' M ;% J ; < < ? [ M "+% +8Z doi: " "&&""j * "+ http://folia.paru.cas.cz
Research Article Helminth parasites of the lesser great cormorant Phalacrocorax carbo sinensis from two nesting regions in the Czech Republic
František Moravec and Tomáš Scholz
M ;% J ; < <= 5; ? % I J DV F % <= > *
Abstract: M ^ 5 " * 5 5 Phalacrocorax carbo sinensis (Blumenbach) 5 9 <= > * ? J 5 ? @ F 9 M ;% <= 5; ? * F ; <= F I 5; ? ; "#3$M"## 5% "# * 5 * 9 % X 5 "" * % < % 5 & * % 9 F 5 * * ;Z * * 5 Phalacrocorax ** 8${ % * - 5 ; 5 "+{ * * &${ | "# * % " { 9 ? @ F % ; &${ "# * ? J 5 X 5 5 * 5 5 ? @ F * * * * 5 ; 9 * F @ " ; 9 F % better ecological and environmental conditions in this warmer region. Scanning electron microscopical examination of three common nematode species parasitising cormorants, Contracaecum rudolphii 9 % "#+&% Desmidocercella incognita ? % "#8 Syncuaria squamata F } 9% "338 % F 5 ^ 5 ; 5* % * F ; * 5 * % as the cephalic structures, numbers and distribution of male caudal papillae or the shapes of spicules. Keywords: M % % 5 % 5 * ;% ;% < ' *
The great cormorant Phalacrocorax carbo (Linnae- * 5 ; ** ? @ F ; "#3 us) (Pelecaniformes: Phalacrocoracidae) is a migratory @ 6 I "#38 ? J 5 % 5 ** "#3 M"#3# " % 9 is very extensive, including all continents except for South six cormorant colonies in the Czech Republic with only America and Antarctica. The type subspecies P. carbo car- 8 * 5 - bo (Linnaeus) is found mainly in Atlantic waters and near- 5 * * M I " by inland areas, e.g. on western European coasts, whereas Because of a very negative impact of the presence of the subspecies P. carbo sinensis (Blumenbach) is distrib- 5 ? J 5 ? uted from northern and central Europe to southern China Moravia (western and eastern parts of the Czech Republic, " "#$ % * F ; 9 F % F great cormorants occurring in the Czech Republic belong the helminth parasites of the lesser great cormorant P. car- to P. carbo sinensis. However, the validity of this subspe- bo sinensis in these two main nesting regions were carried cies has recently been questioned by Kennedy and Spencer ; 5 M ;% "& <= F I 5; ? % I Whereas the European population of P. carbo sinensis J DV F "#3$M"## X * * 9 I was almost extinct in the half of the 20th century, its ex- was mainly to recognise and evaluate the helminth fauna pansive increase began due to protective measures adopted of great cormorants in the two ecologically different re- ' * "#+ M"#3" 5 gions and to indicate a possible importance of cormorants’ Czechoslovakia, the only large nesting colony of great cor- * ? 5 morants was that near the vilage of Biskupice on the Dan- partial results of these studies, mainly those on trematodes ube River, southern Slovakia, which existed from about and acanthocephalans, were already reported in the papers "# "#+$ 66 "#38 * 9 @ F "#33% "##& % @ F "## % # % several unsuccessful attempts of great cormorants to nest ? = "## % F "##8 % % "##& ; * <= > * % @ F ? = "##& % F
* Z [ @ F % M ;% J ; < <= 5; ? % J F I 8"% 8$ I J DV F % <= > * M \& 83 $$$ &8 ] [ ^Z \& 83 8" 833] ' 5 Z 5 F _* =
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Z " "&&""j * "+ Moravec and Scholz: Helminth parasites of cormorants
Table 1. List of the localities from where cormorants, Phalacrocorax carbo sinensis (Blumenbach), were examined.
No. Locality No. of cormorants examined Year(s) and month(s) ? J 5 T \F " M ? = XT N 2 "#3$Z 2 M XT N 88 "#3#% "## % "##"% "## Z ~% ~ % ~ % ~ 8 M F" ~ F ? "" "## Z ~% ~ ? @ F M T 4 M ? " M T 2 "#3#Z 5 M T + "##"Z ~ + F @ " ; 9 F 88 "##"% "## Z ~% ~ $ Jaroslavice # "##"Z ~ 3 M M T } + "#3#Z
Fig. 1. Map showing sampling sites in the Czech Republic from where the cormorants were obtained (numbers designate the localities X " > ? J 5 ? @ F ; 5 I ; 9% * F ; the cormorants’ helminth fauna, as well as more detailed and partly acanthocephalans were mostly stained in carmine and data on cestodes and nematodes, remained unpublished mounted as permanent slides in Canada balsam, whereas the and are presented only herein. nematodes were cleared with glycerine as temporal preparations. After microscopical examination, these materials were mostly MATERIALS AND METHODS * 5 < " * 5 5 Phalacro- Parasitology, Biology Centre of the Czech Academy of Sciences, corax carbo sinensis, including adults and several chicks, was I J DV F *Zjj999 * =j j examined from South Bohemian and South Moravian localities Some nematode and acanthocephalan specimens intended for "#3$M"## X " [ " X ; the scanning electron microscopical (SEM) examination were and a few killed chicks previously collected from nests were ex- * ^ "{ 5 5 ^ * * % ;- amined for the presence of helminth parasites using the method of drated through a graded ethanol series and amylacetate, criti- a complete helminthological dissection. * * 9 ] ; 9 ^ 5 The parasites obtained were treated by usual helmintholog- X J? 8 5 * - 5 % ; 9 ^ &{ 5 % F " I~ ?* 5 * light microscopical (LM) examination, the trematodes, cestodes alphabetically in each of the higher taxonomic groups.
[ M "+% +8Z M "+ Z " "&&""j * "+ Moravec and Scholz: Helminth parasites of cormorants
Table 2. Quantitative data on the occurrence of helminth parasites of Phalacrocorax carbo sinensis (Blumenbach) in South Bohemian and South Moravian localities: total prevalence (number of hosts infected/examined), range of intensity and mean intensity (in parentheses).
Parasite species Group No.* ? J 5 &+ ? @ F + Trematoda Apophallus muehlingi I % "3## 8 - { 8j + ] "M"8 # Ascocotyle longa > 5% "# 8 - { "j + ] " " Cercarioides aharonii % "# # 8 - { "j + ] " " Galactosomum lacteum I % "3#+ 8 - { "j + ] " " Heterophyes aequalis } % "# 8 - { "j + ] +3 +3 Holostephanus dubinini ~ V I ~ I F% "#+3 " - "+{ #j + ] "M8$ 3 Hysteromorpha triloba > * % "3"# 2 "8{ +j&+ ] "M"+ & 83{ "j + ] "M$ "$ Metorchis xanthosomus < * % "3&+ 8 &{ j&+ ] "M ""{ +j + ] "M# 8 Paryphostomum radiatum V % "3& " ""{ j&+ ] "M3 & & { j + ] "M " & Petasiger exaeretus =% "# # " "${ 3j&+ ] "M&$ $ "{ " j + ] "M 8 &3 Petasiger phalacrocoracis 5 % "#8# " ""{ j&+ ] "M"+ $3 +"{ 8&j + ] M" 3"+ # Cestoda Ligula intestinalis } % "$ 3 8 - { "j + ] 8 8 Paradilepis scolecina > * % "3"# 2 &3{ j&+ ] "M$3 #$ &8{ &j + ] "M3 3 " Nematoda Baruscapillaria rudolphii @ F % ? = F% "##& " - &{ j + ] Contracaecum rudolphii 9 % "#+& 2 + { 8 j&+ ] "M&" $8{ &"j + ] "M$8 33 Desmidocercella incognita ? % "#8 8 8 { "&j&+ ] "M "3 8 { ""j + ] M 8 # Syncuaria squamata F } 9% "338 " " { $j&+ ] "M" & { ""j + ] "M& Acanthocephala Andracantha phalacrocoracis 5 % "#8# " - { "j + ] $ $ Southwellina hispida ~ < F % "# 8 - { "j + ] & & " M ; * * 9 5 Phalacrocorax ** F ; F ] M * * 5 ; 5 % 5 ; ; 9 5 ] 8 M * * * 5 ; 5 or even mammals.
RESULTS Galactosomum lacteum I % "3#+ Specimens of this species were found only once in the Survey of helminth parasites recorded from 5 5 5 F @ " ; 9 - Phalacrocorax carbo sinensis within this study during F ? @ F * "## Z ${ "j"&% the period of 1987–1992 " "# * 5 9 5 - rants (Table 2): Heterophyes aequalis } % "# ~ ; 5 ; * 5 9 5 5 - Trematoda 5 F @ " ; 9 F The trematodes of this material have already been ? @ F * "## Z ${ "j"&% +3 9 5 ; F "##8 % "##& Holostephanus dubinini ~ V I ~ I F% "#+3 This species was found in the intestine of cormorants Apophallus muehlingi I % "3## 5 9 ? @ F Z M T ; This trematode was found in the small intestine of "##"Z "j+% & F @ " ; 9 F * "## Z 5 F @ " ; 9 F ? &8{ +j"&% "M"+ ] @ ; "## Z j+% 8M8$ @ F * "##"Z * F 3{ " 5 - j"8 5 ^ 5 % ; "8] Hysteromorpha triloba > * % "3"# @ ; "## Z j+% "M"8 5 ; $ This species was found in the small intestine of cor- morants from seven localities, both in South Bohemia Ascocotyle (Phagicola) longa > 5% "# ? @ F ? J 5 Z * ? = Specimens of this species were found only once in XT N F 5 "#3$Z j % M"+ # * 5 5 5 F @ " ; XT N "#3#Z "j % " "] ; "## Z 9 F * "## Z ${ "j"&% " ? "j+% " ] @ ; "##"Z "j#% 8] @ ; "## Z "j"% & ? Moravia. @ F Z * ? " M T ? * 5 "#3#Z "j % % * M T } ? * 5 Cercarioides aharonii % "# # "#3#Z "j+% " % M T ; "##"Z 8j+% "M "# % A single specimen of this species was found in the cloa- F ; "##"Z +j#% "M$ "$ F @ " ; 5 F @ " ; 9 F 9 F * "## Z +&{ #j"&% "M+ " ] ? @ F * "## Z ${ "j"&% " @ ; "## Z "j+% 8
[ M "+% +8Z M 8 "+ Z " "&&""j * "+ Moravec and Scholz: Helminth parasites of cormorants
Metorchis xanthosomus < * % "3&+ Cestoda Specimens of this species were found in the gall-blad- der of cormorants from both South Bohemian and South Ligula intestinalis } % "$ 3 @ F ? J 5 Z * F" ~ F This cestode species was found only once in the small XT N ; "## Z "j % " * XT - 5 5 * ? " M - N ; "## Z "j+% ? @ F Z M T ; T ? * 5 "#3#Z "j % 8 % ? @ F "##"Z j+% % F ; "##"Z j#% "M& 8 Ligula intestinalis is widely distributed in Europe, Asia, F @ " ; 9 F * "## Z "&{ j"&% M# 5 "#3 F + F % % % Remarks. ; * * * % ? I % 5 <= > * % "+ 5 * - adults of this cestode were recorded from Larus ridibun- ing the gall-bladder of P. carbo in Central Europe to be dus Linnaeus, Podiceps cristatus Linnaeus, P. nigricollis M. bilis J % "$# 9 F % 5 * - Brehm, P. (Pallas) and Sterna hirundo Linnaeus ical features used to distinguish between M. bilis and ? 55 "# &% >; F" "# $% I "#+&% J M. xanthosomus are not clear-cut and no specimens of "#3 % >; F" ? I "## X the present material were studied by molecular methods, of L. intestinalis from P. carbo in this country, but it was 9 * F ; * reported from this host species in nearby Poland (Kanarek material. V ; "& X 5 L. intestinalis is various Paryphostomum radiatum V % "3& species of copepods, in which the procercoid phase of de- This species was found to be a common intestinal par- F *5 I * "#3 X - asite of cormorants in both South Bohemian and South 5 F * 5 @ F ? J 5 Z * ? = cavity of which plerocercoids develop within approxi- XT N F 5 "#3$Z j % M3 % * F" 5 ; ; "#3$ @ F ~ F ; "## Z "j % * XT - " % " * % 5 ; ;* % 9 N "#3#Z "j % 3] "## Z "j8% " ? as hosts of plerocercoids of L. intestinalis in the Czech Re- @ F Z * ? " M T ? * 5 "#3#Z public, but molecular data indicate that there are at least j % M & % * M T } +j+% two morphologically indistinguishable species previously "M " &# % M T ; "##"Z j+% M" $ % - assigned to L. intestinalis J = 3% I F ; "##"Z $j#% "M3 F @ " ; 9 - # F * "## Z { $j"&% "M""8 ] @ ; "## Z "j+% " Paradilepis scolecina > * % "3"# This species was found to be one of the most frequent Petasiger exaeretus =% "# # helminth parasites in cormorants from both South Bohe- Specimens of this species were found in the small mian and South Moravian localites. South Bohemia: pond intestine of cormorants from both South Bohemian and ? = XT N F 5 "#3$Z j % #8M$3 @ F Z ? J 5 Z * +3$ % * XT N "#3#Z j % "8M8 XT N ; "## Z "j+% &$] @ ; "##"Z +j#% "M "] @ ; ] "## Z "${ j" % +M" #] ; "## Z +j+% "## Z "j"% & ? @ F Z * ? " M T 8M" $ 8#] "## Z j8% &M&8 &] @ ; "##"Z j#% ? * 5 "#3#Z j % M8 % M T ; "##"Z "M3 8 * F" ~ F XT N @ ; "## Z 8j+% "M 8 "3 % F ; "##"Z "j#% " "j#% ] ; "## Z j % " &M #8 "## ? @ F Z F @ " ; 9 F * "## Z &8{ +j"&% * ? " M T ? * 5 "#3#Z "j % 3 ] "M"& * M T } ? * 5 "#3#Z j+% "" M" 8 ""$ ] F @ " ; 9 F * "##"Z Petasiger phalacrocoracis 5 % "#8# "j"8% "] * "## Z " j"&% "+M3 3 8 3 ] M T ; This species was commonly found in the small intes- "##"Z j+% "#M+ &" F ; "##"Z+j#% tine of cormorants from both South Bohemian and South M"+$ + @ F ? J 5 Z * ? V = Paradilepis scolecina is a cosmopolitan parasite of XT N F 5 "#3$Z j % 8"M"" $ 5 % 5 ; 5 Phala- * XT N "#3#Z "j % "+ ] ; crocorax carbo and the pygmy cormorant P. pygmaeus "## Z "j+% "] ; "## Z "## Z "j8% 3+ ? (Pallas), as well as some species of Pelecanus } ] @ F Z * ? " M T ? * 5 "#3#Z occasionally, ibises Plegadis falcinellus (Linnaeus) and j % ""M" 8 +$ % * M T } ? *- falcated ducks Anas falcata Georgi become infected (Dzie- 5 "#3#Z 8j+% M " # % M T ; "##"Z &j+% I L I >; I = I "" M3"$ 8 3 % F ; "##"Z #j#% & M"+$ <= > * % P. scolecina were pre- #" F @ " ; 9 F * "##"Z 3{ viously recorded from P. carbo ; @ F "#33 "j"8% 3] * "## Z 3+{ " j"&% +8M"3"+ &3&] @ ; ? J 5 % >; F" ? I "## "## Z 8j+% &M# $ @ F ? I F "### ? @ F % 9
[ M "+% +8Z M & "+ Z " "&&""j * "+ Moravec and Scholz: Helminth parasites of cormorants
* 5 9 * ; ? = ? @ F ? J 5 Z * ? "#3# % ? J 5 @ F " = XT N F 5 "#3$Z j % " M"$ "& % by Scholz et al. (2004) (localities not given). * XT N "#3#Z j % +M"" #] I "#$ % * * Eudiaptomus "## Z & { j" % "M$ 8] ; "## Z 3j#% "M" ] graciloides } V F ^* 5 "## Z 8j8% M" #] @ ; "##"Z $j#% "M8 5 P. scolecina, in the body cavi- * F" ~ F XT N @ ; "## Z "j#% ] ; ; 9 F ^ ; I "#$ "## Z j % " M&" + ? @ F Z * ? " develops within 20 days. The second intermediate host is M T ? * 5 "#3#Z j % 8&M8$ 8+ % * M - F * % 5 ; ;* % T } ? * 5 "#3#Z +j+% "8M $ "# % 5 5 ? = & F @ " ; 9 F * "##"Z 8{ 8j"8% " "] * "## Z " { "&j"&% "M$8 "38] @ ; "## Z Nematoda j+% M8 8 % M T ; "##"Z j+% 3M#& &+ F ; "##"Z #j#% "M $3 +$ Baruscapillaria rudolphii @ F % ? = F% Contracaecum rudolphii was described by Hartwich "##& "#+& 5 5 * 5 5 * This capillariid was found in the small intestine of cor- and stomach of cormorants P. carbo collected in Berlin, 5 ; 5 F @ " ; 9 F * 5 ; @ ; "3"+ 5 ; > * "## Z "&{ j"&% % ? @ F "3"# Ascaris spiculigera > * % "3 # ; Baruscapillaria rudolphii was described as a new spe- Contracaecum microcephalum > * % "3 # - cies from P. carbo ; @ F "##& 5 <= F I % ~ V D F I @ ; F "# above-mentioned specimens collected in South Moravia. >; F" "# 3 * Contracaecum microcephalum On the basis of literature data, the authors elucidated the and C. spiculigerum > * % "3 # % * F ;% 5 taxonomic status of Capillaria carbonis > * % "3"# cormorants P. carbo ^ 5 M V I J I * % (= nomen nudum) and pointed out that different congeneric southern Slovakia (present Slovak Republic), but it is al- species were reported under this name from cormorants by most sure that the nematodes in both these cases belonged, previous authors. They established Baruscapillaria carbonis in fact, to the later described C. rudolphii. From the ter- % "#& F 5 ritory of the present Czech Republic, C. rudolphii was, species parasitising cormorants in Europe, whose morphol- 5 % * ; @ F "#33 5 ogy is very different from that of B. rudolphii] ; - P. carbo in South Bohemia and later from the same host * 5 * ; J ? V F "## * ; J ] J " % as B. carbonis * ; * 9 B. rudolphii. [ F ? I |I 9 = " ? [ F " B. carbonis based on speci- Moravia, South Bohemia and central Moravia, respective- mens collected from P. carbo in the Czech Republic (South ly. The last-named authors recorded C. rudolphii also from J 5 5 ^ 9 * P. pygmaeus "8 * of Baruscapillaria @ F % "#3 5 5 to other genera of birds. Central Europe. Subsequently, both these Baruscapillaria The morphology of nematodes of the present material ** 9 * ; ? I |I 9 = " 5 corresponds well to the original description of C. rudol- cormorants in Moravia: B. carbonis from P. carbo and phii ; 9 "#+& ' * * 5 Phalacrocorax pygmaeus M T ? @ F % well as to the redescription of this species provided by Li X F 6 F < @ F ] "8 }@ ?'@ * - clear from the publication to which host species the giv- imens from P. carbo sinensis in China. As can be seen in en localities refer to) and B. rudolphii from P. carbo in Fig. 2, important taxonomic features such as the cephalic Záhlinice. Baruscapillaria carbonis and B. rudolphii have [ M<%' % 5 recently been reported from cormorants in freshwater and male postanal papillae and phasmids (Fig. 2D,G), and the brackish-water environments from northeastern Poland presence of an unpaired median papilla on the anterior clo- I V ; "& acal lip (Fig. 2D,G) are typical of this species. As already The life cycle of B. rudolphii (as well as that of B. car- * ; 9 "#+& % bonis) remains unknown. Two congeneric species, Barus- of C. rudolphii is the shape of the distal end of spicules capillaria anseris @ % "#& Baruscapillaria (Fig. 2F), by which this species clearly differs from three obsignata @ % "#& % * % F other congeners parasitising birds in Europe, i.e. C. micro- a direct (homoxenous) life cycle without an intermediate cephalum, C. micropapillatum ? % "3# C. var- % @ F " 9 F % iegatum > * % "3 # expected that some paratenic hosts (aquatic oligochaetes M > % C. rudolphii, F F ; B. rudolphii and are mostly from cormorants, was reported in other zooge- probably the source of infection for cormorants. ographical regions in Africa, Nearctic and Neotropical 5 9 "#+&% X Contracaecum rudolphii 9 % "#+& [ % % J @ &% 5 +% Specimens of this nematode were frequently found in ? 5 # % 9 F % 5 F the stomach of cormorants from both South Bohemian indicated that C. rudolphii is a complex of several not yet
[ M "+% +8Z M "+ Z " "&&""j * "+ Moravec and Scholz: Helminth parasites of cormorants
A B
C D
E F G
Fig. 2. Contracaecum rudolphii 9 % "#+& 5 Phalacrocorax carbo sinensis (Blumenbach), scanning electron micrographs. AMC M * % % * F 9 % * F ;] D M 5 % F 9] E M F *] F M * % F 9] G M 5 % F F 9 formally established sibling species, which were designat- * ; ?= I 9 I [ 5 $ - ed as C. rudolphii A, C. rudolphii B, C. rudolphii C, C. ru- fying only C. rudolphii J 5 9 M - dolphii D and C. rudolphii ' "" | land. Their subsequent studies (Szostakowska and Fager- them, only C. rudolphii A and C. rudolphii B are reported 5 " 9 C. rudolphii A from cormorants from Europe. in Finland and Poland occurred in brackish-water regions, According to Mattiucci et al. (2002), colonies of the whereas C. rudolphii B in freshwater sites, although mixed great cormorant P. carbo sinensis living in freshwater en- infections also occurred. Some C. rudolphii specimens of vironments in Central Europe are parasitised by nematodes the present material from cormorants in South Bohemia belonging to the taxonomic unit provisionally designated and South Moravia were examined by molecular methods as C. rudolphii J] 5 ** ; 5 M ;
[ M "+% +8Z M + "+ Z " "&&""j * "+ Moravec and Scholz: Helminth parasites of cormorants
A B
C D E
F G H
I J
Fig. 3. Desmidocercella incognita ? % "#8 5 Phalacrocorax carbo sinensis (Blumenbach), scanning electron micrographs. AMC M * % % F * F 9 % * F ;] D M ^ ; * ] E M ;% F 9] F M * 5 % F F 9 9 * * * ] G M * 5 ] H M 5 * ;] I M * 5 % * F 9] J M AbbreviationZ M * headed by Lia Paggi), Università degli Studi di Roma ‘La external environment (water) and are already infective for ? * = R% ;% 9 5 C. ru- young cormorants. However, a variety of invertebrate (co- dolphii J @ F # * * % F * Adults of C. rudolphii are parasites mainly of cor- usually participate in the transmission of C. rudolphii to morants, less often of some other piscivorous birds (e.g. F % * F @ F # 9 "#+& ' * % ; 5 < ;% ; 5 (reported as C. spiculigerum) was experimentally studied infection of cormorants with C. rudolphii. Cyprinus carpio ; @ = F ; "#+ % "#+3 % ;% Linnaeus and Tinca tinca } 5 * C. rudolphii% ; = I L I >; I > I I $% * @ ; "##" Rutilus rutilus (Linnaeus) 3 @ F # X F 9 5 F @ " ; 9 F "## % the nematode third-stage larvae develop inside eggs in the were recorded as natural paratenic hosts of C. rudolphii
[ M "+% +8Z M $ "+ Z " "&&""j * "+ Moravec and Scholz: Helminth parasites of cormorants
F [ @ M * X F 9 * P ? "#8 % I ; "# % 9 found encapsulated on the host’s gut surface and their mor- never studied in apical view. The present SEM study shows phology was identical with that of larvae from experimen- that the oral aperture is oval, partly covered by two lateral @ F # pseudolabia and surrounded by eight large submedian ce- phalic papillae arranged in two circles (each consisting of Desmidocercella incognita ? % "#8 [ 8 four papillae) and a pair of large dome-shaped amphids lo- This nematode species was commonly found in the air F * * * [ 8 M<%' sacs and lungs of cormorants from both South Bohemi- * F 9% * * 5 - an and South Moravian localities. South Bohemia: pond row, growing up from the lateral wall of the buccal cav- ? = XT N F 5 "#3$Z "j % "3 ity, but the distal portion of pseudolabium is markedly * XT N "#3#Z "j % &] ; "## Z distended dorsally and ventrally. The outer rim of the dis- j+% M$ ] "## Z j8% "M& 8] @ ; "##"Z 3j#% * * 9 F 9 ; &M "3 + ? @ F Z M T ; "##"Z 8j+% directed teeth, arranged in three groups (two teeth in me- "M" % F ; "##"Z &j#% &M 8 " F dian group and three teeth in each dorsal or ventral group) @ " ; 9 F * "## Z #{ &j"&% M"# $ [ 8 M<%' ?I ; "#+$ J [ 5 % * 5 - "#$3 % D. incognita is widely distributed over Europe and ** ^ 5 ; F F [ 8 M @ F "#33 9 ^ ; * [ 8 9 - record this nematode species from cormorants P. carbo served. The presence of seven pairs (three preanals and in the Czech Republic (South Bohemia) and they provid- four postanals) of caudal papillae in the male, as described ed its description based on LM examination of available ; I ; "# @ F "#33 % 9 * 5 } ? I |I 9 = " * 5 ] I * * % * * D. incognita from P. carbo in Záhlinice, central Moravia, the last postanal pair are covered by numerous denticles <= > * I V ; "& [ 8[% from the same host species in northern Poland. The life cycle of D. incognita is unknown, as those of The original description of Desmidocercella incognita other congeneric species. Larvae of the related species (syn. D. skrjabini I ; % "# ; ? "#8 ] Desmidocercella numidica ? % "# 5 ; ?I ; "#+$ 9 5 - ; 9 ^* 5 ; % tailed description of this species (reported as D. skrjabini) Ardea cinerea } % ; "#&# 9 9 * F ; I ; "# % 9 ; adult parasites. Fishes probably serve as paratenic hosts of 9 I F ; ?I ; "#+$ J this nematode, whereas the intermediate hosts are likely "#$3 F @ F "8 - Remarks. ?I ; "#+$ J "#$3 sumed that D. incognita * cited the authority of Desmidocercella skrjabini as Gushan- hosts, which become the main source of infection for cor- I ; % "#&# 9 F % * ; - morants. trated, but not described in the Key to Parasitic Nematodes ; ?I ; "#&# X % 9 Syncuaria squamata F } 9% "338 [ &% < 5 % Specimens of this nematode were found in the stom- * 5 F J * ach of cormorants from both South Bohemian and South * 9 * ; I ; "# % @ F ? J 5 Z * XT - name is D. skrjabini I ; % "# N "#3#Z "j % 8] ; "## Z "j+% 3] "## Z } % 5 F % @ F "#33 - j8% "M ] @ ; "##"Z 8j#% "M" ? @ F Z scribed D. incognita from P. carbo in former Czechoslova- * ? " M T ? * 5 "#3#Z "j % " % M - kia. However, some features in these nematodes, especially T ; "##"Z &j+% "M& 8 % F ; "##"Z * % F }@ 8j#% M& 8 F @ " ; 9 F * "## Z Within the present study, some adult specimens of D. in- "{ 8j"&% "M8 cognita 9 % 5 * % ; "#3+ % S. squamata is a spe- SEM and some new, taxonomically important but previ- * * 5 9 ously unreported features were revealed. ; ; F } 9 "338 Filaria ? "#8 @ F "#33 * squamata solely from females found in P. carbo from nematode body of this species to be transversely striated, < % * 5 9 * ; ; but, in fact, the surface of entire body is densely covered ? F "# & % 9 * F 5 5* * 9 F 9 5 * * I F ] description. Now this nematode is known as a parasite of similar elevations also cover cephalic papillae and am- cormorants in Europe, Palaearctic (Central Asia, Transcau- * [ 8 M X 5 9 casia) and South-East Asia and is also reported from North, 5 5 * I I F * < ? 5 J "#$3% 5 [ 8[% "#3+% @ F "## % [ ; "##$% @ The cephalic end of D. incognita was previously de- + I > I + S. squa- scribed as bearing “two lateral lips and eight cephalic pa- mata from P. carbo sinensis in northern Poland.
[ M "+% +8Z M 3 "+ Z " "&&""j * "+ Moravec and Scholz: Helminth parasites of cormorants
A B C
D E
F G
Fig. 4. Syncuaria squamata F } 9% "338 5 Phalacrocorax carbo sinensis (Blumenbach), scanning electron micrographs. A M * % * F 9] B M 5 % 5 ] C M ] D M ;% F 9] E M * % F 9] F M 5 % F F 9 9 * 5 ] G M * 5 % F 9 AbbreviationZ * M * * *
Based on LM examinations, specimens of S. squa- been properly described, as well as to recognise the actual mata of the present material from P. carbo in the Czech caudal structures in the male. > * 9 ; ; @ F "## '^- "#3+ * cept for two SEM micrographs of the anterior end of adult S. squamata in apical view, but it is very different from S. squamata from Phalacrocorax auritus auritus (Lesson) F ?'@ 5 * * - < * ; "#3$ % per) based on the same material and published by Wong species was not previously studied by SEM. Consequently, "#3$ ** 5 [ & %J%' * ; * F * ; 5 - SEM examination of S. squamata from its type host spe- "#3$ % * F 9% * - cies, P. carbo. This study made it possible, among others, soventrally elongate, slit-like, surrounded by two lateral to study in detail the cephalic structures which have never pseudolabia and two (one dorsal and one ventral) inter-
[ M "+% +8Z M # "+ Z " "&&""j * "+ Moravec and Scholz: Helminth parasites of cormorants
A B C
D E F
G H
Fig. 5. Syncuaria squamata } 9% "338 5 Phalacrocorax carbo sinensis (Blumenbach), scanning electron micrographs. AMF M * F * 5 ] G M * 5 ;% F F 9] H M * 5 % ventral view. AbbreviationsZ M ] F M F F
9 * ^ 5 X * ^ 5 the folds as well as cordons begin at the dorsal and ventral pseudolabium forms a small narrowed, somewhat conver- sides, continue posteriorly and anastomose on lateral sides gent portion with a very thin and rather long dorsal and [ &% M[ a ventral extensions. The region of this pseudolabial nar- "#3+ rowed portion is slightly raised and there is a large rounded deirids of S. squamata % I "# 3 elevation at its base. Each pseudolabium bears a pair of observed a considerable variability in the shape of deirids large submedian cephalic papillae and a lateral amphid at in specimens of S. squamata from P. carbo in the Astrakhan its base (Fig. 4A,B,D,E). Each interlabium divides poste- Nature Reserve, Russia, because deirids with two, three or ; V * F * * * even more posteriorly oriented conical teeth were present. each of its two arms is continuous with the outer cuticular The same was found in specimens of the present material, fold extending posteriorly along the cordon consisting of 9 [ M[ 9 * * [ & M' ] J 9 * 5
[ M "+% +8Z M " "+ Z " "&&""j * "+ Moravec and Scholz: Helminth parasites of cormorants
S. squamata from Phalacrocorax brasilianus (Gmelin) in the trematodes Holostephanus dubinini, Paryphostomum J = @ + radiatum, Petasiger exaeretus and P. phalacrocoracis, the The SEM examination of S. squamata 5 nematodes Baruscapillaria rudolphii and Syncuaria squa- presence of ten pairs of caudal papillae (four preanal and mata, and the acanthocephalan Andracantha phalacroco- six postanal) in the male (Figs. 4F,G, 5H), of which nine racis. pairs are formed by pedunculate papillae and one, located Group 2. Species parasitising mainly cormorants, but more ventrally at the level of the last pair of pedunculate may occasionally occur in water birds belonging to other papillae, is represented by small sessile papillae, being fol- families: the trematode Hysteromorpha triloba, the cestode lowed by a pair of minute phasmids (Fig. 4F). Pedunculate Paradilepis scolecina and the nematode Contracaecum ru- * * * * * - dolphii. nal pair are shifted more ventrally, thus surrounding the Group 3. * * * 5 ; cloacal aperture. A small median cuticular protuberance aquatic birds of different families or even mammals: the is present between ventral sessile papillae and phasmids trematodes Apophallus muehlingi, Ascocotyle longa, Cer- (Fig. 4F). No ventral precloacal cuticular ornamentations carioides aharonii, Galactosomum lacteum, Heterophyes (area rugosa) are present. aequalis and Metorchis xanthosomus, the cestode Ligula [ & 5 intestinalis, the nematode Desmidocercella incognita, and spicule in S. squamata is considerably narrowed, as previ- the acanthocephalan Southwellina hispida. ; ; @ F "## However, it should be remarked that not all data in The life cycle of S. squamata was experimentally stud- the literature seem to be reliable and may include species ; I "# 3 % "#3$ 5 X % F 5 * @ F ? = "##& * should be considered as provisional. (Ostracoda) serve as the intermediate hosts, in which the F % ** 5 V ; &${ 5 F F F * @ ; 5 * ; * * species were found to serve as suitable experimental or * 8] * % 9 9 * * 8${ as natural paratenic hosts, which acquire the infection by 5 ; * * 5 * "] F- "#3$% en species). As to the helminth species placed in group 2 @ F ? = "##& < 5 5 ; (three species), it may well be that they are, in fact, also by swallowing intermediate hosts (ostracods) along with * 5 ? I F % 5 ; ; * - "#+ % H. triloba appears to be an obligate parasite of cor- es) harbouring encapsulated nematode infective larvae. morants and, therefore, its frequent records from birds be- The prepatent period is about one month. longing to other families make doubts. The same concerns C. rudolphii and P. scolecina. Acanthocephala As visible from Table 2, the helminth species in groups The acanthocephalans found in cormorants from South " ^ F ; 5 F * F - Bohemia and South Moravia have already been dealt with lence and the intensity of infection compared with those 5 ; ? = "## * 8 ^ * M. xanthosomus and D. incognita).
Andracantha phalacrocoracis 5 % "#8# Helminths of P. carbo sinensis in South Bohemian and This acanthocephalan species was recorded only once South Moravian localities 5 5 F @ " ; As visible in Table 2, there is a distinct difference be- 9 F * "## Z ${ "j"&% $ % ? @ F tween the number of helminth species from cormorants in South Bohemian localities and that in South Moravian Southwellina hispida ~ < F % "# | 5 "# * 5 Specimens of this species were found only once in the % # &${ 9 ? J 5 posterior part of the small intestine of a cormorant from the "# " { ? @ F F @ " ; 9 F * "## Z ${ "j"&% & % | * * * * South Moravia. * * ; * - * " * 5 * - $3{ ? J 5 % ; 5 ; P. carbo sinensis recorded in the present study 8{ * ? @ F 5 Since all helminth species recorded from cormorants * * * * 5 5 were mature and producing eggs, and because no postcy- ? @ F clic parasitism may occur in them, the cormorants should causative factors, it may be due to a rather high concentra- F ; | * F ; 9 F "#$+ 5 @ " ; 9 F ? @ F % > * ;% * ? J 5 XT N% 9 F - roughly divided into the following groups: 5 5 V 5 ; 5 * Group 1. ? ; * * 9 5 ;% ^ 5 - (Phalacrocorax ** F ; F Z morants were carried out in different months of the year
[ M "+% +8Z M "" "+ Z " "&&""j * "+ Moravec and Scholz: Helminth parasites of cormorants
X " % ; 5 5 9 cies of adult trematodes from P. carbo in several South Bo- dissected, no exact data on qualitative or quantitative sea- hemian and South Moravian localities. At the same time, sonal changes in their helminth fauna could be deduced. experimental studies on the life cycles of three common The same concerns observations on the composition of the parasites of cormorants, the trematode P. radiatum and helminth fauna of cormorants in their different age/size the nematodes C. rudolphii and Syncuaria squamata, were * | "8 5 I ; ""M " 5% 9 * ; F 9 88M" $ 5 F @ " ; "##8 % @ F ? = "##& @ F 9 F 8 * "##"% $ &{ * F # @ F % @ F "##& 9 * % 8 8{ 9 * 9 C. ru- capillariid species, Baruscapillaria rudolphii, from P. car- dolphii F " F % " 3{ 9 P. scolecina " bo F @ " ; 9 F * 5 " { 9 A. muehlingi 3 "8 * - Based on a few P. carbo ^ 5 5 F @ " ; imens). The highest number of helminth species and their 9 F 5 * M T % ? 9 F "& @ F % ? I F "### J * 5 ; $M+$ 5% 9 " $M # I % seven species of helminths and C. rudolphii, respectively. 8 ; ^ 5 5 5 ; * ? ;% [ F "% ^ 5 9 "## % 9 9 5 - 5 5 F ; XT N ? J 5 tode P. phalacrocoracis * F " {] ; * and, in addition to C. rudolphii, she found the capillariid " 3"+ * 5 % P. scolecina (prevalence Baruscapillaria carbonis, not previously reported from the " {] ; * 3 3 * 5 5 Czech Republic. C. rudolphii * F " {] ; * $8 * - 5 * < I ? I + imens) were recorded. The species diversity of helminths ? I |I 9 = " % and the fact that some of them were found only during the own, previously unpublished data on trematodes and nem- early spring suggest that some parasites are brought into atodes, respectively, found in the cormorants (P. carbo and the nesting sites by cormorants coming from their winter P. pygmaeus) examined from some central and southern habitats in southern countries. Moravian localities. Unfortunately, in the case of helminth 5 F 5 + * - species recorded from more species of hosts, the locali- 5 5 M T % ; "##"] # * 5 5 - ties where such parasites were found in cormorants were F % ; "##"] + * 5 5 } % ? * 5 * F % ; * F 5 "#3# 9 F ; 9 * 9 5 % species not previously recorded from great cormorants in the number of species was lower in comparison with that the Czech Republic: the trematodes Renicola secundus found in adult cormorants. Again, the highest intensities ?I ; % "# & Tylodelphys clavata (von Nordmann, of infection (up to several hundreds in one cormorant) ex- "38 ? I + % 5 Cosmo- hibited the three above-mentioned helminth species. Light cephalus obvelatus < * % "3 % Cyathostoma mi- infections with C. rudolphii and P. scolecina were alredy crospiculum ?I ; % "#" Eustrongylides excisus F 5 I "M2 weeks old (see above). I % "# # ? I |I 9 = " [ The most frequent parasite of cormorants in both regions 5 <= > * % ; B. car- under investigation proved to be the nematode C. rudolphii bonis, B. rudolphii, C. rudolphii and P. radiatum from the (see Table 2). pygmy cormorant P. pygmaeus. ** 5 F ^ X % DISCUSSION date, the helminth fauna of great cormorants in the Czech 5 <= F I % * 5 > * * ; * % "8 * parasites of great cormorants Phalacrocorax carbo were { 5 % * 3{ % 3 * - ~ V D F I @ ; F "# >; F" 8 { 5 * 3{ - "# 3 9 F % ^ 5 V 9 cephalans. This is comparable with recent data in the most birds from the only then known Czechoslovakian nesting extensive study on the helminth parasites of P. carbo sin- colony of cormorants on the Danube River (in the so called ensis * 5 ; I V ; "& - Q< 5 R F J I * % - M % ^ 5 &#" 5 ern Slovakia (now Slovak Republic), where they recorded from freshwater and brackish water localities: of a total of two species of trematodes (Paryphostomum radiatum and 8" * % 8 * 9 I- Hysteromorpha triloba), one cestode (Paradilepis scoleci- 9 % 9 ; "3 * 9 9 - na) and one nematode (Contracaecum rudolphii F ; I } I * L I } I ? 5 I 5 C. microcephalum or C. spiculigerum 5 ; I V ; "& [ 5 * <= > * % @ F "#33 and the present study, the species composition of helminths 9 * 5 F - found in the freshwater environment in Poland was very morants, based on two specimens examined in the vicinity similar to that found in the Czech Republic, differing only XT N% ? J 5 % 9 ^ * * 5 * * * 8 5 % " 5 9 ' * % ; 9 * * } % ? = "## * 9 * * ; 9 5 P. carbo were pub- * F "##8 "" * - > 5 "#+#% = % I
[ M "+% +8Z M " "+ Z " "&&""j * "+ Moravec and Scholz: Helminth parasites of cormorants
> I I % I V ; "& % 9 5 ^* 5 ; 5 @ F # % I data on these parasites are found in broader faunistical carp (Cyprinus carpio % 5 <= * % papers or those treating individual helminth species (e.g. very susceptible to infection with larvae of C. rudolphii. I > I + % % = I L I >; I Representatives of some helminth genera recorded in cor- = I "" @ ; * * 9 5 5* morants (Contracaecum > ;% "#" % Eustron- parasite of cormorants, the anisakid C. rudolphii, whose gylides I % "# #% Heterophyes < % "33+ high infections, as found in the present study, were also known as possible agents of serious parasitic diseases in I5* "###% 5 < 9 8 = I L I >; I > I I 3% I ""% > - During dissections of cormorants, the composition of I I ""% ?= I 9 I [ 5 " J; their food was also recorded: this was mostly formed by the way, numerous specimens of C. rudolphii ; small or medium-sized common carp C. carpio (body length the senior author of the present paper) were collected by " M + 5 % ; Tinca tinca (24M8" 5 K. Molnár from the stomach of P. carbo sinensis in Hun- occasionally also by silver carp Hypophthalmichthys mo- ; "" @ "& @ % ~ ; @ litrix ~ 5 9 ;* % > % J * % ; M * Rutilus rutilus. For example, 5 specimens of common carp Undoubtedly, the qualitative and quantitative differenc- " 5 * 5 F * 9 es between the helminth faunas recorded from cormorants in the oesophagus and stomach of a single cormorant from in South Bohemia and South Moravia (Table 2) are asso- F @ " ; 9 F X ciated with different ecological conditions in these two 8" 5 5 5 5 regions. South Moravia represents the warmest region in 5 ; 9 F ; - <= > * % 9 5 F \ 5 * ; 5 X 5 5 as compared to colder South Bohemia. Moreover, whereas * * 5 % - the water bodies in South Bohemia are represented mainly I % * * * ; 5 5 * 9 F % ; 5*- ? @ F % * % 5 5 | 6I F F @ " ; 9 F ;V X ; > F % " % ; I 5 9 \ ; ? @ F * conditions. Since all helminth parasites of cormorants diseases, some of which might be prospectively the source have complex life cycles with participation of a variety of of parasitoses in humans (see above). aquatic invertebrates and vertebrates serving as intermedi- ate or paratenic hosts, conditions in South Moravia seem to Acknowledgements. We would like to express our gratitude to many local representatives of the then State Fishery Enterprise, be much better for completing the helminth life cycles as XT N M T % * F 5 - compared in South Bohemia. Also other ecological factors, rants for examination, namely J. Schönbauer and Mr. Ondra. such as the species composition and density of local water X I ~ F% bird populations, whose helminth communities contribute M ;% <= 5; ? I * * 5 % J DV F % 9 5 F 5 * be considered. material from cormorants and participated in bird dissections, as [ 5 * 5 % - 9 5 % J FI % es serve as the important link in their life cycles (serving I F @ ~ F% 9 ; * 5 ] ^ 5 5 ] J I I F * 9 * * - larvae of these parasites are then the source of infection ration of illustrations and tables. This study was partly supported for cormorants. Heavy infections with larvae of some of by the Grant Agency of the Czech Academy of Sciences (grant + "" % <= ? [ M j" j these species (e.g. C. rudolphii or P. scolecina) may neg- "" M ;% J< < ? F ; \ ** >~|Z + $$8&&
REFERENCES
6ȁ M "#38Z | 5 - pods for Which We Are Home. Second Edition. Taylor & Fran- F 8"Z " # ? F I % } 9 I% " ** ǎǂǕǐ [ > % @ǐǏǕdžNJǓǐ < @ % ǎǂǕǐ ? J +Z Contracae- JǂǓǔǐǏ @ % @ǂǓǔljǂǍǍ J ' 2004: First record of Contracaecum cum rudolphii Hartwich (Nematoda, Anisakidae) from the Neo- ** 5 Z I 5 5 - tropical cormorant, Phalacrocorax brasilianus (Gmelin) (Aves, 9 ? ~ $ Z $&M$3 M % J = > F J 8Z JǂǓǖȪ ~ % ǂLjǂǔǂǘǂ % XdžǏǐǓǂ [ % MǓǐnjdžȪ @ 2000: The head " 3&M" 3# end morphology of Contracaecum rudolphii with remarks on C. ǏDždžǓǔǐǏ > < Z 5 M ~ X himeu and C. umiu (Nematoda, Anisakidae). Acta Univ. Agri- F *5 X 5 ? ' < J M - ? F @ J &3Z +#M$+ % % + ** JǂǓǖȪ ~ % ?džǓLjdždžǗǂ X M % ?ǐǏNJǏ @ % >ǚǛljNJnjǐǗ @ "#$3Z ǔljLJǐǓDž > % <Ǔdžǘdž 8Z X M Homo sapiens. 5 [ ' J M > An Annotated Checklist of the Protozoa, Helminths and Arthro- 5 5 % M % 8"3 **
[ M "+% +8Z M "8 "+ Z " "&&""j * "+ Moravec and Scholz: Helminth parasites of cormorants
JǂǓǖȪ ~ % ?džǓLjdžNjdžǗǂ X M "## Z < * * J J % "# 3M"#+ < M * J M M > 8 Baruscapillaria. Acta Sci. Nat. ? " Z " #M"+8 ? J 5 F J &Z "M 8 ǂǏǂǓdžnj ""Z M * ; Contracaecum rudolphii JǂǓǖȪ ~ % XdžǏǐǓǂ [ % ǓǤȁǎǂǓ ? % MǓǐnjdžȪ @ "Z < 5 5 sensu lato (Nematoda) in the great cormorant (Phalacrocorax and lead concentrations in Contracaecum rudolphii (Nematoda) carbo 5 M M #$Z "3 M"#" and its host, the cormorant Phalacrocorax carbo (Aves). Folia ǂǏǂǓdžnj % >ǐnjNJDŽnjNJ 2005: The status of studies on the hel- M &3Z $$M$3 minth fauna of the great cormorant (Phalacrocorax carbo sinen- JǐǖǛNJDž % ǕdžLJnjǂ % ǚǑȪǂ ~ % }džnj ? % ?DŽljǐǍǛ X % }džLjǂǍ } % sis M M =; "Z "+ JdžǏ ǂǔǔNJǏdž | % }ǐǐǕ 3Z * ; * - ǂǏǂǓdžnj % >ǐǍǃNJdžDŽnjNJ } + Z Syncuaria squamata (Linstow, ;Z 9 9 "338 5 Z 5 Phalacro- parasite Ligula intestinalis < Z * ; corax carbo sinensis J 5 % "$#3 M M 83Z "&+ M"&$# 5 &8Z 88M8+ JǖȪǕǂ % XǐǍnjǂDŽljdžǗǂ } @ % @NJDŽljǤǍdžnj "#3 Z 5 ǂǏǂǓdžnj % >ǐǍǃNJdžDŽnjNJ } + Z X F Anisakis birds of the family Laridae in South Bohemia. Acta Soc. Zool. simplex > * % "3 # 5 Phalacrocorax J 5 F &#Z "$&M"$# carbo sinensis J 5 % "$#3 5 ~ } % džǛLJǖǍNJ J ? % ~ǐǍǑǐǏNJ ? % JdžǍǕǓǂǎNJ % MǐǖǍNJǏ > Z - M | ; ? 8 Z 8M 3 * ; * 9 - ǂǏǂǓdžnj % ǂǍdžȧǏǚ "&Z '^ * - minth parasites of the cormorant, Phalacrocorax carbo sinensis. ent variation in component communities and patterns of aggre- M ; " &Z 8$M && gations in helminth parasites of great cormorant (Phalacrocorax ǖǃNJǏNJǏ ~ J "#&#Z '^* 5 ; ; 5 carbo) from N.E. Poland. Parasitol. Res. ""8Z 38$M3 * 9 5 5 ~ > F M = džǏǏdžDžǚ @ % ?ǑdžǏDŽdžǓ "&Z < 5 - ? % ???> ""Z " +M"+ > 9 @ M ; 'F $#Z &#M $ ǖǃNJǏNJǏǂ @ "#3 Z X * 9 5 < % } [ - ǖǓǐDŽljnjNJǏ ǖ ~ "# 3Z ? ; 5 Skrjab- na of the USSR. Amerind Publishing Co. Pvt. Ltd., New Delhi, inocara 9 % "#&" X I * &Z 8 M88+ 8 ** > ǖǃNJǏNJǏǂ @ "#3$Z < < M X * 9 5 Z | J }NJ } % ǖ % ljǂǏLj } M "8Z [ Contracaecum (Ed.), Key to Parasites of Freshwater Fishes of the USSR Fauna. spasskii @ = F % "# C. rudolphii 9 % "#+& sensu ~ 5 8% M @ = M I % @ 9% ** lato) (Ascaridida: Anisakidae) from piscivorous birds in China. M$+ > ?; M 3&Z M 8+ ǛNJdžnjǐȝǔnjǂ >ǚǏnjǐ % ǛNJnjǂ ' ""Z X * 9 5 Paradilep- ǗǐǏ }NJǏǔǕǐǘ | "338Z 5 % X 5 - is scolecina > * % "3"# < Z <; * ; F phalen gesammelt von Prof. Fedtschenko in Turkestan. Arch. 5 Phalacrocorax carbo sinensis (Blumenbach, &#Z $&M8"& "$#3 5 ; } I ? 5 I - @ǂDŽljǤȁdžnj M "#38Z < 5 ? @ F F 8"Z " 3M M 5 &3Z 8M 3 " # <= ǛNJdžnjǐȝǔnjǂ >ǚǏnjǐ % >ǐnjNJDŽnjNJ $Z '^* 5 - @ǂǕǕNJǖDŽDŽNJ ? % XǖǓDŽljdžǕǕǐ @ % JǓǂLjǂǏǕNJǏNJ [ % ǂǔDŽdžǕǕNJ tation of copepods and amphipods with Contracaecum rudol- 2002: On the occurrence of the sibling species of Contracae- phii F Z < @ 5 ' % M ~ cum rudolphii complex (Nematoda: Anisakidae) in cormorants All-Russian Workshop on Theoretical and Marine Parasitology, (Phalacrocorax carbo sinensis 5 ~ < Z >| M % % ** 3M+ 5 I M &&Z " ǛNJdžnjǐȝǔnjǂ >ǚǏnjǐ % >ǐnjNJDŽnjNJ 3Z I @ǐǏǕdžNJǓǐ < @ % ǎǂǕǐ [ % ǎǂǕǐ ? J +Z M 5 - cormorants (Phalacrocorax carbo sinensis } "$ 3 5 tro de Syncuaria squamata (Linstow) (Nematoda, Acuariidae) the colony on the Selment Wielki, with the nematode Contracae- em biguás, Phalacrocorax brasilianus (Gmelin) (Aves, Phala- cum rudolphii 9 % "#+& 5 % I | - J > F J 8Z " +3M" $ ; ? 8$Z +"M$" @ǐǓǂǗdžDŽ [ "## Z [ 5 Syncuaria squa- [džDžǚǏNJDŽlj @ % MdžǏDŽdž J % JdžǓLjǂǏ [ "##$Z 5 5- mata } 9% "338 5 55 5 Phalacrocorax munity structure and pattern in sympatric populations of dou- carbo } <= F I [ M 8$Z 8+ M8++ ble-crested and Neotropic cormorants. J. Helminthol. Soc. Wash. @ǐǓǂǗdžDŽ [ " Z < I @ = M [ - +&Z "$+M"3 es of the Czech Republic and the Slovak Republic. Academia, [ǓǂǏǕǐǗǤ "Z < * 5 5 Z < * - M % "+3 ** dae) parasitic in the common cormorant (Phalacrocorax carbo), @ǐǓǂǗdžDŽ [ " Z X 5 M with redescription of Baruscapillaria carbonis (Dubinin et Du- < J ~ 5 % M % & # ** % "#& [ M &3Z M 8 @ǐǓǂǗdžDŽ [ #Z '^* 5 F *5 [ǓǂǏǕǐǗǤ 2002: Some parasitic nematodes (Nematoda) of birds Contracaecum rudolphii (Nematoda: Anisakidae) in copepod F <= > * ? J 5 ++Z "8M 3 * [ M +Z "3 M"#8 ǂǓǃNJǏ } % @ǂǕǕNJǖDŽDŽNJ ? % MǂǐǍdžǕǕNJ @ % ǐǏǛǤǍdžǛ DŽǖDzǂ % @ǐǓǂǗdžDŽ [ "8Z M 5 [ 9 [ ' - ǂǔDŽdžǕǕNJ ""Z 5 * F * > F ? ' 5 % M % + " ** existence of a new species of Contracaecum (Nematoda: An- @ǐǓǂǗdžDŽ [ % ǂȪNJǏDŽǐǗǤ ~ % ?DŽljǐǍǛ X "#33Z 9 - isakidae) parasite of Phalacrocorax brasilianus (Gmelin) from 5 * 5 5 Phalacrocorax carbo } < * 9 5 - <= F I [ M 8 Z 83"M838 M #$Z &$+M&# @ǐǓǂǗdžDŽ [ % ?DŽljǐǍǛ X "##&Z | F F *5 ǖǔljǂǏǔnjǂǚǂ } lj "# Z ? ; ?* 9 of Syncuaria squamata (Nematoda: Acuariidae), a parasite of Æ??> X '} &Z M+8 > cormorants, in the intermediate and paratenic hosts. Folia Par- ǂǓǕǘNJDŽlj "#+&Z > F F * 5 &"Z "38M"# @ * Contracaecum Railliet & Henry, @ǐǓǂǗdžDŽ [ % ?DŽljǐǍǛ X % ǂȪNJǏDŽǐǗǤ ~ "##&Z X ; 5 - "#" @ @ J & Z " M 8 tus of Trichosoma carbonis > * % "3"# * ǖDždžDŽ % džǓǏǼ 'Džǔ "#$ Z [ <= F I % "# Baruscapillaria rudolphii n. sp. (Nematoda: Capillariidae), an J M F % M " 5 % M % 8$ ** <= * 5 ?; M 3Z " 8M" 3 ǂǓdžDŽnjǂ } "#$ Z | ; Paradilepis scolecina (Rud., @ǐǛLjǐǗǐǚ % ?ljǂnjljǎǂǕǐǗǂ ~ % ?džǎdžǏǐǗǂ @ "#+ Z "3"# Neogryporhynchus cheilancristrotus % "3 ? ; ; Contracaecum spiculigerum (Ascari- Z I % 5 @
[ M "+% +8Z M "& "+ Z " "&&""j * "+ Moravec and Scholz: Helminth parasites of cormorants
? < Æ ? ; 5 - ?ljǂǎǔNJ ? % ǐǓǎǂǏ > % ǂǔǔdžǓ > % JdžǗdžǓNJDžLjdž # Z > - % @ 9% M &% ** "+#M"$& > scription and genetic characterization of selected Contracaecum @ǐǛLjǐǗǐǚ % ?ljǂnjljǎǂǕǐǗǂ ~ % ?džǎdžǏǐǗǂ @ "#+3Z spp. (Nematoda: Anisakidae) from various hosts in Australia. } ; Contracaecum spiculigerum (Ascaridata: An- M > " &Z " $M" I % * 5 5 X '} ?ljǂǎǔNJ ? % ǐǓǎǂǏ > % ǂǔǔdžǓ > % JdžǗdžǓNJDžLjdž # Z "#Z " #M"8+ > and morphological evidences for the existence of sibling species ǂȪNJǏDŽǐǗǤ ~ % @ǐǓǂǗdžDŽ [ % ?DŽljǐǍǛ X "##8 Z X 5 within Contracaecum rudolphii 9 % "#+& 5 - common cormorant (Phalacrocorax carbo) in Czech Republic. Z I M > " Z #M 83 ? J 5 $Z 8"M&+ ?NJǕnjǐ % JNJǛǐǔ % ?ljdžǓǓǂǓDž ?ǎNJǕlj ' % ?ǕǂǏǕǐǏ % ǐ- ǂȪNJǏDŽǐǗǤ ~ % ?DŽljǐǍǛ X % @ǐǓǂǗdžDŽ [ "##8 Z X ; ǎǐǓǐǗǤ M % džǏdžǃdžǓLj M "+Z F ^ 5; ' - Paryphostomum radiatum V % "3& X 5 Z ' - * * \ 9 5 Metorchis } % "3## nostomatidae), a parasite of cormorants. Folia Parasitol. 40: X 5 Z |* M + Z 3M +$ "#8M " ?NJǕnjǐ % [ǂǍǕǼǏnjǐǗǤ % ?DŽljǐǍǛ X +Z < I ǂȪNJǏDŽǐǗǤ ~ % ?DŽljǐǍǛ X % @ǐǓǂǗdžDŽ [ "##&Z > * Trematodes (Digenea) of Birds of the Czech and Slovak Repub- Petasiger exaeretus =% "# # P. phalacrocoracis (Yama- 5 % M % """ ** % "#8# X 5 Z ' 5 % * 5 - ?NJǕnjǐ % |njǖǍdžǘNJDŽǛ " Z < I 5 ?; M $Z "8#M"&$ Birds in the Czech Republic and the Slovak Republic. Comenius džǍǔǐǏ J 2005: Pelicans, Cormorants and Their Relatives: Pe- @ % MT F% " ** lecanidae, Sulidae, Phalacrocoracidae, Anhingidae, Fregatidae, ?njǓǚǂǃNJǏ % ?ljNJnjljǐǃǂǍǐǗǂ M % ?ǐǃǐǍdžǗ "#&#Z M |^ Æ F ; M % |^ % ** "+ M"+8 ?* [ ?I ; ' % ; M ǐǕǕdžǏnjǧǎǑdžǓ % ǐǓǃdžǍ > % ǷǔǕdžǓǔ "###Z 5 J 5 % ~ M Æ??> ? % @ 9 von Kormoranen (Phalacrocorax carbo sinensis } % "$ 3 } % "# ** > mit Contracaecum rudolphii (Nematoda: Ascaridoidea) im Bez- ?njǓǚǂǃNJǏ % ?ǐǃǐǍdžǗ % ǗǂǔljnjNJǏ ~ @ "#+$Z ?* irk Oberbayern (D) und Kanton St. Gallen (CH). Tierärztl. Prax of Animals and Man and the Diseases Caused by Them. Part $Z $&M $# & | F; 5 "+ I % @ 9% + & ** > - |DždžǏNJǏLj "#$+Z < * 5 ; * - sian.) ; F M "&Z "M#8 ?ǐǍǐǏNJǕǔNJǏ "#8 Z =9 F 5 |ǏDžǓǂȁnjǐǗǤ @ % ~ǂǍǐǗǤ % ǐǓǕǂǏ % ~ǐNjǕdžnj } % DžǤǎdžnj ~ J I M I % | % " &Z 8+"M8+ Z. " Z < 5 Phalacro- ?ǐǎǎdžǓ "# &Z < 5 corax carbo sinensis) predation on parasite infection and body ~ I @ = T6 ? ~ J % J% "3Z "M"8 <= 9 condition of common carp (Cyprinus carpio M > "" Z Russian summary.) "&3$M" ?ǕǓǂnjǐǗǤ "###Z ? 5 9 I 9 5 5 MǐǍǤnj @ " Z J Ë F cormorants (Phalacrocorax carbo } F @ M ? 5 6I } 8" Z @ " ; 9 F ? @ F [ ~ 3M #Z Czech.) " M"+" <= 9 ' 55 ; >džNJǎdžǓ } "#+#Z 5 F 5 F J I ?ǖDžǂǓNJnjǐǗ ~ ' "#+ Z | ? } > % "#8+ ? I- der Deutschen Demokratischen Republik. Wissensch. Z. Ernst- F% "# # M % * 5 ; * 5 % "#8$ Z @ = Æ F 9 "3Z " #M"88 ?I ; ' % X 5 5 @ | F; >ǐnjNJDŽnjNJ % ?ǐǞǕǚǔNJǂnj % ǛNJdžnjǐȝǔnjǂ >ǚǏnjǐ % JǐǓǖDŽNJȝǔ- X 5 "$ M Æ??> ? % @ - njǂ ""Z M ; 9 Contracaecum rudolphii 9% ** " M 8 > (Nematoda: Anisakidae) infection in the great cormorant Phala- ?ǛǐǔǕǂnjǐǘǔnjǂ J % [ǂLjdžǓljǐǍǎ M $Z @ - crocorax carbo } "$ 3 5 &3Z #M8 tion of two strains of third-stage larvae of Contracaecum rudol- >ǖDžǐǍǑljNJ < "3"#Z ' = 5 ; * 5 phii 5 Z I 5 M * ^ * 5 > I ? % J % 3"" ** M #8Z #+"M#+& >ǚȪǂǗǼ J "# $Z [ I 9 5 ?ǛǐǔǕǂnjǐǘǔnjǂ J % [ǂLjdžǓljǐǍǎ M " Z < ^ - <= F I M &Z ##M8 # <= 9 netic variability of Contracaecum rudolphii A and Contracae- German and Russian summaries.) cum rudolphii B (Nematoda: Anisakidae) in cormorants, Phala- >ǚȪǂǗǼ J "# 3Z X 5 5 Phalacroco- crocorax carbo sinensis% J M #3Z rax carbo } <= F I ? J 5 F &$ M&$3 Z " "M" # <= 9 5 > 55 njǂǓDžǂ "#+&Z X 5 5 F >ǚȪǂǗǼ J % ?NJǕnjǐ "## Z X * 9 5 < 5 <= F I ? ~ J % J% " M+ 3Z +#M #8 Moravia (Czech and Slovak Federal Republic). Acta Sci. Nat. Czech with English, German and Russian summaries.) ? J 5 F J +Z "M#8 ǕdžLJnjǂ % ǚǑȪǂ ~ % ?DŽljǐǍǛ X #Z * ; * ; ?ǂNJDžǐǗ ǖ ? "# &Z 9 * * 9 5 and biogeography in population structure of a cosmopolitan en- X '} $Z + M $& > doparasite: microsatellite study of Ligula intestinalis (Cestoda). ?DŽljǐǍǛ X "#3# Z [ F Paradilepis scoleci- @ ' "3Z ""3$M" + na > * % "3"# <; * ; Z * 5 XǐǓǓdžǔ M % |ǓǕdžLjǂ % ?DŽljǍǂǕǕdžǓ > 2005: Nematode parasites <= F I [ M 8+Z + M++ of the digestive tract in Neotropic cormorant chicks (Phalacro- ?DŽljǐǍǛ X "#3# Z 5* < % * corax brasilianus) from the River Cruces Ramsar site in south- <= F I ? ? J 5 F J 8Z < M > #$Z " 8M" $ "M + XǐǓǓdžǔ M % ~ǂǍDžNJǗNJdžǔǐ % ?DŽljǍǂǕǕdžǓ > % @ǐǏǕdžLJǖǔDŽǐ % >dž- ?DŽljǐǍǛ X % JǓǂǚ > % ǖDŽljǕǂ > % SdžǑǐǗǤ > 2004: Larvae ǗdžǏLjǂ % @ǂǓǯǏ [ % }ǂǎNJǍǍǂ % >ǂǎǂǍǍǐ Z ;* ; <; * ; 5 Z F 9 by Contracaecum rudolphii (Nematoda: Anisakidae) in the Ne- [ M "Z "8"M" otropic cormorant Phalacrocorax brasilianus% 5 ?DŽljǐǍǛ X % @ǐǓǂǗdžDŽ [ % ǂȪNJǏDŽǐǗǤ ~ "## Z X9 I 9 ; ~ F F % < ? * [ acanthocephalans from the common cormorant, Phalacroco- ' F 8 Z " "M" 3 rax carbo% <= F I ? J 5 F +Z ~ǐNjǕȊDŽljǐǗǔnjǤ @ǂǚdžǓǐǗǤ @ "# Z 9 * "#$M & 9 5 ? J 5 F "+Z $"M33 Czech with German and Russian summaries.)
[ M "+% +8Z M " "+ Z " "&&""j * "+ Moravec and Scholz: Helminth parasites of cormorants
ǐǏLj M } % ǏDždžǓǔǐǏ > < "#3$Z F *5 Syncuaria ǐǏLj M } % ǏDždžǓǔǐǏ > < % JǂǓǕǍdžǕǕ < @ "#3+Z > F squamata } 9% "338 5 Z the genus Syncuaria % "# $ 5 Z (Ostracoda) and double-crested cormorants (Phalacrocorax au- < +&Z ""3+M""#+ ritus auritus < + Z &M 8"
> F # ; "+ * * "+ M "8 "+
Cite this article as: @ F [ % ? = X "+Z 5 * 5 Phalacrocorax carbo sinensis 5 9 <= > * [ M +8Z
[ M "+% +8Z M "+ "+