1. Ecology
  2. Epidemiology and Global Health

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 Mokoudoum
  6. Lauriane Yacka-Mouele
  7. Alain-Prince Okouga
  8. Larson Boundenga
  9. Bertrand Mve-Ondo
  10. Judicaël Obame-Nkoghe
  11. Philippe Mbehang-Nguema
  12. Flobert Njiokou
  13. Boris Makanga
  14. Rémi Wattier
  15. Diego Ayala
  16. Francisco J Ayala
  17. Francois Renaud
  18. Virginie Rougeron
  19. Francois Bretagnolle
  20. Franck Prugnolle  Is a corresponding author
  21. Christophe Paupy  Is a corresponding author
  1. UMR 6282 CNRS-université de Bourgogne-Franche Comté-EPHE-AgroSup, France
  2. Centre International de Recherches Médicales de Franceville, Gabon
  3. Institut de Recherche en Écologie Tropicale, Gabon
  4. UMR 224-5290 IRD-CNRS-UM, Centre IRD de Montpellier, France
  5. Laboratoire de Parasitologie et Écologie, Faculté des Sciences de l'Université de Yaoundé 1, Cameroun
  6. University of California, United States
https://doi.org/10.7554/eLife.22069
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Cite this article
  1. Paul-Yannick Bitome-Essono
  2. Benjamin Ollomo
  3. Céline Arnathau
  4. Patrick Durand
  5. Nancy Diamella Mokoudoum
  6. Lauriane Yacka-Mouele
  7. Alain-Prince Okouga
  8. Larson Boundenga
  9. Bertrand Mve-Ondo
  10. Judicaël Obame-Nkoghe
  11. Philippe Mbehang-Nguema
  12. Flobert Njiokou
  13. Boris Makanga
  14. Rémi Wattier
  15. Diego Ayala
  16. Francisco J Ayala
  17. Francois Renaud
  18. Virginie Rougeron
  19. Francois 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
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  3. Download .RIS
2 figures and 4 tables

Figures

Figure 1
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Monitoring vertebrate haemosporidian diversity using haematophagous flies.

(a) Localization of the sampling sites (red dots) in Gabon (Central Africa). (b) Number of blood meals originating from the different vertebrate species. (c) Position within the Cytb phylogeny of the haemosporidian Cytb sequences PCR-amplified from the blood meals of engorged flies with identified hosts (red isolates) and unidentified hosts (green isolates). Black isolates: references (Table 4). Bootstrap values at important nodes are shown.

https://doi.org/10.7554/eLife.22069.003
Figure 2
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Number of blood meals identified using the shorter PCR system of Boessenkool et al. (2012) out of the previously unidentified 89 blood meals.
https://doi.org/10.7554/eLife.22069.007

Tables

Table 1

Number and proportion of specimens captured per fly species. The number of engorged specimens and blood meals identified in each fly species are also indicated.

https://doi.org/10.7554/eLife.22069.004
Fly speciesNumber of collected specimensProportion (%)Number of engorged specimensNumber of identified blood meals
Glossinidae225254.941218423
Glossina caliginea1443.518733
G. fusca congolensis2105.1210442
G. fuscipes fuscipes2907.0721493
G. pallicera newsteadi1573.839737
G. palpalis palpalis137233.47662218
G. tabaniformis791.93540
Muscidae136233.2394
Stomoxys calcitrans2455.9852
S. inornatus3348.1400
S. niger niger2536.1742
S. niger bilineatus2245.4600
S. omega omega1974.8100
S. transvittatus1092.6600
Tabanidae48511.8331
Ancala sp41100
Atylotus sp1042.5300
Chrysops sp1563.8131
Haematopota sp130.3100
Tabanus par521.2700
Tabanus taeniola1202.9300
Total40991001230428
Table 2

Number and origin of blood meals according to the fly species (Fsp), park and climatic season.

https://doi.org/10.7554/eLife.22069.005
Number of identified blood meals by fly species (Fsp)
Moukalaba-DoudouLopé
Rainy seasonDry seasonRainy seasonDry season
Taxonomic group/Order/FamilyHost speciesN° IdentifiedFsp1Fsp2Fsp3Fsp4Fsp5Fsp1Fsp2Fsp3Fsp4Fsp5Fsp8Fsp1Fsp2Fsp3Fsp4Fsp5Fsp1Fsp2Fsp3Fsp4Fsp5Fsp6Fsp7
Mammals
  Artiodactyla295143811711421233413
   BovidaeCephalophus
silvicultor		65
kobus
ellipsiprymnus		431
Syncerus caffer12635711329211057128161
Tragelaphus spekii9516415137694121
   HippopotamidaeHippopotamus amphibius211
   SuidaePotamochoerus
porcus		312
  Carnivora1
   HerpestidaeHerpestinae sp11
  Primates67
   HominidaeGorilla gorilla321
Homo sapiens6411132221312141
  Proboscidae10
   ElephantidaeLoxodonta cyclotis10712
Reptiles
  Crocodilia233
   CrocodylidaeCrocodylus niloticus3
Mecistops
cataphractus		19116
Osteolaemus tetraspis11
  Squamata12
   PythonidaePython sebae82
   VaranidaeVaranus sp4211
  Testudines16
   TestunidaeKinixys erosa11
   PelomedusidaePelusios castaneus3111
Pelusios chapini11
Pelusios marani1138
Birds
  Ciconiformes4
   CiconiidaeCiconia sp412
8 orders/12 families20 species428311144122164891671871611112262512

  1. Fsp1 = Glossina caliginea; Fsp2 = G. fusca congolensis; Fsp3 = G. fuscipes fuscipes; Fsp4 = G. pallicera newsteadi; Fsp5 = G. palpalis palpalis; Fsp6 = Stomoxys calcitrans; Fsp7 = S. niger niger; Fsp8 = Chrysops sp.

Table 3

Number and origin of blood meals according to the fly species (Fsp), park and climatic season.

https://doi.org/10.7554/eLife.22069.006
Number of identified blood meals by fly species (Fsp)
La LékédiIvindo
Rainy seasonDry seasonDry season
Taxonomic group/Order/FamilyHost speciesN° IdentifiedFsp1Fsp3Fsp4Fsp5Fsp6Fsp1Fsp2Fsp3Fsp4Fsp5Fsp1Fsp2Fsp3Fsp5
Mammals
  Artiodactyla295213
   BovidaeCephalophus
silvicultor		65
kobus
ellipsiprymnus		4
Syncerus caffer126211610881311
Tragelaphus spekii95131285591
   HippopotamidaeHippopotamus amphibius2
   SuidaePotamochoerus
porcus		3
  Carnivora1
   HerpestidaeHerpestinae sp1
  Primates67
   HominidaeGorilla gorilla3
Homo sapiens6441511
  Proboscidae10
   ElephantidaeLoxodonta cyclotis10
Reptiles
  Crocodilia23
   CrocodylidaeCrocodylus niloticus3
Mecistops
cataphractus		192423
Osteolaemus
tetraspis		1
  Squamata12
   PythonidaePython sebae8222
   VaranidaeVaranus sp4
  Testudines16
   TestunidaeKinixys erosa1
   PelomedusidaePelusios
castaneus		3
Pelusios chapini1
Pelusios marani11
Birds
  Ciconiformes4
   CiconiidaeCiconia sp41
8 orders/12 families20 species4282411318202015321122

  1. Fsp1 = Glossina caliginea; Fsp2 = G. fusca congolensis; Fsp3 = G. fuscipes fuscipes; Fsp4 = G. pallicera newsteadi; Fsp5 = G. palpalis palpalis; Fsp6 = Stomoxys calcitrans; Fsp7 = S. niger niger; Fsp8 = Chrysops sp.

Table 4

Cytb sequences of parasites recovered in this study and of those used as references for phylogenetic analyses and their Genbank accession numbers.

https://doi.org/10.7554/eLife.22069.008
IsolateAccession number
Anopheles coustaniKT367855
An. gabonensis2KT367852
An. gabonensis279KT367853
An. gabonensis3KT367861
An. marshalliiKT367857
An. mouchetiKT367864
An. obscurus2KT367846
An. obscurus78KT367849
Cephalophus_silvicultor_1336KY631949
Cephalophus_silvicultor_1368KY631947
Cephalophus_silvicultor_484KY631963
Ciconia_sp_445KY631985
E15_Podocnemis_expansa_PeruKF049492
E24_Podocnemis_expansa_PeruKF049495
Gorilla_gorilla_34KY631983
Gorilla_gorilla_756KY631982
Gorilla_gorilla_761KY631981
P_sp._JA7_J725GU252027
Haemoproteus_majorisAY099045
Haemoproteus_sp.HM222472
Haemoproteus_sp._GA02CI1HM222486
Haemoproteus_sp._NA16K65HM222487
Hepatocystis_sp. AA201_blikeJQ070951
Hepatocystis_sp.JQ070884
Hepatocystis_sp._AA2012JQ070956
HO11_Cephalophus_nigrofonsKT367819
HO13_Cephalophus_monticolaKT367833
HO613_Cephalophus_monticolaKT367836
HO9_Kinixys_erosaKT367843
Homo_sapiens_476KY631978
Homo_sapiens_481KY631977
Homo_sapiens_57KY631979
Homo_sapiens_574KY631976
Homo_sapiens_635KY631975
Homo_sapiens_636KY631974
Homo_sapiens_638KY631973
Homo_sapiens_639KY631972
Homo_sapiens_668KY631969
Homo_sapiens_806KY631968
Homo_sapiens_832KY631967
Leucocytozoon_caulleryiAB302215
Leucocytozoon_dubreuliAY099063
Leucocytozoon_majorisFJ168563
Leucocytozoon_sabrazesiAB299369
M0278_Cephalophus_monticolaKT367834
NG238_Kinixys_erosaKT367844
NG277_Ceratogymna_atrataKT367825
NY195_Cephalophus_dorsalisKT367838
Nycteria_sp._R_alc_C9_1KF159720
Nycteria_sp._R_lan_G3_1KF159690
OI52_PangolinKT367818
OL123_Cephalophus_monticolaKT367822
OL131_Cephalophus_callipygusKT367830
P_adleriHM235081
P_azurophilumAY099055
P_billcollinsiKP875474
P_blacklockiHM235065
P_cynomolgiAB444126
P_falciparum_3D7AF069605
P_gaboniJF895307
P_gallinaceumAF069612
P_gonderiJF923751
P_knowlesiJQ345504
P_malariaeHM000110
P_ovaleGU723548
P_praefalciparum_MOEBJF923761
P_reichenowiKP875479
P_relictumAY733090
P_sp._DAJJF923753
P_vivaxKF591834
P_atheruriAY099054
P_giganteumAY099053
P_vinckei_isolate_1KJ700853
P_vinckei_isolate_2KJ700854
P_yoelii_killickiDQ414658
P. atheruriHQ712051
P. cyclopsi_Hip_cy_L4_1_SchaerKF159674
P. voltaicum_M_ang_G1_1_1KF159671
Parahaemoproteus_sp._bird_sp.17GQ141581
Parahaemoproteus_sp. _bird_sp.19GQ141585
Parahaemoproteus_vireonisFJ168561
Plasmodium_sp._birdGQ141574
Plasmodium_sp._bird_sp._12HM222485
Plasmodium_sp._GD2_GD201GU252012
Plasmodium_sp._lineage_JA01KM598212
Polychromophilus_melanipherus_haplotype_VIIIKJ131277
Polychromophilus_murinus_haplotype_3HM055585
Polychromophilus_sp._Min_vil_G3_2KF159699
Polychromophilus_sp._Pip_gran_G3_1KF159714
Polychromophilus_sp._Neo_cap_G3KF159700
Syncerus_caffer_1138KY631953
Syncerus_caffer_1417KY631942
Tragelaphus_eurycerus_1324KY631950
Tragelaphus_spekii_1051KY631961
Tragelaphus_spekii_1155KY631959
Tragelaphus_spekii_1175KY631958
Tragelaphus_spekii_1228KY631957
Tragelaphus_spekii_1245KY631956
Tragelaphus_spekii_1291KY631955
Tragelaphus_spekii_1299KY631954
Tragelaphus_spekii_1300KY631952
Tragelaphus_spekii_1306KY631951
Tragelaphus_spekii_1348KY631948
Tragelaphus_spekii_1386KY631946
Tragelaphus_spekii_1394KY631945
Tragelaphus_spekii_1399KY631944
Tragelaphus_spekii_1413KY631943
Tragelaphus_spekii_385KY631964
Tragelaphus_spekii_56KY631965
U65_Podocnemis_unifilis_PeruKF049506
Unknown_host_1036KY631960
Unknown_host_110KY631966
Unknown_host_512KY631962
Unknown_host_520KY631980
Unknown_host_649KY631971
Unknown_host_665KY631970
Unknown_host_819KY631984

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  1. Paul-Yannick Bitome-Essono
  2. Benjamin Ollomo
  3. Céline Arnathau
  4. Patrick Durand
  5. Nancy Diamella Mokoudoum
  6. Lauriane Yacka-Mouele
  7. Alain-Prince Okouga
  8. Larson Boundenga
  9. Bertrand Mve-Ondo
  10. Judicaël Obame-Nkoghe
  11. Philippe Mbehang-Nguema
  12. Flobert Njiokou
  13. Boris Makanga
  14. Rémi Wattier
  15. Diego Ayala
  16. Francisco J Ayala
  17. Francois Renaud
  18. Virginie Rougeron
  19. Francois 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