Ebola Virus Maintenance: If Not (Only) Bats, What Else?

Abstract

The maintenance mechanisms of ebolaviruses in African forest ecosystems are still unknown, but indirect evidences point at the involvement of some bat species. Despite intense research, the main bat-maintenance hypothesis has not been confirmed yet. The alternative hypotheses of a non-bat maintenance host or a maintenance community including, or not, several bat and other species, deserves more investigation. However, African forest ecosystems host a large biodiversity and abound in potential maintenance hosts. How does one puzzle out? Since recent studies have revealed that several bat species have been exposed to ebolaviruses, the common denominator to these hypotheses is that within the epidemiological cycle, some bats species must be exposed to the viruses and infected by these potential alternative hosts. Under this constraint, and given the peculiar ecology of bats (roosting behaviour, habitat utilisation, and flight mode), we review the hosts and transmission pathways that can lead to bat exposure and infection to ebolaviruses. In contrast to the capacity of bats to transmit ebolaviruses and other pathogens to many hosts, our results indicate that only a limited number of hosts and pathways can lead to the transmission of ebolaviruses to bats, and that the alternative maintenance host, if it exists, must be amongst them. A list of these pathways is provided, along with protocols to prioritise and investigate these alternative hypotheses. In conclusion, taking into account the ecology of bats and their known involvement in ebolaviruses ecology drastically reduces the list of potential alternative maintenance hosts for ebolaviruses. Understanding the natural history of ebolaviruses is a health priority, and investigating these alternative hypotheses could complete the current effort focused on the role of bats.

Keywords: Africa; bat; community ecology; ebola virus; filovirus; maintenance host; transmission pathways.

Figure 1

Potential maintenance mechanisms of ebolaviruses in wildlife, according to current knowledge. Circles (plain or dotted) indicate a maintenance function play by the host(s); arrows represent infectious transmission pathways between hosts. Humans, non-human primates, and duikers are examples of known non-maintenance hosts, exposed occasionally to ebolavirus directly or indirectly through the main maintenance host. (A1) Main maintenance hypothesis: there is one bat species maintaining each ebolavirus alone. Currently this is logically the most investigated hypothesis given the available data, and represents the maintenance mechanism for another filovirus, the Marburg virus, as currently understood. (A2) Several bat species are needed to create a maintenance community for Zaire ebolavirus (EBOV); each bat species cannot complete EBOV maintenance alone, as it requires interactions with the other species. (B) Alternate non-bat maintenance host hypothesis: if it exists, it is known that it can transmit ebolaviruses to some bat species. In this article, we review the potential hosts and associated transmission pathways that link this host to bat species (red arrow). (C) The maintenance community hypothesis, in which several hosts are needed to maintain ebolaviruses (ellipses represent different scenarios of community maintenance). This could be one or more alternative hosts involving possibly bat species. By definition, if such an alternative host exists, there are infectious transmission pathways from this host towards bats that are reviewed here (red arrows).