres, an area larger than Switzerland).

The idea that wastelands are unproductive continues to be pervasive and is used by various agencies to gain control over marginal landscapes and remake them for productive purposes, with dire results. Jairam Ramesh, as the Minister for Environment and Forests, sought to cordon off large stretches of grassland for a project to reintroduce cheetahs in India.

“It is important to bring the cheetah back as it will help restore the grasslands of India”, he said when approving the plan (The Guardian, 29 July 2010). A change in his ministerial portfolio to Rural Development appears to have necessitated a different strategy that aimed to acquire savanna grasslands and other habitats for development. “Maharashtra, Madhya Pradesh, Rajasthan, Jammu & Kashmir, Andhra, Himachal have significant percentage of wasteland that can be exploited for development purposes” he is reported to have said (Times of India 16 October 2013). Even the benign sounding Integrated Watershed Development Program under his Ministry has destroyed large tracts of semi-arid savanna grasslands in Maharashtra through massive land transformation using heavy machinery to ostensibly improve these wastelands.

Of the various categories of so-called wasteland, savanna grasslands have suffered the most in India both historically and in current times. Under the British, nomadic pastoralists were sedentarised, and the grasslands they depended on were converted to agriculture using canal irrigation. The resultant salinisation of these soils has now well and truly rendered once productive grasslands to wastelands. The Indian forest administration has also carried on the legacy of the British. They assume that forests were the natural vegetative cover in India, and any forest “blanks” were an aberration, or a sign of a degraded ecosystem, and continue to raise tree plantations across the countryside. Indeed, this mistaken notion that equates “eco-friendly” with tree planting has driven India’s green initiatives such as the “Green India Mission”, and the Compensatory Afforestation Programme and Management Authority (CAMPA). Such thinking betrays a certain ecological illiteracy, and ignores the fact that grasslands, and their associated fauna, have existed in India over many millennia. For instance, C3-grasses existed in India as far as 50 million years ago, as evidenced by fossil records; and C4-grasslands may have been widespread on the Indian subcontinent by about 7 million years ago.

The forest-centric bias in policy and management seems to have also clouded the judgment of scientists and cartographers who have continued to label tropical savannas in India as tropical dry forests, or worse, as tropical dry forests degraded by different forms of human use, especially livestock-grazing and fire. Jayashree Ratnam and co-authors, who have studied savannas all over the world, have suggested that in India some “areas that are categorised as tropical dry forests should in fact be considered tropical mesic savannas”. They draw upon studies from other tropical savannas to suggest that the features distinguishing savannas from tropical dry forests are the presence of a C4-grass-dominated understory and a suite of trees uniquely adapted to the occurrence of fires, unlike trees of tropical dry forests.

The contention that savanna grassland systems are unproductive is untenable. The economies of several countries depend heavily on grasslands. Not for a moment would anyone consider labeling the vast savannas of the Serengeti with their spectacular assemblages of large fauna as wastelands, nor the areas inhabited by reindeer herding Lapps in Norway and Sweden. Why then do we in India, with more than 500 million livestock dependent on our grasslands, and millions of pastoralists dependent on them for their livelihoods, consider these areas as wastelands? Previously this categorisation of wastelands was from an agro-centric perspective, i.e., land that did not grow food that could be taxed was land lying waste; in recent times, declaring land as wasted has become the easiest way to grab it in the name of industrialisation and development.

Examples of such appropriation abound: the allocation of approximately 10,000 acres of “kavals” or grazing lands in Karnataka to defence, atomic research and academic institutions and a handful of private companies; the setting up of solar and wind farms for power generation in many parts of the country; and the implementation of Forest Department working plans that promote the planting of Prosopis juliflora for charcoal production as in Kutch, Gujarat.

Correcting historical biases – the way forward?
To bring some balance to this narrative, and to determine the status of savanna grasslands in India, the first author and his team set about mapping the semi-arid regions of peninsular India. This was trickier than anticipated. Unlike forested areas of India, which are easily delineated using even coarse scale satellite imageries, the spectral signature of grasses is easily confused with rainfed agriculture, and horticulture, forestry plantations and isolated trees in agricultural fields are easily confused with woodlands. Thus, multiple methods at multiple scales were needed to classify savanna systems.

The mapping exercise started at a coarse scale with bioclimatic variables and a “greenness index” (NDVI) derived from satellite imageries to build a model of where savanna grasslands “should” be. They then used this potential savanna map to identify areas where a more detailed supervised classification derived from freely available Landsat imageries could be conducted. However, the supervised classification, which consists of using ground truth points to verify maps generated by remote sensing analysis software, yielded results that were less than satisfactory in terms of their accuracy. To resolve this and to generate finescaled maps at district levels, they used 5.6 m resolution imageries from the ISRO’s IRS P4 satellite. This yielded high-resolution maps of semiarid savanna grasslands for the first time in India.

These maps paint a grim picture. Throughout the Central Indian landscape, large contiguous areas of semi-arid savannas are restricted to only a handful of sites spread across Andhra Pradesh, Karnataka, Madhya Pradesh and Maharashtra. These pockets of savanna cover approximately 20,000 square kilometres and constitute between 2 to 11% of the respective states’ geographical area.

Yet, even as surveys of these grasslands were ongoing, vast areas of grasslands continued to be destroyed. Much to the dismay of the survey team, some of the finest grasslands in Maharashtra were being actively worked using heavy machinery under a government-funded scheme to ostensibly prevent soil erosion and run-off. These, and many other such ill-advised schemes are routinely targeted at improving grasslands and other wastelands. The perception of non-forest areas as being wastelands is deep-rooted and changing this perception will require a recognition of three main issues:

1.  Non-forest areas, especially grasslands, marshes and even rocky outcrops and glades are not marginal habitats, but are as important as other forested systems. Indeed many of these habitats not only have unique sets of flora and fauna, but also human livelihood systems that are exquisitely adapted to these systems. For example, savanna grasslands support several endemic and critically endangered species such as the great Indian bustard and blackbuck. They are also home to nomadic pastoralists who have over centuries developed complex rotational grazing systems to prevent over-grazing and take advantage of the seasonally ephemeral resources.
2. The categories of wastelands developed by the government are based on their ‘productive’ potential resulting in the demarcation of these areas for subsequent ‘improvement’. However, this delineation is based on a highly biased, archaic notion of production, often ignoring the cultural, ecological and traditional association of local people with the land. For example, most of the upper reaches of the Himalayas, and almost the entire district of Ladakh are classified as wastelands. The forms of ‘improvement’ that are envisaged for these non-forested wilderness areas conform to ideas of forested, irrigated or industrialised landscapes, and are ecologically ill informed, culturally insensitive and ignore centuries of customary practice.
3. The exercise of wasteland categorisation violates several laws and policies of the government. Several wildlife sanctuaries and national parks (e.g. Kutch wild ass sanctuary, Hemis national park, Rollapadu blackbuck sanctuary) notified under the Wild Life (Protection) Act (1972), wetlandand marshes that are notified RAMSAR sites, sand dunes that protect our coasts from storm surges and are notified under the Coastal Regulation Zone are all labeled as wastelands.
   

There is thus a clear need for a policy shift away from these archaic and colonial categorisations of landscapes, to one that is more in tune with the socio-ecological fabric of our country. One that values land intrinsically, and not just as a means of production from a very narrow economistic perspective. One could argue that the only ‘wastelands’ in the Wasteland Atlas of India are industrial and mining areas. The rich diversity of landscapes in India deserve better than the ignominy of being called wastelands.

Photographs: Kalyan Varma, Abi Tamim Vanak

Walking along a narrow strip of forest and ducking overhanging branches covered in a thick layer of moss, I took a rattling breath that filled my lungs with water droplets. Heading up the misty mountains without adequate warm clothing was not one of my better decisions. As I peered ahead into the lightening gloom, I could see the trees were thinning out. One last duck, and there was the view I wanted: rolling grassland. Kilometres of gently undulating grassy slopes, the occasional lone tree, and forest clumps in the valleys between mountains.

This habitat, called the shola-grassland mosaic, is found on the mountaintops of the Western Ghats of southern India, a mountain range parallel to the west coast of the country. “Shola” is the word for “forest” or “grove” in Tamil, one of the main languages spoken in southern India. The elevation above which this habitat is found varies from as low as 1050 metres to above 1700 metres. This depends on how isolated a particular mountaintop is, and its distance from the coast. The climate in the upper altitudes, and hence the vegetation, is entirely different from what is found in the lower elevations, just a few kilometres down the mountainside. Shola-grassland ecosystems are thus “sky islands”—habitats that include a chain of mountains and valleys, with the mountaintops akin to “islands” of different vegetation in an “ocean” of valleys.

The shola

The forests that grow in clumps in the valleys of the hills have a distinctive appearance: stunted trees of about 16-20 metres in height, close growing in such a manner that the branches of neighbouring trees interlock. These branches are usually laden with epiphytes—plants like orchids and mosses that grow on larger plants—making the shade underneath almost impenetrable.

Trees of the genus Rhododendron are an excellent example of temperate species having established themselves in a tropical mountain. Botanists first encountered one species of Rhododendron in the Western Ghats, one in Sri Lanka, and a burst of about 87 in the Himalayas. The initial guess was that the Western Ghats and Sri Lankan species would be different from the Himalayan species, given the thousands of kilometres that separate them. Recent studies have shown that the Western Ghats species Rhododendron nilagiricum is technically Rhododendron arboretum subsp nilagiricum—a subspecies of R arboretum, a widespread Himalayan species. The tree genus Pedicularis also has many species in the Himalayan meadows, but only two from the Western Ghats sholas— Pedicularis perrotettii and P. zeylanica, as the name indicates, is also found in the sky islands of Sri Lanka.

Dr Meher Homji from the French Institute, Pondicherry, observed something fascinating about these forest clumps. Their interiors contain species that are tropical in origin, i.e. most of their relatives are found in tropical areas, in this case from Western Ghats and Sri Lanka, or the Indo-Malayan region (South-East Asia). These belong to the plant families Lauraceae, Rubiaceae, Symplocaceae and Myrtaceae. Closer to the edge of these forest clumps, in the areas exposed to the surrounding grassland, the species found are not tropical (as one would expect so close to the equator), but temperate in origin.

This fascinating similarity between the sky islands of Western Ghats and Himalayan vegetation, thousands of kilometres away, has intrigued biologists for many decades. Sunder Lal Hora, a fish biologist who was studying fish living in torrential streams, came up with the most influential hypothesis: there was a once continuous corridor of tropical evergreen forests from the Himalayas of Northeast India and the Western Ghats, via the Vindhya and Satpura ranges of Central India. From 2.5 million years ago to about 11,000 years ago during the Quarternary period, the earth as a whole experienced cycles of dry and wet periods; in India especially, evidence shows that certain tracts of northern India were much wetter than they are today. There is also evidence that at around the same time, large tracts of India were much colder than what they are now, allowing some temperate Himalayan species to reach the Western Ghats. Some lived on in the cold shola grasslands; other species that ended up at lower elevations would probably have died out, after India warmed up to how it is now. The Himalayan species could tolerate the ground frost in the open grasslands much better than the “tropical” species that are found inside the shola forests.

The grasslands

Strobilanthes kunthiana, or “neelakurinji” in Tamil, is a strange plant. It grows in large clumps wherever it can, in the grasslands of the sky islands. Once in 12 years, all the plants flower together, set seed and die. When they flower, entire hillsides transform into a blue carpet. This is what prompted the name Nilgiris, or Blue Mountains (“Nil”–blue, “giris”–mountains). When these plants flower, bees and other insects delight in the rich nectar; when the flowers eventually set fruit, they form rice-like seed that makes rats and other rodents go into a feeding frenzy. However, there are so many seeds that enough survive the rodents, and start growing after the next rains. They remain unremarkable, small green bushes until 12 years after, when they flower and transform the mountains again.

The S. kunthiana flowering is a dramatic event, but the grasslands boast of a bewildering variety of plants. For instance, a rapid assessment of the Mukurthi National Park in the Nilgiris range by a team from Gurukula Botanical Sanctuary came up with an astonishing 198 species from just 77 square kilometres. Some species form mats so dense that no ground can be seen; others grow in patches on hilltops, and still others tolerate fire events and sprout back after a shower. Some species colonise marshes, and others grow on seemingly inhospitable vertical rock faces.

The community composition of the grassland was found to be strongly related to environmental and soil factors, like depth of soil, presence or absence of rocks and boulders, grazed and/or burnt conditions, forest-grassland edges and rocky or nonrocky slopes. Like the Himalayan affinity seen among the shola forests, the grasslands have grass and herb genera that are largely found in temperate areas, like Gentiana, Senecio, Rubus, Potentilla and Geranium.

The genus Impatiens, much cherished in gardens as the popular balsams, have about a hundred known species in the Western Ghats. Some balsams seem to grow out of sheer rock, with nothing but the beautiful flower to mark the plant; some are found near streams, some in marshes, and some are small shrubs along the roadside. After being pollinated, the pod like fruit bursts open when ripe, spewing out seeds in a mini explosion that can feel very powerful in the palm of your hand. Now you know why they’re called Impatiens.

The animals

Perched on one such grassland top in Meesapuli malai in Munnar, a friend and I spotted sudden movement on the adjacent mist-covered hilltop. A herd of tahr leapt gracefully across a craggy, impossibly steep slope with all the grace in the world. Somehow, they could sense our eyes on them, though we were separated by a deep valley unsuited for booted humans, but akin to a highway to the agile mountain goat.

The Nilgiri tahr, Niligiritragus hylocrius, is endemic to the sky islands of the Western Ghats. Its nearest relative is away in the Himalayas, adding to the list of interesting relationships between species separated by thousands of kilometres. The Nilgiri tahr is critically endangered now, with isolated populations in the Anamalais and Nilgiris the last stronghold for this iconic species.

Apart from the Tahr, the high mountains are also home to the elusive Nilgiri marten and the critically endangered Nilgiri langur, whose distinctive whooping calls occasionally pierce the silence of the sky islands, rolling in with the mist. On Chemmunji peak in Peppara Wildlife Sanctuary in the South Indian state of Kerala, one is certain to find herds of gaur grazing near the hut that accommodates trekkers, in this area, which is rightly called “Abode of the Gaur”. Tigers and the wild dog, dhole, can also be seen in the sky islands.

Recent research has been proving the existence of species as yet unknown to us from these sky islands. Since each island is separated from others by valleys of unsuitable climate and vegetation, species that cannot move too much, like frogs, become isolated in these islands over millions of years—there is room for many new species to be discovered in this landscape.

The sky island environment

Most rainfall here is from the Indian monsoons. The southwest monsoon between April and September gives variable rain across the sky islands, in some areas as much as 7000 mm. Because of the geographic orientation of the Ghats, the western slopes, rather than the eastern slopes, receive most of the southwest monsoon rainfall. The eastern slopes receive rainfall from the northeast monsoon and from cyclonic storms in the Bay of Bengal.
The soil from the grasslands is calcium-deficient, derived from parent rocks, which are usually gneiss, charnockites and schists. Typically, the soil is shallower in grasslands than in shola forests; this, combined with a lack of shade, makes it more prone to moisture loss. During the dry season, shola soils have been shown to retain about twice as much moisture as that accumulated in the surrounding grasslands.

The shola forests provide cover and reduce erosion of soils under them. The net amount of precipitation under the shola canopy is indiscriminately high—apart from rainfall, the forests also sequester wind-driven fog onto tree crowns. The forests act as sponges that soak up all forms of precipitation, which is then released as mountain streams that coalesce to form the headwaters of all major rivers originating in the Western Ghats.

A dual climax

Analysis of peat samples from shola fragments in the Nilgiris show that shola and grasslands have undergone cyclical shifts in dominant vegetation type. Raman Sukumar and others found that pollen preserved in peat in the high altitude areas of the Nilgiris provided excellent resolution of past climatic events. Grasses dominated 20,000- 16,000 years ago during an arid period. This was followed by a wetter phase, around 12,000 years ago, which ushered in an age where the shola forests were dominant. Around 6000 years ago, the monsoon weakened, resulting in a drier period where grasses dominated once again; this is approximately what we see today.

There have been many theories about why grasslands and forests exist side-by-side in such a manner, over time. Existence of such “alternate stable states” has been shown theoretically using modelling exercises, but not with actual data from field observations, says Mahesh Sankaran from the National Centre for Biological Sciences, who researches grassland-forest dynamics. “Whether or not the shola-grassland mosaic actually represents a dual climax is unknown. Even if there was such a state, whether the factors responsible are fire, or herbivory, or frost, is as yet unknown.”

He further adds, “We must remember that the sholas typically occur in certain kind of areas in this mosaic, like valley depressions and along streams. This raises the question, Do these areas represent a fundamentally different environment from the grasslands? In that case, they probably do not represent ‘alternate’ states. A way to test this would be to prevent all kinds of external forces from acting upon a shola-grassland system, i.e. experimentally change any/all of the suspected triggers—would the grassland switch to a forested state?” Only further research can solve this intriguing puzzle.

People

The first human occupation of the Western Ghats region occurred around 12,000 years ago during the late Paleolithic. The first signs of agri-pastoralism date to around 3000 to 5000 years ago. We don’t know much about the early settlers or their origins. Some studies have speculated that the Harappan people from the ancient Indus Valley Civilisation, which extended from what today is northwestern India, Pakistan and Afghanistan, migrated southward to the hills. Today, we see a variety of tribes, such as the Kani in the southernmost Agastyamalai hills, the Koravas in the Anamalai hills and the Todas and Badagas in the Nilgiris.

The British rule abolished slash-and-burn cultivation, and began large-scale commercial plantations of cash crops, including different species of eucalyptus, acacia and pine across most areas, and tea in the higher elevations. Their idea was to replace what they considered unproductive grasslands, and tracts of slow-growing shola forests, with fast growing, economically useful species. Post-independence, plantation programmes also received national budgetary support, to feed timber and pulp industries. Settlements in the hills have also increased, with fruit orchards and vegetable gardens replacing both shola and grassland.

Collection of small timber from the sholas, destruction of the shola-grassland habitat and an increase in invasive species like Eupatorium glandulosum and Ulex europaeus have together resulted in about 30 grassland species being categorised as endangered in Eravikulam National Park, and about 70 rare or threatened species in the Palanis.

Conservation

The red-disc bush brown is a butterfly species that lives only in the shola-grassland mosaic of southern Western Ghats, and nowhere else in the world. In a recent study, researchers have shown that the butterfly is finding it difficult to navigate the “valley” between two adjoining sky island complexes—the Munnar area to the west of the Ghats and the Kodaikanal area to the east of the Ghats. The approximately 50-kilometres wide “valley” has higher temperatures and lower rainfall than the sky islands on either side.

Across the same landscape, the white-bellied shortwing, a bird found only in the shola forests of the Western Ghats, has been changing the way it sings. Robin Vijayan and his colleagues have been working on this bird for a few years, and they have recorded birds calling from different forest patches. Birdsong is something chicks learn from parent birds. The isolation of birds into their own forest patches is causing them to develop dialects distinct from those in other forest patches; and since birds are not flying between the forests, the different dialects are not mixing, and their songs are growing more and more different from each other.

These studies are just the beginning, indicating the great extent to which disturbance is affecting this fragile, breathtaking habitat. After the centuries old history of intensive management and land use practices, which began during the British rule, and has been continued, we will never really know how they would have been in all their glory. Travelling in Munnar and Kodaikanal during the last mass flowering of Strobilanthes kunthiana in 2006, I could see isolated patches of blue. Traditionally, the bush would have covered the hillside forming continuous blue carpets. Now invasive bushes like bracken have taken over the space that S. kunthiana would have occupied, making them a figment of my imagination, brought to life after reading descriptions, some as old as ancient Tamil literature. Judging from these sources—and the fact that the entire Nilgiris was named after the blue buds of a single flowering bush—the unspoiled mountains must have been something remarkable. Whether the next generation even sees a fraction of the sky islands’ isolated beauty is truly in our hands.

Further reading:

Bunyan M, S Bardhan & S Jose. 2012. The Shola (Tropical Montane Forest)-Grassland Ecosystem Mosaic of Peninsular India: A Review. American Journal of Plant Sciences, 3, 1632-1639.

Sukumar R, R Ramesh, RK Pant & G Rajagopalan. 1993. A δ13C record of late Quaternary climate change from tropical peats in southern India. Nature, 364: 703-706.

Photographs: Ullasa Kodandaramaiah, Kalyan Varma, Kartik Shanker