Larval Stages of Phyllodistomum sp. (Digenea, Gorgoderidae) from the Duck Mussels Anodonta anatina in Ukraine
Rhopalocercous cercariae were found in the gonads of duck mussels, Anodonta anatina (Linnaeus, 1758) collected from the Sluch River (Zhytomyr oblast, Ukraine). The morphological features observed led to conclusion that this species belonged to the genus Phyllodistomum Braun, 1899. Obtained results s...
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irk-123456789-1099152016-12-25T03:02:12Z Larval Stages of Phyllodistomum sp. (Digenea, Gorgoderidae) from the Duck Mussels Anodonta anatina in Ukraine Kudlai, O.S. Yanovich, L.N. Фауна и систематика Rhopalocercous cercariae were found in the gonads of duck mussels, Anodonta anatina (Linnaeus, 1758) collected from the Sluch River (Zhytomyr oblast, Ukraine). The morphological features observed led to conclusion that this species belonged to the genus Phyllodistomum Braun, 1899. Obtained results suggested that the second intermediate hosts in the life cycle of this trematode were absent. Free-swimming cercariae were observed encysting in water. This species is similar to Phyllodistomum pseudofolium Nybelin, 1926 by overall body proportions and ratio of suckers: lengths of oral to ventral sucker 1 : 1.1; widths of the same organs 1 : 1.2. To confirm the taxonomic position of the species found and establish a possible relationship between it and P. pseudofolium an experimental infection of fish Carassius carassius (Linnaeus, 1758) as potential definitive host was performed. The infection was not successful. Descriptions and figures of all detected larval stages of Phyllodistomum sp.are provided. Булавохвостые церкарии обнаружены в гонадах моллюсков Anodonta anatina (Linnaeus, 1758) из р. Случ (Житомирская обл., Украина). Изучение морфологических особенностей позволило сделать вывод, что этот вид принадлежит роду Phyllodistomum Braun, 1899. Полученные результаты показали, что второй промежуточный хозяин в жизненном цикле данного вида отсутствует. Инцистирование свободноплавающих церкарий происходило в воде. Данный вид наиболее близок к Phyllodistomum pseudofolium Nybelin, 1926 по общим пропорциям тела и соотношению присосок: длины ротовой к брюшной присоске 1 : 1,1; ширины тех же органов, 1 : 1,2. Для подтверждения таксономического положения обнаруженного вида и установления возможной связи между ним и P. pseudofolium проведен эксперимент по заражению рыбы Carassius carassius (Linnaeus, 1758) как потенциального окончательного хозяина. Экспериментальное заражение не было успешным. Приведено описание и рисунки всех обнаруженных личиночных стадий. 2013 Article Larval Stages of Phyllodistomum sp. (Digenea, Gorgoderidae) from the Duck Mussels Anodonta anatina in Ukraine / O.S. Kudlai, L.N. Yanovich // Вестник зоологии. — 2013. — Т. 47, № 6. — С. 483–488. — Бібліогр.: 20 назв. — англ. 0084-5604 DOI 10.2478/vzoo-2013-0051 http://dspace.nbuv.gov.ua/handle/123456789/109915 595.122:594.1(477) en Вестник зоологии Інститут зоології ім. І.І. Шмальгаузена НАН України |
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Фауна и систематика Фауна и систематика Kudlai, O.S. Yanovich, L.N. Larval Stages of Phyllodistomum sp. (Digenea, Gorgoderidae) from the Duck Mussels Anodonta anatina in Ukraine Вестник зоологии |
| description |
Rhopalocercous cercariae were found in the gonads of duck mussels, Anodonta anatina (Linnaeus, 1758) collected from the Sluch River (Zhytomyr oblast, Ukraine). The morphological features observed led to conclusion that this species belonged to the genus Phyllodistomum Braun, 1899. Obtained results suggested that the second intermediate hosts in the life cycle of this trematode were absent. Free-swimming cercariae were observed encysting in water. This species is similar to Phyllodistomum pseudofolium Nybelin, 1926 by overall body proportions and ratio of suckers: lengths of oral to ventral sucker 1 : 1.1; widths of the same organs 1 : 1.2. To confirm the taxonomic position of the species found and establish a possible relationship between it and P. pseudofolium an experimental infection of fish Carassius carassius (Linnaeus, 1758) as potential definitive host was performed. The infection was not successful. Descriptions and figures of all detected larval stages of Phyllodistomum sp.are provided. |
| format |
Article |
| author |
Kudlai, O.S. Yanovich, L.N. |
| author_facet |
Kudlai, O.S. Yanovich, L.N. |
| author_sort |
Kudlai, O.S. |
| title |
Larval Stages of Phyllodistomum sp. (Digenea, Gorgoderidae) from the Duck Mussels Anodonta anatina in Ukraine |
| title_short |
Larval Stages of Phyllodistomum sp. (Digenea, Gorgoderidae) from the Duck Mussels Anodonta anatina in Ukraine |
| title_full |
Larval Stages of Phyllodistomum sp. (Digenea, Gorgoderidae) from the Duck Mussels Anodonta anatina in Ukraine |
| title_fullStr |
Larval Stages of Phyllodistomum sp. (Digenea, Gorgoderidae) from the Duck Mussels Anodonta anatina in Ukraine |
| title_full_unstemmed |
Larval Stages of Phyllodistomum sp. (Digenea, Gorgoderidae) from the Duck Mussels Anodonta anatina in Ukraine |
| title_sort |
larval stages of phyllodistomum sp. (digenea, gorgoderidae) from the duck mussels anodonta anatina in ukraine |
| publisher |
Інститут зоології ім. І.І. Шмальгаузена НАН України |
| publishDate |
2013 |
| topic_facet |
Фауна и систематика |
| url |
http://dspace.nbuv.gov.ua/handle/123456789/109915 |
| citation_txt |
Larval Stages of Phyllodistomum sp. (Digenea, Gorgoderidae) from the Duck Mussels Anodonta anatina in Ukraine / O.S. Kudlai, L.N. Yanovich // Вестник зоологии. — 2013. — Т. 47, № 6. — С. 483–488. — Бібліогр.: 20 назв. — англ. |
| series |
Вестник зоологии |
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AT kudlaios larvalstagesofphyllodistomumspdigeneagorgoderidaefromtheduckmusselsanodontaanatinainukraine AT yanovichln larvalstagesofphyllodistomumspdigeneagorgoderidaefromtheduckmusselsanodontaanatinainukraine |
| first_indexed |
2025-07-07T23:51:01Z |
| last_indexed |
2025-07-07T23:51:01Z |
| _version_ |
1837034124063277056 |
| fulltext |
UDc 595.122:594.1(477)
LARVAL STAGES OF PHYLLODISTOMUM SP. (DIGENEA,
GORGODERIDAE) FROM THE DUCK MUSSELS
ANODONTA ANATINA IN UKRAINE
O. S. Kudlai1, L. N. Yanovich2
1 Schmalhausen Institute of Zoology, NAS of Ukraine, vul. B. Khmelnytskogo, 15, Kyiv, 01601 Ukraine
E-mail: olena.kudlai@gmail.com
2 Zhytomyr Ivan Franko State University, Velyka Berdychivska str., 40, Zhytomyr, 10008 Ukraine
E-mail: yanovichzt@ukr.net
Larval Stages of Phyllodistomum sp. (Digenea, Gorgoderidae) from the Duck Mussels Anodonta anatina in
Ukraine. Kudlai O. S., Yanovich L. N. — Rhopalocercous cercariae were found in the gonads of duck
mussels, Anodonta anatina (Linnaeus, 1758) collected from the Sluch River (Zhytomyr oblast, Ukraine).
The morphological features observed led to conclusion that this species belonged to the genus Phyllodis-
tomum Braun, 1899. Obtained results suggested that the second intermediate hosts in the life cycle of this
trematode were absent. Free-swimming cercariae were observed encysting in water. This species is similar
to Phyllodistomum pseudofolium Nybelin, 1926 by overall body proportions and ratio of suckers: lengths
of oral to ventral sucker 1 : 1.1; widths of the same organs 1 : 1.2. To confirm the taxonomic position
of the species found and establish a possible relationship between it and P. pseudofolium an experimental
infection of fish Carassius carassius (Linnaeus, 1758) as potential definitive host was performed. The
infection was not successful. Descriptions and figures of all detected larval stages of Phyllodistomum sp.
are provided.
Key wo rd s: trematodes, Gorgoderidae, Phyllodistomum, larval stages, Anodonta anatina, Ukraine.
Ëè÷èííî÷íûå ñòàäèè Phyllodistomum sp. (Digenea, Gorgoderidae) èç áåççóáîê Anodonta anatina â Óêðà-
èíå. Êóäëàé Å. Ñ., ßíîâè÷ Ë. Í. — Áóëàâîõâîñòûå öåðêàðèè îáíàðóæåíû â ãîíàäàõ ìîëëþñêîâ
Anodonta anatina (Linnaeus, 1758) èç ð. Ñëó÷ (Æèòîìèðñêàÿ îáë., Óêðàèíà). Èçó÷åíèå ìîðôîëî-
ãè÷åñêèõ îñîáåííîñòåé ïîçâîëèëî ñäåëàòü âûâîä, ÷òî ýòîò âèä ïðèíàäëåæèò ðîäó Phyllodistomum
Braun, 1899. Ïîëó÷åííûå ðåçóëüòàòû ïîêàçàëè, ÷òî âòîðîé ïðîìåæóòî÷íûé õîçÿèí â æèçíåííîì
öèêëå äàííîãî âèäà îòñóòñòâóåò. Èíöèñòèðîâàíèå ñâîáîäíîïëàâàþùèõ öåðêàðèé ïðîèñõîäèëî
â âîäå. Äàííûé âèä íàèáîëåå áëèçîê ê Phyllodistomum pseudofolium Nybelin, 1926 ïî îáùèì ïðî-
ïîðöèÿì òåëà è ñîîòíîøåíèþ ïðèñîñîê: äëèíû ðîòîâîé ê áðþøíîé ïðèñîñêå 1 : 1,1; øèðèíû
òåõ æå îðãàíîâ, 1 : 1,2. Äëÿ ïîäòâåðæäåíèÿ òàêñîíîìè÷åñêîãî ïîëîæåíèÿ îáíàðóæåííîãî âèäà è
óñòàíîâëåíèÿ âîçìîæíîé ñâÿçè ìåæäó íèì è P. pseudofolium ïðîâåäåí ýêñïåðèìåíò ïî çàðàæåíèþ
ðûáû Carassius carassius (Linnaeus, 1758) êàê ïîòåíöèàëüíîãî îêîí÷àòåëüíîãî õîçÿèíà. Ýêñïåðè-
ìåíòàëüíîå çàðàæåíèå íå áûëî óñïåøíûì. Ïðèâåäåíî îïèñàíèå è ðèñóíêè âñåõ îáíàðóæåííûõ
ëè÷èíî÷íûõ ñòàäèé.
Êëþ÷åâûå ñëîâà: òðåìàòîäû, Gorgoderidae, Phyllodistomum, ëè÷èíî÷íûå ñòàäèè, Anodonta ana-
tina, Óêðàèíà.
Introduction
The cosmopolitan trematode genus Phyllodistomum Braun, 1899 includes approximately 100 freshwater
and marine species found primarily in the urinary bladder of teleosts and to a lesser extent in amphibians
(Pigulevsky, 1953; Yamagutti, 1971; Cribb, 1987 b). Phyllodistomum trematodes show a variety of life cycles
with two or three hosts. Much of this variation relates to the morphology and biology of the larval stages.
Cercariae produced in the life cycles of Phyllodistomum species are assigned to three types: microcercous,
cystocercous, rhopalocercous (Cribb, 1987 a).
Rhopalocercous cercariae are a group characterized by a club-shaped, corrugated tail. The tail is capable
of expansion to form a balloon-like chamber within which metacercarial encystment occurs. These cercariae
typically possess markedly well-developed genital primordia. Life cycles are known for two European species
which develop from cercariae of this type: Phyllodistomum angulatum Linstow, 1907 from Anodonta ponderosa
Pfeiffer, 1825 (Ivantsiv, Kurandina, 1985) and P. elongatum Nybelin, 1926 from A. cygnea (Linnaeus, 1758)
Vestnik zoologii, 47(6): e-37–e-42, 2013
DOI 10.2478/vzoo-2013-0051
Ôàóíà è ñèñòåìàòèêà
Unauthenticated
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38 O. S. Kudlai, L. N. Yanovich
(Orecchia et al., 1975). Nine rhopalocercous species were previously described for North America (Fischthal,
1951, 1954; Coil, 1954; Flook, Ubelaker, 1971).
There are 6 species of Phyllodistomum found in the freshwater fishes in Ukraine: P. folium (Olfers, 1816),
P. angulatum, P. elongatum, P. pseudofolium Nybelin, 1926, P. simile Nybelin, 1926, Phyllodistomum sp. (Koval,
1969). Detections of larval stages are reliable only for two out of these species. They were found in bivalves
of the families Unionidae and Sphaeriidae: P. elongatum as Cercaria duplicata Baer, 1827 from A. cygnea,
A. anatina (Linnaeus, 1758) (Zdun, 1961) and as P. folium from A. stagnalis (Gmelin, 1791) (Stadnichenko,
1983), P. angulatum Linstow, 1907 from A. ponderosa (Ivantsiv, Kurandina, 1985). Larvae of Phyllodistomum
sp. from gills of Pisidium amnicum (Müller, 1774) were described by Chernogorenko (1983).
During the investigation of parasites of molluscs from the Sluch River, rhopalocercous cercariae were
found in the gonads of the duck mussels, A. anatina. Detailed study of the morphology of these trematodes
revealed that they belonged to Phyllodistomum sp. and were found for the first time in Ukraine.
In this paper, larval stages of Phyllodistomum sp. are described and some data on the species development
are provided and illustrated.
Material and methods
Molluscs were collected for parasitological investigation from the Sluch River (Baranovka, Zhytomyr
oblast, Ukraine) from July, 2011 to June, 2012. Totally, 374 specimens of unionid molluscs belonging to the
following 6 species were examined: 113 — Unio pictorum (Linnaeus, 1758); 127 — U. tumidus Phil³psson,
1788; 12 — U. crassus Philipsson, 1788; 112 — A. anatinà; 3 — A. cygnea; 7 — Pseudanîdonta complanata
(Rossmässler, 1835). In the laboratory molluscs were dissected. Twenty-eight A. anatinà were placed individu-
ally in glass containers with tap water at temperature 18–22 °C. The containers were examined daily under a
binocular microscope for detection of spontaneous cercariae emission and their encystation. Three carp fish
Carassius carassius (Linnaeus, 1758) (grown from the fry) served as potential definitive hosts for experimen-
tal infection. In addition, a total of 32 fishes including 7 — Rutilus rutilus (Linnaeus, 1758); 1 — Scardinius
erythrophthalmus (Linnaeus, 1758); 1 — Blicca bjoerkna Linnaeus, 1758; 3 — Gobio gobio (Linnaeus, 1758);
and 20 — C. carassius were collected for parasitological investigation by angling from the Sluch River between
July to August 2012 in the locality, where molluscs were collected.
Morphology of the larval stages was studied on living and fixed specimens; neutral red and Nile blue
stains were used for intravital staining. Afterwards, living worms were rinsed in water, killed with hot water
and fixed in 70 % ethanol. For morphological examination, fixed specimens were stained with acetocarmine,
dehydrated in a graded ethanol series, cleared in clove oil, and mounted permanently in Canada balsam.
Drawings were made with the aid of a drawing tube. Photographs were made using Am Scope microscope
equipped with digital camera. All measurements are presented in mm, mean values are given in parentheses.
The systematic positions of trematodes are indicated according to the system proposed by Campbell (2008).
Nomenclature of mollusc species follows Glöer, Meier-Brook (1998), Vasilyeva (2011) and that of fish species
follows Movchan (2011).
Results
Partenitae and cercariae of Phyllodistomum sp. were found in the gonads of only six
specimens of A. anatinà (prevalence 5.4 %). Experimental infection of C. carassius by
metacercariae was not successful. Phyllodistomum trematodes were not detected also in
the fish from the Sluch River.
Description of Phyllodistomum sp. developmental stages
Spo rocy s t ( f i g . 2, 1). Measurements and description are based on 24 live speci-
mens. Motionless, oval, with thick body wall. Body length 0.520–1.620 (0.849), width
0.300–0.870 (0.529). Total number of cercariae per sporocyst 1–7 (3).
Cercaria (fig. 1; 2, 2). Measurements are based on 25 specimens from permanent
mounts. Body elongate, slightly narrower at anterior end and broader at posterior end.
Body 0.395–0.860 (0.593) by 0.123–0.250 (0.173), maximum width at level of anterior
testis. Tegument thin, without spines, with very finely papillate, distributed irregularly
from anterior to posterior end of body, more numerous in posterior part. Oral sucker
subterminal, 0.063–0.143 (0.096) long, 0.063–0.108 (0.084) wide; mouth subterminal.
Ventral sucker round, 0.060–0.145 (0.104) × 0.070–0.138 (0.102). Its center at 0.175–
0.500 (0.325) from anterior end. Papillae noticeable on oral and ventral suckers. Sucker
ratio: lengths of oral to ventral sucker 1 : 1.1; widths of same organs 1 : 1.2. Pharynx
absent. Oesophagus 0.030–0.100 (0.068) long, surrounded by unicellular penetration
glands. Intestinal bifurcation at about midway between oral and ventral suckers. Caeca
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39Larvae of Phyllodistomum sp. (Digenea, Gorgoderidae)…
passing posteriorly beyond testes primordium. Genital primordia (n = 15) well devel-
oped, within posterior third of body. Testes primordium lobed, placed diagonally. Ante-
rior testis 0.025–0.035 (0.029) long, 0.018–0.038 (0.026) wide, posterior testis 0.018–
0.038 (0.030) long, 0.018–0.038 (0.027) wide. Seminal vesicle primordium located at
anterior margin of ventral sucker. Ovary primordium slightly lobed, 0.018–0.028 (0.023)
× 0.015–0.028 (0.021), anterior to testes on the same side as posterior testis. Paired pri-
mordium of vitelline masses transversely elongated, located between ventral sucker and
ovary and anterior testis. Excretory system mesostomate. Excretory vesicle I-shaped,
thin-walled. Total number of flame cells 48–24 on each side (fig. 1, 1). Excretory pore
terminal. Tail club-shaped, 0.423–0.613 × 0.154–0.166, in cross-section consisting of
two distinct layers: outer corrugated cuticle, and beneath and only loosely associated
Fig. 1. Cercariae of Phyllodistomum sp.: 1 — alive specimen; 2 — fixed specimen. Scale bar 0.1 mm.
Ðèñ. 1. Öåðêàðèè Phyllodistomum sp.: 1 — æèâîé ýêçåìïëÿð; 2 — ôèêñèðîâàííûé ýêçåìïëÿð. Ìàñøòàá-
íàÿ ëèíåéêà 0,1 ìì.
1
2
Unauthenticated
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40 O. S. Kudlai, L. N. Yanovich
with it, layer of cells with large, dense nuclei. Anterior part of tail with slight narrowing
from the remaining part. Attachment of tail to body fragile, quite often tail separated
after emergence from sporocyst.
Available experimental results suggest that the second intermediate hosts in the life
cycle of this species are absent. After emerging from mollusc, cercariae encysted inside
the chamber formed from their tail. As a result of contractile movement of tail, its upper
membrane transformed into round balloon-like chamber, containing cercarial body and
tail (fig. 2, 3). Simultaneously, the cyst was forming around the body of the cercaria (fig. 2,
4). The formation of the chamber lasted from 1 to 3 minutes. Encysted cercariae sunk to
the bottom of the glass container. Encystment and tail transformation in Phyllodistomum
sp. conform to Fischthal’s (1951), Flook and Ubelaker’s (1971) descriptions.
Discussion
In the present study rhopalocercous cercariae were found in A. anatina in one
location in Ukraine. In accordance with the system of gorgoderid trematodes proposed
by Pigulevsky (1953), Yamaguti (1971) and Campbell (2008), the cercaria described
Fig. 2. Larval stages of Phyllodistomum sp.: 1 — sporocyst; 2 — cercaria; 3 — metacercaria in the chamber;
4 — metacercaria. Scale bars: 1, 2 — 0.5 mm; 3 — 1 mm; 4 — 0.1 mm.
Ðèñ. 2. Ëè÷èíî÷íûå ñòàäèè Phyllodistomum sp.: 1 — ñïîðîöèñòà; 2 — öåðêàðèÿ; 3 — ìåòàöåðêàðèÿ â
êàìåðå; 4 — ìåòàöåðêàðèÿ. Ìàñøòàáíûå ëèíåéêè: 1, 2 — 0,5 ìì; 3 — 1 ìì; 4 — 0,1 ìì.
1
3 4
2
Unauthenticated
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41Larvae of Phyllodistomum sp. (Digenea, Gorgoderidae)…
here showed the common characteristics of the genus Phyllodistomum, specifically the
forebody tapered anteriorly, hindbody broad, pharynx absent, testes two diagonal in
widest part of hindbody, ovary posterior to ventral sucker. Development and morphology
of Phyllodistomum sp., including the encystment with in transformed tail in water without
second intermediate host, are most similar to two European Phyllodistomum species,
P. angulatum and P. elongatum (Orrechia et al., 1975; Ivantsiv, Kurandina, 1985) and
nine other rhopalocercous cercariae, which have been studied in North America by
Fischthal (1951, 1954), Coil (1954), Flook and Ubelaker (1971).
Two European species appear to be closest to Phyllodistomum sp. Cercariae of
P. angulatum described from A. ponderosa (Ivantsiv, Kurandina, 1985) from Ukraine,
differ from Phyllodistomum sp. mainly in the presence of the lateral protuberance on each
side in the posterior part of body; ratio of suckers: 1 : 1.4 in P. angulatum and 1 : 1.2
in the species described herein. Another differential feature is a total number of flame
cells: 46 in P. angulatum and 48 in Phyllodistomum sp. Cercaria of Phyllodistomum sp.
differs from P. elongatum described from Pisidium amnicum, A. cygnea by Sudarikov et
al. (2002) by location of ventral sucker, and ratio of length of fore to hind parts of body.
Despite of negative results of experimental infection of fish, in our opinion,
the morphological characters suggest that species described herein is most similar
to P. pseudofolium by overall body proportions and ratio of suckers’ size. Adults of
P. pseudofolium are parasites of Sander lucioperca (Linnaeus, 1758), Perca fluviatilis
Linnaeus, 1758, Gymnocephalus cernuus (Linnaeus, 1758) in the Palaearctic (Pigulevsky,
1953; Bauer, 1984). The life cycle of P. pseudofolium is unknown. Its metacercariae were
registered from mantle tissue of A. stagnalis in Russia (Sudarikov et al., 2002).
Our results demonstrate that the life cycle of Phyllodistomum sp. involves the
freshwater molluscs A. anatina as the first intermediate host. Metacercarial encystment
occurs within transformed cercarial tail in water and matacercariae may be eaten by
fish. The natural definitive host of Phyllodistomum sp. has not been identified during the
present study.
The possibility of using a combination of morphological, molecular and experimental
investigations in further study can help, in our opinion, to identify the species affiliation
of Phyllodistomum sp. and fully elucidate its life-cycle.
The authors thank Otto M. Davydov for the fish provided for experiment, and M. Pampura, T. Shevchuk
for their help in collecting of molluscs.
This research was supported by European Union Structural Funds project “Postdoctoral Fellowship Im-
plementation in Lithuania” (VP1–3.1–ŠMM–01–V–02–004).
References
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Unauthenticated
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Received 22 April 2013
Accepted 1 October 2013
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