View of Revision of Gizzard and Intestinal Helminthes of Some Birds in Iraq

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Revision of Gizzard and Intestinal Helminthes of Some Birds in Iraq

Hind D. Hadi 1 Azhar A. Al-Moussawi2*

1,2Iraq Natural History Research Center and Museum, University of Baghdad, Baghdad, Iraq

*Corresponding author e-mail:

[email protected]; [email protected]

ABSTRACT

A revision of 47 references for the last ten years, from 2010 to 2020, concerning gizzard and intestinal helminthic parasites of some birds in Iraq, showed infections with trematodes, cestodes, nematodes and one acanthocephalan. Helminthic infections of birds were arranged in three tables according to bird order, in each table, bird orders arranged according to the number of infected bird species descending. Among the class Trematoda, the bird order with more infected members found each of Anseriformes and Charadriiformes found that 5 bird species infected with trematodes, followed by Gruiformes 2 bird species, then Passeriformes with 2 species and one bird species for each of Pelecaniformes and Phoenicopteriformes. In the class Cestoda, the bird order with more infected members found each of Anseriformes and Galliformes found that 5 bird species, followed by Passeriformes with 4 bird species, then Columbiformes with 3 species, each of Charadriiformes and Gruiformes with 2 species and one bird species for each of Phoenicopteriformes and Podicipediformes. Among the class Nematoda, the bird order with more infected members the Anseriformes found that 9 bird species infected, followed by Pelecaniformes with 7 infected birds, 4 bird species for each of Galliformes, Columbiformes and Passeriformes, then Charadriiformes only 3 bird species. In each of Accipitriformes, Coraciiformes and Gruiformes only 2 species. Only one bird species found infected with nematodes in each of Phoenicopteriformes, Podicipediformes, Pteroclidiformes and Suliformes. At last, 2 bird species were found infected with 2 parasitic acanthocephalans, one recorded from one Anseriform bird, while the other Acanthocephala not determined to

species level was recorded from one Passeriform bird.

INTRODUCTION

Helminth parasites appear in many birds (Clapham, 1957), in case of heavy

intestinal infections they were the probable cause of death of birds (Okulewicz and

Sitko, 2012).

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The survey literature of helminthic infections of Iraqi birds is mostly little, especially those concerns with gizzard and intestinal helminths of birds of Iraq for the period (2010-2020), they are scattered, there are those of Mezhir (2009), Abid Alabas (2010), Al-Awadi et al. (2010), Al-Salim and Ali (2010), Gali et al. (2010), Shubber (2010), Shubber et al. (2010), Al- Bayati (2011), Al-Moussawi and Mohammad ) 2011 ( , Al-Barwari and Saeed (2012), Mohammad and Al-Moussawi (2012), Abdullah ) 2013 ( , Al-Labban et al. (2013), Khoshnaw and Abdullah (2013), Abdullah and Jebur (2014), Abdulrahman et al. (2014)

^,

Abed et al. (2014), Awad et al. (2014), Al-Moussawi (2014, 2015, 2016a, 2016b and 2017), Al-Moussawi and Al-Hamdany (2015), Al–Zubaidei (2015), Mohammad (2015), Omer et al.

(2015), Al-Marsomy and Al-Hamadaani (2016), Hussein (2016), Jameel et al.

(2016), Mohammad and Al-Moussawi (2016), Al-Ibrahimi et al. (2017), Al- Moussawiand Jassim (2017), Alrikaby and Abdullah (2017), Mohammad and Al- Moussawi ) 2017 ( , Hasan et al. (2018), Yaseen and Abdullah (2018), Al- Mahmoudi et al. (2019), Al-Aredhi (2020) and Mizhir et al. (2020).

The aim of this revision is to collect the scattered literature about gizzard and intestinal helminthes of some birds in Iraq for the years 2010-2020, with a special concern to helminthes of aquatic birds of Iraq.

MATERIALS AND METHODS

Data concern the helminthes of gizzards and intestines of Iraqi birds for the period (2010-2020) in local literature were collected, gathered and presented in this revision in three separate tables each for one class (Trematoda, Cestoda and Nematoda), birds in these tables were arranged according to bird order, in addition to only one acanthocephalan parasite. The main electronic sites concerning with the classification (GBIF, 2020, ITIS 2020, WoRMS, 2020) were followed for check the scientific names of birds and their helminthes and their synonyms.

As no previous revision concerning the helminthes of gizzards and intestines of Iraqi birds, this revision present essential information on this subject.

RESULTS AND DISCUSSION

This revision included references on helminthes of gizzards and intestines of Iraqi birds for the period (2010-2020) which gathered and demonstrated in three tables, each one was carried out for one class of parasites.

Table (1) demonstrated the trematodes with a total number of twenty species in

addition to one species of the genusPlagiorchis, they belong to fourteen genera, ten

families isolated from sixteen bird species of thirteen genera, nine families and six

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orders, they were recorded by Al-Awadi et al. (2010), Gali et al. (2010), Abdullah and Jebur (2014), Awad et al. (2014), Yaseen and Abdullah (2018) and Mizhir et al. (2020). From these the trematodes that infected aquatic birds Apharyngostrigea cornu, Apophallus crami, Australapatemon minor, Diplostomum pseudospathaceum,Diplostomum spathaceum, Echinostoma chloropodis, Echinostoma revolutum, Echinoparyphium recurvatum , Heterotestphyes sobolevi, Notocotylus gibbus, Notocotylus urbanensis, Patagifer parvispinosus, Plagiorchis elegans, Plagiorchis nanus, Podocotyle reflexa, Psilochasmus longicirratus, Psilochasmus oxyurus, Spatula clypeata and Stephanopropora denticulata. Of the genera Apharyngostrigea, Apophallus, Australapatemon, Diplostomum, Echinostoma, Echinoparyphium, Heterotestphyes, Notocotylus, Patagifer, Plagiorchis, Podocotyle, Psilochasmus, Spatula and Stephanopropora.

Diplostomidae, Echinostomatidae, Heterophyidae, Notocotylidae, Opecoelidae, Plagiorchiidae, Psilostomidae and Strigeidae from the aquatic birds Anas acuta, Anas platyrhynchos, Ardea purpurea, Aythya fuligula, Chettusia leucura,Fulica atra, Gallinula chloropus,Himantopus himantopus, Phoenicopterus roseus,Larus argentatus, Larus cachinnans, Larus genei, Mareca strepera,Spatula clypeata,Spatula clypeata and Tachybaptus ruficollisbelong tothe families Anatidae, Ardeidae, Charadriidae, Laridae, Phoenicopteridae ,Podicipitidae,Psilostomidae, Rallidae and Recurvirostridae of the ordersAnseriformes, Charadriiformes, Gruiformes, Pelecaniformes, Phoenicopteriformes and Podicipediformes these trematodes were recorded by Al- Awadi et al. (2010), Awad et al. (2014), Yaseen and Abdullah (2018) and Mizhir et al. (2020).

Here we have notes to mention about some of these papers: the genus of the trematode Stephanoprora denticulata was mistakenly mentioned in more than one place in the paper of Yaseen and Abdullah (2018), as it was recorded as Stephanopropora denticulata. The bird Mareca strepera (Linnaeus, 1758) of Mizhir et al. (2020) found as a synonym for Anas strepera Linnaeus, 1758 in GBIF (2020).

In Iraq, twenty trematode species, for the last ten years, belong to fifteen genera, and seven families, were recorded from gizzards and intestines of fourteen aquatic birds belonging to eleven genera and seven families, which belong to six bird orders by Al-Awadi et al. (2010), Awad et al. (2014), Alrikaby and Abdullah (2017), Yaseen and Abdullah (2018) and Mizhir et al. (2020).

Cestodes that found infected gizzards and intestines of Iraqi birds for the period

(2010-2020) were demonstrated in Table 2. We have notes about many papers

concerned with cestodes: Mezhir (2009) recorded the infection of Columba

domestica and C. livia with the cestode Coutugonia cuneata; neither the genus

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Coutugonia, nor C. cuneata were found in databases of GBIF (2020), ITIS (2020) and WoRMS; only the cestode genus Cotugnia Diamare, 1893 found in GBIF (2020) and ITIS (2020). Gali et al. (2010) reported the two cestodes Paradicranotinae anormalis and Raillietina tetragona in addition to two species belong to the genera Allohymenolepis and Haploparaxis, they were isolated from Pycnonotus lecuotis mesoptamiae (we think there is a mistake in the species name of the bird) which did not found in GBIF, but Pycnonotus leucotis (Gould, 1836) appeared as an accepted name for the bird; in ITIS (2020) appeared Pycnonotus leucotis mesopotamia Ticehurst, 1918 as a valid name, the cestode Allohymenolepis isolated from the small intestine of P. leucotis mesopotamia seems doubtful name in GBIF (2020). Aporina delofound which reported from the digestive tract of Streptopelia decaocto by Shubber et al. (2010) and Aporina delafondi of Al- Bayati (2011) could not find in the main databases of GBIF (2020), ITIS (2020) and WoRMS (2020),we found only the genus Aporina Fuhrmann, 1902 which appeared as a doubtful genus in GBIF (2020). Al- Bayati (2011) recorded the genus name mistakenly as Raillientina instead of Raillietina. Al-Barwari and Saeed (2012) reported eight cestodes from the intestine of Columba livia, four of them found in the ileal part of the small intestine, they belong to the genus Raillietina (=Skrjabinia): Raillietina (=Skrjabinia) tetragona, R. carpohagi, R. bonini (=Hymenolepiscolumbae) and R. fuhrmanni. Hymenolepis columbae did not appear as a synonym of Skrjabinia bonini (Megnin, 1899) on GBIF (2020).The domestic chicken, Gallus domesticus of Abdullah (2013) appeared as a synonym on GBIF (2020), and the cestode Hymenolepis carioca not found in GBIF (2020), ITIS (2020) and WoRMS (2020), only the genus Hymenolepis Weinland, 1858 appeared as a valid genus in these three databases.

Omer et al. (2015) did not determine the scientific name of the pigeon’s species.

The site of bird infections with cestodes not found in Al-Moussawi and Al- Hamdany (2015), Al–Zubaidei (2015), and Al-Marsomy and Al-Hamadaani (2016). Hasan et al. (2018) reported two Raillietina species, in addition to two nematodes from the pigeon Columbi livia we think there is mistake in genus name, in GBIF (2020) we found only Columba livia J.F.Gmelin, 1789 as accepted name.

Marecastrepera of Mizhir et al. (2020) found as a synonym in GBIF (2020).Some authors did not determine bird species (Al–Zubaidei, 2015, Omer, 2015 and Al-

Mahmoudi et al., 2019).

Among the cestode of gizzards and intestines of aquatic birds for the period (2010- 2020) in Iraq, one species of the genus Cotugina and fourteen cestodes were found.

These cestodes belong to five families, they were found in eleven bird species, ten

genera of eight families and seven orders, they were recorded by Abid Alabas

(2010), Al-Awadi et al. (2010), Mohammad (2015), Al-Ibrahimi et al. (2017), Al-

Aredhi (2020) and Mizhir et al. (2020).Al-Awadi et al. (2010) found eight cestode

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species of five genera and four families found in the aquatic birds Fulica atra L., 1758, Gallinula chloropus (L., 1758), Himantopus himantopus (L., 1758), Larus argentatus Pontoppidan, 1763 and Tachybaptus ruficollis (Pallas, 1764) , they belong to the genera Fulica, Gallinula, Himantopus, Larus, Tachybaptus and the families Laridae, Podicipitidae, Rallidae and Recurvirostridae in Bahr Al-Najaf depression, mid-Iraq;in GBIF (2020) we did not find Dicranotaenia tsengi which recorded from the intestine of Himantopus himantopus (L., 1758), but we found the genus Dicranotaenia Railliet, 1892 only; as well, we found the cestode Tatria decacantha (Pallas, 1764), which isolated from the intestine of Tachybaptus ruficollis as a synonym of Joyeuxilepis decacantha (Fuhrmann, 1913) Gulyaev, 1989 in the database of WoRMS (2020).

In table (3) there are unidentified nematode species of the genera Ascaridia, Baruscapillaria, Baruscapillarinae, Capillaria, Contracaecum,and Tetrameres, in addition totwenty three nematode species of nineteen genera, fourteen families were found infect forty-three bird species of thirty-one genera, and two unspecified species name: local ducks of Al-Labban et al. (2013) and Native chickens of Al–

Zubaidei (2015). These nematodes were reported by Al-Awadi et al. (2010), Al- Salim and Ali (2010), Shubber (2010), Shubber et al. (2010), Al-Moussawi and Mohammad ) 2011 ( , Al-Barwari and Saeed ) 2012 ( , Mohammad and Al-Moussawi

2012 (

) , Abdullah ) 2013 ( , Al-Labban et al. (2013), Khoshnaw and Abdullah ) 2013 ( , Abed et al. ) 2014 ( , Al-Moussawi (2014), Awad et al. (2014), Al-Moussawi

2015 (

) , Al-Moussawi and Al-Hamdany ) 2015 ( , Al–Zubaidei ) 2015 ( , Mohammad (2015), Al-Moussawi (2016a), Al-Moussawi (2016b), Mohammad and Al- Moussawi (2016), Hussein ) 2016 ( , Jameel et al. ) 2016 ( , Al-Ibrahimi et al. (2017), Al-Moussawi ) 2017 ( , Al-Moussawi and Jassim ) 2017 ( , Alrikaby and Abdullah

2017 (

) , Mohammad and Al-Moussawi (2017), Hasan et al. (2018), Al-Aredhi 2020 (

) and Mizhir et al. (2020).

Of these nematodes, thirteen species were found infecting aquatic birds in Iraq

belong to thirteen genera and unidentified species of the genera Ascardia,

Baruscapillaria, Capillaria, Contracaecum and Tetrameres;andone species belong

to the genus Baruscapillarinae which isolated from little egret Egretta grazetta by

Al-Salim and Ali (2010). These nematodes belong to thirteen families. They were

isolated from thirty- one bird species of twenty-two genera; eleven families and ten

bird orders. These nematodes were reported by Al-Awadi et al. (2010), Al-Salim

and Ali (2010), Al-Moussawi and Mohammad ) 2011 ( , Al-Labban et al. (2013),

Al-Moussawi (2014), Awad et al. (2014), Mohammad (2015), Mohammad and Al-

Moussawi (2016), Hussein (2016), Al-Ibrahimi et al. (2017), Al-Moussawi and

Jassim ) 2017 ( , Alrikaby and Abdullah ) 2017 ( , Mohammad and Al-Moussawi

(2017), Al-Aredhi ) 2020 ( and Mizhir et al. (2020).

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We have to mention here some notes about some papers: Al-Salim and Ali (2010) described Baruscapillarinae gen. sp. fromEgretta grazetta depending on single specimen (male), we didn't find any other information about it in GBIF (2020). Al- Labban et al. (2013) did not mention the scientific name of ducks,in addition to that the nematode Hystrichis tricolour found as Hystrichis tricolor Dujardin, 1845 which seems accepted in GBIF (2020). Al-Ibrahimi et al. (2017) have mentioned Ascardia sp. as endoparasite of Gallinula chloropus, we think that they may had been meant Ascaridia instead of Ascardia.Mizhir et al. (2020) isolated six species of trematodes (Tab.1), three species of cestodes (Tab. 2), two nematodes (Tab.3) and the acanthocephala Polymorphus boschadis from 14 aquatic birds from Bahr Al-Najaf depression, Mareca strepera (Linnaeus, 1758) one of them, this bird

found as a synonym for Anas strepera Linnaeus, 1758 in GBIF (2020).

Finally, we would like to mention here that only two infections with parasitic acanthocephalan were reported in the period (2010-2020): the acanthocephalan spp. (not determined to species level) which isolated by Abdulrahman et al. (2014) from the intestinal tract of Sturnus vulgaris in Sulaimania Province, and Polymorphus boschadis (Schrank, 1788) Railliet, 1919 which recorded from the small intestine of the aquatic bird Mareca Strepera in Bahr Al-Najaf Depression byMizhir et al. (2020).

Table 1: List of trematodes and their bird hosts arranged by bird order.

Reference

site of

infection Trematod genus

and species Trematod family

Bird

genus and species

Bird family Bird order

Mizhir et al.

(2020) intestinal

caeca Notocotylus

urbanensis Cort, 1914

Notocotylidae Mareca

strepera (Linnaeus, 1758) Anatidae

Anseriformes

Mizhir et al.

(2020) small

intestine Australapatemon

minor (Yamaguti, 1933)

Strigeidae Spatula

clypeata (Linnaeus, 1758) Anatidae

Anseriformes

Mizhir et al.

(2020) small

intestine Echinoparyphium

recurvatum (Linstow, 1873) Dietz, 1909 Echinostomatidae

Aythya fuligula

(Linnaeus,1758) Anatidae

Anseriformes

Mizhir et al.

(2020) small

intestine Echinostoma

revolutum

(Fröhlich, 1802) Rudolphi, 1809 Echinostomatidae

Anas

platyrhynchos Linnaeus, 1758 Anatidae

Anseriformes

Mizhir et al.

(2020) small

intestine Echinostoma

revolutum

(Fröhlich, 1802) Echinostomatidae

Spatula clypeata (Linnaeus, Anatidae

Anseriformes

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Rudolphi, 1809 1758)

Mizhir et al.

(2020) intestinal

caeca Notocotylus

Notocotylidae Anas acuta

Linnaeus, 1758 Anatidae

Anseriformes

Mizhir et al.

(2020) intestinal

caeca Notocotylus

Notocotylidae Anas

Anseriformes

Mizhir et al.

(2020) intestinal

caeca Notocotylus

Notocotylidae Spatula

clypeata (Linnaeus, 1758) Anatidae

Anseriformes

Mizhir et al.

(2020) small

intestine Podocotyle reflexa

(Creplin, 1825) Odhner, 1905 Opecoelidae

Spatula clypeata (Linnaeus, 1758) Anatidae

Anseriformes

Mizhir et al.

(2020) small

intestine Psilochasmus

longicirratus Skrjabin, 1913 Psilostomidae

Aythya fuligula (Linnaeus,1758) Anatidae

Anseriformes

Mizhir et al.

(2020) small

intestine Psilochasmus

longicirratus Skrjabin, 1913 Psilostomidae

Mareca strepera (Linnaeus, 1758) Anatidae

Anseriformes

Al-Awadi et al.

(2010) intestine

Diplostomum spathaceum Diplostomidae

Larus argentatus Pontoppidan, 1763 Laridae

Charadriiformes

Awad et al. (2014) Small

intestine Plagiorchis nanus

(Rud, 1802) Plagiorchiidae

Chettusia leucura Charadriidae

Charadriiformes

intestine Plagiorchis nanus

(Rud, 1802) Plagiorchiidae

Himantopus himantopus Recurvirostridae

Charadriiformes

intestine Plagiorchis

elegans (Rud, 1802) Plagiorchiidae

Larus genei Laridae

Charadriiformes

Yaseen and Abdullah (2018) large and

small intestine Apophallus crami

Price , 1931 Heterophyidae

Larus cachinnans Pallas , 1811 Laridae

Charadriiformes

small intestine Diplostomum

pseudospathaceum (Niewiadomska, 1984)

Diplostomidae Larus

cachinnans Pallas , 1811 Laridae

Charadriiformes

small intestine Diplostomum

spathaceum (Rudolphi, 1819) Diplostomidae

Charadriiformes

Yaseen and Abdullah (2018) duodenum

Heterotestphyes sobolevi Leonov,1957 Heterophyidae

Charadriiformes

small intestine Stephanopropora

denticulata ( Rudolphi , 1802) Echinochasmidae

Charadriiformes

Al-Awadi et al.

(2010) intestine

Notocotylus gibbus Notocotylidae

Fulica atra L., 1758

Rallidae Gruiformes

Al-Awadi et al.

(2010) intestine

Notocotylus gibbus Notocotylidae

Gallinula chloropus (L., 1758)

Rallidae Gruiformes

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Al-Awadi et al.

(2010) intestine

Echinostoma chloropodis Echinostomatidae

Rallidae Gruiformes

Al-Awadi et al.

(2010) intestine

Echinostoma chloropodis Echinostomatidae

Rallidae Gruiformes

Al-Awadi et al.

(2010) intestine

Psilochasmus oxyurus Psilostomidae

Rallidae Gruiformes

Mizhir et al.

(2020) intestinal

caeca Notocotylus

Notocotylidae Fulica atra

Linnaeus, 1758 Rallidae

Gruiformes

Gali et al. (2010) intestine

Plagiorchis sp.

Plagiorchiidae Pycnonotus

lecuotis mesoptamiae Pycnonotidae

Passeriformes

Gali et al. (2010) intestine

Mosesia chordeilesia Phaneropsolidae

Pycnonotus lecuotis mesoptamiae Pycnonotidae

Passeriformes

Abdullah and Jebur (2014) Small

intestine Plagiorchis

bulbulii Mehra,1937 Plagiorchiidae

Passer

domesticus (L.) Passeridae

Passeriformes

Al-Awadi et al.

(2010) intestine

Apharyngostrigea cornu

Strigeidae Ardea purpurea

L., 1766 Ardeidae

Pelecaniformes

Mizhir et al.

(2020) intestinal

caeca Notocotylus

Notocotylidae Phoenicopterus

roseus Pallas, 1811

Phoenicopteridae Phoenicopteriformes

Table 2: List of cestodes and their bird hosts arranged by bird order.

Reference site of

infection Parasite genus

and species Parasite family

Bird

genus and species Bird family

Bird order

Mizhir et al.

(2020) intestine

Sobolevicanthus gracilis (Zeder, 1803) Spassky &

Spasskaja, 1954 Hymenolepididae

Anas crecca Linnaeus, 1758 Anatidae

Anseriformes

Mohammad ( 2015) digestive

tract Diploposthe

laevis (Bloch, 1782) Hymenolepididae

aAythya nyroc (Güldenstädt, 1770) Anatidae

Anseriformes

Mizhir et al.

(2020) small

intestine Fimbriaria

fasciolaris (Pallas, 1781) Frölich, 1802 Hymenolepididae

Tadorna tadorna (Linnaeus, 1758) Anatidae

Anseriformes

Mizhir et al.

(2020) intestine

Aythya fuligula (Linnaeus, 1758) Anatidae

Anseriformes

Mizhir et al.

(2020) small

intestine Fimbriaria

fasciolaris (Pallas, 1781) Frölich, 1802 Hymenolepididae

Mareca strepera (Linnaeus, 1758) Anatidae

Anseriformes

Mizhir et al.

(2020) intestine

Sobolevicanthus gracilis (Zeder, Hymenolepididae

Mareca strepera Anatidae

Anseriformes

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1803) Spassky &

Spasskaja, 1954 (Linnaeus,

1758)

Abdullah (2013) gastro-

intestinal tract Amoebotaenia

sphenoides Dilepi

didae Gallus

domesticus Phasianidae

Galliformes

intestinal tract Choanotaenia

infundibulum Dilepididae

Gallus domesticus Phasianidae

Galliformes

intestinal tract Davaniea

proglottina Davaineidae

Galliformes

intestinal tract Hymenolepis

carioca Hymenolepididae

طقف سنجلل Gallus

Galliformes

intestinal tract Raillietina spp.

Davaineidae Gallus

Galliformes

Khoshnaw and Abdullah (2013) Small

intestine Cotugnia

latiproglottina Sawada, Molan et Saeed, 1989 Davaineidae

Alectoris chukar Phasianidae

Galliformes

intestine Raillietina

alectori Schmidt, Greenberg et Wertheim, 1986 Davaineidae

Alectoris chukar Phasianidae

Galliformes

Al–Zubaidei (2015) --

Cotugina spp.

Davaineidae native chickens

Phasianidae Galliformes

Al-Moussawi et al. (2018)

echinobothrida (Megnin, 1881) Davaineidae

Gallus gallus domesticus Linnaeus, 1758 Phasianidae

Galliformes

Al-Aredhi (2020) Small

tetragona Davaineidae

Francolinus francolinus Phasianidae

Galliformes

Al-Aredhi (2020) Small

intestine Cotugina sp.

Davaineida Francolinus

francolinus Phasianidae

Galliformes

Abid Alabas (2010)

intermeda Davaineidae

Corvus corone Corvidae

Passeriformes

Abid Alabas (2010)

micracantha Davaineidae

Corvus corone Corvidae

Passeriformes

Gali et al. (2010) Small

intestine Allohymenolepis

sp.

Hymenolepididae Pycnonotus

Passeriformes

intestine Haploparaxis sp.

Hymenolepididae Pycnonotus

Passeriformes

intestine Paradicranotinae

anormalis Pycnonotus

Passeriformes

Pycnonotus lecuotis mesoptamiae Pycnonotidae

Passeriformes

Mohammad and Al-Moussawi (2013) intestine

Raillietina echinobothrida (Megnin, 1881) Davaineidae

Passer domesticus biblicus Hartret, 1881 Passeridae

Passeriformes

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Abdulrahman et al. (2014)

alimentary canal Choanotaenia

masculosa Dilepididae

Sturnus vulgaris Sturnidae

Passeriformes

Al-Moussawi and Al-Hamdany (2015) -

Passerilepis crenata (Goeze, 1782) Hymenolepididae

Sturnus vulgaris (Gray, 1835)

Sturnidae Passeriformes

Jenzeel et al.

(2017) intestine

Anonchotaenia globate Paruterinidae

Passer domesticus (L.) Passeridae

Passeriformes

Jenzeel et al.

(2017) intestine

Choanotaenia infundibulum Dilepididae

Passeriformes

Jenzeel et al.

(2017) intestine

Choanotaenia passerine Dilepididae

Passeriformes

Jenzeel et al.

(2017) intestine

Raillietina cesticillus (Molin, 1858) Davaineidae

Passeriformes

Jenzeel et al.

(2017) intestine

Raillietina echinobothrida (Megnin 1880) Davaineidae

Passeriformes

Jenzeel et al.

(2017) intestine

Raillietina ransomi Davaineidae

Passeriformes

Jenzeel et al.

(2017) intestine

Raillietina Tetragona (Molin, 1858) Davaineidae

Passeriformes

Al-saadi et al. (2017) Intestine

Anonchotaenia Globat

e Paruterinidae

Passer domesticus Passeridae

Passeriformes

Al-saadi et al. (2017) intestine

Raillietina cesticellus Davaineidae

Passeriformes

Raillietina echinobothrida Davaineidae

Passeriformes

Raillietina ransomi Davaineidae

Passeriformes

Raillietina tetragona Davaineidae

Passeriformes

Choanotaenia infundibulum Dilepididae

Passeriformes

Choanotaenia passerine Dilepididae

Passeriformes

Hadi and Taher (2020)

small intestine Anonchotaenia

Globata

(von Linstow, 1879)

Paruterinidae Passer

domesticus biblicus Hartert, 1904 Passeridae

Passeriformes

Hadi and Taher (2020)

small intestine Raillietina

tetragona (Molin, 1858) Davaineidae

Passer domesticus biblicus Hartert, 1904 Passeridae

Passeriformes

Mezhir (2009) intestine

Coutugonia cuneata Davaineidae

Columba domestica Columbidae

Columbiformes

Raillietina micracantha Davaineidae

Columba domestica Columbidae

Columbiformes

Mezhir intestine

Aporina delafondi Anoplocephalidae

Columba livia Columbidae

Columbiformes

(11)

http://annalsofrscb.ro 358

(2009) Mezhir (2009) intestine

Coutugonia cuneata Davaineidae

Columbiformes

Streptopelia decaocio Columbidae

Columbiformes

Shubber et al.

(2010) digestive

tract Aporina

delofound Anoplocephalidae

Streptopelia decaocto Columbidae

Columbiformes

Shubber et al.

(2010) digestive

tract Choanotania

Columbiformes

Shubber et al.

(2010) digestive

tract Raillietina

Columbiformes

Al- Bayati (2011) Aporina delafondi

Anoplocephalidae Columba livia

Columbidae Columbiformes

Al- Bayati ((2011 intestine

Cotugnia intermedia Davaineidae

Columbiformes

Al- Bayati (2011) Raillientina

microcantha Davaineidae

Columbiformes

Al-Barwari and Saeed (2012), Small

columbae Davaineidae

Columba livia Gmelin, 1789 Columbidae

Columbiformes

Al-Barwari and Saeed (2012) Small

intestine C. digonopora

Davaineidae Columba livia

Gmelin, 1789 Columbidae

Columbiformes

intestine C. polyacantha

Columbiformes

intestine C. satpuliensis

Columbiformes

(=Skrjabinia) bonini Davaineidae

Columbiformes

(=Skrjabinia) carpohagi Davaineidae

Columbiformes

(=Skrjabinia) fuhrmanni Davaineidae

Columbiformes

intestine R. (=Skrjabinia)

Columbiformes

columbae Davaineidae

Columbiformes

digonopora Davaineidae

Columbiformes

polyacantha Davaineidae

Columbiformes

satpuliensis Davaineidae

Columbiformes

bonini

(=Hymenolepis Davaineidae

Columbiformes

(12)

http://annalsofrscb.ro 359

columbae)

carpohagi Davaineidae

Columbiformes

fuhrmanni Davaineidae

Columbiformes

(=Skrjabinia) tetragona Davaineidae

Columbiformes

Abed et al.

(2014) Small

intestine Cotugina spp.

domestica Columbidae

Columbiformes

Abed et al.

(2014) Small

intestine Raillietina spp.

Columbiformes

Omer et al.

(2015) small

pigeons columbidae

columbiformes

Al-Marsomy and Al-Hamadaani (2016) ---

Columbiformes

Afrasiab et al.

(2017) intestine

Columbiformes

Afrasiab et al.

(2017) intestine

Idiogenes sp.

Davaineidae Streptopelia

decaocto Columbidae

Columbiformes

Hasan et al.

(2018) Small

echinobothrida Davaineidae

Columbiformes

Hasan et al.

(2018) Small

Columbiformes

Jasim et al.

(2019) small

Columbiformes

Jasim et al.

(2019) small

Streptopelia decaocio Columbidae

Columbiformes

Al-Mahmoudi et al. (2019) intestine

Raillietina spp.

Davaineidae Pigeons

Columbidae Columbiformes

Al-Awadi et al.

(2010) intestine

Dicranotaenia tsengi

Hymenolepididae Himantopus

himantopus (L., 1758) Recurvirostridae

Charadriiformes

Al-Awadi et al.

(2010) intestine

Diplophallus polymorphus Acoleidae

Himantopus himantopus (L., 1758) Recurvirostridae

Charadriiformes

Al-Awadi et al.

(2010) intestine

Paricterotaenia porosa

Dilepididae Larus

argentatus Pontoppidan, 1763 Laridae

Charadriiformes

Al-Awadi et al.

(2010) Intestine

Diorchis brevis Hymenolepididae

Rallidae Gruiformes

Al-Awadi et al.

(2010) intestine

Diorchis brevis Hymenolepididae

Rallidae Gruiformes

Al-Awadi et al.

(2010) intestine

Diorchis inflatus Hymenolepididae

Rallidae Gruiformes

Al-Ibrahimi et al.

(2017) Gastro-

intestinal tract Choanotania

Gallinula chloropus Rallidae

Gruiformes

Al-Ibrahimi et al.

Gastro- Hymenolepis

Hymenolepididae Gallinula

Rallidae Gruiformes

(13)

http://annalsofrscb.ro 360

(2017) intestinal

tract carioca

chloropus

Al-Ibrahimi et al.

(2017) Gastro-

intestinal tract Railletina

cesticillus Davaineidae

Gallinula chloropus Rallidae

Gruiformes

Mizhir et al.

(2020) small

intestine Diorchis

americanus Ransom, 1909 Hymenolepididae

Fulica atra Linnaeus, 1758 Rallidae

Gruiformes

Mizhir et al.

(2020) intestine

Phoenicopterus roseus Pallas, 1811

Al-Awadi et al.

(2010) intestine

Tatria

acanthorhyncha Amabiliidae

Tachybaptus ruficollis (Pallas, 1764) Podicipitidae

Podicipediformes

Al-Awadi et al.

(2010) intestine

Tatria decacantha Amabiliidae

Podicipediformes

Table 3: List of nematodes and their bird hosts arranged by bird order.

Ref.

site of

infection Nematode

genus and species

nematode family Bird

Genus and species Bird family

Bird order

Al-Labban et al. (2013) proventriculus

Hystrichis tricolor Dujardin, 1845

Dioctophymidae local ducks

Anatidae Anseriformes

Al-Moussawi, (2014) gizzard

Amidostomoides acutum

(Lundahl,1848) Seurat, 1918 Amidostomatidae

Anas clypeata Linnaeus, 1758 Anatidae

Anseriformes

Al-Moussawi, (2014) gizzard

Epomidiostomum uncinatum (Lundahl,1848) Seurat, 1918 Amidostomatidae

Anseriformes

Al-Moussawi, (2014) proventriculus

Tetrameres sp.

Creplin,1846 Tetrameridae

Anseriformes

Mohammad

and Al-

Moussawi (2016) gizzard

Amidostomum acutum

Amidostomatidae Anas

Platyrhynchos L., 1758 Anatidae

Anseriformes

Mohammad

and Al-

Epomidiostomum uncinatum (Lundahl,1848) Seurat

Amidostomatidae Anas

Anseriformes

Mohammad

and Al-

Hadjelia truncata Habronematidae

Anas

Anseriformes

Mohammad ( 2015) digestive tract

Amidostomoides acutum

(Lundahl, 1848) Amidostomatidae

Aythya nyroca (Güldenstädt, 1770) Anatidae

Anseriformes

(14)

http://annalsofrscb.ro 361

Mohammad ( 2015) digestive tract

Epomidiostomum uncinatum (Lundahl, 1848) Amidostomatidae

Aythya nyroca (Güldenstädt, 1770) Anatidae

Anseriformes

Mizhir et al.

(2020) duodenum

Amidostomum acutum Seurat, 1918

Amidostomatidae Mareca strepera

(Linnaeus, 1758) Anatidae

Anseriformes

Mizhir et al.

(2020) proventriculus

Tetrameres sp.

Tetrameridae Anas acuta

Anseriformes

Mizhir et al.

Tetrameres sp.

Tetrameridae Anas crecca

Anseriformes

Mizhir et al.

Tetrameres sp.

Tetrameridae Anas

Anseriformes

Mizhir et al.

Tetrameres sp.

Tetrameridae Aythya ferina

Anseriformes

Mizhir et al.

Tetrameres sp.

Tetrameridae Aythya fuligula

Anseriformes

Mizhir et al.

Tetrameres sp.

Tetrameridae Mareca

penelope (Linnaeus, 1758) Anatidae

Anseriformes

Mizhir et al.

Tetrameres sp.

Tetrameridae Mareca

strepera (Linnaeus, 1758) Anatidae

Anseriformes

Mizhir et al.

Tetrameres sp.

Tetrameridae Spatula clypeata

Anseriformes

Al-Awadi et al.

(2010) Proventriculus

Contracaecum sp.

Anisakidae Ardea purpurea

L., 1766 Ardeidae

Pelecaniformes

Al-Awadi et al.

Contracaecum sp.

Anisakidae Ardeola

ralloides (Scopoli, 1769) Ardeidae

Pelecaniformes

Al-Awadi et al.

Contracaecum sp.

Anisakidae Botaurus

stellaris (L., 1758)

Ardeidae Pelecaniformes

Al-Awadi et al.

Contracaecum sp.

Anisakidae Egretta alba (L.,

1758) Ardeidae

Pelecaniformes

Al-Awadi et al.

Contracaecum sp.

Anisakidae Egretta garzetta

(L., 1766) Ardeidae

Pelecaniformes

Al-Salim and Ali (2010) Mid intestine

Baruscapillaria sp.

Capillariidae Ardea cinerea

Ardeidae Pelecaniformes

Al-Salim and Ali (2010) Cloaca

Baruscapillarinae gen. sp.

Superfamily:

Trichinellida Egretta garzetta

(L., 1766) Ardeidae

Pelecaniformes

Awad et al.

Microtetrameres spiralis

(Seurat, 1915) Tetrameridae

Bubulcus ibis Ardeidae

Pelecaniformes

intestinal tract Heterakis

gallinarum Heterakidae

Galliformes

intestinal tract Ascaridia galli

Ascaridiidae Gallus

Galliformes

Abdullah gastro-

Capillaria spp.

Trichuridae Gallus

(15)

http://annalsofrscb.ro 362

(2013) intestinal tract

domesticus

intestinal tract Cheilospirura

hamulosa Acuariidae

Galliformes

intestine Ascarida

numidae (Leiper, 1908; Travassos 1913)

Ascaridiidae Alectoris chukar

Khoshnaw and Abdullah (2013) Intestinal

caecum Hartertia

gallinarum (Thieler 1919) Hartertiidae

Alectoris chukar Phasianidae

Galliformes

Al–Zubaidei, (2015) _

Heterakis gallinarum Heterakidae

Native chickens Phasianidae

Galliformes

Al-Moussawi (2016b) Intestinal

caecum Heterakis

Gallinarum (Shrank, 1788) Hartertiidae

Meleagris gallopavo Phasianidae

Galliformes

Al-Aredhi (2020) Cecum

Heterakis gallinarum Heterakidae

Galliformes

Al-Aredhi (2020) Cecum

Heterakis isolanche Heterakidae

Galliformes

intestine Ascaridia

columbae Ascaridiidae

Columbiformes

intestine Ascaridia galli

Ascaridiidae Columba livia

Columbiformes

intestine Capillaria

obsignata Capillariidae

Columbiformes

intestine Capillaria sp.

Capillariidae Columba livia

Columbiformes

intestine Synhimantus

spiralis Acuariidae

Columbiformes

Abed et al.

(2014) _

Ascaridia spp.

Ascaridiidae Columba livia

Columbiformes

Hasan et al.

(2018) Small

intestine Ascaridia

columbae Ascaridiidae

Columbi livia Columbidae

Columbiformes

Hasan et al.

(2018) Small

intestine Heterakis

gallinarum Heterakidae

Columbi livia Columbidae

Columbiformes

Jameel et al.

(2016) gizzard

Hadjelia truncata Habronematidae

Columba livia domestica Columbidae

Columbiformes

Shubber (2010) _

Hadjelia truncata Creplin, 1825 Habronematidae

Columbiformes

Shubber (2010) _

Columba .palumbus Columbidae

Columbiformes

Shubber (2010) _

Columbiformes

Shubber (2010) _

Streptopelia turtur Columbidae

Columbiformes

Shubber et al.

(2010) digestive tract

Amidostomoides anseris

Amidostomatidae Streptopelia

decaocto Columbidae

Columbiformes

Shubber et al.

(2010) digestive tract

Epomidiostomum uncinatum Amidostomatidae

Columbiformes

Al-Moussawi (2015) Gizzard

Hadjelia truncata Creplin , 1825 Habronematidae

Lanius collurio Linnaeus, 1758 Laniidae

Passeriformes

(16)

http://annalsofrscb.ro 363

Al-Moussawi

and Al-

Hamdany (2015) _

Dispharynx nasuta

(Rudolphi, 1819) Acuariidae

Sturnus vulgaris (Gray, 1835) Sturnidae

Passeriformes

Al-Moussawi (2016a) Gizzard

Dispharynx nasuta (Rudolphi, 1819)

Acuariidae Pycnonotus

leucogenys (Gray, 1835) Pycnonotidae

Passeriformes

Mohammad

and Al-

Moussawi (2012) Gizzard

Acuaria skrjabini Ozerskaya, 1926 Acuariidae

Passer domesticus biblicus Hartret Passeridae

Passeriformes

Mohammad

and Al-

Moussawi (2012) Gizzard

Dispharynx nasuta (Rudolphi, 1819) Stiles and Hassall, 1920 Acuariidae

Passer domesticus biblicus Hartret Passeridae

Passeriformes

Al-Awadi et al.

Capillaria sp.

Capillariidae Larus

argentatus Pontoppidan, 1763 Laridae

Charadriiformes

Awad et al.

Tetrameres spp.

Tetrameridae Larus genei

Laridae Charadriiformes

Alrikaby and Abdullah (2017) Proventriculus

Tetrameres nouveli Tetrameridae

Himantopus himantopus (L.) Recurvirostridae Charadriiformes

Hussein (2016) Gizzard

Contracaecum sp.

Raphidascarididae Circus cyaneus

cyaneus Accipitridae

Accipitriformes

Hussein (2016) Gizzard

Desportesius invaginatus Acuariidae

Circus cyaneus cyaneus

Accipitridae Accipitriformes

Hussein (2016) proventriculus

Tetrameres sp.

Tetrameridae Circus cyaneus

Accipitriformes

Hussein (2016) intestine

Contracaecum sp.

Raphidascarididae Milvus m.milvus

L.

Accipitridae Accipitriformes

Hussein (2016) proventriculus

Tetrameres sp.

Tetrameridae Circus cyaneus

Accipitriformes

Al-Awadi et al.

Contracaecum sp.

Anisakidae Ceryle rudis (L.,

1758) Alcedinidae

Coraciiformes

Al-Moussawi and Jassim (2017)

Gizzard Hadjelia truncata

( Creplin, 1825) Habronematidae

Halcyon Smyrnensis (Linnaeus, 1758) Alcedinidae

Coraciiformes

Al-Awadi et al.

Capillaria sp.

Capillariidae Fulica atra L.,

1758 Rallidae

Gruiformes

Al-Awadi et al.

Tetrameres sp.

Habronematidae Fulica atra L.,

1758 Rallidae

Gruiformes

Al-Ibrahimi et al. (2017) Gastro-

intestinal tract Ascardia sp.

Ascaridiidae Gallinula

chloropus Rallidae

Gruiformes

Mizhir et al.

(2020) duodenum

Amidostomum acutum Seurat, Amidostomatidae

Fulica atra Linnaeus, 1758 Rallidae

Gruiformes

(17)

http://annalsofrscb.ro 364

1918

Mizhir et al.

(2020) duodenum

Amidostomum acutum Seurat, 1918

Amidostomatidae Gallinula

chloropus (Linnaeus, 1758) Rallidae

Gruiformes

Mizhir et al.

Tetrameres sp.

Tetrameridae Fulica atra

Linnaeus, 1758 Rallidae

Gruiformes

Mizhir et al.

Tetrameres sp.

Tetrameridae Gallinula

chloropus (Linnaeus, 1758) Rallidae

Gruiformes

Mizhir et al.

Tetrameres sp.

Tetrameridae Phoenicopterus

roseus Pallas, 1811

Al-Awadi et al.

Eustrongylides tubifex Dioctophymidae

Podicipediformes

Mohammad,

and Al-

Moussawi (2017) intestine

Hartertia gallinarum (Theiler, 1919) Hartertiidae

Pterocles senegallus (Linnaeus, 1771) Pteroclididae

Pteroclidiformes

Al-Moussawi and

Mohammad (2011) proventriculus

and ventriculus Contracaecum

rudolphii Hartwich, 1964 Anisakidae

Phalacrocorax carbo

(Linnaeus, 1758) Phalacrocoracidae

Suliformes

Al-Moussawi (2017) Proventriculus

and ventriculus Contracaecum

rudolphii Hartwich, 1964 Anisakidae

Phalacrocorax carbo

(Linnaeus, 1758) Phalacrocoracidae

Suliformes

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