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Nematodes of birds of Armenia

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DOI: 10.17420/ap6604.285

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Annals of Parasitology 2020, 66(4), 447–455 Copyright© 2020 Polish Parasitological Society
doi: 10.17420/ap6604.285

Review article

Nematodes of birds of Armenia

Sergey O. MOVSESYAN1,2, Egor A. VLASOV3, Manya A. NIKOGHOSIAN2,
Rosa A. PETROSIAN2, Mamikon G. GHASABYAN2,4,
Dmitry N. KUZNETSOV1,5
1
Centre of Parasitology, A.N. Severtsov Institute of Ecology and Evolution RAS, Leninsky pr., 33, Moscow 119071,
Russia
2
Institute of Zoology, Scientific Center of Zoology and Hydroecology NAS RA, P. Sevak 7, Yerevan 0014, Armenia
3
V.V. Alekhin Central-Chernozem State Nature Biosphere Reserve, Zapovednyi, Kursk district, Kursk region, 305528,
Russia
4
Armenian Society for the Protection of Birds (ASPB), G. Njdeh, 27/2, apt.10, Yerevan 0026, Armenia
5
All-Russian Scientific Research Institute of Fundamental and Applied Parasitology of Animals and Plants - a branch
of the Federal State Budget Scientific Institution “Federal Scientific Centre VIEV”, Bolshaya Cheremushkinskaya str.,
28, Moscow 117218, Russia

Corresponding Author: Dmitry N. KUZNETSOV; e-mail: dkuznetsov@mail.ru

ABSTRACT. The review provides data on species composition of nematodes in 50 species of birds from Armenia
(South of Lesser Caucasus). Most of the studied birds belong to Passeriformes and Charadriiformes orders. One of the
studied species of birds (Larus armenicus) is an endemic. The taxonomy and host-specificity of nematodes reported in
original papers are discussed with a regard to current knowledge about this point. In total, 52 nematode species
parasitizing birds in Armenia are reported. Most of the reported species of nematodes are quite common in birds outside
of Armenia. One species (Desmidocercella incognita from great cormorant) was first identified in Armenia. Great snipe
was recorded as a new host for Hystrichis tricolor. Zoonotic nematode Trichinella pseudospiralis was reported in
Armenia from Eurasian blackbird.

Keywords: Armenia, Lesser Caucasus, birds, parasitic nematodes

Introduction Species composition of nematodes

parasitizing birds from Armenia
The fauna of birds in Armenia (south of the
Lesser Caucasus) is featured by a big diversity. In Data on the species composition of nematodes
total, more than three hundred species of birds are recorded for birds in Armenia are presented in Table
registered on this quite small area [1]. The study of 1. Systematic position of birds, their English and
nematodes parasitizing birds in Armenia have been Latin names are given according to digital checklist
started in the 1920s [2–4] and resulted in a of the birds of the world [5]. The taxonomic
significant number of papers. However, the vast affiliation of the detected nematodes is discussed
majority of them have never been published in below.
international scientific literature. In total, there were studied 50 species of birds
The aim of the present review is to summarize from 13 orders: Galliformes (5 species), Anseri-
the data concerning the fauna of nematodes of birds formes (3 species), Podicipediformes (3 species),
in Armenia in the light of contemporary concepts of Columbiformes (2 species), Pterocliformes (1
their taxonomy and distribution. species), Caprimulgiformes (1 species), Gruiformes
(1 species), Pelecaniformes (4 species), Suliformes
(1 species), Charadriiformes (9 species), Accipi-
448 S.O. MOVSESYAN et al.

triformes (3 species), Coraciiformes (1 species) and mum (family Amidostomidae) were found in
Passeriformes (16 species). Passeriformes, world- Armenia: A. anseris from greylag goose, A. che -
wide, is the most numerous order of birds, which vreuxi from tree pipit and A. fulicae from Eurasian
explains the biggest number of the studied species in coot. It is worth mentioning that tree pipit is not a
Armenia. A significant amount of the reviewed typical host for A. chevreuxi, and previously this
studies were conducted nearby the largest body of nematode was reported in black-winged stilt [13].
water in the Caucasus (Lake Sevan), which explains We believe that nematodes from common coot
a large amount of data concerning birds from classified as A. anseris in fact belong to A. fulicae,
Charadriiformes. One of the species from this order which is a specific parasite of this bird in Holarctic
(Larus armenicus) is an endemic species. The [13]. Besides that, we have reclassified Epomidio -
studies detected 52 species of nematodes, seven of stomum orispinum from white-winged tern to
which belong to class Enoplea, and 45 belong to Epomidiostomum sp. since the original description
Chromadorea. We have redefined some of these based on immature forms [14] does not allow to
species based on their original descriptions and surely attribute them to any species of this genus
current knowledge concerning their taxonomy and and, moreover, this host is unusual for this species.
host-specificity. The classes, orders and families of As concerning Subuluridae, we believe that there
nematodes are presented according to De Ley and are two confidently identified species of this family
Blaxter [6], and Schmidt-Raesa [7]. Enoplea is (Subulura brumpti and S. skrjabini) in Armenia.
presented in birds of Armenia by the orders The records on S. suctoria for some birds from
Trichinellida (families Trichinellidae and Capilla- Armenia [15–18] we consider as erroneous since
riidae) and Dioctophymatida (family Diocto- this species is known as a parasite of Caprimulgi -
phymatidae). Trichinella pseudospiralis, which is formes in South America [19]. S. coturnicis,
potentially dangerous for human [8], was found in reported for chukar [15–17], we listed as S. skrja-
Eurasian blackbird [9]. As T. pseudospiralis is more bini, in agreement with Barus and Sonin [20]. The
typical for carnivorous birds [10], the finding of this record of S. leprincei from common quail and
parasite in Eurasian blackbird seems to be unusual. chukar in Armenia was questioned [21], and this
However, Asatrian [9] provided measurements of nematode is known as a typical parasite of European
the T. pseudospiralis larvae found in Eurasian nightjar [19]. We agree that these records [15–17]
blackbird, so we have no doubt that this detection is are erroneous identifications. On the other hand, S.
correct. Since there are few studies concerning T. suctoria was reported from European nightjar in
pseudospiralis in avian hosts, we believe that this Armenia [16]. We consider this detection as
finding [9] worth an attention. As concerning erroneous by the reasons described above and
Capillariidae taxonomy, we are following to believe that this could be either S. leprincei or S.
Moravec [11] and therefore this family is presented subulata, which recorded as parasites of European
with three genera (Aonchotheca, Eucoleus and nightjar in Europe [19]. It worth to mention, that
Capillaria). The family Dioctophymatidae is Barus et al. [19] listed S. leprincei in fauna of
presented with Hystrichis tricolor, a common Armenia, however we consider this as insufficiently
parasite of birds associated with water [7]. H. tri- substantiated, since in the cited publications [15,16]
color was reported in Armenia from the great snipe, this nematode reported from atypical hosts (C.
and this is the first known record of this parasite coturnix and A. chukar). The record of S. allodapa
from this host [12]. from chukar is considered to be wrong [19] since
Chromadorea is presented by order Rhabditida this species is a specialized parasite of red-legged
with 15 families: Syngamidae (1 species), Amido- seriema (Cariama cristata) from Brazil. Based on
stomidae (4 species), Ornithostrongylidae (1 morphological features, Barus et al. [19] supposed
species), Subuluridae (2 identified species), that S. allodapa recorded from chukar in Armenia
Acuariidae (14 species), Aproctidae (2 species), could be either S. brumpti or S. differens.
Desmidocercidae (1 species), Diplotriaenidae (5 Fourteen species from 10 genera (Acuaria,
species), Heterakidae (2 species), Ascaridiidae (2 Chevreuxia, Cheilospuirura, Cosmocephalus, Dis -
species), Heteroxynematidae (1 species), Anisa- pharynx, Echinuria, Paracuaria, Rusguniella, Stre-
kidae (2 species), Ascarididae (4 species), Habrone- ptocara and Syncuaria) from the family Acuariidae
matidae (3 species) and Physalopteridae (1 species). were left in the list after our revision. The genus
The following species from the genus Amidosto - Acuaria is presented with two species: A. anthuris
Nematodes of birds 449

and A. rotundata. We considered A. ornata as a Two species from the Ascaridiidae (Ascaridia galli
junior synonym of A. anthuris following and A. compar) were found in birds in Armenia. A.
Mutafchiev et al. [22]. Interestingly, that the finding alectoris, also reported from Armenia [15–18], now
of A. rotundata [16] is just the second report of this treated as a junior synonym of A. galli [21]. A.
species since its description by Linstow et al. [23]. ketzkhoveli, reported from Caucasian grouse
Other species referred to the genus Acuaria in [16,17], was recognized as a junior synonym of A.
original papers [15–17] we are ranking to the genus compar [21]. In the family Anisakidae we listed two
Cheilospirura in agreement with Schmidt-Raesa species from the genus Contracaecum (C.
[7], Sonin and Barus [21], Smogorzhevskaya [24]. microcephalum and C. rudolphii). And we are
The genus Skrjabinocara was recognized as a junior treating the last one as “sensu lato” since some
synonym of Syncuaria [25], therefore we noted cryptic species have been found within “C.
Skrjabinocara squamata from great cormorant rudolphii” [31]. C. spiculigerum reported from great
[15,17] as Syncuaria squamata. The only one crested grebe [17] was recognized as a junior
species from the genus Dispharynx (D. nasuta) was synonym of C. microcephalum [31]. C. spiculigerum
found in Armenia (in common starling) [15]. This from great cormorant [15] is treated as incorrect
nematode was reported also as Acuaria identification of C. rudolphii [31]. However, since a
(Dispharynx) spiralis [4,17], but we listed it as D. few other species of Contracaecum were found in
nasuta in agreement with Skrjabin et al. [26]. grebes [32], we presume that additional studies
Cosmocephalus aduncus found in Armenian gull concerning the identity of Contracaecum spp. in
was transferred to the genus Paracuaria by grebes from Armenia would be useful. Three species
Anderson and Wong [27]. In addition, the name from Habronematidae (Cyrnea eurycerca, Procyrnea
Rusguniella transcaucasica was listed as one of the leptoptera and Viguiera euryoptera) were reported
synonyms in re-description of this species [28]. from Armenia [15–17]. We took into account the
Rusguniella wedli reported from black-necked taxonomic revisions of Cyrnea and Procyrnea
grebe was synonymized with Rusguniella elongata proposed by Skrjabin and Sobolev [33], and Chabaud
[24]. Streptocara crassicauda, a well-known [34]. As concerning Physalopteridae, we listed
parasite of Anatidae, was reported in Armenia from Physaloptera alata (for Eurasian sparrowhawk) and
gadwall and great crested grebe [15,17]. But, Physaloptera sp. for Eurasian buzzard and tree pipit.
usually Streptocara recta was recorded as a parasite For the last one host we reassigned Physaloptera sp.
of crested grebe [24], thus we presume that from recorded Ph. alata, because tree pipit is an
additional studies would be useful to precise what unusual host for Ph. alata and there is no data on
species of Streptocara parasitizing grebes in morphology of the detected nematode in the report
Armenia. There is also one species from Acuariidae [15].
that possibly have been found in Armenia. The In conclusions, the studies of nematodes
original paper on Acuariidae of starlings from Don, parasitizing birds in Armenia showed rather high
Armenia and Turkestan [4] does not specify clearly species diversity. In total, 52 nematode species have
the host and spot of finding for Syncuaria sturni. been found in birds from Armenia. However, host-
Thus, S. sturni could be described from either specificity and taxonomical position of some of the
common starling or rosy starling and from one of reported nematodes require additional studies and
the areas in the paper title [4]. It is worth mentioning clarification. Zoonotic nematode T. pseudospiralis
that Wong et al. [25] consider S. sturni as a species has been found in Eurasian blackbird, which is
inquirenda. unusual host for this parasite. One species (D. inco-
As concerning Desmidocercidae, the species gnita from great cormorant) has been first described
from this family (Desmidocercella incognita) has in Armenia. H. tricolor has been registered in a new
been first described from the territory of Armenia host (great snipe). Most of the reviewed species of
(in great cormorant) [29]. Five of the identified and nematodes are quite common in birds outside of
one unidentified species from the family Armenia.
Diplotriaenidae (all from the genus Diplotriaena)
were found. It is worth to mention that Sonin [30] Acknowledgements
considered reports of Diplotriaena ozouxi from
thrushes as dubious, so the finding of this nematode The authors are grateful to the staff of the
in rufous-tailed rock-thrush [17] could be erroneous. National Academy of Sciences of Armenia for the
450 S.O. MOVSESYAN et al.

Table 1. Species composition of nematodes parasitizing in birds of Armenia

Host species Species of nematodes Location References
Common quail Cyrnea eurycerca Seurat, 1914
Coturnix coturnix (L., 1758) P [15-17]
(recorded in original paper as Seurocyrnea eurycerca)
Heterakis gallinarum (Schrank, 1788) Madsen, 1949 C [15-18]
Ascaridia galli (Schrank, 1788) Freeborn, 1923 SI [15-18]
Subulura brumpti (Lopez-Neyra, 1922) Cram, 1926 C [15-17]
Subulura sp. (recorded as Subulura leprincei) C [16,17]

Chukar Aonchotheca caudinflata (Molin, 1858) Moravec, 1982

SI [15-17]
Alectoris chukar (Gray, 1830) (recorded as Capillaria caudinflata)
(recorded in original paper as Cheilospirura gruveli (Gendre, 1913) Cram, 1927 (recorded
A. graeca) as Acuaria gruveli and also as A. rotundata, A. spinosa, A. UCG [15-17]
coturnicola)
Ch. hamulosa (Diesing, 1851) Diesing, 1861 UCG [15-17]
H. gallinarum C [16,18]
Ascaridia compar (Schrank, 1790) Travassos, 1913 SI [16-18]
A. galli (recorded as A. alectoris) SI [16,17]
S. brumpti C [15,16]
Subulura skrjabini (Semenov, 1926)
C [15,17,18]
(recorded as S. coturnicis)
Subulura spp.
C [15-17]
(recorded as S. suctoria, S. leprincei, S. allodapa)
Chicken A. caudinflata
Gallus gallus f. domestica L., 1758 SI [18]
(recorded as Capillaria caudinflata)
H. gallinarum C [16,18]

A. galli (recorded also as A. alectoris) O, P, G, SI, C [16,18]

A. compar SI [18]

S. brumpti – [16]

Subulura sp. (recorded as S. suctoria) C [16,18]

Syngamus trachea (Montagu, 1811) Chapin, 1925 T, B [18]

Turkey
H. gallinarum C [18]
Meleagris gallopavo L., 1758
Caucasian grouse A. caudinflata
SI [15-17]
Lyrurus mlokosiewiczi (recorded as Capillaria caudinflata)
(Taczanowski, 1875)
H. gallinarum C [16,17]

A. compar (recorded as A. ketzkhoveli) SI [16,17]

A. galli (recorded as A. alectoris) SI [15-18]

Greylag goose Heterakis dispar (Schrank, 1790) Dujardin, 1845

– [15,17,18]
Anser anser (L., 1758) (recorded as Ganguleterakis dispar)
Amidostomum anseris (Zeder, 1800)
– [15,18]
Railliet et Henry, 1909
Echinuria uncinata
Gadwall – [15,17]
(Rudolphi, 1819) Soloviev, 1912
Mareca strepera (L., 1758)
(recorded as Anas strepera) Streptocara crassicauda (Creplin, 1829)
– [15,17]
Railliet, Henry et Sisoff, 1912
Nematodes of birds 451

Table 1. Species composition of nematodes parasitizing in birds of Armenia

Host species Species of nematodes Location References

Mallard Hystrichis tricolor Dujardin, 1845
P [18]
Anas platyrhynchos L., 1758
Red-necked grebe Podiceps Contracaecum rudolphii Hartwich, 1964 (s.l.)
– [14]
grisegena Boddaert, 1783
Great crested grebe P. cristatus (L., S. crassicauda – [15]
1758) Contracaecum microcephalum (Rudolphi, 1819) Baylis, 1920
G, SI [17]
(recorded as C. spiculigerum)
Black-necked grebe Rusguniella elongata (Rudolphi, 1819) Seurat, 1919 (recorded
– [14]
P. nigricollis Brehm, 1831 as R. wedli)
(recorded also as P. caspicus) C. microcephalum
– [15]
(recorded also as C. spiculigerum)
Common pigeon
S. trachea – [15,17]
Columba livia Gmelin, 1789

European turtle-dove H. gallinarum – [15–17]

Streptopelia turtur (L., 1758)
Ornithostrongylus quadriradiatus
– [15,17]
(Stevenson, 1904) Travassos, 1914
Black–bellied sandgrouse Syphaciella capensis Moennig, 1924
– [15,17]
Pterocles orientalis (L., 1758)
European nightjar Subulura sp.
C [16]
Caprimulgus europaeus L., 1758 (recorded as S. suctoria)
Common coot Fulica atra L., 1758 Amidostomum fulicae (Rudolphi, 1819) Seurat, 1918
UCG [14,15,17]
(recorded as A. anseris)
Squacco heron Ardeola ralloides C. microcephalum
– [14,17]
(Scopoli, 1769)
Porrocaecum ardeae (Froelich, 1802) Baylis, 1936 – [14]
Grey heron Ardea cinerea L., 1758 C. microcephalum – [14]

Purple heron A. purpurea L., 1766 C. microcephalum – [14]

Great white pelican Pelecanus C. rudolphii (s.l.)
– [14]
onocrotalus L., 1758
Great cormorant Syncuaria squamata (Linstow, 1883) Wong, Anderson et
– [15,17]
Phalacrocorax carbo (L., 1758) Bartlett, 1986 (recorded as Skrjabinocara squamata)
Desmidocercella incognita Ssolonitzin, 1932 – [17,29]
C. rudolphii (s.l.)(recorded also as C. spiculigerum) – [15]
Black-winged stilt Chevreuxia revoluta
– [14,17]
Himantopus himantopus L., 1758 (Rudolphi, 1819) Seurat, 1918
Kentish plover Aprocta turgida Stossich, 1902
– [15,17]
Charadrius alexandrinus L., 1758
Northern lapwing Eucoleus vanelli (Rud., 1819) Lopez-Neyra, 1947
– [14,17]
Vanellus vanellus (L., 1758) (recorded as Thominx vanelli)
E. contortus (Creplin, 1839) Gagarin, 1951
– [14]
(recorded as Thominx contorta)
Ch. revoluta – [15,17]
Sociable lapwing
Porrocaecum ensicaudatum (Zeder, 1800) Baylis, 1920 – [15]
V. gregarius (Pallas, 1771)
Great snipe
Gallinago media (Latham, 1787) H. tricolor – [12,15,18]
(recorded as Capella media)
452 S.O. MOVSESYAN et al.

Table 1. Species composition of nematodes parasitizing in birds of Armenia

Host species Species of nematodes Location References

Common snipe G. gallinago (L.,
Cosmocephalus capellae Yamaguti, 1935 – [15]
1758) (recorded as Capella gallinago)
Common sandpiper Actitis hypoleucos
Porrocaecum semiters (Zeder, 1800) Baylis, 1920 – [14]
L., 1758
Armenian gull Eucoleus laricola Wassilkowa, 1930
– [15,17]
Larus armenicus Buturlin, 1934
(recorded as Larus argentatus
armenicus and L. argentatus) Cosmocephalus obvelatus (Creplin, 1825) Seurat, 1919 – [15,17]
Paracuaria adunca (Creplin, 1846) Anderson et Wong, 1981
(recorded as Cosmocephalus aduncus – [15,17]
and Rusguniella transcaucasica)
White-winged tern Chlidonias Epomidiostomum sp.
SI [14]
leucopterus (Temminck, 1815) (recorded as E. orispinum)
Western marsh-harrier Procyrnea leptoptera (Rudolphi, 1819) Chabaud, 1958
Circus aeruginosus (L., 1758) – [15,17]
(recorded as Habronema leptoptera)
Porrocaecum depressum (Zeder, 1800) Baylis, 1920 – [15,17]
Eurasian sparrowhawk Physaloptera alata Rudolphi, 1819
– [17]
Accipiter nisus (L., 1758)
Eurasian buzzard Physaloptera sp.
– [17]
Buteo buteo (L., 1758)
European roller Squamofilaria coraciae (Gmelin, 1790) Dollfuss, 1962
– [2,3]
Coracias garrulus L., 1758 (recorded as S. coronata )
Red-backed shrike Acuaria rotundata (Linstow, 1907) Railliet, Henry et Sisoff,
– [16]
Lanius collurio L., 1758 1912
Lesser grey shrike Viguiera euryoptera (Rudolphi, 1819)
– [17]
L. minor Gmelin, 1788 Seurat, 1913
Eurasian jackdaw Acuaria anthuris (Rudolphi, 1819)
– [17]
Corvus monedula L., 1758
Rook C. frugilegus L., 1758 A. anthuris – [15,17]
Diplotriaena tricuspis (Fedtschenko, 1874)
– [17]
Henry et Ozoux, 1909
S. trachea – [17]
Carrion crow E. contortus
C. corone L., 1758 – [15,17]
(recorded as Thominx contorta)
A. anthuris – [17]
Great reed-warbler Diplotriaena sp.
– [17]
Acrocephalus arundinaceus (L., 1758)
White-throated dipper A. rotundata
– [16]
Cinclus cinclus (L., 1758)
Common starling P. ensicaudatum – [15,17]
Sturnus vulgaris L., 1758
(recorded also as S. caucasicus) P. semiteres – [15,17]
Dispharynx nasuta (Rudolphi, 1819) Railliet, Henry et
– [4,15,17]
Sisoff, 1912 (recorded also as Acuaria (Dispharynx) spiralis)
Diplotriaena obtusa (Rudolphi, 1802) Henry et Ozoux, 1909 – [15,17]

A. anthuris (recorded also as A. ornata) – [4,17]

Rosy starling
Capillaria tridens (Dujardin, 1845) Travassos, 1915
Pastor roseus (L., 1758) – [17]
(recorded as Thominx tridens)
(recorded as Sturnus roseus)
Nematodes of birds 453

Table 1. Species composition of nematodes parasitizing in birds of Armenia

Host species Species of nematodes Location References

Eurasian blackbird Trichinella pseudospiralis Garkavi, 1972 M [9]

Turdus merula L., 1758
P. semiteres – [17]

Rufous-tailed rock-thrush Diplotriaena pungens (Schneider,1866)

– [17]
Monticola saxatilis (L., 1766) Henry et Ozoux, 1909
D. ozouxi (Railliet et Henry, 1909)
– [17]
Henry et Ozoux, 1909
Isabelline wheatear Diplotriaena isabellina
Oenanthe isabellina Koroliowa, 1926 – [17]
(Temminck, 1829)
Pied wheatear P. ensicaudatum
– [15,17]
Oe. pleschanka (Lepechin, 1770)
Tree pipit Physaloptera sp.
Anthus trivialis (L., 1758) – [15]
(recorded as Ph. alata)
Amidostomum chevreuxi Seurat, 1918 – [15,17]
Western yellow wagtail D. ozouxi
– [17]
Motacilla flava L., 175)
Common linnet Agamospirura sp. (larvae)
Linaria cannabina L., 1758 – [17]
(recorded as Cannabina cannabina)
Explanations: T – trachea; B – bronchi; O – oesophagus; P – proventriculus; UCG – under cuticle of gizzard; G – gizzard; SI –
small intestine; C – caecum; M – muscles; “–” means location was not defined in the cited sources.

help of finding rare sources of literature used in this garrula L.]. Zentralblatt für Bakteriologie,
review. Our gratitude also goes to anonymous Parasitenkunde, Infektionskrankheiten und Hygiene.
reviewers for valuable comments regarding the Zweite Naturwissenschaftliche Abteilung 63: 267-271
manuscript. (in German).
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References of nematodes of starlings (Sturnidae) of the Don,
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