REDESCRIPTION OF THE MONOZOIC CESTODE KHAWIA ARMENIACA (CHOLODKOVSKY, 1915) SHULMAN, 1958 (CESTODA: CARYOPHYLLIDEA) FROM CYPRINID FISH IN TANA ...

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REDESCRIPTION OF THE MONOZOIC CESTODE KHAWIA ARMENIACA (CHOLODKOVSKY, 1915) SHULMAN, 1958 (CESTODA: CARYOPHYLLIDEA) FROM CYPRINID FISH IN TANA ...
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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第 45 卷 第 4 期                                          水 生 生 物 学 报                                                          Vol. 45, No. 4
  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

                                                    1, 2, 3                    1                     1                1, 4
                     KIBET Caroline Jepkorir               , ZHAO Wen-Ting , SARWAR Huda and NIE Pin
     (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 me-
     dian 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 mar-
     gin. 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,
                                                                                         [5]
be grouped into unsegmented or monozoic, and seg-                         Scholz, et al. 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,
         [1, 2]
cotylidea . 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,
                                                                                [6]
laeidae Leuckart, 1878, Capingentidae Hunter, 1930                        et al. reported a new species, K. abbottinae from
and Balanotaeniidae Mackiewicz & Blair, 1978,                             the gudgeon Abbottina rivularis (Cyprinidae: Gobio-
                                                      [3]
based on the arrangemnt of longitudinal musculature .                     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
                                 [4]
carp Cyprinus carpio in China , was considered as                         on the basis of ssrDNA and D1-D3 lsrDNA, or mito-
                                    [5]
probably the most specious genus . 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: kibetcaroline40@gmail.com
    Corresponding author: Nie Pin, E-mail: pinnie@ihb.ac.cn; pinnie@qau.edu.cn
918                                            水 生 生 物 学 报                                                     45 卷

               [5]
these markers . 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
                                                                      [10]
species are medullarilly located and vitellarium cor-      markers , 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-
                                                                     [11]
mainly from barbels in some middle Asian countries         stratum . 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-       trine habitats since the formation of Tana Lake
                        [5]
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 19 to 25 in
                                                                                                            th     th

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
                            [9]                            six Labeobarbus intermedius and eighteen L. tsanen-
of Khawia sp. in the lake .
                                                           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-
                          2
surface area of 3673 km , with a surrounding drain-        cohol. For light microscopy, the specimens were
                      2
age area of 11650 km , 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
      [10—14]
20′′E         .                                            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-
                                         [5, 16]
dried and mounted in Canada balsams              . 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%—
                                                                          49.30% of the body width. Vas deferent looped at the
2     Result
                                                                          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 approximately200 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

A                                         B                                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 an-
                                                                           terior margin, butterfly shaped and follicular ovary,
                                                                           few postovarian vitelline follicle, < 100 in number,
C                                         D                                and postovarian vitelline follicle touching the poste-
                                                                           rior region of the ovarian arm, while in other species
                                vd                                                                           [5]
                                                                 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,
                                                                                                                           [17]
                                                                           while in other species the posterior arm joins . 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 situa-
ted at the medullary and vitellarium at the cortical                       3   Discussion
parenchyma. It possesses diagnostic features of                                  Khawia armeniaca in the present study highly
                                                     [5]                                                                      [19]
Khawia spp. proposed to be valid by Scholz, et al. ,                       resembles K. baltica studied by Chubb, et al.           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
                                                                                                                                   [5]
most to the posterior margin of the cirrus sac. The                        smooth anterior margin, as indicated by Scholz et al.
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-
                                                                                                     [19]
follicles are present along the uterine loop, and few or                   traction during fixation . 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
                                                                                    [20]
and the posterior region of the cirrus sac, not extend-                    in Iran . 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.
                                                                                         [23]
presence of constriction on the cirrus sac region,                             sinensis , but formed after the eggs being released
                                                      [5]                                   [24—26]
which is proposed to be an artifact by Scholz et al. ,                         into water           . 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
                                               [21]
tures provided by Al-Kalak and Rahemo               have                       SSR. Even though it was placed in the family Caryo-
some discrepancies: vitelline follicle situated both in                        phyllaeidae, the Caryophyllaeus Gmelin, 1970, the
                       A                                                   B                 C
                                                                                                                               te
                                                                                                                                vf
                                                                                                                                vd
                                                                                                                               cs

                                                            fvf                                                                ug

                                                                                                                               ut
                                                              fte                                                              ov

                                                                                                                               ieg
                                                                                      1 mm

                                                                                                                               povf
                                                   0.5 mm

                                                                                                                      0.7 mm

                       D                                                   E                     F

                                                                                                                                vf

                                                                                                                                te

                                                                                                                                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 vitel-
line 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.
                                                                                                                   [5]
       Character             This study        Scholz, et al., 2011     tropidolepis in Tanganyika Lake . Some of the pub-
                                                                                                                                               [34]
                           Labeobarbus                                  lications are in Russian, such as Cholodkovsky ,
                                               Capoeta c. sevangi,
Host                      intermedius, L.                                         [27]                   [34]            [32]                   [33]
                             tsanensis
                                                 Barbus, et al.         Popov , Kulakovskaya , Paperna , Mikailov ,
                                                                                   [28]                            [35]
Country                       Ethiopia
                                               Armenia, Portugal,       Dinnik , Rahemo and Al-Kalal , Poddubnaya and
                                               Iraq, Uganda, et al.               [30]
                                                                        Karen           references are cited from William and Gib-
Body Length                   30—40                  15—47                   [20]                       [5]
                                                                        son and Scholz, et al. .
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×             follicles along the uterine loop and ovarian arm mar-
Testis size μm (L/W)
                            99.75—247                76—252
Testis number                  >200                 150—640
                                                                        gin and the extent of postvitelline follicle at the pos-
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                                                  existence of morphological plasticity not only in dif-
                            2.26—4.38
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
length: Body length %
                           47.51—61.87                                  further molecular verification. The classification in
Cirrus sac size (L/W)
                            0.39—0.70×             0.34—1.18×           the Caryophyllidea based on the shape of scolex, start
                             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            extent of testes and vitelline follicle, presence or ab-
ovarian arm (B)
Ratio to the length                                                     sence of vitelline follicle along the uterine loop and
                            0.24—0.67
anterior ovarian arm
Vitelline follicle μm     71.82—159.6×              47—280×
                                                                        ovarian arm are incongruent with circumscription sta-
                                                                                              [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
                                                                                                                       [3, 22]
Uterus extent               2.23—4.92                                   classification of caryophyllideans                     . In addition,
Ratio to body length                                                    the shape of scolex combined with the shape of ovary
                            7.43—12.29
%
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
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                                                      923
                               (Cholodkovsky, 1915) Shulman, 1958 (绦虫纲: 鲤蠢目) 的形态鉴定

versity of Chinese Academy of Sciences, and the                               Labeobarbus Species Flock (Cypriniformes: Cyprinidae): A
State Key Laboratory of Freshwater Ecology and Bio-                           Future of Biodiversity Conservation and Sustainable Exploita-
technology, through the Ichthyology Section, Nation-                          tion [C]//Snoeks J, Getahum A (Eds.), Proceedings of the 4th
al Museums of Kenya.                                                          International Conference on African Fish and Fisheries, Ad-
                                                                              dis Ababa, Ethiopia. Tervuren: Royal Museum for Central
                                                                              Africa, Zoological Documentation Online Series, 2008: 31-
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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
                                                       1, 2, 3          1                                1               1, 4
              KIBET Caroline Jepkorir                            赵文婷         SARWAR Huda                     聂       品
  (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
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