Tracking zoonotic pathogens using blood-sucking flies as 'flying syringes'

  1. Paul-Yannick Bitome-Essono  Is a corresponding author
  2. Benjamin Ollomo
  3. Céline Arnathau
  4. Patrick Durand
  5. Nancy Diamella Moukodoum
  6. Lauriane Yacka-Mouele
  7. Alain-Prince Okouga
  8. Larson Boundenga
  9. Bertrand Mve-Ondo
  10. Judicaël Obame-Nkoghe
  11. Pierre Philippe Mbehang Nguema
  12. Flobert Njiokou
  13. Boris Kevin Makanga
  14. Rémi Wattier
  15. Diego Ayala
  16. Francisco J Ayala
  17. Francois Renaud
  18. Virginie Rougeron
  19. François Bretagnolle
  20. Franck Prugnolle  Is a corresponding author
  21. Christophe Paupy  Is a corresponding author
  1. Biogéosciences Unit, UMR 6282 CNRS-uB-EPHE-AgroSup, Équipe Écologie-Évolutive, France
  2. Centre International de Recherches Médicales de Franceville, Gabon
  3. UMR 224-5290 IRD-CNRS-UM, Centre IRD de Montpellier, France
  4. Université de Yaoundé 1, Cameroon

Abstract

About 60% of emerging infectious diseases in humans are of zoonotic origin. Their increasing number requires the development of new methods for early detection and monitoring of infectious agents in wildlife. Here, we investigated whether blood meals from hematophagous flies could be used to identify the infectious agents circulating in wild vertebrates. To this aim, 1230 blood-engorged flies were caught in the forests of Gabon. Identified blood meals (30%) were from 20 vertebrate species including mammals, birds and reptiles. Among them, 9% were infected by different extant malaria parasites among which some belonged to known parasite species, others to new parasite species or to parasite lineages for which only the vector was known. This study demonstrates that using hematophagous flies as 'flying syringes' constitutes an interesting approach to investigate blood-borne pathogen diversity in wild vertebrates and could be used as an early detection tool of zoonotic pathogens.

Article and author information

Author details

  1. Paul-Yannick Bitome-Essono

    Biogéosciences Unit, UMR 6282 CNRS-uB-EPHE-AgroSup, Équipe Écologie-Évolutive, Dijon, France
    For correspondence
    bitomessono@yahoo.fr
    Competing interests
    The authors declare that no competing interests exist.
  2. Benjamin Ollomo

    Centre International de Recherches Médicales de Franceville, Franceville, Gabon
    Competing interests
    The authors declare that no competing interests exist.
  3. Céline Arnathau

    MIVEGEC Unit, UMR 224-5290 IRD-CNRS-UM, Centre IRD de Montpellier, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Patrick Durand

    MIVEGEC Unit, UMR 224-5290 IRD-CNRS-UM, Centre IRD de Montpellier, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Nancy Diamella Moukodoum

    Centre International de Recherches Médicales de Franceville, Franceville, Gabon
    Competing interests
    The authors declare that no competing interests exist.
  6. Lauriane Yacka-Mouele

    Centre International de Recherches Médicales de Franceville, Franceville, Gabon
    Competing interests
    The authors declare that no competing interests exist.
  7. Alain-Prince Okouga

    Centre International de Recherches Médicales de Franceville, Franceville, Gabon
    Competing interests
    The authors declare that no competing interests exist.
  8. Larson Boundenga

    Centre International de Recherches Médicales de Franceville, Franceville, Gabon
    Competing interests
    The authors declare that no competing interests exist.
  9. Bertrand Mve-Ondo

    Centre International de Recherches Médicales de Franceville, Franceville, Gabon
    Competing interests
    The authors declare that no competing interests exist.
  10. Judicaël Obame-Nkoghe

    Centre International de Recherches Médicales de Franceville, Franceville, Gabon
    Competing interests
    The authors declare that no competing interests exist.
  11. Pierre Philippe Mbehang Nguema

    Centre International de Recherches Médicales de Franceville, Franceville, Gabon
    Competing interests
    The authors declare that no competing interests exist.
  12. Flobert Njiokou

    Département de Biologie Animale et Physiologie, Université de Yaoundé 1, Yaoundé, Cameroon
    Competing interests
    The authors declare that no competing interests exist.
  13. Boris Kevin Makanga

    Centre International de Recherches Médicales de Franceville, Franceville, Gabon
    Competing interests
    The authors declare that no competing interests exist.
  14. Rémi Wattier

    Biogéosciences Unit, UMR 6282 CNRS-uB-EPHE-AgroSup, Équipe Écologie-Évolutive, Dijon, France
    Competing interests
    The authors declare that no competing interests exist.
  15. Diego Ayala

    Centre International de Recherches Médicales de Franceville, Franceville, Gabon
    Competing interests
    The authors declare that no competing interests exist.
  16. Francisco J Ayala

    Centre International de Recherches Médicales de Franceville, Franceville, Gabon
    Competing interests
    The authors declare that no competing interests exist.
  17. Francois Renaud

    MIVEGEC Unit, UMR 224-5290 IRD-CNRS-UM, Centre IRD de Montpellier, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  18. Virginie Rougeron

    Centre International de Recherches Médicales de Franceville, Franceville, Gabon
    Competing interests
    The authors declare that no competing interests exist.
  19. François Bretagnolle

    Biogéosciences Unit, UMR 6282 CNRS-uB-EPHE-AgroSup, Équipe Écologie-Évolutive, Dijon, France
    Competing interests
    The authors declare that no competing interests exist.
  20. Franck Prugnolle

    Centre International de Recherches Médicales de Franceville, Franceville, Gabon
    For correspondence
    franck.prugnolle@ird.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8519-1253
  21. Christophe Paupy

    Centre International de Recherches Médicales de Franceville, Franceville, Gabon
    For correspondence
    christophe.paupy@ird.fr
    Competing interests
    The authors declare that no competing interests exist.

Funding

Agence Universitaire de la Francophonie

  • Paul-Yannick Bitome-Essono
  • Flobert Njiokou
  • François Bretagnolle
  • Franck Prugnolle
  • Christophe Paupy

Service de Coopération et d'Action Culturelle de l'ambassade de France au Gabon

  • Paul-Yannick Bitome-Essono
  • François Bretagnolle

LMI ZOFAC IRD

  • Benjamin Ollomo
  • Franck Prugnolle
  • Christophe Paupy

CIRMF

  • Paul-Yannick Bitome-Essono
  • Benjamin Ollomo
  • Diego Ayala
  • Virginie Rougeron
  • Franck Prugnolle
  • Christophe Paupy

ANR JCJC 07-2012-ORIGIN

  • Virginie Rougeron
  • Franck Prugnolle
  • Christophe Paupy

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Ben Cooper, Mahidol Oxford Tropical Medicine Research Unit, Thailand

Version history

  1. Received: October 4, 2016
  2. Accepted: March 14, 2017
  3. Accepted Manuscript published: March 28, 2017 (version 1)
  4. Version of Record published: May 11, 2017 (version 2)

Copyright

© 2017, Bitome-Essono et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 5,609
    views
  • 704
    downloads
  • 33
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Paul-Yannick Bitome-Essono
  2. Benjamin Ollomo
  3. Céline Arnathau
  4. Patrick Durand
  5. Nancy Diamella Moukodoum
  6. Lauriane Yacka-Mouele
  7. Alain-Prince Okouga
  8. Larson Boundenga
  9. Bertrand Mve-Ondo
  10. Judicaël Obame-Nkoghe
  11. Pierre Philippe Mbehang Nguema
  12. Flobert Njiokou
  13. Boris Kevin Makanga
  14. Rémi Wattier
  15. Diego Ayala
  16. Francisco J Ayala
  17. Francois Renaud
  18. Virginie Rougeron
  19. François Bretagnolle
  20. Franck Prugnolle
  21. Christophe Paupy
(2017)
Tracking zoonotic pathogens using blood-sucking flies as 'flying syringes'
eLife 6:e22069.
https://doi.org/10.7554/eLife.22069

Share this article

https://doi.org/10.7554/eLife.22069

Further reading

    1. Ecology
    2. Evolutionary Biology
    Théo Constant, F Stephen Dobson ... Sylvain Giroud
    Research Article

    Seasonal animal dormancy is widely interpreted as a physiological response for surviving energetic challenges during the harshest times of the year (the physiological constraint hypothesis). However, there are other mutually non-exclusive hypotheses to explain the timing of animal dormancy, that is, entry into and emergence from hibernation (i.e. dormancy phenology). Survival advantages of dormancy that have been proposed are reduced risks of predation and competition (the ‘life-history’ hypothesis), but comparative tests across animal species are few. Using the phylogenetic comparative method applied to more than 20 hibernating mammalian species, we found support for both hypotheses as explanations for the phenology of dormancy. In accordance with the life-history hypotheses, sex differences in hibernation emergence and immergence were favored by the sex difference in reproductive effort. In addition, physiological constraint may influence the trade-off between survival and reproduction such that low temperatures and precipitation, as well as smaller body mass, influence sex differences in phenology. We also compiled initial evidence that ectotherm dormancy may be (1) less temperature dependent than previously thought and (2) associated with trade-offs consistent with the life-history hypothesis. Thus, dormancy during non-life-threatening periods that are unfavorable for reproduction may be more widespread than previously thought.

    1. Ecology
    Ari Grele, Tara J Massad ... Lora A Richards
    Research Article

    Declines in biodiversity generated by anthropogenic stressors at both species and population levels can alter emergent processes instrumental to ecosystem function and resilience. As such, understanding the role of biodiversity in ecosystem function and its response to climate perturbation is increasingly important, especially in tropical systems where responses to changes in biodiversity are less predictable and more challenging to assess experimentally. Using large-scale transplant experiments conducted at five neotropical sites, we documented the impacts of changes in intraspecific and interspecific plant richness in the genus Piper on insect herbivory, insect richness, and ecosystem resilience to perturbations in water availability. We found that reductions of both intraspecific and interspecific Piper diversity had measurable and site-specific effects on herbivory, herbivorous insect richness, and plant mortality. The responses of these ecosystem-relevant processes to reduced intraspecific Piper richness were often similar in magnitude to the effects of reduced interspecific richness. Increased water availability reduced herbivory by 4.2% overall, and the response of herbivorous insect richness and herbivory to water availability were altered by both intra- and interspecific richness in a site-dependent manner. Our results underscore the role of intraspecific and interspecific richness as foundations of ecosystem function and the importance of community and location-specific contingencies in controlling function in complex tropical systems.