Helminth Parasites of the Lesser Great Cormorant Phalacrocorax Carbo Sinensis from Two Nesting Regions in the Czech Republic
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'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 JDVF%<=>* Abstract: M^5"*55Phalacrocorax carbo sinensis (Blumenbach) 59<=>*?J5?@F9M;% <=5;?*F;<=FI5;?;"#3$M"##5%"#* 5*9%X5""*%<%5&*%9 F5**;Z**5Phalacrocorax**8${%*- 5;5"+{**&${|"#*%"{9?@F% ;&${"#*?J5X55*55?@F ****5;9*F @";9F% better ecological and environmental conditions in this warmer region. Scanning electron microscopical examination of three common nematode species parasitising cormorants, Contracaecum rudolphii9%"#+&%Desmidocercella incognita ?%"#8 Syncuaria squamataF}9%"338%F5^5;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 @6I"#38?J5%[5 [ **"#3M"#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**MI" 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 [ ? J5 ? uted from northern and central Europe to southern China Moravia (western and eastern parts of the Czech Republic, ""#$% *F;9F[%F great cormorants occurring in the Czech Republic belong the helminth parasites of the lesser great cormorant P. car- to P. carbo sinensis. However, the validity of this subspe- bo sinensis in these two main nesting regions were carried cies has recently been questioned by Kennedy and Spencer ;5M;% "& <=FI 5; ?% I Whereas the European population of P. carbo sinensis JDVF"#3$M"##X**9I 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 "#"#+$66"#38*9 @F "#33% "##&% @F "##% #% several unsuccessful attempts of great cormorants to nest ?="##%F"##8%%"##& ; *<=>*%[ @F?="##&%F *Z[@F%M;%J;<<=5;?%JFI8"%8$I JDVF%<=>*M\&83$$$&8][^Z\&838"833]'5Z5F_*= 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) ?J5T\F " M? =XTN 2 "#3$Z 2 MXTN 88 "#3#%"##%"##"%"##Z~%~%~%~ 8 MF"~F? "" "##Z~%~ ?@FMT 4 M?"MT 2 "#3#Z 5 MT + "##"Z~ + F @";9F 88 "##"%"##Z~%~ $ Jaroslavice # "##"Z~ 3 MMT} + "#3#Z Fig. 1. Map showing sampling sites in the Czech Republic from where the cormorants were obtained (numbers designate the localities X">?J5?@F;5I;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< "*55 Phalacro- Parasitology, Biology Centre of the Czech Academy of Sciences, corax carbo sinensis, including adults and several chicks, was I JDVF*Zjj999*=jj 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- *^"{55^**%;- 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- XJ?85*- 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.* ?J5&+ ?@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 ~VI~IF%"#+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+]"M8&3 Petasiger phalacrocoracis 5%"#8# " ""{j&+]"M"+$3 +"{8&j+]M"3"+# Cestoda Ligula intestinalis}%"$3 8 - {"j+]88 Paradilepis scolecina >*%"3"# 2 &3{j&+]"M$3#$ &8{&j+]"M33" Nematoda Baruscapillaria rudolphii@F%?=F%"##& " - &{j+] Contracaecum rudolphii 9%"#+& 2 +{8j&+]"M&" $8{&"j+]"M$833 Desmidocercella incognita ?%"#8 8 8{"&j&+]"M"38 {""j+]M8# Syncuaria squamata F}9%"338 " "{$j&+]"M"& {""j+]"M& Acanthocephala Andracantha phalacrocoracis 5%"#8# " - {"j+]$$ Southwellina hispida ~<F%"# 8 - {"j+]&& "M;**95Phalacrocorax**F;F]M**5;5% 5;;95]8M***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 555F @";9- Phalacrocorax carbo sinensis within this study during F?@F*"##Z${"j"&% the period of 1987–1992 " "#*595- rants (Table 2): Heterophyes aequalis }%"# ~;5;*5955- Trematoda 5F @";9F The trematodes of this material have already been ?@F*"##Z${"j"&%+3 9 5 ; F "##8% "##& Holostephanus dubinini ~VI~IF%"#+3 This species was found in the intestine of cormorants Apophallus muehlingi I%"3## 5 9 ? @F Z MT ; This trematode was found in the small intestine of "##"Z"j+%&F @";9F*"##Z 5 F @"; 9 F ? &8{+j"&%"M"+]@;"##Zj+%8M8$ @F*"##"Z*F3{"5- j"8 5 ^5% ; "8] Hysteromorpha triloba>*%"3"# @;"##Zj+%"M"85;$ This species was found in the small intestine of cor- morants from seven localities, both in South Bohemia Ascocotyle (Phagicola) longa>5%"# ?@F?J5Z*? = Specimens of this species were found only once in XTNF5"#3$Zj%M"+#* 555F @"; XTN"#3#Z"j%""];"##Z 9 F * "##Z ${ "j"&% " ? "j+% "] @; "##"Z "j#% 8] @; "##Z "j"% & ? Moravia. @FZ*?"MT?*5"#3#Z "j% % * MT } ?*5 Cercarioides aharonii%"## "#3#Z "j+% "% MT ; "##"Z 8j+% "M "#% A single specimen of this species was found in the cloa- F;"##"Z+j#%"M$"$F @"; 5F @";9F 9 F * "##Z +&{ #j"&% "M+ "] ?@F*"##Z${"j"&%" @;"##Z"j+%8 [M"+%+8Z M8"+ 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}%"$3 @F?J5Z*F"~F This cestode species was found only once in the small XTN;"##Z"j%"*XT- 5 5 * ?" M- N;"##Z"j+%?@FZMT; T?*5"#3#Z"j%8%?@F "##"Zj+%%F;"##"Zj#%"M&8 Ligula intestinalis is widely distributed in Europe, Asia, F @";9F*"##Z"&{j"&%M# 5"#3F + F[%%% Remarks.;***%?I % 5 <= >*% "+5*- adults of this cestode were recorded from Larus ridibun- ing the gall-bladder of P. carbo in Central Europe to be dus Linnaeus, Podiceps cristatus Linnaeus, P. nigricollis M. bilisJ%"$#9F%5*- Brehm, P. [(Pallas) and Sterna hirundo Linnaeus ical features used to distinguish between M. bilis and ?55"#&%>;F""#$%I"#+&%J M. xanthosomus are not clear-cut and no specimens of "#3%>;F"?I"##X[ the present material were studied by molecular methods, of L. intestinalis from P. carbo in this country, but it was 9 *F; * [ reported from this host species in nearby Poland (Kanarek material. V;"& X[5L. intestinalis is various Paryphostomum radiatumV%"3& species of copepods, in which the procercoid phase of de- This species was found to be a common intestinal par- F*5I*"#3X- asite of cormorants in both South Bohemian and South 5F*[5 @F?J5Z*? = cavity of which plerocercoids develop within approxi- XTNF5"#3$Zj%M3%*F" 5;;"#3$@F ~F;"##Z"j%*XT- "%"[*%5;;*%9 N"#3#Z"j%3]"##Z"j8%"? as hosts of plerocercoids of L. intestinalis in the Czech Re- @FZ*?"MT?*5"#3#Z public, but molecular data indicate that there are at least j% M &% * MT } +j+% two morphologically indistinguishable species previously "M"&#%MT;"##"Zj+%M"$%- assigned to L. intestinalis J=3%I F;"##"Z$j#%"M3F @";9- # F*"##Z{$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