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Acta Sci. Pol., Zootechnica 10 (4) 2011, 115–124
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, 71-466 Szczecin, Poland, e-mail: [email protected]
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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.
Occurrence of Tetrameres spinosa (Maplestone, 1931) Baylis, 1939...
117
(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 1999–2009 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 13 333 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
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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 3829.5 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 956.9 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 413.8 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.
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Occurrence of Tetrameres spinosa (Maplestone, 1931) Baylis, 1939...
Table 1. Morphological description of male Tetrameres spinosa, µm
Tabela 1. Charakterystyka morfometryczna samca Tetrameres spinosa, µm
Measurement
Skrjabin and Sobolev Borgarenko Own material
Pomiar
[1963]
[1990]
Materiał własny
Length of body
3829.5
4700
2680–3930
Długość ciała
(2680–4680)
Width of body (max)
120–400
90–140
124.8 (87.5–150)
Największa szerokość ciała
Width of body at buccal capsule
Szerokość ciała na wysokości torebki
51.0 (45–63)
gębowej
Width of body at smal spicule
Szerokość ciała na wysokości
62.4 (54–75)
małej spikuli
Depth of buccal capsule
32
20–30
26.4 (18–36)
Długość torebki gębowej
Width of buccal kapsule
20
10–20
15.1 (10–20)
Szerokość torebki gębowej
Thickness of wall buccal capsule
6
4.5 (3.6–6)
Grubość ścianki torebki gębowej
Length of spines on anterior body end
19–30
21.7 (17.5–30)
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
Zootechnica 10 (4) 2011
H
320
1000
400
44
10–15
9.5 (7.2–15)
140–300
313.4 (140–400)
20–40
26.6 (20–40)
430–780
643.5 (430–780)
40–70
52.9 (40–70)
360–410
413.8 (360–475)
10
11.1 (9–14.4)
20
17.0 (10–20)
70–190
91.3 (63–190)
3
5.6 (3–7.2)
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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
Aythya ferina. n = 20
A. fuligula. n = 236
A. marila. n = 157
Clangula
hyemalis n = 112
Melanitta
nigra. n = 108
Extensivity
Ekstensywność
Intensivity
Intensywność
zarażenia
Relative Indicator
of
density
domination
Względne
zagęszczenie Wskaźnik
dominacji
5.0
11.9
8.3
range
zakres
11
1–23
1–87
mean value
średnia
11.0
3.4
15.0
0.55
0.40
1.24
0.0275
0.0478
0.1028
1
0.9
67
67.0
0.60
0.0053
3
2.8
4–7
5.0
0.14
0.0038
n
%
1
28
13
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 1.24. 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
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Occurrence of Tetrameres spinosa (Maplestone, 1931) Baylis, 1939...
121
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)
CONCLUSIONS
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)
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.
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A. Stapf et al.
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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: 3.11.2011
Zootechnica 10 (4) 2011