Background: Biodiversity and human health are intimately linked to each other, human beings are an integral and inseparable part of the natural ecosystem as human health depends ultimately on the health of its species. Human interference with biodiversity affects ecosystem both structurally and functionally, consequently biodiversity is continuously declining globally. Objective: The objective of this study is to understand the effect of biodiversity loss on dynamics of infectious disease transmission and its impact on the magnitude and impact of epidemics. Methods: This is a literature review. Discussion: Correlation has been observed between decrease in disease frequency with increase in biodiversity. A region rich in diversity of species of vertebrates has protective effect against vulnerability of Infectious diseases especially Vector-borne zoonotic diseases. This phenomenon in nature is known as Dilution effect. Biodiversity in host can either lead to amplification or buffering of epidemics. Dilution effect lowers the incidence of the disease among humans while the richness of biodiversity reduces the prevalence of directly transmitted diseases leading to buffering effect. Fragmentation of natural habitat leads to lowered biodiversity leads to higher risk of exposure to diseases. Conclusion: While some human health effects due to biodiversity loss may be direct and easily perceptible while others are indirect may not be appreciated currently. According to the World Health Organization, the adverse health effects brought in by loss of biodiversity far exceeds dangers of implication of climate change to human health. Health professionals should advocate for the preservation of biodiversity as it has a powerful impact on frequency of disease transmission in the community.
Keywords: Biodiversity, climate change, dilution effect, epidemics, zoonosis
|How to cite this article:
Patil RR, Kumar C, Bagvandas M. Biodiversity loss: Public health risk of disease spread and epidemics. Ann Trop Med Public Health 2017;10:1432-8
|How to cite this URL:
Patil RR, Kumar C, Bagvandas M. Biodiversity loss: Public health risk of disease spread and epidemics. Ann Trop Med Public Health [serial online] 2017 [cited 2020 Mar 24];10:1432-8. Available from: http://www.atmph.org/text.asp?2017/10/6/1432/222642
World Health Organization (WHO) defines Biodiversity as the variety of life on earth that defines life on Earth and has reference to the variety found in biota from the genetic makeup of plants and animals to cultural diversity. The importance of Biodiversity for human sustainance is undervalued. Human interference with biodiversity affects ecosystem both structurally and functionally, consequently biodiversity is continuously declining globally, throughout the world species are being lost at alarming rate to the tune of 100–1000 times faster than the natural extinction rate. WHO has in recent years has paid close attention to the association between biodiversity and human health because changes in biodiversity will invariably have impact on human health. Human life is dependent on the services and products provided by the ecosystem which includes fresh air, potable water, and energy source. Loss of biodiversity can adversely affect these services and products of ecosystems leading to depletion of resource which may be totally inadequate to address the social requirements. The intricacies biodiversity and human health are intertwined because man is part of ecological systems which is made up of diverse species of flora and fauna. It is emphasized that different units of ecosystem are not only interconnected but also interdependent. Every human action that alters the ecological balance and put fellow species to risk of extinction will have direct bearing on human health., While some human health effects due to biodiversity loss may be direct and easily perceptible, others are indirect may not be appreciated currently. One of the direct adverse health effects due to biodiversity disturbance is evidenced through its influence on communicable disease epidemiology which is highly sensitive to ecological alteration. It must be stressed that the correlation between biodiversity and human health is not simple and linear.
Since biodiversity is fundamental in supporting human life and health, there have been many international initiatives in tackling the biodiversity crisis on a global level. The convention on biological diversity, treaty was adopted at Earth Summit in Rio de Janeiro and came into force 1993. The Nagoya Protocol on Access to Genetic Resources and the Fair and Equitable Sharing of Benefits of biodiversity was adopted in 2010 Aichi Province, Japan. The “Intergovernmental Platform on Biodiversity and Ecosystem Services” (IPBES) was established in April 2012 which is an equivalent to the UN intergovernmental panel on climate change. The work program for 2014–2018 is being developed by the IPBES for strengthening the science-policy interface for biodiversity and ecosystem services for the conservation and sustainable use of biodiversity, long-term human well-being and sustainable development. Keeping with gravity of the current situation, UN has declared 2011–2020 as the United nation decade on Biodiversity.
|Biodiversity Disturbance and Increased Disease Risk|
Human encroachment into natural ecosystems is causing biodiversity degradation in newer areas. Human beings are an integral and inseparable part of the natural world, human health depends ultimately on the health of its species and on the natural functioning of its ecosystems. Disturbance of natural habitat alters the biodiversity of the region both structurally and functionally. Such alteration of ecosystem leads to reduction of abundances of some of organisms while causing increase in population of others. Change in the flora and fauna of a given region leads to modification of interaction among the biota which in turn lead to altered relationship between the organisms and their physical environments. The cumulative effects of all such changes leads to diseases transmission dynamics in the given region ,
Ever increasing population and unplanned development are leading to encroachment of natural habitats of ecosystem which is deleteriously affecting well-being of wildlife species. Increased proximity between human settlement and wildlife is leading increasing rates of disease transmission between domestic animals and wildlife. Alteration of natural habitat by man is leading to increase in the risk of epidemic which can be evidenced through reports of nepah and hendra viral outbreaks. Such outbreaks are attributed to destruction of forests that have adversely affected the roosting site for fruit bat species which is the reservoir for these pathogens. Consequently, fruit bats have shifted to the fruit trees in human settlements thereby increasing the contacts between human and bats leading to the disease outbreaks.,
Biodiversity can be described in terms of species richness and species evenness. Species richness provides representation of diversity in number of species, and species evenness represents proportional representation of each species. With reference to disease transmission dynamics, species evenness would be an important factor as it provides total distribution of opportunities for vectors to feed from each host. It is now established fact that fragmentation of habitat leads to lowered biodiversity within host communities which in turn leads to higher risk of exposure to diseases due to increase in both absolute and relative density of host population within disturbed habitat. Conceptually, this very same logic can be extrapolated to different vector-borne diseases, for example, plague, cutaneous leishmaniasis, babesiosis, human granulocytic ehrlichiosis, Chagas disease, relapsing fever, tularemia, Crimean Congo hemorrhagic fever, and LaCrosse virus.
|Biodiversity and Epidemics Relation|
Human Colonization has resulted in increase in regional and global biogeopgraphical homogeneity as consequence of introduction on plants and animals that are not native to a given region., Widespread human infringement and introduction of foreign species into new ecosystems have been termed as biological pollution. Introduction of nonnative pathogen in new regions that are predomi69 + natantly are anthropogenic in nature is known as pathogen pollution and has been major reason for loss of biodiversity and emergence of new diseases. A decreased number of competing species may allow the abundance of other species to increase, facilitating the spread of diseases of those species.
Historically, it was observed that widespread human movement across different continents following military invasion or for the reason of trade and commerce during early fifteenth century have led to introduction of highly infectious diseases such as measles, smallpox, or plague from one continent to another. Introduction of new diseases into newer areas have caused disease outbreaks in the immunologically naive population that had no previous history of contact with the pathogen resulting in devastating epidemics and catastrophic loss of human lives. Many regions have experienced what is termed as “ first contact” depopulation following ravaging epidemics.
Human mediated pathogenic pollution is a major threat to global diversity apart from the potential of depopulation in newly invaded regions. While, depopulation may be the acute manifestation following an epidemic, over the period of time the same disease stabilizes in the new population and become endemic in the region. Continued presence of disease in the population leads to chronic population depression which could progressively lead to local extinction if the threshold of host density for the disease infection transmission in reduced. Pathogen pollution in a given region may have adverse impact on man as a result of being direct victim of infection or indirect victim, if it affects livestock on which human depends economically thereby affecting human health indirectly.
Biodiversity has great influence on magnitude and impact of epidemics. Correlation has been observed between decrease in disease frequency with increase in host diversity This phenomenon in the nature is termed as dilution effect exerted by species-rich environment on epidemic potential of the disease. The presence of incompetent reservoir hosts dilutes rates of infection transmission between vector and competent hosts. The concept of dilution effect illustrates that the rates of infection among the vectors, and hence, the consequently risk of infection among human will be reduced in the host communities that are rich in species diversity. Dilution effect helps in reduction of exposure risk to zoonotic diseases. Diversity in animals bring down probability of disease and its transmission to humans.
|Lyme Disease as a Demonstration for Dilution Effect|
Lyme disease is a vector-borne zoonotic disease transmitted by ticks from white-footed mice to humans. These white-footed mice are found in varied habitats and can survive wide range of feeds hence are found plenty endemic regions. As a result of their widespread distribution, these mice are found in both species-rich and species-poor habitats. Consequently, species-poor region will show higher proportion of white-footed mice resulting in greater contact between tick and white-footed mouse. Ticks take on major portion of their blood meals from these mice and invariably show higher prevalence of infection in the tick population. Addition of new species to the host community will dilute the presence of white-footed mice. They also provide alternate source for blood meals from these additional species which are incompetent reservoir. Blood meal diversion from the mice to alternative hosts as a source, results into lower infection prevalence in ticks resulting in lower incidence of Lyme disease in humans. Similar effect can also be witnessed if there is reduction in density of white-footed mice while other alternative hosts densities remain constant or increase.
Any factor that leads to reduction of representation of white-footed mice relative to other invertebrate host community would in effect reduce the proportion of infected ticks carrying lyme disease. This can result from two situations either when there is reduction in abundance of white-footed mice while retaining alternative host species. Alternative situation would be when there is increase in the frequency of alternative incompetent reservoir of infection.
A region rich in diversity of species of vertebrates has protective effect against vulnerability of human vector-borne communicable diseases. Infection reduction in vector is brought about by lowering the probability of uninfected vector to feed on alternative to competent host. Ecological demonstration of correlation between higher occurrence of species diversity within small mammals and lower Lyme disease incidence in humans is well document.,
|Frequency Dependent-Density Dependent Coexistance and Extinction|
The reduction in the incidence of diseases can be brought about by two modes. The first mode could be through density-dependent dilution where increase in species richness is accompanied by corresponding decrease in abundance of individuals in species. The second mode is through frequency-dependent dilution where increase in species richness in itself brings about decrease in the incidence of disease. It would occur even if addition of species leads to increase absolute number of individual in the community. Disease dynamics is most frequently influenced by the frequency (proportion) of population of infected individuals in the population.
Density-dependent disease transmission increases the frequency of contacts between infected individuals and potential susceptible hosts. In frequency, dependent disease dynamics increases the inter-specific transmission consequently reducing the within-species diseases transmission.
Host species diversity can either lead to amplification or buffering of epidemics. The density-dependent transmission will flare up epidemics, especially in case of pathogen-transmitted aerial route. Frequency-dependent transmission or vector-mediated infection will buffer the epidemic. When infection transmission is considerably high between species (interspecies) but lesser than within species (intraspecies) transmission then pathogen-hosts demonstrate stable dynamics leading to persistence of pathogen.
|West Nile Virus Disease as an Demonstration of Dilution Effect|
Dilution effect is also demonstrated in West Nile Virus (WNV) another mosquito-borne disease in which primary reservoir is wild birds. Human beings are infected with WNV following epizootic in birds and mosquitoes leading to spill over of infection to humans who are incidental host. While, there are multiple hosts for WNV, but passerine birds are the most competent. Nonpasserine birds although do get infected with WNV, however, are comparatively incompetent hosts. In the context of the dilution effect, these nonpasserine birds provide the alternative blood meals to the mosquito, hence, reducing the probability of contact between the mosquitoes and passerine birds leading to lesser infection in the competent host. Since nonpasserine is incompetent host will find it difficult to maintain epizootic in bird population as a result vector get less infected leading to lesser infection transmission among humans due to increased biodiversity among nonpasserine birds.,
Apart from passerine birds, horses, crows, and crocodilians can be alternative host to WNV. Fortunately, human is only incidental hosts who is incapable of transmitting infection back to mosquitoes, hence, do not pose any threat to other hosts, in epidemiological terms, they exert zero force of infection on other hosts. Crows also can get infected but mortality among infected crows is unusually high  because of very short survival time following the infection; hence, they too exert very low force of infection to other hosts. In stark comparison passerine birds, house sparrows show very low pathogenicity of WNV infection but are capable of transmitting infection back to mosquitoes. In epidemiological dynamics, abundance of house sparrows and their lower resistance to infection and their higher survival rate exert major force of infection and is ideal for maintaining continued disease transmission, thereby exerting higher force of infection on other species.
|Effect of Biodiversity on Amplification and Buffering Effect on Epidemics|
Basic reproductive number (R0) of an infecting orgnanism is the primary determinant of extent to which it can infect the host species. Biodiversity changes that affect the host diversity will influence R0 which in turn will have bearing on the potential for outbreaks. Increase in the host diversity has direct effect on the intensity of within and between species transmission.
In density-dependent transmission, increase in species diversity leads to larger magnitude of R0 and hence greater risk of disease outbreaks because of increased number of contacts between infected individual and potential hosts. The risk is particularly high when rates of between species transmission approach close to within-species transmission. In contrast, transmissions with frequency dependent dynamics increase inter-species transmission leading to decrease in within-species transmission. This decrease tends to buffer the potential for outbreak due to increased diversity of host lowering the magnitude of R0.
When richness of biodiversity reduces the prevalence of directly transmitted diseases this phenomenon is called Buffering effect. While, dilution effect is the effect biodiversity on the incidence of the disease, similar effect that lowers the prevalence of disease is buffering effect. Lower prevalence of hantavirus infection in panama is hyptothesized to be due to the presence of closer interaction with multiple species which lead to regulation of abundance of pathogen host. Buffering effect was demonstrated by experimental removal of species leading to increase in prevalence of hantavirus. Regions rich in biodiversity of species have reduced densities hantavirus host and thus overall lower disease prevalence. The reverse is true for regions with lower biodiversity.
Within the infection cycle, pathogen that show tendencies to infect multiple hosts, infection transmission is determined by the magnitude in terms of relative size host within the species and between the species. Significant intraspecies transmission promotes pathogen transmission, when intraspecies transmission increases to the level of interspecies transmission then one of the species may risk extinction compared to species that are able to recover from epidemic. Apart from the Lyme disease and West Nile virus infection discussed in the paper, recent evidence do support dilution effect by demonstrating higher species richness brings down the prevalence of flea-borne rodent bacterial infection.
|Biodiversity and Reservoir Distribution|
Macroparasite distribution in a host population is determined by multiple factors of positive and negative density-dependent process. It is observed that parasite is concentrated in small proportion host population when there is overdispersion of parasites. Thus, it can be inferred that overdispersion of parasites is driven by positive density-dependent process whereas underdispersion of parasite population is driven by negative density-dependent process. Negative density-dependent process is more dominant and parasite distribution in the host population tend to become less dispersed.
Any public health intervention that brings down the parasite burden will invariably cause parasite distribution to become overdispersed. This is evidenced by the time series data on Onchocerciasis infection wherein the decade-long vector control activity reduced the parasite burden resulting in over-dispersed distribution.
Within the infection cycle, pathogen that shows tendencies to infect multiple hosts, infection transmission is determined by the magnitude in terms of relative size host within the species and between the species. Significant intraspecies transmission promotes pathogen transmission, when intraspecies transmission increases to the level of interspecies transmission then one of the species may risk extinction compared to species that is able to recover from epidemic.
|Effect of Climate Change on Biodiversity and Disease Transmission|
Climate change has a great influence on dynamics of disease transmission which is being evidenced by expansion tropical diseases into temperate zones. Expansion of vector-borne diseases is brought about by changes in temperature and humidity which are predominant factors in influencing breeding and survival of vectors. Patten of rainfall and spell of dry seasons that a region experiences and the intervals between the seasons influence the rate at with mosquitoes take blood meals from the hosts, incubation periods of parasites in vectors, and rates of infection transmission ,
Nature and types of water bodies is determined by soil type and elevation of a given region. In general, any forest floor in its natural setting will be over shaded and covered with thick layer of decomposing matter that has tendency to absorb water and tend to be more acidic. Deforested lands obviously are more sunlit due to loss of forest canopy and encourage puddle formation with pH of water content tends to more be netural, making it less acidic which in turn makes it conducive for breeding of anopheline vectors. Apart from mosquito, other fresh water vectors such as snail also prosper when the water in the puddles of deforested get less acidic and tend toward neutral side thereby increasing the risk of disease transmission by snails, for example, Schistosomiasis.
The ongoing climate change will push infection presently confined to tropical will expand into temperate regions., When pathogen move from tropical to temperate zone, it will encounter completely new ecosystem that of highly diverse host community to lesser biodiverse environment. Frequency-dependent dynamics in the new areas will have huge impact on susceptible host in the temperate region due to reduced choice of alternative host. Due to lack of biodiversity and reduced alternative source for blood meals, vector tends to concentrate on humans hence force of infection on humans will be highest. The adverse health effects brought in by loss of biodiversity far exceed dangers of implication of climate change to human health.
It is predicted that spatial patterns of biodiversity degradation is ultimately determined by overpopulation and increased scarcity of natural resources to support the growing human population leading to rate of species loss that is unparalleled in the history of humankind also termed as 6th mass extinction. It has been estimated that there have been at least five mass extinctions in the history of our planet earth. The most recent extinction being of dinosaurs around 65 million years back. In the past species, extinction was brought on by changes in environment such as extreme climate events or huge asteroids collision and major volcanism. The present ongoing mass extinction is termed as 6th mass extinction is being largely driven by the furious completion due to anthropogenic factors such as over overpopulation, felling of trees, destruction of forest for increased agricultural activities, overfishing, pollution, etc., leading to rapid decline and degradation of natural habitats for many species. The degraded habitats makes species highly vulnerable to the adverse impact by the ongoing climate change which results in disproportional impact on ecosystems that are highly fragmented.
Forest encroachment by human population and destruction natural habitat have resulted into increase in the density of wildlife emerging infectious diseases., Movement of livestock internationally and adoption of mechanized agricultural practices have contributed to outbreak of recently reported Bovine Spongiform encephalitis. Changes in farming practices such as arable farming and shifting agriculture have tremendous the influence of biodiversity. Changes in dynamics of disease result from changes in the host ecology, or ecology of disease agent. Due to unregulated growth and expansion of human population has resulted in increase in density in urban population resulting in spiking of vector- and water-bone disease. Various models of transmission dynamics of disease point to the fact that the richness in biodiversity lowers overall prevalence of disease in different infection transmission cycles of other diseases.
Public Health approach to control of pandemic diseases may pose a unique challenge in the control of zoonotic diseases in the context of biodiversity conservation, for example, culling of birds or targeting certain wildlife may pose challenge to spirit of biodiversity conservation. While the public health approach of targeting the reservoir of infection involve culling certain species of wildlife. The logic of interrupting chain of infection, thereby protecting human from the risk of exposure to new emerging disease takes higher priority than conservation of biodiversity, hence may be justified.
Dynamics of infection should not be viewed in narrow and simplistic paradigm of the source of infection and target of infection as if other species are nonplayers in infection dynamics. On the contrary, it is the interplay between varied network of different species within a given habitat where change in one species influences the disease dynamics in other species. Changes in biodiversity have led to enormous changes in distribution and dynamics of pathogens, vectors, and their respective hosts. Public health professionals should advocate for the preservation of biodiversity as it has a powerful impact on the frequency of disease transmission in the community. The link between biodiversity and human health needs to be further investigated and continuously monitored. It will take interdisciplinary collaboration among the experts in public health, biological sciences, microbiologists, ecologists, and veterinarians to unravel the effects of loss of biodiversity.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
What is known
- Biodiversity and Human health are intimately linked to each other; human beings are an integral and inseparable part of the natural ecosystem as human health depends ultimately on the health of its species
- Human interference with biodiversity affects ecosystem both structurally and functionally, consequently biodiversity is continuously declining globally
- A region rich in diversity of species of vertebrates has protective effect against vulnerability of infectious diseases, especially Vector-borne zoonotic diseases.
What this paper adds
- Effect of Biodiversity loss on dynamics of infectious disease transmission and its impact on the magnitude and impact of epidemics
- Advocacy for the preservation of biodiversity by showing powerful impact of biodiversity on frequency of disease transmission in the community.
Pimm SL, Russell GJ, Gittleman JL, Brooks TM. The future Science. 1995;269:347-50.
WHO. Ecosystems and Human Well-Being: Health Synthesis. Millennium Ecosystem Assessment. Washington, DC: World Resources Institute; 2005.
José Sarukhán Anne MA. Ecosystems and Human Well-Being: Biodiversity Synthesis. Millennium Ecosystem Assessment. Washington, DC: World Resources Institute; 2005.
Chivian E, Bernstein A. Sustaining Life: How Human Health Depends on Biodiversity. New York: Oxford University Press; 2008. p. 568.
Chivian E. Biodiversity: Its Importance to Human Health Center for Health and the Global Environment. Cambridge, MA: © 2002 Center for Health and the Global Environment Harvard Medical School 2003 2nd printing;2002.
Text of the Nagoya Protocol. Convention on Biological Diversity. Available from: http://www.cbd.int. [Last accessed on 2017 Oct 17].
IPBES 2013 Intercessional Process. IPBES Programme Draft for Review. Available from: http://www.ipbes.net. [Last accessed on 2017 Oct 17].
United Nation Decade on Biodiversity 2011-2020. Available from: http://www.cbd.int/2011-2020/. [Last accessed on 2017 Oct 17].
Gómez A, Nichols E. Biodiversity Conservation and Human Health. Lessons in Conservation; 2010. Available from: http://www.ncep.amnh.org/linc. [Last accessed on 2017 Oct 17].
Murray K, Selleck P, Hooper P, Hyatt A, Gould A, Gleeson L, et al. A morbillivirus that caused fatal disease in horses and humans. Science 1995;268:94-7.
Osofsky SA, Karesh WB, Deem SL. Conservation medicine: A veterinary perspective. Conserv Biol 2000;14:336-7.
Ostfeld RS, Keesing F. The function of biodiversity in the ecology of vector-borne zoonotic diseases. Can J Zool 2000;78:2061-78.
Van Buskirk J, Ostfeld RS. Controlling Lyme disease by modifying the density and species composition of tick hosts. Ecol Appl 1995;5:1133-40.
Pimm SL, Russell GJ, Gittleman JL, Brooks TM. The futureScience 1995;269:347-50.
Steadman DW. Prehistoric extinctions of pacific island birds: Biodiversity meets zooarchaeology. Science 1995;267:1123-31.
Stuart Chapin III F, Walker BH, Hobbs RJ, Hooper DU, Lawton JH, Sala OE, et al. Biotic control over the functioning of ecosystems. Science 1997;277:500-4.
Durrell L. Biodiversity and Conservation 1998;7:841. Available from: https://doi.org/10.1023/A:1008955319736. [Last accessed on 2017 Mar 03].
Daszak P, Cunningham AA, Hyatt AD. Emerging infectious diseases of wildlife – Threats to biodiversity and human health. Science 2000;287:443-9.
Schmidt KA, Ostfeld RS. Biodiversity and the dilution effect in disease ecology. Ecology 2001;82:609-19.
Mitchell CE, Tilman D, Groth JV. Effects of grassland plant species diversity, abundance, and composition on foliar fungal disease. Ecology 2002;83:1713-26.
Ostfeld RS, Keesing F. Biodiversity and disease risk: The case of Lyme disease. Conserv Biol 2000;14:722-8.
Matuschka FR, Fischer P, Musgrave K, Richter D, Spielman A. Hosts on which nymphal ixodes ricinus most abundantly feed. Am J Trop Med Hyg 1991;44:100-7.
Van Buskirk J, Ostfeld RS. Habitat heterogeneity dispersal, and local risk of exposure to Lyme disease. Ecol Appl 1998;8:365-78.
Rudolf VH, Antonovics J. Species coexistence and pathogens with frequency-dependent transmission. Am Nat 2005;166:112-8.
LoGiudice K, Ostfeld RS, Schmidt KA, Keesing F. The ecology of infectious disease: Effects of host diversity and community composition on Lyme disease risk. Proc Natl Acad Sci U S A 2003;100:567-71.
Bernard KA, Maffei JG, Jones SA, Kauffman EB, Ebel G, Dupuis AP 2nd, et al. West Nile virus infection in birds and mosquitoes, New York State, 2000. Emerg Infect Dis 2001;7:679-85.
Ezenwa VO, Godsey MS, King RJ, Guptill SC. Avian diversity and West Nile virus: Testing associations between biodiversity and infectious disease risk. Proc Biol Sci 2006;273:109-17.
Campbell GL, Marfin AA, Lanciotti RS, Gubler DJ. West Nile virus. Lancet Infect Dis 2002;2:519-29.
Anderson JF, Andreadis TG, Vossbrinck CR, Tirrell S, Wakem EM, French RA, et al. Isolation of West Nile virus from mosquitoes, crows, and a Cooper’s hawk in Connecticut. Science 1999;286:2331-3.
Hayes CG. West Nile fever. In: Monath TP, editor. Arboviruses: Epidemiology and Ecology. Boca Raton: CRC Press; 1989. p. 59-88.
Dobson A. Population dynamics of pathogens with multiple host species. Am Nat 2004;164 Suppl 5:S64-78.
Dublin HT, Sinclair AR, Boutin S, Anderson E, Jago M, Arcese P, et al. Does competition regulate ungulate populations? Further evidence from Serengeti, Tanzania. Oecologia 1990;82:283-8.
Telfer S, Bown KJ, Sekules R, Begon M, Hayden T, Birtles R, et al. Disruption of a host-parasite system following the introduction of an exotic host species. Parasitology 2005;130:661-8.
Anderson RM, Gordon DM. Processes influencing the distribution of parasite numbers within host populations with special emphasis on parasite-induced host mortalities. Parasitology 1982;85 (Pt 2):373-98.
Plaisier AP, van Oortmarssen GJ, Habbema JD, Remme J, Alley ES. ONCHOSIM: A model and computer simulation program for the transmission and control of onchocerciasis. Comput Methods Programs Biomed 1990;31:43-56.
Sutherst RW. Arthropods as disease vectors in a changing environment. Environmental Change and Human Health. Chichester: Wiley; 1993. p. 124-45.
Dobson AP, Carper ER. Health and climate change: Biodiversity. Lancet 1993;342:1096-9.
Dobson AP, Kutz S, Pascual M, Winfree R. Pathogens and parasites in a changing world. In: Lovejoy T, Posey DA, editors. Climate Change and Biodiversity: Synergistic Impacts. Advances Inapplied Biodiversity Sciences. Vol. 4. New Haven, Conn: Yale University Press; 2003. p. 14-26.
Southgate VR. Schistosomiasis in the Senegal River Basin: Before and after the construction of the dams at Diama, Senegal and Manantali, Mali and future prospects. J Helminthol 1997;71:125-32.
Pounds JA, Fogden MP, Campbell JH. Biological response to climate change on a tropical mountain. Nature 1999;398:611-5.
Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, et al. Climate warming and disease risks for terrestrial and marine biota. Science 2002;296:2158-62.
Nabhan GP, Buchmann SL. Services provided by pollinators. In: Daily G, editor. Nature’s Services: Societal Dependence on Natural Ecosystems. Ch. 8. Washingtodn DC: Island Press; 1997. p. 133-50.
Fidler DP. Globalization, international law, and emerging infectious diseases. Emerg Infect Dis 1996;2:77-84.
McMichael AJ, Bolin B, Costanza R, Daily GC, Folke C, Lindahl-Kiessling K, et al. Globalization and the sustainability of health: An ecological perspective. Bioscience1999;49:205-10.
Jenkins M. Prospects for biodiversity. Science 2003;302:1175-7.
Donnelly CA, Woodroffe R, Cox DR, Bourne FJ, Cheeseman CL, Clifton-Hadley RS, et al. Positive and negative effects of widespread badger culling on tuberculosis in cattle. Nature 2006;439:843-6.