OCCURRENCE OF TETRAMERES SPINOSA (MAPLESTONE, 1931) BAYLIS, 1939 (NEMATODA: TETRAMERIDAE) IN WILD DUCKS FROM NORTH-WESTERN POLAND

Transkrypt

1 Acta Sci. Pol., Zootechnica 10 (4) 2011, OCCURRENCE OF TETRAMERES SPINOSA (MAPLESTONE, 1931) BAYLIS, 1939 (NEMATODA: TETRAMERIDAE) IN WILD DUCKS FROM NORTH-WESTERN POLAND Agata Stapf, Katarzyna Kavetska, Katarzyna Królaczyk, Bogumiła Pilarczyk West Pomeranian University of Technology, Szczecin, Poland Abstract. Nematodes from the genera Tetrameres (Creplin 1846) are cosmopolitan and polyxenic parasites of birds living inland or associated with aquatic environment. These parasites are characterized by a strong sexual dimorphism and strict topospecificity, limited to the proventriculus of the host. The aim of this paper is the presentation of the morphological and ecological characteristics of T. spinosa rarely observed in Europe (Maplestone, 1931) yet typical for wild birds from the Far East. The examined nematodes were isolated from the alimentary canals of 1005 wild Anatinae (Anseriformes: Anatidae). The parasites were measured using a micrometer eyepiece, and the analysis of the quantitative structure was performed using the following parameters: extensiveness, intensity, relative density, and dominance index. The morphological description of T. spinosa in this paper is generally consistent with known information on the species, although certain differences were observed in the anatomy of some structures near the mouth of the nematode. The nematode was found in 46 out of the 1005 examined ducks (4.6%), and representing the following species: Aythya ferina, A. fuligula, A. marila, Clangula hyemalis and Melanitta nigra. The typical hosts are ducks from the genus Aythya wintering in the southwestern Baltic. Keywords: Anatinae, Nematoda, Tetrameres spinosa INTRODUCTION Nematodes from the Tetrameres genus, Creplin, 1846 (Tetrameridae Travassos, 1914) are widely spread cosmopolitan parasites of almost all groups of birds: both typical land birds, and water birds [Skrjabin et al. 1963, Baruš et al. 1978, Borgarenko 1990, Anderson 2000]. Those parasites are characterised by high topical specificity (they are limited to the glandular stomach) and a strong sex dimorphism. The sexually mature form of the Corresponding author Adres do korespondencji: dr hab. Katarzyna Kavetska prof. nadzw., Department of Biology and Ecology of Parasites, West Pomeranian University of Technology, Szczecin, Doktora Judyma 20, Szczecin, Poland, katarzyna.kavetska@zut.edu.pl

2 116 A. Stapf et al. females is relatively large, and they do not resemble nematodes in outer appearance they are strongly truncated, and owing to a swollen, egg-filled uterus, they become almost spherical, with only slightly protruding, thin and conical anterior and posterior body ends. This strong swelling of the central part of the female s body is the reason why it cannot be mistaken for any other parasite, however, for the same reason, it is also very difficult to isolate it from the stomach gland, in which it resides (the female ruptures and is easily destroyed), as well as to strictly determine its systematic position. The latter is de facto possible only on the basis of the male accompanying the female. The small male residing in the superficial layer of the mucous membrane has a filiform body, distinct crosswise stripes, rows of spines along he body, and a strongly variegated, depending on the species (either large, or small) spicule [Skrjabin et al. 1963, Baruš et al. 1978, Borgarenko 1990]. The life cycle is accurately known only as far a few species of Tetrameres are concerned, w especially T. fissispina (Diesing, 1861) [Garkavi 1947, Czapliński1960, 1962 a, b]. This parasite s intermadiate hosts are aquatic inverterbrates; Daphnia pulex, Gammarus lacustris, G. pulex, G. maeoticus, G. lacustris, and the primary hosts are several dozen of birds from different systematic groups, including domestic birds: ducks geese, hens [Skrjabin et al. 1963, Anderson 2000, Czapliński 1960, Kovalenko 1960]. The primary host is infected by eating a gammarus or a daphnia with invasive larvae, which are released by the digestive influence of gastric acid and drill into the mucous membrane of the glandular stomach and develop into mature, egg-laying female in 18 [Anderson 2000, Czapliński1960]. Kovalenko [1960] indicates a possibility of paratenic host occurence (including fish: Caspialosa brashnikovi maeotica, Lucioperca lucioperca, Neogobius fluviatilis, N. melanostomum, Rutilus rutilus and Scardinius erythrophtalmus). This fact justifies hight occurence rates of these parasites in the Mergini tribe. The pathogenic effect is caused mostly by females, which, by settling deep inside the glands, cause cattarhal inflammmation of the glandular stomach mucous membrane and increased mucus secretion. This causes disturbance in the stomach s physiological function, impairing digestive processes. In consequence, it leads to weakening the bird s system, sometimes even to ravaging the organism and death. The disease is often accompanied by anemia [Czapliński 1960]. According to Czapliński [1960], presence of the parasites is better endured by mature ducks, than by the young ones. However, own observations [Kavetska 2006] indicate, that T. fissispina belongs to parasites considerably more often found in young birds, which is furthermore characterised by high host sex specificity (choosing young duck females). The studies addressing wild duck nematode fauna in Poland, conducted in the late fifties of the previous century, encompassed only south-western regions of the country [Czapliński 1960]. At that time, they indicated the presence of only one species, Tetrameres fissispina (Diesing, 1861), found in a domestic duck Anas platyrhynchos f. dom. And five species of wild ducks (the garganey, the green-winged teal, the mallard, the ferruginous duck and the goosander). Extensivity of occurence of the parasite in the studied bird group amounted to 20.9%, and the intensivity ranged from 1 to 189 [Czapliński 1962 a, b]. The complex studies of the helminth fauna of wild Anatinae in north-western Poland, conducted since 1999 in the Laboratory of Biology and Parasite Zoology on the West Pomeranian Technical University, indicated at least for species of nematodes in those birds Acta Sci. Pol.

3 Occurrence of Tetrameres spinosa (Maplestone, 1931) Baylis, (Tetrameres fissispina (Dresing, 1861) Travassos, 1914, T. pavonis Tshertkova, 1953, T. somateriae Ryzhikov, 1963, T. ryjikovi Chuan, 1961) from the Tetrameres genus, characterised by different prevalence and intensivity of occurence [Kavetska et al. 2003, Kavetska et al. 2004, Kavetska 2005 a, b, c, Kavetska 2006]. As it appears from Kavetska s research [Kovalenko 1960, Kavetska 2005 a, b, Kavetska i Kalisińska 2009], one of the most often recorded parasites in ducks like Aythya fuligula, A. marila, A. ferina i Buephala clangula is T. spinosa (Maplestone, 1931). The aim of this thesis is to conduct a morphological and ecological analysis of T. spinosa (Maplestone, 1931) Baylis, 1939 population in the ducks of north-western Poland. MATERIAL AND METHODS The research material was constituted by nematodes isolated from the gastrointestinal tracts of 1005 wild ducks (Anseriformes: Anatidae), originating from the territory northwestern Poland. The host specimens represented 17 species of 8 genera, belonging to three ecologically different tribes: Anatini (n = 225), Aythyini (n = 413) and Mergini (n = 367). Research conducted over the years encompassed game species (the mallard, the green-winged teal, the common pochard, and the tufted duck; 471 specimens altogether), and species protected by law (other duck species, 534 birds altogether). All birds were (except game mallards) were acquired dead from fishing nets. Isolated nematodes were fixed and stored in 70% ethanol, cleared in glycerine or 80% lactic acid. The parasites were measured using a measuring eyepiece, and species were determined on the basis of the specimens characteristic morphological and anatomical features, with the use of a Zeiss optical microscope; the determination was based on descriptions available in literature. Characteristics of the quantitative structure of the grouping were defined by using parameters of occurence like: extensivity, intensivity of infestation, relative density, and indicator of domination [Pojmańska 1993, Kavetska 2006, 2008]. RESULTS AND DISCUSSION Among nematodes isolated from the birds gastrointestinal tracts, a presence of 1198 nematodes from the Tetrameres genus was noted. They belonged to five species, from which 371 (30.96%) were determined to be Tetrameres spinosa (Maplestone, 1931) Baylis, 1939, 772 (64.44%) T.fissispina, 10 (0.83%) T. pavonis, 43 (3.58%) T. ryjikovi, and 1 (0.083%) T. somateriae. T. spinosa was first described by Maplestone in 1931 [citation from Skrjabin et al. 1963]. In his characteristics, the author included a detailed description of the structures in the frontal section of the body, which surround the mouth and are nearby the bursa. Skriabin [1963], referring to Maplestone s species description, provides information that the parasite s cuticular lips are massive, bilobial in their frontal section, and they have two glands each. Furthermore, the author described triangular chitin plates in the posterior section of Zootechnica 10 (4) 2011

4 118 A. Stapf et al. the lips, connected to the bursa. He also indicated the presence of oblong structures starting at the basis of the lips and continuing down the body in lateral wings [citation from Skrjabin et al. 1963]. The presence of these structures created doubts about qualifying this nematode to the proper genus. Initially, T. spinosa was assigned to the Echinuria genus, according to Maplestone s suggestion. However, according to Baylis, the oblong forms do not resemble real bands characteristic for the Echinuria genus. That is why the author of the species moved this nematode to the Tetrameres genus. According to Maplestone s description, spines on the parasite s body are placed in four rows, and their size and the number of rows decrease towards the posterior end of the body. The longer spicule has a clear, spherical swelling in the proximal part, and in the distal part it is narrowed and has a shoe shaped ending [citation from Skrjabin et al. 1963]. Another description of Tetrameres spinosa was presented in 1990 by Borgarenko [Borgarenko 1990]. The morphological characteristics given by this author is significantly shorter than Maplestone s description; it mostly consistent with it, with just one difference. Borgarenko [1990] indicates, that the spines are placed on the body densely and without any order, and their size decreases towards the tail. Furthermore, the author noticed, that the proximal part of the long spicule has a groove in it, and its distal part, just like in Maplestone s work, was compared to the shape of a shoe. The parasite s dwelling place is typical for all Tetrameres. The females settle in glands, and the males in the mucous secretion of the host s organ. Males surrounded by mucus are very slightly visible against the background of the organ. Owing to the importance of the females, caused by freezing the research material in smaller studies, the parasite species was determined on the basis of the male s characteristic features, such as: the shape and placement of the lips, shape of the bursa, length and width of the spiculae, and the size and placement of the spines. Description of T. spinosa in this thesis is slightly different from the works of other authors. No massive, bilobial lips with two glands each, or triangular plates were noticed in the researched material, and those elements were observed by Maplestone in his material. The researched males have milk-coloured bodies with a mean length of µm (Table 1). The mouth is surrounded by pseudolips, and, because of specimen quality, neither cephalic papillae, nor the secretory orifice were noticed. The bursa is short, rather untypically shaped. It is significantly widened right next to its border with the pharynx. The walls of the bursa are thick and distinct. Furthermore, cephalic wings with longitudinal bands are visible, one on each side of the body (Fig. 1). The overall length of the pharynx is on average µm. The glandular part of the pharynx is clearly longer and wider (on average 52.9 µm). In the posterior part of the body of the male there are two spiculae. These structures differ diametrically by size and shape. The longer spicule (with an average length of µm) is quite narrow, even though it has some uneven edges with a mace-shaped swelling on its proximal end. The distal end of the spicule has a pointed ending and it is shaped like the characteristic shoe. The smaller spicule is almost five times smaller from the long spicule (average 91.3 µm) and it resembles a straight stick of an even girth (Fig. 2). Both ends of the male s body are sharply ended. The whole body is covered with cuticular spines, which tend to decrease in length towards the tail. In the posterior part of the body the spines are the biggest and they are placed rather chaotically. The tail of the parasite is straight and very sharply ended. Acta Sci. Pol.

5 Occurrence of Tetrameres spinosa (Maplestone, 1931) Baylis, Table 1. Morphological description of male Tetrameres spinosa, µm Tabela 1. Charakterystyka morfometryczna samca Tetrameres spinosa, µm Measurement Skrjabin and Sobolev Pomiar [1963] Length of body Długość ciała Width of body (max) Największa szerokość ciała Width of body at buccal capsule Szerokość ciała na wysokości torebki gębowej Width of body at smal spicule Szerokość ciała na wysokości małej spikuli Depth of buccal capsule Długość torebki gębowej Width of buccal kapsule Szerokość torebki gębowej Thickness of wall buccal capsule Grubość ścianki torebki gębowej Length of spines on anterior body end Długość kolców na przednim końcu ciała Length of spines on posterior body end Długość kolców na tylnym końcu ciała Length of muscular oesophagus Długość gardzieli mięśniowej Width of muscular oesophagus Szerokość gardzieli gruczołowej Length of glandular oesophagus Długość gardzieli gruczołowej Width of glandular oesophagus Szerokość gardzieli gruczołowej Length of large spicule Długość dużej spikuli Width of posterior part of large spicule Szerokość dużej spikuli (część dystalna) Width of anterior part of large spicule Szerokość dużej spikuli (część proksymalna) Length of small spicule Długość małej spikuli Width of small spicule Szerokość małej spikuli Borgarenko [1990] Own material Materiał własny ( ) ( ) 51.0 (45 63) 62.4 (54 75) (18 36) (10 20) (3.6 6) ( ) (7.2 15) ( ) (20 40) ( ) (40 70) ( ) (9 14.4) (10 20) (63 190) (3 7.2) Zootechnica 10 (4) 2011

6 120 A. Stapf et al. Ecological analysis T. spinosa is a very rarely noted parasite of wild ducks in Central and Southern Asia [Skrjabin et al. 1963, Borgarenko 1990]. Its typical host is Aythya ferina [Skrjabin et al. 1963, Borgarenko 1990, Kavetska 2006, 2005 a, b, c], although in Central Asia (Tajikistan, Kazakhstan, Turkmenistan, Azerbaijan) it was also noted in Anas penelope, Netta rufina, and Aythya fuligula [Borgarenko 1990]. In our research this nematode was found in Aythya ferina, A. fuligula, A. marila, Clangula hyemalis and Melanitta nigra (Table 2). The parasite s presence in Europe (Poland) was previously reported in our own works [Kavetska 2006, 2005 a, b, c, 2008, Kavetska and Kalisińska 2009]. Only the presence of T. spinosa in Ukraine remains arguable. The nematode s occurence in this part of Europe was reported by Kurasvili [1983]. The author indicates the existence of T. spinosa synonyms, which are: Tetrameres asiatica (Merdivenci, Buyurman, 1965) and Tetrameres crami asiatica Ryjikov, 1963 [Kurashvili et al. 1983]. Based on the species characteristics of T. spinosa included in the work of Skrjabin [1963] and Borgarenko [1990] we cannot agree with this statement. T. crami asiatica males have the largest spines in the anterior part of the body, placed close of each other. The large spicule has diagonally cut ends, and a swelling resembling a stomach in its central part [Skrjabin et al. 1963]. Table 2. Ecological description of population T. spinosa in examination ducks Tabela 2. Charakterystyka ekologiczna populacji T. spinosa u badanych kaczek Host Żywiciel Extensivity Ekstensywność Intensivity Intensywność zarażenia Relative density Względne zagęszczenie Indicator of domination Wskaźnik dominacji n % range zakres mean value średnia Aythya ferina. n = A. fuligula. n = A. marila. n = Clangula hyemalis n = Melanitta nigra. n = The ecological characteristics of the species are shown in Table 2. The nematode was noted in 46 out of 1005 examined ducks (4.6%). The highest occurence rates were noticed for ducks from the Aythyini tribe: the tufted duck, and the greater scaup. As far as the greater scaup (A. marila) is concerned, T. spinosa appears to be a subdominant species (WD>0.1), which relative density amounted to In the helminth fauna of other host species, the analysed parasite is a rare species (the domination indicator WD did not exceed 0.1). The biggest range of intensivity of infestation by the researched parasite (from 1 to 87 specimens) was found in the greater scaup population. It was observed, that the nematode quite numerously occurs in the Aythyini tribe ducks, which is confirmed by Acta Sci. Pol.

7 Occurrence of Tetrameres spinosa (Maplestone, 1931) Baylis, the means of intensivity in Table 2. The research results therefore indicate, that in Europe T. spinosa is typical for the diving ducks (Aythyini) spending the winter in this area and it probably does not close its life cycle here. Fig. 1. Interior body end of male Tetrameres spinosa Maplestone, 1931 (scale bar: 100 µm) Rys. 1. Przedni odcinek ciała samca Tetramers spinosa Maplestone, 1931 (skala: 100 µm) Fig. 2. Posterior body end of male Tetrameres spinosa Maplestone, 1931 (scale bar: 100 µm) Rys. 2. Tylny odcinek ciała samca Tetrameres spinosa Maplestone, 1931 (skala: 100 µm) CONCLUSIONS To sum up, can say that, our execute description of nematodes, combine various characteristic which done by two autors, Borgarenko and Maplestone. While it remain in contradiction with description of T. crami asiatica as synonym. Remains unknown if morphological difference are a result of ontogenetic changeability or it prove about new species. This unclears suggest to replicate research on wider material and execute genetic analysis. Zootechnica 10 (4) 2011

8 122 A. Stapf et al. REFERENCES Anderson R.C., Nematode parasites of vertebrates. Their Development and Transmission. CABI Publishing, Wallingford. Baruš V., Sergejeva T.P., Sonin M.D., Ryzhikov K.M., Helminths of fish-eating birds of the Palaearctic region. I. Nematoda. USSR Academy of Sciences. Helminthological Laboratory Czechoslovak Academy of Sciences. Institute of Parasitology, Moscov. Borgarenko L.F., Gel minty ptic Tadžikistana [Birds helmints from Tajikistan]. T. 3. Nematody. Doniš, Dušanbe [in Russian]. Czapliński B., Robaczyce drobiu i ich zwalczenie [Poultry s helminthiasis and their fight]. PWN, Warszawa [in Polish]. Czapliński B., 1962 a. Nematodes and acanthocephalans of domestic and wild Anseriformes in Poland. II. Nematoda (excl. Amidostomum) and Acanthocephala. Acta Parasitol. Pol. 10, Czapliński B., 1962 b. Nematodes and acanthocephalans of domestic and wild Anseriformes in Poland. III. General comment. Acta Parasitol. Pol. 10, Garkavi B.L., Cikl razwitja Tetrameres fissispina [Life cycle of Tetrameres fissispina]. Dokl. AN CCCP. 64, [in Russian]. Kavetska K.M., 2005 a. Nematodofauna krohalepodobnyh (Anatinae: Mergini) severo-zapadnoj Pol ši [Fauna of nematode Sea ducks (Anatinae: Mergini) from north-west Poland]. Vestn. Zool. (Suppl.) 19 (I), [in Russian]. Kavetska K.M., 2005 b. Nicienie przewodu pokarmowego grążyc (Aythyini) z terenu Pomorza Zachodniego [The intenstinal nematodes of diving ducks (Aythyini) from West Pomerania region]. Wiad. Parazytol. 51, [in Polish]. Kavetska K.M., 2005 c. The intestinal nematodes of wild ducks (Anatinae) from North-West region of Poland. Wiad. Parazytol. 51, Kavetska K.M., Biologiczne i ekologiczne uwarunkowania kształtowania się struktury nematofauny przewodu pokarmowego dzikich kaczek (Anatinae) w północno-zachodniej Polsce [Biological and ecological background of namatode fauna structure formation in the alimentary tracts of Wild Anatinae ducks in northwestern Poland]. Rozpr. hab AR, Szczecin [in Polish]. Kavetska K.M., Nematofauna of duck of the genus Melanitta (Mergini, Anseriformes) from the south Baltic Sea. Wiad. Parazytol. 54, Kavetska K.M., Kalisińska E., Nicienie z rodzaju Tetrameres, Creplin 1846 u dzikich kaczek (Anatinae) Północno-zachodniej Polski [Nematodes from genus Tetrameres Creplin 1846 in wild ducks (Anatinae) north-west Poland]. XVIII Wrocławska Konferencja Parazytologiczna Różnorodność oddziaływania układów pasożyt żywiciel w środowisku maja 2009, Wrocław Karpacz [in Polish]. Kavetska K.M., Kalisińska E., Kornyushin V.V., Nematody želudka dikih utok (podsemejstvo Anatinae) s Severo-Zapadnoj Pol ši v ekologičeskom aspekte (in: Problemy sovremennoj parazitilogii) [Nematodes of stomach wild ducks from north-west Poland in ecological aspect]. Meždunarodnaâ konferenciâ i III s ezd Parazitologičeskogo obŝestva, Petrozavodsk, Respublika Kareliâ, 6 12 Oktâbrâ 2003, Sankt-Peterburg, [in Russian]. Kavetska K.M., Kalisińska E., Kornyushin V.V., Kuzmin Yu., Stomach nematodes of wild ducks (subfamily Anatinae) from Northwestern Poland. Acta Parasitol. 49, Acta Sci. Pol.

9 Occurrence of Tetrameres spinosa (Maplestone, 1931) Baylis, Kovalenko I.I., Study of the life cycles of some helminthes of domestic ducks from farms on Azov coast. Doklady Academii Nauk SSSR 133, Kurashvili B.E. (Ed.), Nematodes and acanthocephalans of birds of Black Sea and Caspian Sea Regions. Tbilisi, Mecnierba. Pojmańska T., Przegląd terminów ekologicznych stosowanych współcześnie w parazytologii [Survey of ecological terminology nowadays applied in parasitology]. Wiad. Parazytol. 39, [in Polish]. Skrjabin K.I., Sobolev A.A., Spiruraty životnyh i čeloveka i vyzyvaemye imi zabolevaniâ [Spirurata animals and humans and cause of the disease]. Akademiâ Nauk SSSR, Moskva [in Russian]. WYSTĘPOWANIE TETRAMERES SPINOSA (MAPLESTONE, 1931) BAYLIS, 1939 (NEMATODA: TETRAMERIDAE) U DZIKICH KACZEK PÓŁNOCNO-ZACHODNIEJ POLSKI Streszczenie. Nicienie z rodzaju Tetrameres (Creplin, 1846) to kosmopolityczne i polikseniczne pasożyty ptaków zarówno lądowych jak i związanych ze środowiskiem wodnym. Pasożyty te charakteryzuje daleko posunięty dymorfizm płciowy oraz ścisła topospecyficzność, ograniczona do żołądka gruczołowego żywiciela. Celem niniejszego opracowania jest przedstawienie charakterystyki morfologicznej i ekologicznej rzadko notowanego w faunie Europy gatunku z tego rodzaju, T. spinosa (Maplestone, 1931), pasożyta dzikich Dalekiego Wschodu. Materiał do badań stanowiły nicienie wyizolowane z przewodów pokarmowych 1005 dzikich Anatinae (Anseriformes: Anatidae). Pasożyty utrwalano i przechowywano w 70-procentowym alkoholu etylowym, a prześwietlano w glicerynie lub 80-procentowym kwasie mlekowym. Do pomiarów pasożyta zastosowano okular pomiarowy, a charakterystykę struktury ilościowej zgrupowania określono wykorzując podstawowe parametry występowania, takie jak: ekstensywność, intensywność, względne zagęszczenie oraz wskaźnik dominacji. Przedstawiony w niniejszej pracy opis morfologiczny T. spinosa odpowiada w znacznej mierze charakterystyce gatunku, jakkolwiek zanotowano pewne różnice w budowie niektórych struktur występujących blisko otworu gębowego. Nicienia zanotowano u 46 spośród 1005 zbadanych kaczek (4,6%) reprezentujących następujące gatunki: Aythya ferina, A. fuligula, A. marila, Clangula hyemalis i Melanitta nigra, jednak typowymi żywicielami są kaczki z rodzaju Aythya zimujące na południowo-zachodnim Bałtyku. Słowa kluczowe: Anatinae, Nematoda, Tetrameres spinosa Accepted for print Zaakceptowano do druku: Zootechnica 10 (4) 2011