Charles L. Nunn’s research while affiliated with Duke University and other places

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Publications (276)


How market integration impacts human disease ecology
  • Article

September 2024

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4 Reads

Evolution Medicine and Public Health

Lev Kolinski

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Tyler M Barrett

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Charles L Nunn

Market integration (MI), or the shift from subsistence to market-based livelihoods, profoundly influences health, yet its impacts on infectious diseases remain underexplored. Here, we synthesize the current understanding of MI and infectious disease to stimulate more research, specifically aiming to leverage concepts and tools from disease ecology and related fields to generate testable hypotheses. Embracing a One Health perspective, we examine both human-to-human and zoonotic transmission pathways in their environmental contexts to assess how MI alters infectious disease exposure and susceptibility in beneficial, detrimental and mixed ways. For human-to-human transmission, we consider how markets expand contact networks in ways that facilitate infectious disease transmission while also increasing access to hygiene products and housing materials that likely reduce infections. For zoonotic transmission, MI influences exposures to pathogens through agricultural intensification and other market-driven processes that may increase or decrease human encounters with disease reservoirs or vectors in their shared environments. We also consider how MI-driven changes in noncommunicable diseases affect immunocompetence and susceptibility to infectious disease. Throughout, we identify statistical, survey and laboratory methods from ecology and the social sciences that will advance interdisciplinary research on MI and infectious disease.


Disentangling social, environmental, and zoonotic transmission pathways of a gastrointestinal protozoan (Blastocystis spp.) in northeast Madagascar

September 2024

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18 Reads

American Journal of Biological Anthropology

Tyler M Barrett

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Mark M Janko

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[...]

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Charles L Nunn

Objectives Understanding disease transmission is a fundamental challenge in ecology. We used transmission potential networks to investigate whether a gastrointestinal protozoan ( Blastocystis spp.) is spread through social, environmental, and/or zoonotic pathways in rural northeast Madagascar. Materials and Methods We obtained survey data, household GPS coordinates, and fecal samples from 804 participants. Surveys inquired about social contacts, agricultural activity, and sociodemographic characteristics. Fecal samples were screened for Blastocystis using DNA metabarcoding. We also tested 133 domesticated animals for Blastocystis . We used network autocorrelation models and permutation tests (network k ‐test) to determine whether networks reflecting different transmission pathways predicted infection. Results We identified six distinct Blastocystis subtypes among study participants and their domesticated animals. Among the 804 human participants, 74% ( n = 598) were positive for at least one Blastocystis subtype. Close proximity to infected households was the most informative predictor of infection with any subtype (model averaged OR [95% CI]: 1.56 [1.33–1.82]), and spending free time with infected participants was not an informative predictor of infection (model averaged OR [95% CI]: 0.95 [0.82–1.10]). No human participant was infected with the same subtype as the domesticated animals they owned. Discussion Our findings suggest that Blastocystis is most likely spread through environmental pathways within villages, rather than through social or animal contact. The most likely mechanisms involve fecal contamination of the environment by infected individuals or shared food and water sources. These findings shed new light on human‐pathogen ecology and mechanisms for reducing disease transmission in rural, low‐income settings.


Infectious disease responses to human climate change adaptations
  • Literature Review
  • Full-text available

August 2024

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117 Reads

Global Change Biology

Many recent studies have examined the impact of predicted changes in temperature and precipitation patterns on infectious diseases under different greenhouse gas emissions scenarios. But these emissions scenarios symbolize more than altered temperature and precipitation regimes; they also represent differing levels of change in energy, transportation, and food production at a global scale to reduce the effects of climate change. The ways humans respond to climate change, either through adaptation or mitigation, have underappreciated, yet hugely impactful effects on infectious disease transmission, often in complex and sometimes nonintuitive ways. Thus, in addition to investigating the direct effects of climate changes on infectious diseases, it is critical to consider how human preventative measures and adaptations to climate change will alter the environments and hosts that support pathogens. Here, we consider the ways that human responses to climate change will likely impact disease risk in both positive and negative ways. We evaluate the evidence for these impacts based on the available data, and identify research directions needed to address climate change while minimizing externalities associated with infectious disease, especially for vulnerable communities. We identify several different human adaptations to climate change that are likely to affect infectious disease risk independently of the effects of climate change itself. We categorize these changes into adaptation strategies to secure access to water, food, and shelter, and mitigation strategies to decrease greenhouse gas emissions. We recognize that adaptation strategies are more likely to have infectious disease consequences for under‐resourced communities, and call attention to the need for socio‐ecological studies to connect human behavioral responses to climate change and their impacts on infectious disease. Understanding these effects is crucial as climate change intensifies and the global community builds momentum to slow these changes and reduce their impacts on human health, economic productivity, and political stability.

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Astrovirus detection in small terrestrial Malagasy mammals captured in the different habitat types in and around the Marojejy National Park
(A) Map presenting the different habitat types at the study sites and (B) map showing the locations of each trapping grid together with the exact position of trapped animals colored in green (AstV negative) or red (AstV positive). The map was obtained using leaflet R package and the Map image is the intellectual property of Esri and is used herein under license. Source: Esri, i-cubed, USDA, USGS, AEX, Getmapping, Aerogrid, IGN, IGP, UPR-EGP, and the GIS User Community (https://arcg.is/1uyPfH).
Astrovirus positivity rates in introduced rodents according to habitat, in and outside of Marojejy National Park (Madagascar)
Model-averaged results of logistic regression predicting AstV infection based on habitat type (with semi-intact forest as the reference level), species (with Rattus as the reference level), sex (with female as reference level), and body mass
Midpoint rooting maximum likelihood tree obtained with 90 Astrovirus (AstV) RNA-dependent RNA-polymerase partial nucleotide sequences (389 bp)
The phylogenetic analysis was conducted with the TVM + I + Г evolutionary model (I = 0.14; α = 1.04) and 1000 bootstraps. Sequences derived from this study are colored in red. AstVs previously detected in Malagasy bats are colored in orange. Bootstrap values are reported when higher than 80. Scale bar: mean number of nucleotide substitutions per site.
Astrovirus detection in small terrestrial Malagasy mammals captured in and outside of Marojejy National Park
Species that were found positive (i.e. positive through hemi-nested PCR and with a Sanger sequence) are emphasized in bold. “E” refers to Endemic small mammals and “I” refers to Introduced small mammals.
Astroviruses in terrestrial Malagasy mammals

June 2024

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78 Reads

Small terrestrial mammals are major hosts of infectious agents responsible for zoonotic diseases. Astroviruses (AstVs)–the cause of non-bacterial gastroenteritis mainly affecting young children–have been detected in a wide array of mammalian and avian host species. However, understanding the factors that influence AstV infection within and across hosts is limited. Here, we investigated the impact of land use changes on AstVs in terrestrial small mammals in rural northeastern Madagascar. We sampled 515 small mammals, representing seven endemic and four introduced species. Twenty-two positive samples were identified, all but one of which were found in the introduced species Mus musculus and Rattus rattus (family Muridae), with a positivity rate of 7.7% (6/78) and 5.6% (15/266), respectively. The non-introduced rodent case was from an endemic shrew-tenrec (family Tenrecidae). We found the highest positivity rate of AstVs infection in brushy regrowth (17.5%, 7/40) as compared to flooded rice fields (4.60%, 8/174), secondary forest (4.1%, 3/74), agroforest (3.6%, 1/28), village (2.61%, 3/115), and semi-intact forest (0%, 0/84). A phylogenetic analysis revealed an association between AstVs and their rodent host species. None of the viruses were phylogenetically related to AstVs previously described in Malagasy bats. This study supports AstV circulation in synanthropic animals in agricultural habitats of Madagascar and highlights the need to assess the spillover risk to human populations in rural areas.




Effect of habitat degradation on hantavirus infection among introduced and endemic small mammals of Madagascar

December 2023

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102 Reads

Hantaviruses are globally distributed zoonotic pathogens capable of causing fatal disease in humans. Rodents and other small mammals are the typical reservoirs of hantaviruses, though the particular host varies regionally. Addressing the risk of hantavirus spillover from animal reservoirs to humans requires identifying the local mammal reservoirs and the predictors of infection in those animals, such as their population density and habitat characteristics. We screened native and non-native small mammals and bats in northeastern Madagascar for hantavirus infection to investigate the influence of habitat, including effects of human land use on viral prevalence. We trapped 227 bats and 1663 small mammals over 5 successive years in and around Marojejy National Park across a range of habitat types including villages, agricultural fields, regrowth areas, and secondary and semi-intact forests. Animals sampled included endemic tenrecs (Tenrecidae), rodents (Nesomyidae) and bats (6 families), along with non-native rodents (Muridae) and shrews (Soricidae). A hantavirus closely related to the previously described Anjozorobe virus infected 9.5% of Rattus rattus sampled. We did not detect hantaviruses in any other species. Habitat degradation had a complex impact on hantavirus prevalence in our study system: more intensive land use increase the abundance of R. rattus . The average body size of individuals varied between agricultural and non-agricultural land-use types, which in turn affected infection prevalence. Smaller R. rattus had lower probability of infection and were captured more commonly in villages and forests. Thus, infection prevalence was highest in agricultural areas. These findings provide new insights to the gradients of hantavirus exposure risk for humans in areas undergoing rapid land use transformations associated with agricultural practices.


A New Paradigm for Pandemic Preparedness

November 2023

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166 Reads

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1 Citation

Current Epidemiology Reports

Purpose of Review Preparing for pandemics requires a degree of interdisciplinary work that is challenging under the current paradigm. This review summarizes the challenges faced by the field of pandemic science and proposes how to address them. Recent Findings The structure of current siloed systems of research organizations hinders effective interdisciplinary pandemic research. Moreover, effective pandemic preparedness requires stakeholders in public policy and health to interact and integrate new findings rapidly, relying on a robust, responsive, and productive research domain. Neither of these requirements are well supported under the current system. Summary We propose a new paradigm for pandemic preparedness wherein interdisciplinary research and close collaboration with public policy and health practitioners can improve our ability to prevent, detect, and treat pandemics through tighter integration among domains, rapid and accurate integration, and translation of science to public policy, outreach and education, and improved venues and incentives for sustainable and robust interdisciplinary work.


Explaining the primate extinction crisis: predictors of extinction risk and active threats

September 2023

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67 Reads

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1 Citation

Explaining why some species are disproportionately impacted by the extinction crisis is of critical importance for conservation biology as a science and for proactively protecting species that are likely to become threatened in the future. Using the most current data on threat status, population trends, and threat types for 446 primate species, we advance previous research on the determinants of extinction risk by including a wider array of phenotypic traits as predictors, filling gaps in these trait data using multiple imputation, and investigating the mechanisms that connect organismal traits to extinction risk. Our Bayesian phylogenetically controlled analyses reveal that insular species exhibit higher threat status, while those that are more omnivorous and live in larger groups have lower threat status. The same traits are not linked to risk when repeating our analyses with older IUCN data, which may suggest that the traits influencing species risk are changing as anthropogenic effects continue to transform natural landscapes. We also show that non-insular, larger-bodied, and arboreal species are more susceptible to key threats responsible for primate population declines. Collectively, these results provide new insights to the determinants of primate extinction and identify the mechanisms (i.e. threats) that link traits to extinction risk.


Sociodemographic Variables Can Guide Prioritized Testing Strategies for Epidemic Control in Resource-Limited Contexts

March 2023

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45 Reads

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4 Citations

The Journal of Infectious Diseases

Background: Targeted surveillance allows public health authorities to implement testing and isolation strategies when diagnostic resources are limited, and can be implemented via the consideration of social network topologies. Yet, it remains unclear how to implement such surveillance and control when network data are unavailable. Methods: We evaluated the ability of socio-demographic proxies of degree centrality to guide prioritized testing of infected individuals compared to known degree centrality. Proxies were estimated via readily-available socio-demographic variables (age, gender, marital status, educational attainment, and household size). We simulated SARS-CoV-2 epidemics via a SEIR individual-based model on two contact networks from rural Madagascar to further test the applicability of these findings to low-resource contexts. Results: Targeted testing using socio-demographic proxies performed similarly to targeted testing using known degree centralities. At a low testing capacity, using the proxies reduced the infection burden by 22-33% while using 20% fewer tests, compared to random testing. By comparison, using known degree centrality reduced the infection burden by 31-44% while using 26-29% fewer tests. Conclusions: We demonstrate that incorporating social network information into epidemic control strategies is an effective countermeasure to low testing capacity and can be implemented via socio-demographic proxies when social network data are unavailable.


Citations (56)


... Species traits such as body mass and home range have been associated with extinction risk in some taxa [7][8][9][10][11][12][13]. Body mass is often related to both resource requirements and life history, as larger animals require more habitat (i.e. ...

Reference:

Global primary predictors of extinction risk in primates
Explaining the primate extinction crisis: predictors of extinction risk and active threats

... Unraveling these interactions may also be relevant for designing conservation strategies that rely on identifying individuals that could be superspreaders Snijders et al. 2017). For instance, network-based interventions were suggested to be effective methods for preventing or slowing outbreaks (Miller and Hyman 2007;Salathé et al. 2010; Rushmore et al. 2014;Singh et al. 2021;Moradmand, Siami, and Shafai 2021;Evans et al. 2023;Berec et al. 2023). When social network data are not available, it may be possible to consider interventions based on individual traits like sex and age that stand in for centrality (Sosa 2016), as has been suggested for chimpanzees (Rushmore et al. 2014) and humans (Evans et al. 2023). ...

Sociodemographic Variables Can Guide Prioritized Testing Strategies for Epidemic Control in Resource-Limited Contexts
  • Citing Article
  • March 2023

The Journal of Infectious Diseases

... /fmed. . (6), the spread of the Zika Virus in the Americas (7) and, of course, the devastating COVID-19 pandemic (8,9). The emergency nature of this research exerts additional pressure on a research community that is already living under a "publish-or-perish" mindset due to the limited number of university positions (10). ...

COVID-19 and Evolution, Medicine, and Public Health

Evolution Medicine and Public Health

... ERGMs are established with foundations in spatial statistics and graph theory analysis [54,55,58] but have had limited applications in ecology [59]. In broad terms, the ERGM searches the observed network for explicitly stated sub-structures (dyads, triads, vertex attributes, etc.) and uses several stochastic techniques to estimate the probability of that structure (i.e., a triad) occurring given the presence of other structures (i.e., dyads). ...

Predicting primate–parasite associations using exponential random graph models

... This study focuses on the recent geologic history of Lake Alaotra, which is located 750 m above sea level in the Ambatondrazaka area in eastern Madagascar (Fig. 1). It is the biggest lake on the island and the surrounding area is used for rice-cultivation and is regarded as the most productive area on the island (e.g. Wright and Rakotoarisoa, 2003). Unfortunately, due to the climate changes and dramatic deforestation (Dufils, 2003), the lake has been dramatically reduced in recent years; its size and its shape have changed and the rice production has decreased. ...

CHAPTER 5 : HUMAN ECOLOGY. The New Natural History of Madagascar. Book.
  • Citing Chapter
  • December 2022

... Radhakrishna's (2023) careful analysis suggests a more nuanced understanding is needed of the synergistic human-environment interactions that can create local ecologies or "anthromes" that lead to the emergence and spread of infectious disease. Werner et al. (2023) also underscore the need for better understanding of the factors that leads to disease emergence in order to better predict future zoonotic outbreaks but point to the paucity of data to inform surveillance measures. The authors present a novel-link prediction method that incorporates both phylogenetic and geographic predictors to estimate nonhuman primate (NHP)-parasite interaction that could affect human health. ...

Using phylogeographic link‐prediction in primates to prioritize human parasite screening
  • Citing Article
  • August 2022

American Journal of Biological Anthropology

... It is well known that individuals with high social connectivity are at higher risk of infection and can contribute disproportionately to the spread of diseases such as COVID-19 [63][64][65]. While research on at-risk occupational activities in Africa has mostly focused on healthcare workers [25], a better understanding of the role played by other socioeconomic groups with high mobility and social connections on COVID-19 spread could open new possibilities for disease control [66]. ...

Targeting SARS-CoV-2 superspreading infections could dramatically improve the efficiency of epidemic control strategies in resource-limited contexts

... Non-human primate Plasmodium species are naturally and experimentally transmissible to humans and vice versa [31,[50][51][52]. Such cross-species infections are an emerging area of concern to current malaria transmission patterns facilitated by increased invasion, contact, and proximity to shared forest environments with non-human primates. ...

Primate malarias as a model for cross- species parasite transmission

eLife

... Beyond nutritional issues, Madagascar suffers a high burden of water-borne illness and infectious diseases including malaria and increasing prevalence of non-communicable diseases (39,40). Diarrheal diseases, driven by infections like Rotavirus (41) and limited access to clean water and sanitation, are the number one cause of death in Madagascar (42). ...

Comparing transmission potential networks based on social network surveys, close contacts and environmental overlap in rural Madagascar