Trichomonas	gallinae	is	an	emerging	avian	pathogen	in	the	UK	and	across	Europe,	leading	to	

population	declines	in	songbirds	(especially	greenfinches	Carduelis	chloris)	where	prevalence	

is	high	(Robinson	et	al.,	2010).	The	parasite	is	present	worldwide,	and	elsewhere	it	is	

typically	a	pathogen	of	columbiformes,	where	it	can	have	population	limiting	effects	

(Bunbury	et	al.,	2008).	Recent	work	has	shown	a	high	prevalence	in	UK	columbiformes,	with	

the	highest	rates	of	infection	(86%)	in	the	migratory	European	Turtle	Dove	Streptopelia	

turtur (Lennon	et	al.,	2013).	Infected	individuals	do	not	necessarily	exhibit	clinical	signs,	and	

carriers	without	clinical	signs	may	transfer	disease	organisms	between	sites	during	migration	

(e.g.	Rappole et	al.,	2000)	and	exhibit	reduced	survival	(Bunbury	et	al.,	2008).	European	

Turtle	Doves	breeding	in	the	UK	are	thought	to	have	a	non-breeding	range	spanning	much	of	

the	Sahel	in	West	Africa,	coinciding	with	the	range	of	several	species	of	Afro-tropical	

columbids.	T.	gallinae may	be	transmitted between	infected	individuals	at	shared	food	and	

water	sources,	with	this	being	of	particular	concern	at	those	sites	utilised	by large	numbers

of	birds.	Such	events	may	be	frequent	in	the	Sahel,	where	birds	congregate	at	scarce	water	

sources	in	an	otherwise	arid	environment.	This	leads	to	concerns	that	intra-	and	interspecies

transmission	rates	may	be	high	during	the	non-breeding	period

Dunn, Jenny

Issa, Aly

Issa, Oumar

Sheehan, Danae

Thomas, Rebecca

University of Lincoln Institutional Repository

A	  report	  from	  a	  BOU-­‐funded	  Project	  Jenny	  Dunn	  et	  al	   Trichomonas	  galllinae	  infection	  in	  European	  Turtle	  Doves	  Streptopelia	  turtur	  in	  Africa	  and	  potential	  for	  transmission	  among	  co-­‐occurring	  African	  columbiformes	  	  ©	  The	  authors	  &	  BOU	  2014	  	  	   1	  Trichomonas galllinae infection in European Turtle Doves Streptopelia turtur in Africa and potential for transmission among co-occurring African columbiformes 	  JENNY	  C.	  DUNN1,	  REBECCA	  C.	  THOMAS2,	  DANAË	  K.	  SHEEHAN1,	  ALY	  ISSA3	  &	  OUMAR	  ISSA3	  1	  RSPB	  Centre	  for	  Conservation	  Science,	  RSPB,	  The	  Lodge,	  Potton	  Road,	  Sandy,	  Bedfordshire,	  SG19	  2DL,	  UK.	  2	  School	  of	  Biology,	  Irene	  Manton	  Building,	  University	  of	  Leeds,	  Leeds,	  LS2	  9JT,	  UK.	  3	  Fondation	  NATURAMA,	  Secteur	  30,	  01	  BP	  6133,	  Ouagadougou	  01,Burkina	  Faso.	  	  	  BACKGROUND Trichomonas	  gallinae	  is	  an	  emerging	  avian	  pathogen	  in	  the	  UK	  and	  across	  Europe,	  leading	  to	  population	  declines	  in	  songbirds	  (especially	  greenfinches	  Carduelis	  chloris)	  where	  prevalence	  is	  high	  (Robinson	  et	  al.,	  2010).	  The	  parasite	  is	  present	  worldwide,	  and	  elsewhere	  it	  is	  typically	  a	  pathogen	  of	  columbiformes,	  where	  it	  can	  have	  population	  limiting	  effects	  (Bunbury	  et	  al.,	  2008).	  Recent	  work	  has	  shown	  a	  high	  prevalence	  in	  UK	  columbiformes,	  with	  the	  highest	  rates	  of	  infection	  (86%)	  in	  the	  migratory	  European	  Turtle	  Dove	  Streptopelia	  turtur	  (Lennon	  et	  al.,	  2013).	  Infected	  individuals	  do	  not	  necessarily	  exhibit	  clinical	  signs,	  and	  carriers	  without	  clinical	  signs	  may	  transfer	  disease	  organisms	  between	  sites	  during	  migration	  (e.g.	  Rappole	  et	  al.,	  2000)	  and	  exhibit	  reduced	  survival	  (Bunbury	  et	  al.,	  2008).	  European	  Turtle	  Doves	  breeding	  in	  the	  UK	  are	  thought	  to	  have	  a	  non-­‐breeding	  range	  spanning	  much	  of	  the	  Sahel	  in	  West	  Africa,	  coinciding	  with	  the	  range	  of	  several	  species	  of	  Afro-­‐tropical	  columbids.	  T.	  gallinae	  may	  be	  transmitted	  between	  infected	  individuals	  at	  shared	  food	  and	  water	  sources,	  with	  this	  being	  of	  particular	  concern	  at	  those	  sites	  utilised	  by	  large	  numbers	  of	  birds.	  Such	  events	  may	  be	  frequent	  in	  the	  Sahel,	  where	  birds	  congregate	  at	  scarce	  water	  sources	  in	  an	  otherwise	  arid	  environment.	  This	  leads	  to	  concerns	  that	  intra-­‐	  and	  inter-­‐species	  transmission	  rates	  may	  be	  high	  during	  the	  non-­‐breeding	  period.	  	  	  STUDY SITES AND FIELD METHODS  The	  original	  site	  that	  had	  been	  selected	  for	  this	  study,	  in	  the	  north	  of	  Nigeria	  could	  not	  be	  used	  due	  to	  escalating	  security	  concerns	  in	  the	  region.	  Consequently,	  birds	  were	  sampled	  in	  Burkina	  Faso	  and	  Senegal	  (further	  details	  below).	  	  Doves	  –	  both	  migratory	  and	  resident	  species	  (further	  details	  below)	  –	  were	  caught	  using	  mist	  nets.	  	  Each	  bird	  was	  ringed	  using	  a	  metal	  ring	  (Ghana	  Ringing	  Scheme	  in	  Burkina	  Faso,	  BTO	  in	  Senegal)	  fitted	  to	  the	  tarsus,	  and	  standardised	  biometrics	  (wing	  length,	  tarsus	  length,	  weight;	  Redfern	  &	  Clark,	  2001)	  recorded.	  	  In	  Senegal,	  for	  a	  subset	  of	  birds	  of	  each	  species,	  we	  also	  recorded	  whether	  the	  bird	  was	  actively	  moulting,	  along	  with	  the	  primary	  moult	  score	  (Redfern	  &	  Clark,	  2001)	  to	  allow	  us	  to	  assess	  whether	  delayed	  moult	  may	  be	  associated	  with	  parasite	  infection.	  	  	  	  	  	  A	  report	  from	  a	  BOU-­‐funded	  Project	  Jenny	  Dunn	  et	  al	   Trichomonas	  galllinae	  infection	  in	  European	  Turtle	  Doves	  Streptopelia	  turtur	  in	  Africa	  and	  potential	  for	  transmission	  among	  co-­‐occurring	  African	  columbiformes	  	  ©	  The	  authors	  &	  BOU	  2014	  	  	   2	  Burkino	  Faso	  The	  study	  site	  in	  Burkina	  Faso	  was	  located	  at	  Oursi,	  in	  the	  far	  north-­‐east	  of	  the	  country	  (14.67°N,	  0.46°W).	  Catching	  and	  sampling	  of	  turtle	  doves	  and	  other	  Afro-­‐tropical	  Streptopelia	  species	  was	  carried	  out	  between	  October	  2012	  and	  Feb	  2013	  by	  AI	  and	  OI,	  using	  mist	  nets	  erected	  at	  regularly	  used	  roost	  sites.	  	  Samples	  were	  collected	  from	  a	  total	  of	  139	  doves:	  36	  European	  Turtle	  Doves	  Streptopelia	  turtur,	  88	  Laughing	  Doves	  Streptopelia	  senegalensis,	  3	  African	  Collared	  Doves	  Streptopelia	  roseogrisea,	  4	  Vinaceous	  Doves	  Streptopelia	  vinacea,	  and	  8	  Mourning	  Doves	  Streptopelia	  decipiens.	  	  However,	  despite	  considerable	  effort,	  the	  necessary	  export	  permits	  were	  not	  forthcoming	  within	  the	  required	  time	  scale.	  These	  samples	  are	  currently	  still	  in	  cold	  storage	  in	  Ouagadougou,	  but	  are	  now	  likely	  to	  have	  deteriorated	  beyond	  the	  point	  at	  which	  there	  would	  be	  any	  value	  in	  pursuing	  their	  export.	  	  Senegal	  The	  study	  site	  in	  Senegal	  was	  located	  approximately	  6km	  to	  the	  south	  of	  Sandiara,	  to	  the	  south-­‐east	  of	  Dakar	  (14.38°N,	  16.81°W),	  within	  an	  area	  of	  enclosed	  acacia	  scrub	  where	  estimates	  placed	  the	  number	  of	  wintering	  European	  turtle	  doves	  at	  around	  1000	  individuals.	  	  JCD	  and	  RCT	  visited	  the	  site	  for	  12	  days	  during	  late-­‐February	  and	  early	  March	  2014,	  with	  6	  species	  of	  dove	  observed	  to	  be	  using	  the	  site	  to	  roost	  (European	  Turtle	  Dove,	  Laughing	  Dove,	  Vinaceous	  Dove,	  Mourning	  Collared	  Dove,	  Namaqua	  Dove	  Oena	  capensis	  and	  Black-­‐Billed	  Wood	  Dove	  Turtur	  abyssinicus).	  	  Doves	  were	  caught	  using	  a	  combination	  of	  two-­‐shelf	  wader	  mist	  nets	  and	  four-­‐shelf	  Japanese	  mist	  nets	  (whoosh	  nets	  with	  which	  to	  specifically	  target	  Turtle	  Doves	  had	  been	  lost	  by	  the	  airline	  on	  route)	  positioned	  near	  a	  water	  source	  where	  doves	  had	  been	  observed	  drinking	  in	  small	  flocks.	  	  	  	  Samples	  were	  collected	  from	  a	  total	  of	  130	  doves	  of	  5	  species:	  11	  European	  Turtle	  Doves,	  30	  Laughing	  Doves,	  1	  Vinaceous	  Dove,	  73	  Namaqua	  Doves	  and	  19	  Black-­‐billed	  Wood	  Doves.	  	  Two	  Namaqua	  doves	  and	  two	  black-­‐billed	  wood	  doves	  were	  re-­‐trapped	  within	  the	  capture	  period,	  but	  were	  not	  re-­‐sampled.	  	  Trichomonas	  sampling	  methodology	  All	  birds	  that	  were	  ringed	  were	  sampled	  for	  the	  presence	  of	  Trichomonas	  gallinae	  parasites	  by	  taking	  an	  oral	  swab	  as	  described	  by	  Lennon	  et	  al.	  (2013).	  	  	  Once	  the	  oral	  cavity	  and	  upper	  gastrointestinal	  tract	  had	  been	  swabbed,	  each	  swab	  was	  immediately	  used	  to	  inoculate	  a	  uniquely	  identifiable,	  individual	  ‘InPouch’	  Culture	  kit	  (BioMed	  diagnostics,	  Oregon,	  US).	  Culture	  kits	  were	  then	  incubated	  for	  a	  minimum	  of	  72	  hrs	  at	  37˚C	  before	  the	  parasites	  were	  isolated	  and	  stored	  in	  PBS	  prior	  to	  export	  to	  the	  UK.	  	  A	  report	  from	  a	  BOU-­‐funded	  Project	  Jenny	  Dunn	  et	  al	   Trichomonas	  galllinae	  infection	  in	  European	  Turtle	  Doves	  Streptopelia	  turtur	  in	  Africa	  and	  potential	  for	  transmission	  among	  co-­‐occurring	  African	  columbiformes	  	  ©	  The	  authors	  &	  BOU	  2014	  	  	   3	  MOULT Analysis	  of	  variance	  of	  the	  subsample	  of	  individuals	  from	  which	  moult	  data	  were	  collected	  (n=55)	  indicated	  significant	  differences	  in	  moult	  score	  between	  species	  (F4,51=3.14,	  p=0.02),	  with	  the	  European	  Turtle	  Dove	  being	  further	  ahead	  in	  its	  moult	  that	  the	  four	  resident	  species	  (Figure	  1).	  	  Further	  analysis	  will	  assess	  whether	  parasite	  infection	  is	  linked	  to	  delayed	  moult	  within	  species.	  	  	  	   Figure	  1.	  Mean	  ±	  1	  SE	  moult	  score	  for	  the	  five	  dove	  species	  caught	  in	  Senegal	    ANALYSIS OF TRICHOMONAS SAMPLES  Laboratory	  analyses	  of	  samples	  collected	  during	  this	  work	  are	  expected	  to	  be	  complete	  in	  autumn	  2014,	  and	  results	  will	  be	  presented	  in	  a	  paper	  to	  be	  submitted	  for	  publication	  early	  in	  2015.	  	  	  ACKNOWLEDGEMENTS This	  project	  was	  awarded	  a	  research	  grant	  of	  £2000	  from	  the	  BOU	  in	  2012,	  and	  was	  also	  supported	  by	  the	  African	  Bird	  Club	  and	  the	  RSPB.	  	  We	  are	  extremely	  grateful	  for	  the	  BOU’s	  generous	  contribution,	  which	  met	  the	  cost	  of	  Trichomonas	  culture	  pouches	  and	  field	  equipment.	  	  Research	  in	  Burkina	  Faso	  was	  carried	  out	  with	  the	  permission	  of	  the	  Director	  of	  Wildlife	  and	  Hunting,	  and	  research	  in	  Senegal	  was	  carried	  out	  under	  a	  permit	  granted	  by	  Direction	  des	  Eaux,	  Forêts,	  Chasses	  et	  de	  la	  Conservation	  des	  Sols.	  	  Samples	  were	  imported	  to	  the	  UK	  under	  licences	  PATH/201/2012/1	  and	  PATH/201/2012/2.	  	  0	  5	  10	  15	  20	  25	  30	  35	  40	  45	  50	  Black-­‐billed	  wood	  dove	   European	  Turtle	  Dove	   Laughing	  dove	   Namaqua	  dove	   Vinaceous	  dove	  Moult	  score	  A	  report	  from	  a	  BOU-­‐funded	  Project	  Jenny	  Dunn	  et	  al	   Trichomonas	  galllinae	  infection	  in	  European	  Turtle	  Doves	  Streptopelia	  turtur	  in	  Africa	  and	  potential	  for	  transmission	  among	  co-­‐occurring	  African	  columbiformes	  	  ©	  The	  authors	  &	  BOU	  2014	  	  	   4	  REFERENCES Bunbury,	  N.,	  Jones,	  C.	  G.,	  Greenwood,	  A.	  G.,	  &	  Bell,	  D.	  J.	  2008.	  Epidemiology	  and	  conservation	  implications	  of	  Trichomonas	  gallinae	  infection	  in	  the	  endangered	  Mauritian	  Pink	  Pigeon.	  Biol.	  Conserv.,	  141,	  153–161.	  Lennon,	  R.	  J.,	  Dunn,	  J.	  C.,	  Stockdale,	  J.,	  Goodman,	  S.	  J.,	  Morris,	  A.	  J.,	  &	  Hamer,	  K.	  C.	  2013.	  Trichomonad	  parasite	  infection	  in	  four	  species	  of	  Columbidae	  in	  the	  UK.	  Parasitol.,	  140,	  1368–1376.	  Rappole,	  J.	  H.,	  Derrickson,	  S.	  R.,	  &	  Hubálek,	  Z.	  2000.	  Migratory	  birds	  and	  spread	  of	  West	  Nile	  virus	  in	  the	  Western	  Hemisphere.	  Emer.	  Infect.	  Dis.,	  6,	  319–28.	  Redfern,	  C.,	  &	  Clark,	  J.	  2001.	  Ringers’	  Manual.	  Thetford:	  British	  Trust	  for	  Ornithology.	  Robinson,	  R.	  A.,	  Lawson,	  B.,	  Toms,	  M.	  P.,	  Peck,	  K.	  M.,	  Kirkwood,	  J.	  K.,	  Chantrey,	  J.,	  Clatworthy,	  I.	  R.,	  Evans,	  A.	  D.,	  Hughes,	  L.	  A.,	  Hutchinson,	  O.	  C.,	  John,	  S.	  K.,	  Pennycott,	  T.	  W.,	  Perkins,	  M.	  W.,	  Rowley,	  P.	  S.,	  Simpson,	  V.	  R.,	  Tyler,	  K.	  M.	  &	  Cunningham,	  A.	  A.	  2010.	  Emerging	  infectious	  disease	  leads	  to	  rapid	  population	  declines	  of	  common	  British	  birds.	  PloS	  One,	  5,	  e12215.	  	  	  

Trichomonas galllinae infection in European turtle doves Streptopelia turtur in Africa and potential for transmission among co-occurring African columbiformes

Trichomonas galllinae infection in European turtle doves Streptopelia turtur in Africa and potential for transmission among co-occurring African columbiformes

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