埃塞俄比亚塔纳湖鲤科鱼类体内亚美尼亚许氏绦虫khawia Armeniaca

埃塞俄比亚塔纳湖鲤科鱼类体内亚美尼亚许氏绦虫Khawia armeniaca (Cholodkovsky, 1915) Shulman, 1958 (绦虫纲: 鲤蠢目) 的形态鉴定 KIBETCaroline Jepkorir 赵文婷 SARWARHuda 聂品 REDESCRIPTION OF THE MONOZOIC CESTODE KHAWIA ARMENIACA (CHOLODKOVSKY, 1915) SHULMAN, 1958 (CESTODA: CARYOPHYLLIDEA) FROM CYPRINID FISH IN TANA LAKE, ETHIOPIA KIBET Caroline Jepkorir, ZHAO Wen-Ting, SARWAR Huda, NIE Pin 在线阅读 View online: https://doi.org/10.7541/2021.2020.095

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2021 年 7 月 ACTA HYDROBIOLOGICA SINICA July, 2021 doi: 10.7541/2021.2020.095

REDESCRIPTION OF THE MONOZOIC CESTODE KHAWIA ARMENIACA (CHO- LODKOVSKY, 1915) SHULMAN, 1958 (CESTODA: CARYOPHYLLIDEA) FROM CYPRINID FISH IN TANA LAKE, ETHIOPIA

KIBET Caroline Jepkorir1, 2, 3, ZHAO Wen-Ting1, SARWAR Huda1 and NIE Pin1, 4 (1. State Key Laboratory of Freshwater Ecology and Biotechnology, Key Laboratory of Aquaculture Disease Control, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China; 2. University of Chinese Academy of Sciences, Beijing 100049, China; 3. Zoology Department, Ichthyology Section, National Museums of Kenya, P.O Box 40568-00100, Nairobi, Kenya; 4. School of Marine Science and Engineering, Qingdao Agricultural University, Qingdao 266109, China)

Abstract: Khawia armeniaca (Cholodkovsky, 1915) (Cestoda: Lytocestidae) is described from cyprinids Labeobarbus intermedius and Labeobarbus tsanensis in Tana Lake in Ethiopia. It is characterised with its afossate scolex in a semi-bulbate shape and a smooth anterior margin. Testes are distributed at the median, with the testicular field reaching the anterior region of cirrus sac. Previtelline follicles are distributed at median and lateral body, extending to anterior or posterior region of the cirrus sac. Uterus is looped between the posterior region of the ovary and the posterior region of the cirrus sac, not reaching the anterior region of the cirrus sac. Few vitelline follicles are present along the uterus margin and few or rare along the ovarian margin. K. armeniaca possesses follicular and butterfly-shaped ovary, with gonopores separated but close to each other, and male gonopore is at the anterior region of the female gonopore, but form a common genital atrium at the surface. Postovarian vitelline follicles are less than 100, touching or far from the posterior ovarian arm.

Key words: Lytocestidae; Khawia armeniaca; Morphology; Morphometrics; Tana Lake; Ethiopia CLC number: S941.5 Document code: A Article ID: 1000-3207(2021)04-0917-08

Cestodes, which are obligate endoparasites, can vision with morphological and molecular data, be grouped into unsegmented or monozoic, and seg- Scholz, et al. [5] only recognized seven valid species mented or polyzoic tapeworms, the former of which from all seventeen nominal species in the genus, in- are classified in the subclass Cestodaria, containing cluding K. sinensis Hsü, 1935, K. armeniaca (Cho- three orders, Amphilinidea, Caryophyllidea, Gyro- lodkovsky, 1915) Shulman, 1958, K. baltica Szidat, cotylidea[1, 2]. Species in the Caryophyllidea van Bene- 1941, K. japonensis (Yamaguti, 1934) Hsü, 1935, K. den in Carus, 1863, are normally intestinal parasites parva (Zmeev, 1936) Kulakovskaya, 1961, K. rossit- of teleost fish, and can be further classified into four tensis (Szidat, 1937) Markevich, 1951, K. saurogobii families: Lytocestidae Hunter, 1927, Caryophyl- Xi, Oros, Wang, Wu, Gao et Nie, 2009. Recently, Xi, laeidae Leuckart, 1878, Capingentidae Hunter, 1930 et al. [6] reported a new species, K. abbottinae from and Balanotaeniidae Mackiewicz & Blair, 1978, the gudgeon Abbottina rivularis (Cyprinidae: Gobio- based on the arrangemnt of longitudinal musculature[3]. ninae) in Taihu Lake, Wuxi, and from the Yangtze In the order Caryophyllidea, Khawia Hsü, 1935 River in Wuhan, China. However, as presented in the in the Lytocestidae, which was erected for the new revision, K. baltica Szidat, 1941 was phylogeneti- species, Khawia sinensis, in the intestine of common cally separated from other six species of the Khawia carp Cyprinus carpio in China[4], was considered as on the basis of ssrDNA and D1-D3 lsrDNA, or mito- probably the most specious genus[5]. However, in a re- chondrial nad3 and cox1 genes, or the combination of

Received date: 2020-04-30; Accepted date: 2020-09-15 Foundation item: Supported by the “First Class Fishery Discipline” Program ([2018]8) in Shandong Province Brief introduction of author: Caroline Jepkorir Kibet (1991—), female, major in fish parasitology. E-mail: [email protected] Corresponding author: Nie Pin, E-mail: [email protected]; [email protected] 918 水生生物学报 45 卷 these markers [5]. Much recently, it has been reported try, and the Biosphere Reserve is part of the Eastern that K. baltica Szidat, 1941 should be replaced into Afromontane Biodiversity Hotspot with the distribu- the genus Caryophyllaeus Gmelin, 1970, as C. bal- tion of many Palaearctic migrant water birds, indige- tica (Szidat, 1941) Barčák, Oros, Hanzelová et nous trees and agricultural crops. Fish community in [7] Scholz, 2017 . the lake is dominated with cyprinid fish, of which Khawia armeniaca was originally described as about twenty species are endemic. Cyprinids in the Caryophyllaeus armeniacus Cholodkovsky, 1915 in lake are represented by four genera, Varicorhinus, the family Caryophyllaeidae, from Capoeta capoeta Garra, Labeobarbus and Barbus. A total of fifteen sevangi (Cyprinidae: Barbinae) from Sevan Lake in species of labeobarbs, Labeobarbus spp., which be- Armenia. But, this species was transferred to the long to a unique flock of endemic cyprinids, were Lytocestidae and the Khawia, because testes in the supported by the examination of mitochondrial DNA species are medullarilly located and vitellarium cor- markers[10], and it was reported that they occupied dif- [8] tically located . This cestode has been reported ferent habitats in relation with water depth and sub- mainly from barbels in some middle Asian countries stratum[11]. The possible adaptive speciation hypothe- such as Armenia, Azerbaidjan, Georgia, Iran, Iraq, Is- sis was proposed to explain the existence of labeo- rael, and in some African countries such as Egypt, barb species in the lake, in which available new lacus- Morocco, Tanzania, Uganda (for details see the revi- [5] trine habitats since the formation of Tana Lake sion by Scholz, et al. In an investigation into the through the volcanic blocking with the lower Blue helminth parasite fauna in fish in Tana Lake of Nile might have resulted in the speciation of labeo- Ethiopia, Africa in 2017, a monozoic cestode was col- barbs[12, 13], and in the presence of highly variable popu- lected and it was indicated in an initial examination lations of riverine L. intermedius in the lake[14]. that this cesotde should belong to the genus Khawia. 1.2 Cestode collection and examination In consideration of the lack of morphological descrip- Investigations into the helminth parasites of fish tion of any Khawia sp. in the lake, cestodes colleted in Tana Lake were conducted from the 19th to 25th in from intestines of Labeobarbus intermedius and L. May, 2017. Fish were purchased from fishermen in a tsanensis (Cyprinidae: Barbinae) in Tana Lake, fishery dock, and fish were either trapped using trap Ethiopia were described in detail. The present study net or caught using fyke net. All fish samples were thus represents the first finding of Khawia armeniaca brought back to a local research station, where they in the Caryophyllidea from fish in Tana Lake, al- were dissected under a microscope. A total of eighty- though a previous report has indicated the occurrence six Labeobarbus intermedius and eighteen L. tsanen- of Khawia sp. in the lake [9]. sis, with the mean body length of 23.70 cm (± 1.80 1 Materials and methods SD) and 24.65 cm (± 2.62 SD), respectively, were exa- 1.1 Sample locality mined during the investigation. Tana Lake is situated about 1800 m above sea The cestodes were collected from the intestines level in the north-western highland of Ethiopia, and is of freshly killed L. intermedius and L. tsanensis of the the largest lake in the country, which is formed Ethiopian largest lake, Tana Lake, a UNESCO Bio- [15] through volcanic activity, ca 5 million years ago to sphere reserve . Parasites were washed in 0.9% sa- block the course of inflowing rivers. The lake has a line, fixed in hot formalin and transferred to 70% al- surface area of 3673 km2, with a surrounding drain- cohol. For light microscopy, the specimens were age area of 11650 km2, and a maximum depth of 14 m. stained in iron acetocarmine solution, destained in The water level has been regulated recently since the 70% hydrochloric acid alcohol, dehydrated in a series construction of control weir, and the lake drains to its of gradually increasing percentages of ethanol, 70%, southern extremity and to its only outflowing river, 80%, 95% and 100%, clarified in clove oil and moun- the Blue Nile by about 40 m high spectacular falls at ted in Canada balsam. Measurements were taken un- Tissisat. In 2015, the Tana Lake region was nomina- der BH-2 Olympus Japan microscope and illustra- ted as UNESCO Biosphere Reserve in recognition of tions were made using a drawing attachment of Olym- its national and international natural and cultural im- pus MVX10 microscope with the use of Nomarski in- portance. The geographical location of the lake is terference contrast. For histological sectioning, the 11°25′07′′—12°29′18′′ N, and 36°54′01′′E—37°47′ specimens were embedded in wax, sectioned in 4—8 μm 20′′E[10—14]. thick through cross and longitudinal sections, stained Being the largest lake in Ethiopia,Tana Lake ac- using Harris’ hematoxylin stain, destained in 1% hy- counts for 50% of the total inland water of the coun- drochloric acid, counterstained in 1% water soluble 4 期 KIBET Caroline Jepkorir 等: 埃塞俄比亚塔纳湖鲤科鱼类体内亚美尼亚许氏绦虫 Khawia armeniaca 919 (Cholodkovsky, 1915) Shulman, 1958 (绦虫纲: 鲤蠢目) 的形态鉴定 eosin, dehydrated in alcohol, cleared in Xylene, air- The testicular field reaches almost the anterior mar- dried and mounted in Canada balsams [5, 16]. Speci- gin of the cirrus sac, representing 47.51%—61.87% mens are deposited at the Institute of Hydrobiology, of the body length. Cirrus sac is thick and oval in Chinese Academy of Sciences, Wuhan, Hubei Pro- shape (Fig. 2B, 2C, and 2D), with a size of vince, China. (0.39—0.70)×(0.68—1.43), representing 44.63%— 2 Result 49.30% of the body width. Vas deferent looped at the anterior region of the cirrus sac (Figs. 2C and 3A, B, 2.1 Morphology and morphometric analysis C, D, E), and the inner seminal receptacle is present. Family: Lytocestidae Hunter, 1952 Ovary is follicular, and butterfly shaped with wide Species: Khawia armeniaca (Cholodkowsky, and short arms (Fig. 3C, 3D and 3E) at a total length 1916), Shulman, 1958 of 0.76—1.80, representing 2.52%—4.48% of the Synonyms: Caryophyllaeus armeniacus Cho- body length. The total width at the isthmus is 0.68— lodkowsky, 1915; Khawia barbi Rahemo et Mo- 1.24, representing 77.27%—88.03% of the body hammad, 2002; Khawia lutei Al-Kalak et Rahemo, width. The anterior arm is longer than the posterior 2003, Khawia baltica described by Chubb, et al., arm by 0.24—0.67. Seminal receptacle is present at 1997 the dorsal of ovarian isthmus (Fig. 2D). Host: Labeobarbus intermedius and Labeobar- Vitelline follicles are numerous, spherical to al- bus tsanensis, with the prevalence of 16.28%, 16.67%, most oval in shape, being 71.82—159.60 μm×71.82— and the intensity ranging from 0—31, 0—10, respec- 175.56 μm, located at cortical parenchyma (Fig. 2A), tively. the anteriormost vitelline follicle begins at 1.09—2.15 Site of infection: Intestine from anterior extremity. Preovarian vitelline follicle Locality: Tana Lake, Ethiopia almost reaches the anterior margin of the cirrus sac Description based on 10 gravid samples, all (Fig. 3D), while in some specimens it reaches almost measurements are in mm unless otherwise indicated. the posterior margin of the cirrus sac (Fig. 3C and 3E). Body length of (n=8) 30—40, maximum width at 1/3 Few vitelline follicles are present along the uterus of the body from the anterior region, being 0.88— margin and few or rare along the ovarian arm (Fig. 3C, 1.41, and narrows towards the posterior end. The 3D, and 3E). Preovarian and postovarian vitelline scolex is afossate, with a semi-bulbate shape and a follicles are separated. The postovarian vitelline smooth anterior margin (Fig. 1A) with a width of follicles are approximately<100 in number and touch- 1.27—1.79, slightly wider than the neck. The neck ing the ovarian arm (Fig. 3C), while in other species, width (n=3) is 0.74—1.21. The genital pores are seen it is far from the posterior ovarian arm. Uterus looped on surface, but are separate, being close to each other. between posterior region of the ovary and posterior The body is covered with acicular fillitriches (Fig. 1B). region of the cirrus sac, with a length of 2.23—4.92, Tetes are medullary (Fig. 2A), almost oval to spheri- representing 7.43%—12.29 % and 47.52%—61.87 % cal, being (95.76—247.38) μm×(99.75—247.38) μm of the body and testicular field length respectively. (n=9) in size, and approximately>200 in number, dis- The uterine gland is present (Fig. 2C). Vagina tubular, tributed at the median and intermingled with vitelline almost straight and joins with the uterus to form uter- follicles. Anteriormost testis begins at 2.26—4.38 ovaginal duct (Fig. 2C and 2D). Genital pores are se- from the anterior extremity and (n=8) 0.40—2.23 parated but close to each other. The male gonopore is from the posterior of anteriormost vitelline follicle. situated at the anterior region of the uterovaginal

A B

Fig. 1 Scanning electron micrograph (SEM) of Khawia armeniaca from Labeobarbus intermedius in Tana Lake, Ethiopia A. shape of the scolex; B. acicular fillitriches. Scale: A. 1 mm; B. 5 μm 920 水生生物学报 45 卷

AB ing to the anterior region of the cirrus sac with the vf presence of uterine gland. The seminal receptacle is

te vf present at the dorsal of the ovarian isthmus. Genital oc te gonopores are separated, forming a common genital atrium at the surface. The present caryophyllidean ilm highly resembles K. armeniaca Cholodkovsky, 1915 in the scolex afossate, semi-bulbate with smooth anterior margin, butterfly shaped and follicular ovary, few postovarian vitelline follicle, < 100 in number, CD and postovarian vitelline follicle touching the posterior region of the ovarian arm, while in other species [5] vd va not reaching at the ovarian arm . cs Khawia armeniaca is distinguished from K. ov parva Zmeev, 1936 in the shape of ovarian arm which is H-shaped with posterior arm bent slightly inward. It va sr is separated from K. sinensis which possesses a fes- ut toon-like scolex with deep folds, long H-shaped ovary ug and extensive postovarian vitelline follicles. It differs

from K. rossittensis Szidat, 1937 which has a long Fig. 2 Histological sectioning of Khawia armeniaca from Labeo- ovarian arm and posterior arm bent inwards forming barbus intermedius in Tana Lake, Ethiopia an inverted A-shaped and extensive postovarian vitel- A. cross section anterior to the cirrus sac; B. longitudinal at testi- [5] line follicles . It is distinguished from K. saurogobii cular region; C. longitudinal at uterine region; D. longitudinal at ovarian region. Abbreviations: cs. cirrus sac; ilm. inner longitudi- Xi, Oros, Wang, Wu, Gao et Nie, 2009 which pos- nal musculature; oc. osmoregulatory canal; ov. ovary; sr. seminal sesses a truncated cuneiform-flabellate scolex with receptacles; te. testis; ut. uterus; ug. uterine glands; va. vagina; vd. superficial groove, long ovarian arm which is bent to- vas deferent; vf. vitelline follicle wards each other almost forming inverted A shaped, while in other species the posterior arm joins [17]. It is pore, but forms common genital atrium at surface. In- also different from K. abbottinae which possesses two trauterine eggs are oval in shape, operculated and un- longitudinal bands formed by testes and equal ovary embryonated, with the size of 35.91—55.86 μm× arm length, posterior arm bent slightly inwards [6, 18]. 47.88—83.79 μm (Tab. 1). The tapeworm described in the present study from 2.2 Remarks Tana Lake is considered as K. armeniaca (Cho- The tapeworm in the present study is placed in lodkovsky, 1915). the Lytocestidae family because the testes are situated at the medullary and vitellarium at the cortical 3 Discussion parenchyma. It possesses diagnostic features of Khawia armeniaca in the present study highly Khawia spp. proposed to be valid by Scholz, et al. [5], resembles K. baltica studied by Chubb, et al. [19] in including K. sinensis Hsü 1935, K. armeniaca (Cho- important taxonomical features, such as in having few lodkovsky, 1915), K. baltica Szidat 1941, K. parva vitelline follicles along the margin of uterine loop and Zmeev, 1936, K. rossittensis Szidat, 1937, K. sauro- few or absent along the ovarian arm. The postovarian gobii Xi, Oros, Wang, Wu, Gao et Nie 2009. The an- vitelline follicles touch the posterior region of the teriormost testis starts at distance from the anterior ovarian arm, while in other species it is far from the extremity and testicular field extends to the anterior ovarian arm with the ovary being a butterfly-shaped margin of the cirrus sac. Anteriormost vitelline not an H-shaped. However, K. baltica Chubb et al. follicle begins pretesticularly. Preovarian vitelline 1997 possesses fan-shaped scolex with incision, while follicle extends backwards reaching the anterior or al- K. armeniaca possesses a semi-bulbate scolex with most to the posterior margin of the cirrus sac. The smooth anterior margin, as indicated by Scholz et al. [5] preovoarian vitelline follicles are separated from and observed in the present study. However, the in- postovarian vitelline follicles, and few vitelline cision in K. baltica could be resulted from the con- follicles are present along the uterine loop, and few or traction during fixation [19]. K. armeniaca identified in absent along the ovarian arm. The uterine is looped the present study resembles K. armeniaca collected in between the posterior region of the ovarian isthmus Copeata copeata and C. bushei from River Zayandeh and the posterior region of the cirrus sac, not extend- in Iran [20]. However, K. armeniaca from Iran has a 4 期 KIBET Caroline Jepkorir 等: 埃塞俄比亚塔纳湖鲤科鱼类体内亚美尼亚许氏绦虫 Khawia armeniaca 921 (Cholodkovsky, 1915) Shulman, 1958 (绦虫纲: 鲤蠢目) 的形态鉴定 long posterior arm than the anterior arm, but in the cortical and medullary is a classification feature of the present study, the anterior arm is slightly longer than Caryophyllaeidae Leuckart, 1878 (Mackiewicz 1982), the posterior arm. K. barbi Rahemo et Mohammad, formation of an oncosphere in the uterus, in which no 2002 was distinguished from K. armeniaca in the oncosphere is formed in the uterus as observed in K. presence of constriction on the cirrus sac region, sinensis [23], but formed after the eggs being released which is proposed to be an artifact by Scholz et al. [5], into water [24—26]. However, K. barbi Rahemo and Mo- and K. barbi also has frilled scolex, which is diffe- hammad, 2002 and K. lutei Al-Kalak and Rahemo, rent from K. armeniaca with smooth anterior margin. 2003 possess the important morphological features as K. lutei Al-Kalak et Rahemo, 2003 was separated observed in K. armeniaca, such as follicular butterfly from K. armeniaca based on the size of cirrus sac, shaped ovary and few postovarian vitelline follicles. separate genital opening and the lack of seminal vesi- Khawia armeniaca was originally recorded by cle in which these are partial morphological features Cholodkowsky, 1915 as Caryophyllaeus armeniacus used in the classification. Other characteristic fea- from Varicorhinus sp. in Sevan Lake in Armenian tures provided by Al-Kalak and Rahemo [21] have SSR. Even though it was placed in the family Caryo- some discrepancies: vitelline follicle situated both in phyllaeidae, the Caryophyllaeus Gmelin, 1970, the

ABC te vf vd cs

fvf ug

ut fte ov

ieg

povf 1 mm 0.5 mm 0.7 mm DEF

oc ilm 0.7 mm 0.7 mm

Fig. 3 Khawia armeniaca from Labeobarbus intermedius in Tana Lake, Ethiopia A, B. anterior region of the parasite; C, D, E. posterior region; F. cross section. Abbreviations: cs. cirrus sac; fte. first testis; fvf. first vitelline follicle; ieg. intrauterine egg; ilm. inner longitudinal musculature; oc. osmoregulatory canal; povf. postovarian vitelline follicles; te. testes; ug. uterine glands; ut. uterus; vd. vas deferent; vf. vitelline follicles 922 水生生物学报 45 卷

Tab. 1 Morphometrics analysis of Khawia armeniaca (Cho- and B. grypus in Iraq, B. callensis from Altas Moun- lodkovsky, 1915) from different hosts and regions (in millimetres tain, Morocco. It has also been recorded in B. al- unless otherwise stated) tianalis from Victoria Lake, Uganda and from B. Character This study Scholz, et al., 2011 tropidolepis in Tanganyika Lake [5]. Some of the pub- Labeobarbus [34] Capoeta c. sevangi, lications are in Russian, such as Cholodkovsky , Host intermedius, L. [27] [34] [32] [33] Barbus, et al. tsanensis Popov , Kulakovskaya , Paperna , Mikailov , [28] [35] Armenia, Portugal, Country Ethiopia Dinnik , Rahemo and Al-Kalal , Poddubnaya and Iraq, Uganda, et al. Karen [30] references are cited from William and Gib- Body Length 30—40 15—47 son [20] and Scholz, et al. [5]. Maximum width 0.88—1.41 1.15—3.13 K. armeniaca identified in the present study ex- Scolex shape Semi-bulbate bulbate hibits some morphological variability in the shape of Scolex width 1.27—1.79 1.24—2.15 scolex, such as start of anteriormost testes, extent of Neck width 0.74—1.21 0.66—1.80 vitelline follicle at cirrus sac, number of vitelline 95.76—247× 106—330× Testis size μm (L/W) follicles along the uterine loop and ovarian arm mar- 99.75—247 76—252 gin and the extent of postvitelline follicle at the pos- Testis number >200 150—640 Distance from first terior region of ovarian arm. The intraspecific varia- 0.40—2.23 vitelline follicle tion in K. armeniaca in the present study shows the Distance from anterior 2.26—4.38 existence of morphological plasticity not only in dif- extremity [5] Length of testicular ferent geographical regions , but also in a same loca- 14.26—24.75 field lity as in the present study. However, this requires Ratio testicular 47.51—61.87 length: Body length % further molecular verification. The classification in 0.39—0.70× 0.34—1.18× the Caryophyllidea based on the shape of scolex, start Cirrus sac size (L/W) 0.68—1.43 0.45—0.95 of anteriormost testes and vitelline follicle, posterior Length of posterior 0.08—0.60 0.71—1.92 ovarian arm (B) extent of testes and vitelline follicle, presence or ab- Ratio to the length 0.24—0.67 sence of vitelline follicle along the uterine loop and anterior ovarian arm ovarian arm are incongruent with circumscription sta- Vitelline follicle μm 71.82—159.6× 47—280× [36] (L/W) 71.82—175.56 32—221 bility of taxon . This is because of the features Distance from anterior [5, 7, 37] 1.10—2.15 0.99—2.46 shared by species in different families . The posi- extremity posterior region of anterior half of cirrus- tion of inner longitudinal musculature in relation to Reach up to the cirrus sac sac internal genital organ is a key feature in the family Uterus extent 2.23—4.92 classification of caryophyllideans [3, 22]. In addition, Ratio to body length 7.43—12.29 the shape of scolex combined with the shape of ovary % Ratio to Testicular should be considered. This is because they are fea- 47.52—61.87 [5, 7] length % tures rarely shared at the species level . The ex- Intrauterine eggs μm 35.91—55.86× 54—76× (L/W) 47.88—83.79 35—56 tend of postvitelline follicles in relation to the ovari- Genital pores Separate an arm should be considered as a preliminary feature [5] Post Ovarian vitelline in K. armeniaca, as proposed by Scholz, et al. , as <100 37—109 follicles number and extent of postovarian vitelline follicle to the ovary, and the shape it forms at posterior region description was very brief without any diagrammatic are taxonomical features in Pseudoglaridacris sp. [37] illustration. Later, extensive studies have been done [27—30] and presence or absence of post-ovarian vitelline on the same tapeworm in the same locality . follicle in Promonobothrium sp. [37]. Shulman [31] redescribed the species and transferred it to the family Lytocestidae due to the position of testes Acknowledgements: and vitellarium in relation to inner longitudinal mus- Thanks are due to Ms. Hui Liang at Wuhan Uni- culature. versity for preparing scanning electron microscope Khawia armeniaca has been reported in diffe- photomicrographs. The samples were obtained with rent geographical regions and in different fish species. the assistance from Professor E Zhang and Dr. Liang It has been recorded in Barbus longiceps from Ga- Cao at the Institute of Hydrobiology, Chinese Aca- lilee Lake, Israel [32], Capoeta capoeta sevangi in demy of Sciences, and Ms. Wang He at Hunan Fish- Mingechaursk and Barbarinsk resevoivor [33], C. capoe- eries Science Institute in Changsha, Hunan Province, ta and C. bushei from River Zayandeh, Iran [20], Bar- and also local fishery administration in Ethiopia. Ca- bus bynni from River Nile, Cairo, Silurus triostegus roline J. 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埃塞俄比亚塔纳湖鲤科鱼类体内亚美尼亚许氏绦虫Khawia armeniaca (Cholodkovsky, 1915) Shulman, 1958 (绦虫纲: 鲤蠢目) 的形态鉴定

KIBET Caroline Jepkorir 1, 2, 3 赵文婷1 SARWAR Huda1 聂品1, 4 (1. 中国科学院水生生物研究所淡水生态与生物技术国家重点实验室, 农业部淡水养殖病害防治重点实验室, 武汉 430072; 2. 中国科学院大学, 北京 100049; 3. 肯尼亚国家博物馆鱼类学科组动物学系, 肯尼亚内罗毕P.O Box 40568-00100; 4. 青岛农业大学海洋科学与工程学院, 青岛 266109)

摘要: 在埃塞俄比亚境内塔纳湖中发现了1种寄生于鲤科鱼类: 间魮 (Labeobarbus intermedius)和Labeobarbus tsanensis体内的许氏绦虫, 经形态学鉴定其为亚美尼亚许氏绦虫Khawia armeniaca (Cholodkovsky, 1915)(绦虫纲: 鲤蠢目)。该绦虫鉴别特征为头节呈半球状, 边缘光滑, 无皱褶; 睾丸分布区域从虫体中部至阴茎囊之前; 卵巢前卵黄腺分布于虫体中后部至阴茎囊前部区域, 少数排列在阴茎囊之后; 子宫起始于阴茎囊后方弯曲环绕直至卵巢后部区域, 有少许卵黄腺排列在子宫和卵巢的两侧。此外, K. armeniaca卵巢呈滤泡状或蝴蝶状, 雌雄生殖孔分离但彼此距离很近, 开口于体表并形成同一生殖腔, 且雄性生殖孔位于雌性生殖孔前方。卵巢后卵黄腺数目少于100个, 分布于虫体末端, 卵黄腺距离卵巢后翼较远, 部分样品内卵黄腺接近卵巢后翼。

关键词: 纽带科; 亚美尼亚许氏绦虫; 形态学; 形态测量学; 塔纳湖; 埃塞俄比亚