CYRNEA COLUMBI SP.N. (NEMATODA: SPIRUROIDEA) FIRST AND NEW REPORT OF THE GENUS FROM AN AVAIN HOST COLUMBA LIVIA (DOMESTIC PIGEON) IN SINDH, PAKISTAN

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CYRNEA COLUMBI SP.N. (NEMATODA: SPIRUROIDEA) FIRST AND NEW REPORT OF THE GENUS FROM AN AVAIN HOST COLUMBA LIVIA (DOMESTIC PIGEON) IN SINDH, PAKISTAN *Siyal Bushra 1, Sanjota Nirmal Das 1, Rafia Rehana Ghazi 2, Aly Khan 3 1 Department of Zoology, University of Sindh, Jamshoro-76080, Sindh, Pakistan. 2 Vertebrate Pest Control Laboratory, Southern Zone Agricultural Research Centre, Karachi University Campus, Karachi 75270. 3 Crop Diseases, Research, Institute (CDRI), University of Karachi campus, Karachi- 75270, Pakistan. *Corresponding author: syalbushra@gmail.com Abstract: A new species of the genus Cyrnea columbi sp.n. is described from an Avian host Columba livia. The new species is characterized by having smaller body size of male, larger body size of female, number and arrangement of caudal papillae, presence of 2 3 large lateral papilla in the caudal region, size of spicules, shape of proximal end of large spicule, shape of gubernaculum, presence of finger like projections in the caudal region of males, smaller size of eggs and new host and locality record. Keywords: Cyrnea columbi sp.n., Spirurideae, Columba livia, Nausharo Feroze, Sindh, Pakistan INTRODUCTION The genus Cyrnea Seurat, 1914 belongs to the family Spirurideae Oerley, 1885 and subfamily Spirurinae Railliet, 1915. Cyrnea is divided into two sub-genera Cyrnea Seurat, 1914 and Procyrnea Chabaud 1958. These are specific Avain parasites infecting the gizzard. Species of the genus are reported from Africa, Asia, Europe, and North America. Single species reported from Pakistan is Cyrnea (Procyrnea Chabaud,1958) chabaudi Rasheed, 1965 from a fish host Parastromateus sp. in Karachi, Pakistan. Yamaguti, 1961 have listed eleven species with Cyrnea eurycerca Seurat, 1914 as type species in Perdixrougs and also reported in Caccabis, Coturnix, Francolinus, Merops, Phasianus, in Europe and Africa. Other species have been reported from avian hosts from all over the world. 15

Species of the genus reported from India are: Cyrnea bulbosa (Linstow, 1906) Ortlepp, 1925 reported from Pavo muticus (Green peafowl); C. euplocami found in Euplocamus Leucomelanos (Nepal Kalij); C. indicum reported in Coracias benghalensis (Indian roller); C. imbricate reported in Asio otus (Long-eared owl); C. asymmetricum found in Circus macrourus (Pallid harrier); C. diesingi reported in Acryllium vulturinum (Vulturine guineafowl); C. casuarii recorded in Casuarius (Cassowary); C. magnilabiatum reported in Ichthyophaga humilis plumbeus (Lead fish eagle) and Pseudo Gyps Bengalensis (Indian grier), the mentioned species have all been reported by Maplestone, 1930 and Chabaud, 1958; C. coraci Mirza et Basir,1938 is reported in Coracias benghalensis (Indian roller) and C. thapari Sanwal, 1951is from Coracias benghalensis (Blue jay). Present specimens have been recovered from Columba livia (Domestic pigeon) from Nausharo Feroze, Sindh, Pakistan. The genus and species Cyrnea columbi sp.n. are reported for the first time from a new Avian host Columba livia in Pakistan. MATERIAL AND METHODS Fifteen bird s Columbia livia (Domestic pigeon) belonging to the family Columbidae were caught from Nausharo Feroze of District Sindh at random intervals. These were brought to the Parasitology Laboratory, Department of Zoology, University of Jamshoro, Sindh, Pakistan. The birds were dissected and examined for collection of internal Helminth parasites. During examination of gut contents and visceral organs, the gizzard of pigeons was found infected with numerous tiny yellowish white nematodes. Eight male and one hundred and twenty-two female specimens were collected from the gizzard of twenty two birds. Later the nematodes were removed from the host s body. These were either fixed in Berland s fluid (1 Part formalin + 19 parts G.A.A) in which the nematodes die, uncoil and stretch in less than a minute depending upon their size (Berland, 1984) or hot steaming 70 % ethanol. Later the nematodes were stored in a solution of 5 parts glycerine and 95 parts 70 % ethanol and cleared in either glycerine or lacto phenol for detailed study. Line drawings were prepared with the aid of a camera Lucida. Body measurements (Length and width) are given in millimeters (mm). Photomicrographs were prepared with the courtesy Department of Zoology Karachi University Campus, Karachi. Specimens are deposited in senior author s collection, Department of Zoology, University of Sindh, Jamshoro. Cyrnea columbi sp.n. (Fig: 1) Host : Columba livia (Domestic pigeon) Location : Gizzard Locality : Nausharo Feroze, Sindh, Pakistan No of hosts examined/ infected: 22/16 No. of specimens recovered: (130), 08 males, 122 female Etymology : Species name refers to the host bird 16

DESCRIPTION IS BASED UPON 8 MALE AND 30 FEMALE SPECIMENS, MOUNTED TEMPORARILY IN ALCOHOL/GLYCERINE MIXTURE. Small, thin worms, dirty or light yellowish in colour. Cuticle with fine transverse striations. Mouth terminal, with two well developed lateral lips, each lip with three lobes on its inner surface additionally there are dorsal and ventral lips. Each labia possess pair of papillae. Buccal vestibule long, roughly U shaped with less chitinized walls. Oesophagus long, divided into short muscular and long glandular portions. MALE: Much smaller and thinner than female 5 to 6 mm long. Maximum width attained at the posterior region directly in front of caudal wing. Head region 0.03 0.06 long and 0.02 0.05 wide. Vestibule 0.04-0.06 long. Total length of oesophagus 2.20 2.50. Tail wings well developed, asymmetrical, commence from approximately near the starting of large spicule and reach up to the end of the tail. Tail wings have maximum width at first pair of stalked papillae measure 0.06 0.09 wide. There are 6 7 pairs of stalked papillae, of which 4 5 pairs are pre-anal, one pair ad-anal and one pair is post-anal. Two to three large lateral papilla are present in male specimens in the posterior caudal region. In male specimens the posterior end of caudal region possesses three to four longitudinal fingers like process instead of sessile pairs of papillae. Spicules are un-equal and dissimilar in shape. Smaller spicule 0.27 0.29, having simple proximal end, while the longer spicule has typical proximal end with three unequal dissimilar processes measure 1.33-1.37 long. The spicules ratio is 1:4.724 1:4.925. Gubernaculum irregular in shape, situated at distal end of the spicule 0.02 by 0.032 in size. Tail length is 0.12 0.14. FEMALE: Larger than male specimens. Body length 20 22 long. Head region 0.09 0.l2 long, 0.06 0.08 wide. Total length of oesophagus 2.70 3.91. Vulva lies in the posterior region of the body at a distance of 0.26 0.34 from posterior end. Vagina highly muscular, those appear a large unpaired lateral papilla near the ventrally opening vulva. Vagina highly muscular. Tail is rounded in shape, 0.37 0.51 long. Eggs are very small, double walled and barrel shaped 0.025 0.028 by 0.01 to 0.011 in size. DISCUSSION Yamaguti, 1961 have listed eleven species of the genus Cyrnea Seurat, 1914 with Cyrnea eurycerca Seurat, 1914 as type species in Perdixrougs and also in Caccabis, Coturnix, Francolinus, Merops, Phasianus, in Europe and Africa. Other species reported from avian hosts are from different countries. A single species Cyrnea (Procyrnea Chabaud,1958) chabaudi Rasheed, 1965 have been reported from a fish host Parastromateus sp. in Karachi, Pakistan. Type species C. eurycerca Seurat, 1914 was also reported by Semenov, 1926; Kurashvili, 1941; Gvzodev 1958; Barus et al., 1977 from Gallinaceous birds in USSR. 17

Literature search reveal several species of the genus Cyrnea. Those reported from India are: C. bulbosa (Linstow, 1906) Ortlepp, 1925; C. euplocami; C. indicum; C. imbricate; C. asymmetricum; C. diesingi; C. casuarii; C. magnilabiatum, the mentioned species have all been reported by (Maplestone, 1930) Chabaud, 1958; C. coraci Mirza et Basir, 1938; C. thapari (Sanwal, 1951). In present specimens the male is relatively smaller in size than the female, having unequal spicules, the ratio being 1:4.724 1:4.925, asymmetrical wings of caudal alae and total number of 6 7 stalked papillae of which four to five are pre-anal, one pair is ad-anal and one pair is post-anal. In posterior end of caudal region there are three to four fingers like projections. Gubernaculum is irregular in shape. The body size of female is 20 22 long, it is nearly 4 times longer than male. Vulva opening is situated at distance of 0.26 0.34 from the posterior end; eggs are very small, somewhat barrel shaped 0.025 0.028 by 0.01 to 0.011 in size. The present specimens do not match exactly with the above reported Indian and type species. (Comparative body measurements of Indian species are mentioned in Table. 1). Species reported from Asia and Europe are: C. capitellata (Schneider, 1866) Guschanskaja, 1937 was reported in Coracias garrula (Roller) from Europe and Asia. Body length of male is 7.55 and female is 11.27. Nine pairs of caudal stalked papillae of which 3 pre-anal and six pairs are post-anal, spicules size is 0.89 0.96 and 0.36 0.41. C. seurati Lopez-Neyra, 1918 was found in Alectoris rufa (Red rock partridge) from Spain. Body length of male is 8.0 13.6 and female is 13.0 17. Lateral lips provided with teeth like projections on the internal surface. Tail wings are symmetrical, 9 pairs of stalked papillae 3 pre-anal, six pairs post-anal, proximal and distal end of spicules are rounded in shape, spicules size are 1.25 1.39 and 0.45 0.500. This species is also reported by Meszaros, 1968 from Predatory birds in Hungary. C. excisiformis Yamaguti, 1935 was reported in the Asio otus (Long-eared owl). Body length of male is 8.0 8.4 and female body length is 11.6 11.95. Tail is blunt, 4 pairs of stalked papillae are pre-anal and as many shorter seating post-anal, 1 big unpaired papilla in front of cloaca is present, smaller spicule end is rounded, distal end of larger spicule is pointed, spicules size are 1.05 1.12 and 0.39 0.42. C. graphophasiani Yamaguti, 1935 was found in Syrmaticus soemmerringii (Copper pheasant) from Japan. Male length is 7.8 12.7, while female body length is 14.0 24.0. Nine pairs of long pedunculate papillae are present, spicule endings are simple rounded 0.42 0.48 and 1.1 1.35 long. C. lyruri Fedjushin, 1946 was reported in birds of Tetraonidae family from USSR. Male body length is 10.14 18.92 and female is 12.0 28.0. Caudal end is provided with 6 pairs of 18

stalked papillae, six pairs of sessile papillae at the end of the tail, length of the left spicule is 2.06 2.92 and right spicule is 0.782 1.098. Right spicule is wider with claw like structure at distal end. This species also reported by Gvozde 1958 in Kazakhstan. The present specimens mainly differing from C. lyruri in having much smaller body size of male specimens, right spicule is much smaller and left spicule is larger. Present specimens are also different from above, other reported species, in having smaller size of male and larger size of female, size of spicules, shape of endings of spicules, number and arrangement of caudal papillae, smaller size of eggs, different host and locality. Spicule size of present specimen approximately matches with size of spicules in C. capitellata. Species recorded from Africa are: C.ficheuri (Seurat, 1916) Chabaud, 1958 was recorded in Bubulcus ibis (Cattle egret) from Algeria and also in Mexico. Male body length is 8.4 and female is 12.8. Cephalic end is provided with 2 pairs of lateral papillae. Tail wings are symmetrical and narrower in width, 6 pairs are stalked papillae of which 4 are pre-anal, 2 post anal, 1 unpaired papilla present in front of cloacal opening, 4 sessile papillae are at the end of tail, egg size are 0.047 by 0.023. C. parroti Seurat, 1917 was reported in Alectoris graeca (Rock partridge) from Algeria. Body length of male is 11.7 and female body length is 18.8. Spicules length is 1.34 and 0.490, nine pairs of long stalked papillae situated in caudal region, of which 3 are pre-anal, 6 post-anal and very small papilla at the anterior of cloaca. Eggs size are 0.052 by 0.024. This species is also reported by Lopez- Neyra 1918, Junker et al., 2007 in Guinea fowls from Limpopo province of South Africa. C. numidae (Ortlepp, 1938) Chabaud, 1958 was recorded in Numididae (Gunieafowl) from Nessalend, Transvaal and Svasilend. The body length of male is 11.0 13.0 and female is18.0 19.0. Lateral lips are almost rectangular and provided with ventral horn outgrowth in each. Caudal end contains 12 pair of papillae s, spicule endings are simple,1.08 1.11 and 0.420 0.438, eggs measure 0.042 0.045 by 0.024 0.03; C. buckleyi (Bisseru, 1955) Chabaud, 1958 was found in Otididae (Bustard) from Northern Rhodesia. Male body length is 7.9 8.0 and female body length is 12.0 14.1. Mouth is dorsoventral slit, two lateral lips separated by three blades. Spicules are sharp and thin, larger spicules are 0.36 0.41 and the smaller is 0.21 0.28, asymmetric tail wings supported by 6 pairs of stalked papillae of which 4 are pre-anal, 2 posteriors, 4 pairs sessile papillae placed at end of the tail, 1 papilla located at the opening of cloaca. Eggs are 0.03 0.043 by 0.021 0.027 in size. C. antennijera Chabaud et Rousselot, 1957 was reported in genus Francolins from the Zoo in Brazzaville (measurements were not given in literature). 19

The present species differ from above reported species in having: smaller body size of male, larger body size of female, different shape of mouth lips and cephalic papillae from C. numidae and C. buckleyi, have different number and arrangement of caudal papillae and sensitive papilla, different size of spicules (in C. buckleyi size of large spicule is very smaller than in the present specimen), smaller size of eggs, different host and locality. Species reported from America are: C. semilunaris Molin, 1860 was reported in Piaya cayana macroura (Squirrel cuckoo) and Trogon collaris (Collared trogon) from Brazil, Paraguay, this species was also recorded in USSR (body measurements are not found in literature). Tail is provided with 6 pairs of stalked papillae, 3 pairs are sessile at the end of the tail, spicule endings are simple. C. incerta (Smith, 1908) Chabaud, 1958 was recorded in Psittaciformes (Parrots), Gallus gallus domesticus (Chicken) and Lophortyx californica (California Quail). Male body length is 8.0 and female body length is 14.0. Six pairs of stalked caudal papillae, 1 unpaired papillae situated in front of cloaca, spicule ends are pointed (Size not mentioned). Eggs are 0.034 0.042 by 0.02 in size. C. mansioni (Seurat, 1914) Chabaud, 1958 was found in Buzzards, Milvus korschun (Black kite), Falco sparverius (American kestrel) from South America, North America, Europe, USSR and in Asia.Tail wings provided with leaf like Gubernaculum, 6 pairs are the stalked papillae, 3 pair are sessile papillae and 1 unpaired papilla in front of Gubernaculum, spicules distal ends are pointed (sizes are not mentioned). C. longispicula (Walton, 1927) Chabaud, 1958 was reported in genus Strix (owl) from North America. Male body length is 5.07. Right spicule length is 3.24, its distal end provided with one sided beard and left spicule ends with spherical bumps, length is 1.08, tail wings narrower, 4 pairs stalked papillae are pre-anal, 2 post-anal and 1 papilla located on dorsal lip of cloaca, two groups of small papillae, 5 in each beam. C. colini Cram, 1927 was reported in Colinus virginianus (Virginia quail), Meleagris gallopavo (Wild turkey), Lyrurus tetrix (Black grouse), Pediocetes phasianellus (Sharp-tailed Grouse) from United States George. This species is also reported by Davidson et al., 1977 from Wild turkeys in Southern United states. Male body length is 6.0 and female length is 14.0 18.0. Ten pairs are stalked papillae form continuous rows, 4th pair is ad-anal, left spicule length is 2.0 and right is 0.36. Eggs size is 0.0405. C. piayaei Sandground, 1929 was recorded in Piaya cayana (Squirrel cuckoo) from Yucatan. Male body length is 8.5 and female body length is 16.4. Tail wings are symmetrical provided with 9 pairs of papillae of which 6 are stalked papillae, 3 pairs are sessile; spicule endings are simple, spicule lengths are 0.58 and 1.22. C. americanum (Chandler, 1941) Chabaud, 1958 was found Buteo platypterus (Broad-winged 20

hawk) from Texas. Male body length is10.0 and female is 15.0. Tail wings are with massive wedge-shape provided with 5 stalked papillae and 8 sessile papillae at the end of the tail, spicule endings are rounded to pointed, right spicule length is 0.22 and left is 0.725. Eggs are 0.034 by -0.019 in size. C. longistriata (Molin, 1859) Chabaud, 1958) was found in family of Picidae from South America. Male body length is 6.0 0.90 and female is 10.0. Tail wings are symmetrical provided with 6 pairs of stalked papillae, 3 pairs are sessile papillae at the end of the tail, 1 papilla is in-front of cloacal opening, right spicule distal end is pointed and in left it is rounded. C. neeli Davidson et al., 1977 was reported from Meleagris gallopavo (Wild turkeys) in United States. Body size of male is 12.8 (11.6 13.6). Ten pairs of lateral pedunculated caudal stalked papillae of which 2 pre-anal, 1 is ad-anal, 2 post-anal and 5 small pairs are arranged near posterior extremity, length of left spicule is 2.2 (2.1 2.3) and right is 734 (670 800). Female body size is 18.0 (17.3 18.9), vulva 626 (560 660) from posterior extremity, eggs size is 41 (40 42), tail is 180(160 200). The present specimens differ from above reported species from America in having; smaller size of male (except C. longispicula and C. colini) and larger size of female, number and arrangement of caudal papillae, size and endings of spicules, shape of Gubernaculum, eggs size, host and locality. Male body size of present specimens approximately matches with C. longispicula and C. colini. Species recovered from South Australia: C. aegotheles (Johnston et Mawson, 1941) Chabaud, 1958 was parasitized in Aegotheles cristatus (Owl nightjar). Male body length is 2.5 mm; female body size is 4.8. Spicules length is 0.18 and 0.7. There are four stalked preanal papillae at one side and on the other side there are six, one pair of small sessile papillae lie directly behind the anus, one pair of large stalked papillae behind them, tail is curved dorsally. Present specimens totally differ in having; larger size of male and female specimens, number of cephalic papillae, number and arrangement of caudal papillae, size of spicules, shape of tail, host and locality. C. antennifera reported by Chabaud et Rousselot, 1957. (Locality and host is not given in literature) Male body length is 10.0 and female 15.5. Tail wings are symmetrical, contain 9 pairs of papillae and two phasmids, right spicule length is 0.43 and left is 1.2, spicule endings are simple, gubernaculum symmetrical and heart shaped. C. lycur recorded by Mamaev, 1959 (host, locality and body measurements are not given in literature). Tail wings are symmetrical provided with 6 pairs of stalked papillae of which 3 are pre-anal, 1 ad-anal and 3 pairs post-anal, at the end of tail4 pairs of small finger like papillae are present, distal end of right spicule is leaf like. 21

Present specimens are different from all above reported species; main differences noted are in having different: Host and locality Larger size of female (except C. lyruri 12 28) and mostly smaller size of male Number and arrangement of caudal papillae Presence of 2 3 large lateral papilla in caudal region. Size and shape of proximal end of larger spicules Shape of gubernaculum Presence of finger like projections in the region of caudal end and Smaller size of eggs As present specimens do not match with the reported species of the genus Cyrnea and thus propose as a new species C. columbi sp.n. The species name refers to the common avian host Columba livia. 22

Table-1 Comparative body measurements of some species of the Cyrnea reported from Avain hosts in India. Species name C. bulbosa (Linstow, 1906) Ortlepp, 1925 C.euplocami (Maplestone, 1930) Chabaud, 1958 C. indicum (Maplestone, 1930) Chabaud, 1958 C. imbricate (Maplestone, 1930) Chabaud, 1958 C. asymmetrium (Maplestone, 1930) Chabaud, 1958 C. diesingi (Maplestone, 1930) Chabaud, 1958 Host Pavo muticus (Green peafowl) Euplocamus Leucomelanos (Nepal Kalij); Coracias benghalensis (Indian roller) Asio otus (Long-eared owl) Circus macrourus (Pallid harrier) Acryllium vulturinum (Vulturine guineafowl) Male Body size 10.4 by 0.325 10.4 by 0.25 7.1 8.3 by 0.23 7.5 by 0.23 8.8 by 0.257 No. of caudal papillae 4 pairs of stalked, of which 2 preanal, 2 postanal, pair couple adanal often stalked, 4 5 pairs small stalked papillae (10 pairs) 5 pairs stalked papillae with long stalked alternate with short stalked, of 2 preanal, 1 adanal, 2 postanal and 5 pairs sessile papillae (9 pairs) four pairs preanal, 1 adanal, 4 pairs sessile papillae. (5 pairs) 4 of which preanal, 1 is located behind cloaca In left 8 papillae, right 11 papillae. 5 left and 7 right preanal, 1 each side adanal and remaining are postanal (10 pairs) nine stalked of which 2 preanal, 7 post anal 1 pair of seats (adanal) Spicules size 1.0 by 0.436 0.694 and 0.357 1.38 and 0.38 0.65 and 0.24 1.7 and 0.297 Gubernaculum Triangular shape Boat shape Short Not described Wide gubernaculum Female Body size 24.0 by 0.455 18.5 19.5 by 0.34 0.44 10.75 by 0.35 10.6 by 0.26i 11.0 by 0.29 14.5 by 0.336 Position of vulva 1.2 from the end of the body 1.45 from rear end Located near anus to 0.59 from rear end 5.7 from the front end of the body Located anterior to the mid of the body from 5 9 its rear end 1.74 distance from rear end Egg size 0.044 by 0.026 0.045 by 0.021 0.040 0.45 by 0.020 0.026 0.036 by 0.15 0.16 0.025 0.028 by 0.01 to 0.011 23

Species name C. casuarii (Maplestone, 1932) Chabaud,1958 C. magnilabiatum (Maplestone, 1930)Chabaud, 1958 C. coracimirza et Basir, 1938 C. thapari Sanwal, 1951 C. columbi sp.n. (Present specimen) Host Casuarius (Cassowary) Ichthyophaga Humilis Plumbeus (Lead fish eagle) Coracias benghalensis (Indian roller) Coracias benghalensis (Blue jay) Columba livia (Domestic pigeon) Male Body size 26.5 by 0.544 9.1 by 0.26 8.2 0.24 5 6 Number of caudal papillae (11 pairs) 5 pairs large stalked papillae of which 3 preanal, 1 adanal, 1 post anal, 2 pairs subventral, six pairs sessile (6 pairs) 4 pairs long preanal, 2 pairs short papillae behind cloaca 1.78 and 0.554 Asymmetrical shape (10 pairs) of which 3 stalked (10 pairs) 9 satlked and pair stalked sessile papillae of which 10 pairs, 3 preanal, 1 adanal, 6 postanal 6 7 pairs of stlked papillae of which 4 5 pairs preanal, 1 adanal, 2 postanal, 2 3 large papillae on lateral side Spicule size 3.1 3.9 and 1 1.3 15.6 by 0.39 0.27-0.29 and 1,33-1.37 Gubernaculum Triangular shape 7.5 distance from the front of the end Irregular Female Body size 53 by 0.89 0.04 by 0.030 20 22 Position of vulva Behind middle body 8.3 9.2 from rear end Posterior region at distance 0.26 0.34 Egg size 0.02 0.l025 by 0.01 0.011 24

Fig.1: Cyrnea columbi sp.n. A. Enlarged view of anterior region of male (Ventral view) B. Enlarged view of caudal region of male (Ventral view) C. Posterior region of male showing complete spicules and caudal wings D. Proximal end of small spicule E. Proximal end of large spicule 25

Fig.2: Cyrnea columbi sp.n. A. Anterior region of female (Lateral View) B. Posterior region of female (Lateral View) C. Enlarged view of muscular vagina, genital opening and eggs (Ventral view) 26

A B 20x5 C 20x5 10x5 Fig.3: Photomicrographs of Cyrnea columbi sp.n. A. Enlarged anterior region of male. B. Enlarged posterior caudal region of male C. Posterior region of male showing complete spicules 27

10x5 10x5 Fig.4: Photomicrographs of Cyrnea columbi sp.n. A. Anterior region of female B. Posterior region of female C. Enlarged eggs 28

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Seurat, L. G., 1916. Sur un nouveau type de Spiruridae. C. R. Soc. Biol., 79(11): 517 519. Smith, A.J., 1908. Synopsis of studies in metazoan parasitology in McManus laboratory of pathology, University of Pennsylvania. Univ. Penn. Med. Bull. 20(12): 262 282. Walton, A.C., 1927. A revision of the nematodes of the Leidy collections. Proc.Acad. Nat. Sc. Phila. 79: 49 163. Yamaguti, S. 1935. Studies on helminth fauna of Japan. Pt. 12. Avian nematodes, I. Jap. J. Zool., 6(2): 403 431. Yamaguti, S. 1961. Systema Helminthum. Vol. III. The Nematodes of Vertebrates. Interscience Publishers, New York. 1259 p. 31