Bioecological Drivers of Rabies Virus Circulation in a Neotropical Bat Community

Abstract

Introduction: In addition to the commonly accepted importance of the vampire bat in the maintenance and transmission of the rabies virus (RABV) in South America, RABV infection of other species is widely evidenced, challenging their role in the viral cycle.

Methodology / principles findings: To identify the bioecological drivers of RABV circulation in neotropical bat communities, we conducted a molecular and serological survey on almost 1,000 bats from 30 species, and a 4-year longitudinal survey in two colonies of vampire bats in French Guiana. RABV was molecularly detected in a common vampire and in a frugivorous bat. The sequences corresponded to haematophagous bat-related strains and were close to viruses circulating in the Brazilian Amazon region. Species' seroprevalence ranged from 0 to 20%, and the risk of seropositivity was higher in bats with a haematophagous diet, living in monospecific colonies and in dense forests. The longitudinal survey showed substantial temporal fluctuations, with individual waves of seroconversions and waning immunity. The high prevalences observed in bat communities, in most habitats and in species that do not share the same microhabitats and bioecological patterns, the temporal variations, and a rather short period of detectable antibodies as observed in recaptured vampires suggest (i) frequent exposure of animals, (ii) an ability of the infected host to control and eliminate the virus, (iii) more relaxed modes of exposure between bats than the commonly assumed infection via direct contact with saliva of infected animals, all of which should be further investigated.

Conclusions / significance: We hypothesize that RABV circulation in French Guiana is mainly maintained in the pristine forest habitats that may provide sufficient food resources to allow vampire bats, the main prevalent species, to survive and RABV to be propagated. However, on the forest edge and in disturbed areas, human activities may induce more insidious effects such as defaunation. One of the ecological consequences is the disappearance of resources for tertiary or secondary consumers. Populations of vampires may then shift to alternative resources such as cattle, domestic animals and humans. Therefore, a good forest status, allowing both a dilution effect in highly rich bat communities and the maintenance of large populations of medium-sized and large mammals used as prey by vampires, should prevent their migration to anthropized areas.

Fig 1. French Guiana map with the location of the trapping sites in empty squares and the caves (cave 1 and cave 2) in black squares investigated in the study.

For clarity, close sites (<10 km) are presented together. Pie chart indicates rabies seroprevalence, with small charts indicating prevalence rates < 5%, medium-sized, charts prevalence rates from 5 to 15%, and large charts, prevalence rates > 15%. The number associated to the chart indicates the number of species sampled at the trapping site. Background of the map shows the vegetation type (Gond et al. 2011), the main environmental variable associated to the variation of the seroprevalence.

Fig 2. Phylogenetic tree constructed using Bayesian methods based on 1314 nucleotides of the nucleoprotein gene.

Virus names are associated with their accession numbers. Novel sequences generated from the two rabid bats in this study are shown in bold. Support for nodes is provided by the posterior probabilities of the corresponding clades. All resolved nodes have a posterior probability greater than 0.8. Scale bar indicates nucleotide sequence divergence among sequences.

Fig 3. Phylogenetic tree constructed using Bayesian methods based on 1572 nucleotides of the complete glycoprotein gene.

Virus names are associated with their accession numbers. Novel sequences generated from the two rabid bats in this study are shown in bold. Support for nodes is provided by the posterior probabilities of the corresponding clades. All resolved nodes have a posterior probability greater than 0.8. Scale bar indicates nucleotide sequence divergence among sequences.

Fig 4. Changes in the percentage of RABV seropositive vampire bats from November 2009 to May 2013 in the two caves and the number of animals captured and recaptured during the same period.

Grey line: % of seropositive animals. Black bar: total number of animals captured. Grey bar: number of recaptured animals.