The oviduct fluke, Prosthogonimus species in wild birds, Türkiye

Abstract

Background
Prosthogonimus species is considered one of the most important pathogen parasites of poultry and wild birds because it causes defective egg formation, and deaths can be seen as a result of peritonitis. The genus Prosthogonimus is all‐around and has been reported in many areas worldwide. This study is research on the presence of Prosthogonimus species, one of the most pathogen trematodes of birds, in Türkiye and wild birds.

Objective
We conducted the present study to investigate the presence and prevalence of Prosthogonimus spp. in Türkiye.

Methods
We studied 183 individuals of 62 wild bird species in the Kızılırmak Delta. Wild birds that died naturally were necropsied and searched for oviducal flukes.

Results
After performing our parasitological study, we found that 4/180 birds were infected with Prosthogonimus spp. Aythya ferina, Ciconia ciconia, Erithacus rubecula and Turdus philomelos were infected with Prosthogonimus pellucidus, Prosthogonimus macrorchis, Prosthogonimus cuneatus and Prosthogonimus ovatus, respectively. Prosthogonimus species was reported for the first time from Türkiye, together with all species found.

Conclusion
The presence of Prosthogonimus species in Türkiye and wild birds was determined. We constructed a key of our found Prosthogonimus species based on their morphological characters.

Full text

DOI: 10.1002/vms3.1209
ORIGINAL ARTICLE
The oviduct fluke, Prosthogonimus species in wild birds, Türkiye
Mehmet Öztürk ¸Sinasi Umur
Department of Parasitology, Faculty of
Veterinary Medicine, Ondokuz Mayıs
University, Samsun, Turkey
Correspondence
Mehmet Öztürk, Department of Parasitology,
Faculty of Veterinary Medicine, Ondokuz
Mayıs University,Samsun, Turkey.
Email: 19220155@stu.omu.edu.tr
Funding information
Türkiye Bilimsel ve Teknolojik Ara¸stırma
Kurumu, Grant/AwardNumber: 222O228
Abstract
Background: Prosthogonimus species is considered one of the most important pathogen
parasites of poultry and wild birds because it causes defective egg formation, and
deaths can be seen as a result of peritonitis. The genus Prosthogonimus is all-around and
has been reported in many areas worldwide. This study is research on the presence of
Prosthogonimus species, one of the most pathogen trematodes of birds, in Türkiye and
wild birds.
Objective: We conducted the present study to investigate the presence and preva-
lence of Prosthogonimus spp. in Türkiye.
Methods: We studied 183 individuals of 62 wild bird species in the Kızılırmak Delta.
Wild birds that died naturally were necropsied and searched for oviducal flukes.
Results: After performing our parasitological study, we found that 4/180 birds were
infected with Prosthogonimus spp. Aythya ferina,Ciconia ciconia,Erithacus rubecula
and Turdus philomelos were infected with Prosthogonimus pellucidus,Prosthogonimus
macrorchis,Prosthogonimus cuneatus and Prosthogonimus ovatus, respectively. Prosthogo-
nimus species was reported for the first time from Türkiye, together with all species
found.
Conclusion: The presence of Prosthogonimus species in Türkiye and wild birds was
determined. We constructed a key of our found Prosthogonimus species based on their
morphological characters.
KEYWORDS
oviduct fluke, Prosthogonimus, Türkiye, wild birds
1INTRODUCTION
Prosthogonimus is a genus of trematodes belonging to the family
Prosthogonimidae and includes several species. First, Hanow, 1753
found two specimens in a newly laid chicken egg. These specimens were
later determined as Prosthogonimus ovatus. The genus Prosthogonimus
was created by Lühe in 1899, based on P. ov at us. These flatworms infect
the bursa Fabricius, the oviduct and the posterior intestine of various
poultry and wild bird species, including chicken, ducks, geese and other
birds. The genus Prosthogonimus is widespread and has been reported
This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any
medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.
© 2023 The Authors. Veterinary Medicine and Science published by John Wiley & Sons Ltd.
in many regions worldwide, including Africa, Asia, Europe, North and
South America (Boddeke, 1960;Macy,1934).
The adult parasites live in the oviducts of the definitive host and
excrete their eggs in the host’s faeces. The freshwater snail takes up
these eggs, which act as the first intermediate host. In the intestines of
infected freshwater snails, miracidium-sporocyst-daughter sporocyst-
cercariae forms develop. The cercariae leave the freshwater snail
and infect the dragonfly nymph. Metacercariae forms develop in the
dragonfly’s body, which acts as a second intermediate host. The defini-
tive hosts become infected by ingesting infected dragonfly nymphs
Vet Med Sci. 2023;9:2329–2335. wileyonlinelibrary.com/journal/vms3 2329

2330 ÖZTÜRK and UMUR
or dragonflies. The adult parasites are placed in the final host’s bursa
Fabricius, oviduct and cloaca. In the definitive host, poultry and wild
birds, it can cause eggshells to be absent or thin and/or deformed shell
eggs. The resulting damage can rarely cause rupture, peritonitis and
death. A milk-like discharge comes from the cloaca of infected final
hosts. It is assumed to be one of the most pathogenic trematodes of
avians due to the harm it causes (Soulsby, 1982).
The Kızılırmak Delta, located in the Bafra district of Samsun
province, is one of the 13 Ramsar sites of Türkiye. There is a bird
sanctuary within the borders of the Kızılırmak Delta, which Ramsar,
an international convention, protects. The natural migration routes of
wild birds pass through the country, and many migratory birds stay in
the Kızılırmak Delta. Approximately 360 of the nearly 500 bird species
identified so far in Türkiye have been ringed in the Kızılırmak Delta
Bird Sanctuary (Karata¸setal.,2021). Approximately 850 bird species
are in the Western Palearctic area, which is west of the Ural Mountains
and includes the Middle East and North Africa. In the Kızılırmak Delta,
40% of the birds of the Western Palearctic area and 73% of the birds
of Türkiye can be seen, and 170 birds were found to breed within the
delta borders (DKMP, 2021).
2MATERIALS AND METHODS
In order to investigate the presence and prevalence of Prosthogonimus
in Türkiye, we investigated 183 individuals of 62 wild bird species. The
examined bird species are given in the table based on groups (Table 1).
These wild bird species died naturally and were collected between
2018 and 2023 in the Kızılırmak delta. They were then transported to
the Faculty of Veterinary Medicine, Ondokuz Mayıs University, for a
necropsy. As a result of the parasitological examination, parasites were
encountered and preserved in 70% ethanol for morphological analysis
before identification. The specimens were stained within Semichon’s
carmine and mounted with Canada balsam. Then, the parasites were
identified using the morphological features under a Nikon Eclipse 80i
light microscope. The special morphological characters were measured
and photographed using the MDX4—T Mshot camera integrated into
the microscope and then drawn with Adobe Illustrator 2020.
3RESULTS
After conducting a parasitological examination, we found that only 4
out of the 183 examined birds were infected with Prosthogonimus spp.
We determined the parasites found using the relevant articles (Bod-
deke, 1960; Heneberg et al., 2015;Macy,1934, 1965). Aythya ferina,
Ciconia ciconia, Erithacus rubecula and Turdus philomelos were infected
with Prosthogonimus pellucidus,P. macrorchis,P. cuneatus and P. ovatu s,
respectively.
3.1 Prosthogonimus cuneatus (Figure 1a,b)
Species identification card
Host: Erithacus rubecula
TAB LE 1 The list of bird species.
Accipitriformes Gaviiformes Regulus regulus
Accipiter nisus (3) Gavia arctica Saxicola torquatus
Haliaeetus albicilla Gruiformes Spinus spinus
Anseriformes Gallinula chloropus Sturnus vulgaris
Anas platyrhynchos (4) Rallus aquaticus Sylvia atricapilla (4)
Aythya ferinaaFalconiformes Sylvia borin (5)
Mareca strepera Buteo buteo (8) Sylvia communis
Mergus albellus Buteo rufinus (4) Sylvia nisoria
Netta rufina Circus aeruginosus Turdu s me rula (7)
Apodiformes Pernis apivorus Turdus philomelosd(6)
Apus apus (5) Passeriformes Pelecaniformes
Caprimulgiformes Aegithalos caudatus Ardea alba
Caprimulgus europaeus Corvus corax Ardea cinerea
Charadriiformes Corvus cornix (3) Ardea purpurea
Chroicocephalus
ridibundus
Cyanistes caeruleus Botaurus stellaris
Larus cachinnans (10) Delichon urbicum (2) Egretta garzetta (14)
Scolopax rusticola (2) Erithacus rubeculac(16) Podicipediformes
Columbiformes Ficedula hypoleuca Podiceps cristatus (3)
Columba livia (19) Fringilla coelebs (2) Tachybaptus ruficollis
Spilopelia senegalensis Luscinia luscinia Strigiformes
Streptopelia turtur Luscinia svecica Aegolius funereus
Coraciiformes Passer domesticus (4) Asio otus
Alcedo atthis Phoenicurus phoenicurus Athene noctua
Ciconiiformes Phylloscopus collybita (5) Tyt o al ba
Ciconia ciconiab(7) Phylloscopus trochilus (8) Suliformes
Ciconia nigra Prunella modularis Phalacrocorax carbo
a–dHave been infected with Prosthogonimus pellucidus, Prosthogonimus
macrorchis, Prosthogonimus cuneatus and Prosthogonimus ovatus, respec-
tively.
Site of infection: Bursa Fabricii
Locality: Bafra, Samsun, (41◦36′N36
◦05′E), Black Sea Region,
Türkiye.
Material deposited: Specimens were deposited in the Helminth
Coll. No. OMUPAR.842.23.01 Department of Parasitology, Faculty of
Veterinary Medicine, Ondokuz Mayıs University, Samsun, Türkiye.
3.1.1 Description
Body oval, with maximum width at the level of testes, length 2705 µm
full width 1463 µm, length: width ratio 1.84 µm. Oral sucker subter-
minal, round 178 ×175 µm. Ventral sucker at the end of the anterior
third of the body, broadly oval 521 ×564 µm, oral: ventral sucker
length ×width ratio 2, 92 ×3,22 µm prepharynx absent, pharynx
broadly oval 72 ×95 µm. Testes without lobation, elongated oval, in
the medial part of the body, left testes 345 ×242 µm, right testes

ÖZTÜRK and UMUR 2331
FIGURE 1 Prosthogonimus cuneatus was recovered in Erithacus rubecula. They were drawn with Adobe Illustrator 2020 (a) and coloured with
Semichon’s carmine (b). Bar: 1000 µm.
342 ×220 µm. Cirrus extending distal to intestinal bifurcation, size
479 ×70 µm. Genital pore lateral on the anterior border of oral sucker.
Ovary broadly oval, lobular and partway surrounding the posterior
border of ventral sucker 312 ×320 µm. Vitelline glands, follicles in
typical rosettes, enclosing the whole area between the body margin
and intestinal ceca, branches near longer, left vitelline gland 1340 µm,
right vitelline gland 1441 µm. The uterus is distinct; its coils fill the
whole area posterior to the testes up to the body margin and cover the
intestinal ceca and partial borders of the testes. Eggs, 26 ×15 µm.
3.2 Prosthogonimus macrorchis (Figure 2a,b)
Species identification card
Host: Ciconia ciconia
Site of infection: Bursa Fabricii
Locality: Bafra, Samsun, (41◦36′N36
◦05′E), Black Sea Region,
Türkiye.
Material deposited: Specimens were deposited in the Helminth
Coll. No. OMUPAR.871.23.01 Department of Parasitology, Faculty of
Veterinary Medicine, Ondokuz Mayıs University, Samsun, Türkiye.
3.2.1 Description
Body pear-shaped, with maximum width at the level of testes, length
6995 µm full width 4318 µm, length: width ratio 1.61 µm. Oral sucker
subterminal, oval 574 ×518 µm. Ventral sucker at the end of the ante-
rior third of the body, round 1131 ×1107 µm, oral: ventral sucker
length ×width ratio 1,97 ×2,13 µm. Prepharynx absent, pharynx
broadly oval 263 ×286 µm. Testes without lobation, oval, as symmet-
ric in the medial part of the body, left testes 1052 ×1153 µm, right
testes 1086 ×1025 µm. Cirrus is not extending distal to intestinal
bifurcation, size 1490 µm. Genital pore lateral on the anterior edge of
oral sucker. Ovary broadly oval, lobular and partially covering poste-
rior edge of ventral sucker 726 ×896 µm. Vitelline glands, follicles in
typical rosettes, broad, the surrounding area between body margin and
intestinal ceca, extended posteriorly to the midline of testes, branches
near longer, left vitelline gland 3335 µm, right vitelline gland 3320 µm.
The uterus is distinct; its coils fill the total area posterior to the testes
up to the body margin and cover the testes’ intestinal ceca and partial
borders. Eggs, 22 ×13 µm.
3.3 Prosthogonimus ovatus (Figure 3a,b)
Species identification card
Host: Turdus philomelos
Site of infection: Bursa Fabricii
Locality: Bafra, Samsun, (41◦36′N36
◦05′E), Black Sea Region,
Türkiye.
Material deposited: Specimens were deposited in the Helminth
Coll. No. OMUPAR.841.23.01 Department of Parasitology, Faculty of
Veterinary Medicine, Ondokuz Mayıs University, Samsun, Türkiye.
3.3.1 Description
Body pear-shaped, with the greatest width at the level of testes, length
2367 µm, maximum width 1094 µm, length: width ratio 2.16 µm.
Oral sucker subterminal, round 166 ×146 µm. Ventral sucker at the
end of the anterior third of the body, broadly oval 280 ×314, oral:

2332 ÖZTÜRK and UMUR
FIGURE 2 Prosthogonimus macrorchis was recovered in Ciconia ciconia. They were drawn with Adobe Illustrator 2020 (a) and coloured with
Semichon’s carmine (b). Bar: 1000 µm.
FIGURE 3 Prosthogonimus ovatus was recovered in Turdus philomelos. They were drawn with Adobe Illustrator 2020 (a) and coloured with
Semichon’s carmine (b). Bar: 1000 µm.
ventral sucker length ×width ratio 1,68 ×2,15 µm. Prepharynx absent,
pharynx round, broadly oval 111 ×129 µm. Testes without lobation,
elongate oval, asymmetrically in the medial part of the body, left testes
487 ×293 µm, right testes 456 ×364 µm. Cirrus is not extending dis-
tal to intestinal bifurcation, size 494 µm. Genital pore sideways on the
anterior border of the oral sucker. Ovary lobular and partially covering
anterior side of ventral sucker 373 ×357 µm. Vitelline glands, follicles
in regular rosettes, relatively wide, encompassing whole area between
body margin and intestinal ceca, one branch longer than the other,
anterior edge slightly anteriorly of ventral sucker, posterior edge in dis-
tal from posterior margin of testes, left vitelline gland 1062 µm, right
vitelline gland 876 µm. The uterus is indistinct, and its coils fill the area

ÖZTÜRK and UMUR 2333
FIGURE 4 Prosthogonimus pellucidus was recovered in Aythya ferina. They were drawn with Adobe Illustrator 2020 (a) and coloured with
Semichon’s carmine (b). Bar: 1000 µm.
posterior to the testes up to the intestinal ceca and borders of the body
margin. Eggs, 29 ×17 µm.
3.4 Prosthogonimus pellucidus (Figure 4a,b)
Species identification card
Host: Aythya ferina
Site of infection: Bursa Fabricii
Locality: Bafra, Samsun, (41◦36′N36
◦05′E), Black Sea Region,
Türkiye.
Material deposited: Specimens were deposited in the Helminth
Coll. No. OMUPAR.832.23.01 Department of Parasitology, Faculty of
Veterinary Medicine, Ondokuz Mayıs University, Samsun, Türkiye.
3.4.1 Description
Body pear-shaped, with the highest width at the level of testes, length
2616 µm, highest width 1207 µm, length: width ratio 2.16 µm. Oral
sucker subterminal, oval 268 ×227 µm. Ventral sucker at the end of
the anterior third of the body, round 407 ×378 µm, oral:ventral sucker
length ×width ratio 1,51 ×1,36 µm. Prepharynx absent, pharynx oval
104 ×130 µm. Testes without lobation elongate, as symmetrical in the
medial part of the body, with left testes 184 ×140 µm and right testes
216 ×90 µm. Cirrus is outstretching distal to intestinal bifurcation,
size 515 µm. Genital pore sideways on the anterior border of the oral
sucker. Ovary oval and lobular and is not in contact with the poste-
rior margin of the ventral sucker, size 212 ×183 µm. Vitelline glands,
follicles in typical rosettes, encompassing the whole area between the
surrounding area between the posterior edge of the ventral sucker and
the posterior edge of the testis, branches same longer, left vitelline
gland 719 µm, right vitelline gland 719. The uterus does not fill the
whole area from the testes to the body margin. Eggs, 25 ×16 µm.
4DISCUSSION
Prosthogonimus species have two intermediate hosts and one definitive
host. Anisus sp., Bithynia sp., Gyraulus sp., Planorbarius sp. and Viviparus
sp. species have been reported from the first host, freshwater snails,
whereas Aeschna sp., Anax sp., Cordulia sp., Epitheca sp., Gomphus sp.,
Leucorrhinia sp., Libellula sp., Orthetrum sp., Platycnemis sp., Somatochlora
sp. and Sympetrum sp. have been reported from the second host, drag-
onfly nymphs or dragonflies (Boddeke, 1960; Heneberg et al., 2015). All
freshwater snail species of Prosthogonimus reported as the first inter-
mediate hosts have been reported in Türkiye (Gürlek et al., 2019).
Among the Odonata species reported as the second intermediate host
of Prosthogonimus, all species, except Epitheca sp., have been reported
in Türkiye (Kalkman et al., 2003). Since the intermediate host species
of Prosthogonimus species are found in Türkiye, and the wild birds in
the Kızılırmak delta are migratory, our opinion that the presence of
Prosthogonimus species poses a danger both for poultry and wild birds
in the region and for other countries where wild birds migrate.
Prosthogonimus species distribute widely throughout the world. As a
result of the study in the Czech Republic, P. cuneatus, P. ovatus, P. pellu-
cidus and Prosthogonimus rarus species were reported (Heneberg et al.,
2015). In a study conducted in Korea, P. cuneatus was reported in a little
grebe (Tachybaptus ruficollis) (Cheong et al., 2010). A study was con-
ducted on chickens in Indonesia, and the P. ov at us specie was reported

2334 ÖZTÜRK and UMUR
(Leok et al., 2002). P. macrorchis was described in the albumen of an
egg in Iran (Naem & Golpayegani, 2003). In a study conducted in Pak-
istan, researchers examined pet birds’ faeces and blood samples and
reported the presence of P. ov atu s and P. macrorchis (Sadaf et al., 2021).
Prosthogonimus spp. has been shown among trematodes seen in chick-
ens in Türkiye (Ünlü, 2012), despite when the citations were examined,
it was seen that any Prosthogonimus species had not been reported in
Türkiye before (Güçlü, 1992; Merdivenci, 1967; Özdal & Ayaz, 2015;
Tolg ay, 1973; Yardibi, 2004).
In Indonesia, an accidental report of Prosthogonimus sp. was
reported in a 9-month-old infant (Sutanto, 1974).
Key of found species:
1. The body length of adult specimens is more than 6000 µm,
and cirrus does not extend distally to the intestinal bifurca-
tion........................P. macrorchis.
The body length of adult specimens is less than
3000 µm............2.
2. The uterus is indistinct, and its coils fill the area; the ovary is in con-
tact with the anterior margin of the ventral sucker, and cirrus does
notextenddistallytotheintestinalbifurcation............P. ova tus .
Cirrusextends distallytotheintestinalbifurcation...............3.
3. The uterus does not fill the whole area from the testes to the body
margin, and the ovary is not in contact with the posterior margin of
theventralsucker............P. pellucidus.
The uterus is distinct, and its coils fill the area; the
ovary is in contact with the posterior margin of the ventral
sucker........................................P. cu ne at u s.
5CONCLUSION
As a consequence of this research, P. cuneatus,P. ova tu s,P. pellucidus
and P. macrorchis species were reported for the first time in Türkiye.
Although the birds analysed in this study were collected in Türkiye,
they are significant for other countries where they migrate because
they are migratory birds.
Although Prosthogonimus sp. is thought to be accidentally transmit-
ted in a 9-month-old infant, many parasites affect human and animal
health in wildlife. More studies on these parasites in Türkiye should be
increased and supported.
AUTHOR CONTRIBUTIONS
In this research, the first author (Mehmet Öztürk) investigates the
methodology, project administration, laboratory work and manuscript
write-up, whereas the second author (¸Sinasi Umur) contributes to
supervision and manuscript write-up.
ACKNOWLEDGEMENTS
The first author is a PhD student in the 100/2000 YÖK Doctorate
Programs.
CONFLICT OF INTEREST STATEMENT
The authors declare they have no financial or non-financial conflicts of
interest.
ETHICS STATEMENT
The authors confirm that the ethical policies of the journal, as noted
on the journal’s author guidelines page, have been adhered to. Specific
Ethics and Welfare Committee approval was not required as the wild
birds used in the studies died naturally and were not interfered with in
any way.
DATA AVAILABILITY STATEMENT
All data in this study are obtainable from the corresponding authors
upon reasonable request.
ORCID
Mehmet Öztürk https://orcid.org/0000-0002- 3559-0587
¸Sinasi Umur https://orcid.org/0000-0001- 9766-2817
TRANSPARENT PEER REVIEW
The peer review history for this article is available at https://publons.
com/publon/10.1002/vms3.1209.
REFERENCES
Boddeke, R. (1960). The life history of Prosthogonimus ovatus Rudolphi.
I. Experiments in birds. II. The intermediate hosts. III. Taxonomy and
economical aspects. Tropical and Geographical Medicine,12, 263–387.
Cheong, K. S., Kim, J. T., Ahn, D. C., Jung, B. D., Park, B. K., & Kim, H. C. (2010).
First record of Prosthogonimus cuneatus (Prosthogonimidae) from the lit-
tle grebe, Tachybaptus ruficollis, in Korea. The Korean Journal of Veterinary
Research,50(1), 71–74.
DKMP (2021). Ringing report. (Accessed 26 April 2023). https://www.
tarimorman.gov.tr/DKMP/Duyuru/439/2021-Halkalama-Raporu
Güçlü, F. (1992). Ankara civarında tavuk, hindi, ördek ve kazlarda helmint
faunası (Dissertation). University of Ankara.
Gürlek, M. E., ¸Sahin, S. K., Dökümcü, N., & Yıldırım, M. Z. (2019). Checklist
of the freshwater Mollusca of Turkey (Mollusca: Gastropoda, Bivalvia).
Fresenius Environment Bulletin,28(4), 2992–3013.
Heneberg, P., Sitko, J., & Bizos, J. (2015). Integrative taxonomy of cen-
tral European parasitic flatworms of the family Prosthogonimidae Lühe,
1909 (Trematoda: Plagiorchiida). Parasitology International,64(5), 264–
273. https://doi.org/10.1016/j.parint.2015.02.003
Kalkman, V.J., Wasscher, M., & Van Pelt, G. J.(2003). An annotated checklist
of the Odonata of Turkey. Odonatologica,32(3), 215–236.
Karata¸s, A., Erciyas, Y. K., Yavuz, N., Ünlü, M., Necipo˘
glu, Ö., Kahraman, V.,
Salman, M., Özkoç, Ö. Ü., Bacak, E., Kulaço˘
glu, K. C., Kurnuç, Z., Gezgin,
C., Güngör, U., Özkan, K., Döndüren, Ö., Kap, B., & Yeltekin, O. Ö. (2021).
Tra ku ¸sTürkiye’ninKu¸sları (1st ed.). Türkiye ˙
I¸s Bankası Kültür Yayınları.
Leok, C. S., Inoue, I., Sato, T., Haritani, M., Tanimura, N., & Okada, K.
(2002). Morphology of the oviduct fluke, Prosthogonimus ovatus,iso-
lated from Indonesian native chickens and histopathological observation
of the infected chickens. Journal of Veterinary Medical Science,64(12),
1129–1131. https://doi.org/10.1292/jvms.64.1129
Macy, R. W. (1934). Prosthogonimus macrorchis n. sp., the common oviduct
fluke of domestic fowls in the northern United States. Transactions of the
American Microscopical Society,53(1), 30–34. https://doi.org/10.2307/
3222333

ÖZTÜRK and UMUR 2335
Macy, R. W. (1934). Studies on the taxonomy, morphology and biology of
Prosthogonimus macrorchis. Macy, a common oviduct fluke of domestic
fowls in North America. Bulletin: Agricultural Experiment Station, University
of Minnesota,98, 71, https://doi.org/10.2307/3222333
Macy, R. W. (1965). On the life cycle of the trematode Prosthogonimus
cuneatus (Rudolphi, 1809) (Plagiorchiidae) in Egypt. Transactions of the
American Microscopical Society,84(4), 577–580. https://doi.org/10.2307/
3224804
Merdivenci, A. (1967).Türkiye’nin Marmara Bölgesinde Evcil Tavuk, Hindi,
Ördek ve Kazlarda Görülen Trematod, Sestod ve Nematodlara Dair Ara¸stır-
malar.˙
Ist Üniv Tıp Fak Yay. No 37, Kutulmu¸sMatb.
˙
Istanbul.
Naem, S., & Golpayegani, M. H. (2003). Prosthogonimus macrorchis in the
albumin of the egg from Sari, Iran. Iranian Journal of Veterinary Research,
4(2), 160–162.
Özdal, N., & Ayaz, E. (2015). Van’da bir tavuk otopsisinde gördü˘
gümüz
helmintler. Yüzüncü Yıl Üniversitesi Veteriner FakültesiDergisi,16(2), 7–10.
Sadaf, T., Javid, A., Hussain, A., Bukhari, S. M., Hussain, S. M., Ain, Q., Ashraf,
S., Suleman, S., Saleem, M., Azam, S. M., Ahmad, U., & Ali, W. (2021). Stud-
ies on parasitic prevalence in pet birds from Punjab, Pakistan. Brazilian
Journal of Biology: Revista Brasileira de Biologia,83, e246229. https://doi.
org/10.1590/1519-6984.246229
Soulsby, E. J. L. (1982). Helminths, Arthropods and Protozoa of Domesticated
Animals (7th ed.). Bailliere Tindall, London.
Sutanto, A. H. (1974). Prosthogonimus Sp. in an infant. Paediatrica Indone-
siana,11(1), 38–43.
Tolgay, N. (1973). Evcil ve Yabani Kanatlıların Önemli Parazitleri. Ankara Üniv
Vet Fak Yayın No:294, Ankara Üniv. Basımevi, Ankara.
Ünlü, H. (2012). Aydın yöresinde ev kümeslerinde yeti¸stirilen tavuk-
larda helmint faunası (Dissertation). University of Adnan Menderes.
Aydın.
Yardibi,M. E. (2004). Hindilerde sindirim sistemi helmintlerinin ara ¸stırılması
(Dissertation). University of Ankara. Ankara.
How to cite this article: Öztürk, M., & Umur, ¸S. (2023). The
oviduct fluke, Prosthogonimus species in wild birds, Türkiye.
Veterinary Medicine and Science,9, 2329–2335.
https://doi.org/10.1002/vms3.1209