Professor David Hayman's Covid-19 Research

Linking Habitat Fragmentation and Biodiversity Loss to the Risk of Infectious Disease Emergence

A research Project being undertaken by Massey University Professor David Hayman

1. Summary:
From first reported cases in December 2019 to early October 2020, the coronavirus that causes COVID has spread to 214 countries, infected >36 million people, killed >1,000,000, and led to almost a third of humankind being in some form of ‘lockdown’, unable to socialise or work normally. Researchers internationally agree this event was likely triggered after a single person was infected with a virus from an animal.

The risk of infectious disease emergence from wildlife and pandemics is determined largely by human behaviours. COVID and the other most recent and greatest pandemics, including plague, influenza, Zika, SARS, and HIV/AIDS, have wildlife as the original, natural reservoirs.

Professor David Hayman’s work builds on his previous Ebola virus disease research. He will build new models of pathogen emergence based on where people are encroaching and fragmenting biodiverse rich regions, like southern and eastern China. These models will identify the high-risk areas for disease emergence and then he and his team will model the pandemic potential from local, regional and global populations and their movement.

These models will first focus on China and Southeast Asia and the risk from viruses from bats, which are hosts of the coronaviruses that cause diseases like COVID and SARS. They will then be developed to determine the relative probability of the emergence of undescribed pathogens and their pandemic potential from different regions, and test intervention strategies to mitigate pandemics from different regions no matter what their source.

Importantly they will identify if and how the same processes that are leading to the biodiversity crisis are also increasing the risk of pathogen emergence.

2. Research description:
The ongoing Coronavirus disease 2019 (COVID-19) pandemic is claiming human lives and disrupting the functioning of human societies in unprecedented ways. The most pressing questions about whether, when, and how this pandemic will end are being studied at similarly unprecedented rates.

Understanding where and why the virus emerged is essential to prevent future pandemics.

Recent years have seen a rise in the recorded number of epidemics from emerging diseases (EIDs). Such epidemics constitute a major public health threat because of our limited knowledge of prevention and treatment therapies1. Most emerging infectious diseases originate from pathogen “spillovers” of infection from wildlife to humans2,3.

Crucial to the understanding of emerging infectious disease outbreaks is the analysis of the factors facilitating the spillover from wildlife to the first human case (or “index case”), which is then followed by further spread within human populations.

In the case of Severe acute respiratory syndrome (SARS) Coronavirus (CoV)-2 (SARS-CoV-2), the cause of COVID19, genomic sequencing has shown that the virus found in humans is very closely related (~96%) to a strain present in a bat species, the intermediate horseshoe bat, sampled from Yunnan province, China in 20134. The timing of SARS-CoV-2 spillover from bats to humans, and whether an intermediate host species was involved, remain undetermined5.

For instance, there is evidence of the presence of a strain of coronavirus very similar to the SARS-CoV-2 (though the relationship is not as “close” as the one found in bats) in the Malayan Pangolin6, a wild mammal that has been documented to be illegally smuggled from Southeast Asia into China and sold in the markets7. There is also evidence that this virus can spread from pangolin to pangolin, though there is no documented spillover from pangolin to human8.

Bats, however, are the likely mammalian ancestral hosts of all alpha (α-) and beta (β-) CoVs9-11. Alpha-CoVs of likely bat origin include the causative agent of swine acute diarrheal syndrome that caused mass mortality of piglets on farms in Guangdong province, China,12 and a variant strain of porcine epidemic diarrhoea virus that spread rapidly from China in recent decades and caused mass piglet mortality in the USA13,14. Established human CoVs, NL63 and 229E, also likely had their evolutionary origins in bats15,16. Two recent human disease epidemics (SARS, Middle East respiratory syndrome [MERS]) and now the current COVID-19 pandemic were caused by viruses that probably originated from β-CoVs circulating in bat populations in regions where the outbreak occurred4,5,17-21.

Emergence of coronavirus diseases like these from the same general region strongly indicates a close association between CoVs that are likely to be pathogens and the wildlife reservoirs from which they originate4,18,21. Specific bat-virus associations can be difficult to discern because bats often roost together in multi-species aggregations that can facilitate viral sharing, with each capable of asymptomatically harbouring multiple CoV lineages. Host shifts to more divergent, non-bat hosts (i.e., that lead to spillover) are more difficult to predict because the potential host range for CoVs is broad6,22 and host susceptibility and onward transmission involve complex, multi-stage processes23,24.

Regardless of the specific spillover pathway (i.e., bat-human or bat-pangolin-human, or through other intermediary species), the pathogen flow of emerging zoonotic diseases to humans is the result of human interactions with wildlife.
The risk of these events occurring is driven by population growth, urbanization, changes in affluence, diet and associated agriculture25. Demand for animal products, for example, can lead to agricultural expansion at the expense of forests or other natural ecosystems. The penetration into wildlife habitat as a result of urbanization or agricultural expansion favours the interaction between humans and wildlife species, either directly or through other species such as livestock that are in closer contact with humans4,12,26-32.

While reports and opinion pieces in the media have proposed a link between deforestation and the emergence of the ongoing COVID19 pandemic, such a hypothesis still has to be supported by a comprehensive analysis of land use patterns. Studies that analyse land use, human, wildlife and domestic animal population changes are required to explain if and how the risk of SARS-related coronavirus outbreaks or viral disease may emerge and how this is related to the biodiversity crisis ( This proposal addresses these issues and will rigorously address the concept that through connecting biodiversity loss and the emergence of viral disease we can mitigate future related crises. The studies also link socioeconomic dynamics through identifying if urbanisation and agriculture are drivers of disease emergence and have implications for early warning and preparedness, because they will identify processes that increase disease emergence risk and locations where this is occurring.

State of the art
Research assessing infectious disease risk generally focuses on identifying geographic regions and wildlife species from which transmission from wildlife to humans is most likely2,6,8,10,20,21,32-34. Research has shown that risk may be highest in disturbed ecosystems where there is an elevated frequency of human-wildlife interactions or disruption of ecological patterns27,31.

Bats are among the most ecologically important, but underappreciated, mammals in most of Earth’s ecosystems; bats are the primary nocturnal predators of invertebrates and small vertebrates, as well as pollinators and seed dispersers of many tropical plants35. Bats are among the world’s most diverse mammals, with approximately 1,400 species, and the global distribution and diversity of CoVs in bats proportionally reflects that of their hosts36. Available evidence indicates that bats are natural reservoirs of CoVs, some of which have the potential to cause diseases in humans, livestock, and other types of domestic animals and wildlife10. However, while species are well described, bat distributions in China are poorly characterised. Plenty of survey data has been identified, but few species distribution models predicting the potential localities of them in China. There are many different techniques to model the distributions of species, including using presence only data and ensemble techniques that combine different model results (e.g. generalised additive models, multivariate adaptive regression splines, etc.) to lead to more robust predictions37.

Models and studies of habitat fragmentation are numerous38, but very few have linked these mechanistically to infection emergence. We previously quantified fragmentation with a composite fragmentation index (CFI)31, defined as the ratio between the sum of number of “edges”, “perforated”, “patches”, or smaller core areas (i.e.,<200 ha), and the total number of pixels (wooded + non-wooded) in the 30km circles used to characterize land cover and land use in the surroundings of the points of actual Ebola virus disease observations or the randomly generated points. We further advanced this through developing a framework to look at habitat fragmentation and infectious disease emergence that exploits the species-area-relationship to link disease risk with habitat biodiversity27. This model is independent of knowledge regarding the specific pathogens, most of which are currently uncultured. We can model changes in risk that result from habitat encroachment and defined classes of fragmentation, and we have predicted increased habitat fragmentation increases risk in most scenarios. Our results suggest that by exploiting an understanding of ecological theory it is possible to identify high-risk areas for infectious disease emergence mitigation, as well as habitat loss. Human travel data has been modelled within and from China to understand the transmission of SARS-CoV-2 (e.g. 39,40), but not from habitat changes27 yet. This research will address these gaps.

About Professor David Hayman:
David Hayman is the epidemiologist and co-directs the Molecular Epidemiology & Public Health Laboratory at Massey University, one of 7 research teams in the School of Veterinary Sciences. The team is a World Organization for Animal Health (OIE) Collaborating Centre for Veterinary Epidemiology & Public Health.

David manages epidemiologists and microbiologists of all career stages who make real research and training impact. He studies infectious diseases that primarily cause devastating human illness (e.g. Ebola and rabies), are highly contagious (e.g. measles), or cause serious ecological problems (e.g. white-nose syndrome). David is a recognized expert in the epidemiology of emerging bat infections.

David has a veterinary degree from The University of Edinburgh, a Master’s degree from The University of Kent, UK, a PhD from the University of Cambridge, and was a postdoctoral fellow jointly between Colorado State University and University of Florida, USA. The US Research and Policy for Infectious Disease Dynamics program made David a Research Associate from 2010-2015 at the Fogarty International Center, National Institutes of Health, the International Union for Conservation of Nature Wildlife Health Specialist Group granted him membership, and the European Board of Veterinary Specialization awarded David the European College of Zoological Medicine Wildlife Population Health Diplomate status.

David combines field, laboratory, and quantitative methods to understand how infections persist within populations, how cross-species transmission of infection leads to new disease emergence events, such as COVID and the West African Ebola virus outbreak, and how science can inform policy.

Massey’s team and laboratory have been used for human COVID diagnostics and David currently leads an OIE Laboratory Twinning Project to enhance capacity for early detection of viral haemorrhagic fevers (e.g. Ebola virus) in Liberia through epidemiological and laboratory training.

Since 2014 he has been on the NGO Steering Committee for the then US White House led Global Health Security Agenda and since 2015 he has been an invited US National Academy of Sciences Ad hoc committee member.

David’s work has been featured in major international media outlets, such as der Spiegel, BBC, The Guardian, Radio France International and NPR’s ‘Morning Edition’ with 13+ million listeners. He has published 78 peer-reviewed articles, including in prestigious journals, such as Science and Proceedings of the National Academy of Sciences, and led reports to government ministries on infectious disease in New Zealand, informing national policy.

David has received substantial and continuous funding as Principal Investigator since his first major award in 2008, comprising notable fellowships: a UK Wellcome Trust Research Training Fellowship; a US David Smith Fellowship, and a New Zealand Royal Society Te Apārangi Rutherford Discovery Fellowship, all to study emerging infectious diseases in bats, which are the hosts for the COVID causing SARS coronaviruses.

List of the people most involved in the project and their main role
• Prof David Hayman, Massey University, New Zealand: Principal Investigator, epidemiologist, bat virus expertise: conceptualization, methodology, data curation, formal analysis, project administration, writing, and science communication.
• Dr Renata Muylaert, Massey University, New Zealand: Postdoctoral researcher, landscape ecologist, mammologist, statistics; methodology, data curation, formal analysis, writing, and science communication.
• TBD, Massey University, New Zealand: Postdoctoral researcher, mathematician, data curation, formal analysis, writing, and science communication.
• Prof Paolo D'Odorico, University of California, Berkeley, USA: Associate Investigator, ecological processes engineer; conceptualization, methodology, writing.
• Prof Maria Cristina Rulli, Politecnico di Milano, Italy: Associate Investigator, ecological processes engineer: conceptualization, methodology, writing.
• Dr Jonathan Marshall, Massey University, New Zealand: Associate Investigator, statistician, mathematician: methodology, formal analysis.
• Dr Paul Cryan, USGS, USA: Associate Investigator, mammologist bat specialist: formal analysis

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27 Wilkinson*, D. A., Marshall, J. C., French, N. P. & Hayman, D. T. Habitat fragmentation, biodiversity loss and the risk of novel infectious disease emergence. Journal of the Royal Society Interface 15, 20180403 (2018).
28 Bloomfield, L. S. P., McIntosh, T. L. & Lambin, E. F. Habitat fragmentation, livelihood behaviors, and contact between people and nonhuman primates in Africa. Landscape Ecology 35, 985-1000, doi:10.1007/s10980-020-00995-w (2020).
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30 Chua, K. et al. Nipah virus: a recently emergent deadly paramyxovirus. Science 288, 1432-1435 (2000).
31 Rulli, M. C., Santini, M., Hayman, D. T. & D’Odorico, P. The nexus between forest fragmentation in Africa and Ebola virus disease outbreaks. Scientific reports 7, 41613 (2017).
32 Barrette, R. W. et al. Discovery of swine as a host for the Reston ebolavirus. Science 325, 204-206 (2009).
33 Hayman, D. T. As the bat flies. Can virus transmission from bats to humans be predicted? Science 354, 1099-1100 (2016).
34 Hayman, D. T. African primates: likely victims, not reservoirs, of Ebolaviruses. The Journal of infectious diseases 220, 1547-1550 (2019).
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40 Lai, S. et al. Effect of non-pharmaceutical interventions to contain COVID-19 in China. (2020).
41 Hayman, D. T. et al. Evolutionary history of rabies in Ghana. PLoS Neglected Tropical Diseases 5 (2011).
42 Hayman, D. T., Fooks, A. R., Marston, D. A. & Garcia-R*, J. C. The global phylogeography of lyssaviruses-challenging the'out of Africa'hypothesis. PLoS neglected tropical diseases 10, e0005266 (2016).
43 Hayman, D. et al. Ebola virus antibodies in fruit bats, Ghana, west Africa. Emerging infectious diseases 18, 1207 (2012).
44 Hayman, D. T. et al. Long-term survival of an urban fruit bat seropositive for Ebola and Lagos bat viruses. PloS one 5 (2010).
45 Hayman, D. T. Biannual birth pulses allow filoviruses to persist in bat populations. Proceedings of the Royal Society B: Biological Sciences 282, 20142591 (2015).
46 Han, B. A Han, B. A., Schmidt, J. P., Alexander, L. W., Bowden, S. E., Hayman, D. T., & Drake, J. M. (2016). Undiscovered bat hosts of filoviruses. PLoS neglected tropical diseases 10 (2016).
47 Hranac*, C. R., Marshall, J. C., Monadjem, A. & Hayman, D. T. Predicting Ebola virus disease risk and the role of African bat birthing. Epidemics 29, 100366 (2019).
48 Muylaert*, R.L., Sabino-Santos, G., Prist, P.R., Oshima, J.E., Niebuhr, B.B., Sobral-Souza, T., Oliveira, S.V.D., Bovendorp, R.S., Marshall, J.C., Hayman, D.T. and Ribeiro, M.C. Spatiotemporal Dynamics of Hantavirus Cardiopulmonary Syndrome Transmission Risk in Brazil. Viruses 11, 1008 (2019).
49 Muylaert*, R.L., Bovendorp, R.S., Sabino-Santos Jr, G., Prist, P.R., Melo, G.L., de Fátima Priante, C., Wilkinson*, D.A., Ribeiro, M.C. and Hayman, D.T. Hantavirus host assemblages and human disease in the Atlantic Forest. PLoS neglected tropical diseases 13, e0007655 (2019).
50 Wang, X., Liu, C., Mao, W., Hu, Z. & Gu, L. Tracing the largest seasonal migration on earth. arXiv preprint arXiv:1411.0983 (2014).

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