Land use gradients drive spatial variation in Lassa fever host communities in Eastern Sierra Leone.

Author

Affiliation

David Simons

The Royal Veterinary College

Abstract

1. The natal multimammate mouse (Mastomys natalensis) is the primary reservoir host of Lassa mammarenavirus (LASV), a zoonotic pathogen causing Lassa fever that is endemic to West Africa. The occurrence and abundance of this species is regulated by the human environment and biotic interactions with other small-mammal species, but these ecological drivers remain poorly understood in the regions where Lassa fever outbreaks are observed.
2. We developed a Bayesian multi-species occupancy model incorporating incomplete detection to assess habitat use from data obtained as part of a multi-year small-mammal trapping study (43,226 trap nights across four village sites in Sierra Leone, 2020-2023). We investigated the effects of land use gradients and small-mammal community dynamics on the spatial distribution of M. natalensis.
3. Mastomys natalensis occupancy increased along a gradient from forest to agriculture to village habitats but was reduced in peri-urban settings compared to rural settings. Invasive rodent species influenced this pattern, with Mus musculus presence associated with reduced M. natalensis occupancy in peri-urban settings. We did not observe a similar effect when considering the co-occurrence of invasive Rattus rattus with M. natalensis in rural settings.
4. These findings suggest that land use and species interactions drive spatial heterogeneity in M. natalensis populations, potentially explaining reduced Lassa fever incidence in urban areas. The results highlight the importance of considering community dynamics when predicting the risk of outbreaks of endemic zoonoses and the need to widen the context of studies of LASV transmission beyond the primary reservoir host species.
5. To better assess public health risk and improve allocation of limited resources, we recommend more precise characterisation of small-mammal communities in LASV endemic regions, particularly in areas undergoing rapid land use change which may alter community level small-mammal biodiversity.

Authors

David Simons ^1,2,3, Rory Gibb ^2,4, Umaru Bangura ^5,6, Dianah Sondufu ⁶, Joyce Lamin ⁶, James Koninga ⁷, Momoh Jimmy ⁷, Mike Dawson ⁶, Joseph Lahai ⁶, Rashid Ansumana ⁶, Elisabeth Fichet-Calvet ⁵, Deborah Watson-Jones ^3,8, Richard Kock ¹, Kate E. Jones ^2,4.

¹ Centre for Emerging, Endemic and Exotic Diseases, The Royal Veterinary College, London, United Kingdom

² Centre for Biodiversity and Environment Research, Department of Genetics, Evolution and Environment, University College London, London, United Kingdom

³ Clinical Research Department, London School of Hygiene and Tropical Medicine, London, United Kingdom

⁴ People & Nature Lab, UCL East, Department of Genetics, Evolution and Environment, University College London, London, United Kingdom

⁵ Bernard-Nocht Institute for Tropical Medicine, WHO Collaborating Centre for Arbovirus and Hemorrhagic Fever Reference and Research, 20359 Hamburg, Germany

⁶ Njala University, Bo, Sierra Leone

⁷ Kenema Government Hospital, Kenema, Sierra Leone

⁸ Mwanza Intervention Trials Unit, National Institute for Medical Research, Mwanza, Tanzania

Motivation

This study was designed to investigate the effect of changes in landuse on the occurrence of different rodent species in a Lassa fever endemic region of Eastern Sierra Leone. While habitat preferences of Mastomys natalensis have been well studied in West Africa to better understand the risk to human populations from Lassa mammarenavirus spillover (Fichet‐Calvet et al. 2010), there is limited understanding of the wider rodent species communities. Biotic interactions between different species will drive occurrence and abundance in different habitats and this study was designed to understand how these species co-exist in these habitats.

We conducted repeated, systematic, rodent trapping in the Eastern province of Sierra Leone, along a landuse gradient to model the association of landuse and occurrence of M. natalensis and more generally small mammal communities. We aimed to investigate the following questions. First, what is the diversity of rodent communities in varied landuse types in Eastern Sierra Leone? Second, how do patterns of landuse affect the occupancy of M. natalensis and other sympatric rodents? Finally, is there evidence that the local spatial distribution of M. natalensis is regulated by biotic interactions with co-occurring species? We expect these analyses to further our understanding of rodent community structures that may explain observed patterns of Lassa fever spillover.

A protocol was developed prior to a pilot trapping session in November 2020. This protocol is archived on the Open Science Framework. All field data is collected using the Open Data Kit (ODK).

Preprint

This manuscript has been submitted to the Journal of Animal Ecology. The pre-peer reviewed version is available from ecoevoRxiv.

Data availability and draft manuscript

Data are available in the project’s GitHub repository.

EEID 2022 presentation

I presented data from the first year of trapping at the 2022 Ecology and Evolution of Infectious Diseases conference, the slides are available and the talk is embedded below.

References

Fichet‐Calvet, Elisabeth, Leen Audenaert, Patrick Barrière, and Erik Verheyen. 2010. “Diversity, Dynamics and Reproduction in a Community of Small Mammals in Upper Guinea, with Emphasis on Pygmy Mice Ecology.” African Journal of Ecology 48 (3): 600–614. https://doi.org/10.1111/j.1365-2028.2009.01144.x.