ISSN 0704-3716
Canadian Translation of Fisheries and Aquatic Sciences
No. 5618
On the parasitic worms of mammals and birds of the USSR
A.I. Krotov and S.L. Delamure
Original title:
In:
K
faune
paraziticheskikh
mlekopitayushchikh i ptits SSSR
chervei
Trudy gelmintologicheskoi laboratorii (Transactions of the
Helminthological Laboratory of the USSR Academy of Sciences;
vol. 6, pp.278-292; 1952
Original language: Russian
Available from:
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National Research Council
Ottawa, Ontario, Canada KlA 0S2
1994
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N. De.
Trudy gelmintologicheskoi laboratorii, Akad. nauk SSSR [Transactions of the Hehninthological
Laboratory of the USSR Academy of Sciences], 1952, v. 6, pp. 278-292
On the parasitic worms of mammals and birds of the USSR
by A.I. 'Crotoy and S.L. Delamure
Sakhalin branch of the USSR Academy of Sciences, in addition to studying
the helminth fauna of the vertebrates of Sakhalin Is., also examined the helminths
of the ocean mammals and birds that breed on the Sakhalin coast and the adjacent
Tyuleniy and Moneron islands or stop there during their migrations.
Helminthological dissections of fur seals were carried out by G.V. Bobrovaya,
the helminths of birds from Moneron Is. were collected by N.L. Kovalevskaya, and
the rest of the dissections were carried out by A.I. Krotov. A total of 250 animals
belonging to 27 species (5 mammals, 22 birds) was dissected by the method of
Academician K.I. Skryabin, and in these animals we recorded 36 species of parasitic
The
worms.
The following are the identification
other important information.
results, the descriptions of new forms and
MAMMALS
I. Beluga Delphinapterus leucas Pallas
-
some fishermen caught two young belugas in Aniva Bay. Both
animals were found to be infested with helminths belonging to four species.
On 26 May 1949,
2
Leucasiella mironovi n. gen. n. sp.
(Fig. 1)
Eighty-four trematodes were discovered in the middle part of the small
intestine of one of the belugas. They were identified as belonging to the family
Campulidae (Milner, 1926, subfamily Campulinae Stunkard et Alvey, 1929. These
trematodes proved to be representatives of a new genus which we have named
Leucasiella n. gen.
Di agn osis o f gen u s. Campulinae with elongate body flattened
dorsoventrally. Oral sucker somewhat larger than ventral one. Intestine with two
caeca directed towards base of oral sucker. Lateral and median intestinal processes
usually absent. Genital pore opens medianly, directly in front of ventral sucker.
Genital bursa larger than diameter of ventral suc.ker, contains large prostate glands.
Cirrus and metraterm without armature. Sex glands behind ventral sucker. Testes
entire, one behind the other lengthwise or across the body. Ovary entire, in front of
testes. Mehlis' gland present. Vitellaria represented by minute scattered follicles
which occupy 2/3 of body, extend to posterior boundary or to middle of front testis,
but never to ventral sucker. Eggs triangular in cross-section.
Instestinal parasites of cetaceans.
Di ff er en ti al di agn o si s. The absence of an armed cirrus distinguishes
our genus from the genera Synthesium Stunkdard et Alvey, 1929, Orthosplanchnus
Odhner, 1905, Oschmarinella Skrjabin, 1947, and Odneriella Skrjabin, 1915.
The new genus is differentiated from the genus Synthesium by entire testes
and the absence of armature on the metraterm; from the genus Orthosplanchnus by
entire testes and the absence of armature on the cuticle of the entire body; from the
genus Oschmarinella by the presence of armature on the cuticle and the presence of
a prepharynx; from the genus Odhneriella by the absence of a rosette-like distribution of the vitelline glands.
The new genus is distinguished from the genera Lecithodesmus Braun, 1902,
Zalophotrema Stunkard et Alvey, 1929 and Campula Cobbold, 1858, which also have
no armature on the cirrus, by the following characteristics: from Lecithodesmus by
the absence of lobulation in the ovary and the absence of rectangular groups of vitelline follicles; from Zalophotrema by the absence of lobulation in the ovary and the
presence of a triquetrous form in the eggs; from Campula by the absence of lateral
intestinal processes and also by weakly developed vitelline glands which, as we
3
•
know, extend to the pharynx in the genus Cam pula and not past the middle of the
front testis in the new genus.
Description of species.
Elongate body up to 8.90-12.89 mm long with
maximum width of 0.725-1.250 mm, at level
of ventral sucker 1.326 mm. Transverse
constriction varying in definition present in
region of uterus and testes; body gradually
narrows towards anterior and posterior ends
of body. Cuticle of anterior one-third of body
armed with spines about 0.040 mm long. Oral
sucker occupies terminal position; 0.350-1.000
x 0.525-1.150 mm with depth of 0.534 mm.
Ventral sucker in anterior third of body;
diameter 0.625-1.000 x 0.625-0.800 mm.
Prepharynx 0.276 mm long, pharynx 0.2750.375 x 0.275-0.400 mm. Esophagus very short.
Anterior part of intestine on each side of
pharynx forms one diverticulum directed
towards oral sucker; remaining part of intestine does not usually form lateral or median
processes. Only some individuals have small
median diverticula in region of uterus.
Intestinal trunks terminate 0.050-0.125 mm
from posterior end of body. Excretory pore
occupies terminal position.
Genital pore occupies median position,
near anterior margin of ventral sucker.
Genital bursa overlaps boundary of posterior
margin of ventral sucker. Cirrus without
armature; large prostate glands in genital
bursa. Testes arranged one behind the other
lengthwise or right to left from median line
Fig. 1. Leucasiella mironovi nov. gen. n. sp.
4
of body at the end of its first one-third; entire, oval. Front testis 0.625-0.865 x 0.2250.350 mm, posterior one 0.525-0.975 x 0.250-0.460 mm. Ovary round or slightly oval,
0.125 x 0.275 mm long; lies in front of testes, with Mehlis' gland to the side of it.
Vitellaria represented by individual minute follicles (0.035 mm in diameter) which
occupy entire posterior part of body and extend anteriorly to posterior boundary of
front testis or to its middle. Uterus consists of small number of loops which lie
between ovary and ventral sucker. Eggs oval, 0.072-0.092 x 0.033-0.037 mm, triangular in cross-section.
Stenurus minor (Kühn, 1829)
More than 1000 specimens of this species were found in the nasal passages and
frontal sinuses of one animal.
Anisakis kükenthalii (Cobbold, 1889) Baylis, 1920
This species was redescribed by Mozgovoi (1949) from material taken from a
beluga in the Sea of Okhotsk (near Nikolayevsk). Both Mozgovoi and the authors
before him indicate that A. kükenthalii become localized in the stomach. In belugas
dissected in Aniva Bay, A. kükenthalii were found in both the stomach and esophagus (perhaps the helminths got into the esophagus after they died); from 200 to 300
of these parasites were recorded in each animal.
Corynosoma strumosum (Rudolphi, 1802)
These parasites were found in the small intestine of both belugas (35 and 84
specimens respectively).
H. Kurile fur seal
-
Callorhinus ursinus curilensis Jord et Clark
Forty-six fur seals were dissected on Tyuleniy Is. in July and August 1949, and
thirty of them were found to be infested. Nematodes were recorded in 28 of the
animals, cestodes in 20, and acanthocephalans in 2.
All of the underyearling fur seals (2-3 months old) proved to be sterile (8 dissected). Out of 38 adults, only eight were not infested with helminths. Six species of
5
helminths were found in the fur seals; this does not include the anisakid larvae
which could not be identified to the species.
Diphyllobothrium hians (Diesing, 1850)
These tapeworms were iecorded in 20 fur seals; they were localized near the
caecum in the small and large intestine. The number of parasites varied from 2 to 5.
Diphyllobothrium sp.
One specimen of this parasite was found in the small intestine of two animals.
Terranova (Terranova) decipiens (Krabbe, 1878) Baylis, 1920
From 1 to 71 of these nematodes were found in 14 animals. They were
localized in the pyloric part of the stomach, their anterior end embedded in its
mucosa. The stomachs of fur seals infested with T. decipiens were usually characterized by severe hemorrhagic inflammation.
T. decipiens from the Kurile fur seal is much larger than the previously
described specimens of this species, and therefore we have included their basic
measurements (in mm) here (see table on p. 282).
Anisakidae sp. (larvae)
From 20 to 300 larvae of these helminths were found primarily in the stomach,
but they were also encountered in both the small and the large intestine. Eighteen
animals were found to be infested with anisakid larvae. We have reason to believe
that these larvae included the young of Contracoecum osculatum.
Bolbosoma nipponicum Yamaguti, 1939
Six specimens of this species were found in the small intestine of one fur seal.
Yamaguti described this species from the toothed whale (Balaenoptera acutirostrata
Lecepede) of the Pacific Ocean. Our specimens fit Yamaguti's description of the
species, but they are differentiated by an extra spine per row, and by a more constant
number of rows of spines on the proboscis.
6
According to Yamaguti, there are 5-6 (mostly 6) spines in each of the 17-23
longitudinal rows; according to our material (from a fur seal, a ringed seal and a
black-tailed gull), there are 6-7 spines in each row on the proboscis, and there are 2022 longitudinal rows in all the worms. The following are the measurements of the
spines on the proboscis in B. nipponicum (in mm).
Size of spines on proboscis in Bolbosoma nipponicum (in mm)
Spines
I
II
III
IV
V
VI
Free part
length I width
Root
length I width
0.089
0.089
0.080
0.075
0.075
0.048
0.053
0.097
0.084
0.086
0.066
0.040
0.010
0.026
0.026
0.026
0.022
0.013
0.013
0.026
0.026
0.031
0.026
0.022
Bolbosoma bobrovi n. sp.
(Fig. 2)
One animal was found to contain four acanthocephalans of this new species.
Description of species. Acanthocephalans 8 mm long, coiled in a
spiral, orange. Anterior bulbous part of body reaches 1.042 mm in width, remaining
part of body 0.47 mm wide. Bulbous part of body densely covered with large spines
0.067 mm long and 0.033 mm wide; spines with double contour at base. Proboscis
0.459 mm long with width of 0.333 mm; sheath of proboscis 0.833 mm long with
width of 0.375 mm. Proboscis armed with spines arranged in 14-16 longitudinal
rows, 4-5 spines in each. First four spines well-developed, 5th spine very small.
Measurements of spines given in table below.
Differential diagnosis.The new species is similar to Bol bosoma
turbinella (Diesing, 1851), Porta, 1908 and B. nipponicum Yamaguti, 1939 in the
number and distribution of spines on the proboscis; they have 20-22 longitudinal
rows of spines with 6-7 spines in each row. However, our species differs sharply
even from these similar species. For example, B. bobrovoi has only 14-16 longitudinal rows of spines with 4-5 spines in each row. Another characteristic feature is
that the last (4th or 5th) spine in each row is 4-5 times smaller than the rest of the
spines on the proboscis.
7
i
Cs- .
gird,
Fig. 2. Bolbosoma bobrovoi n. sp.
as
8
Size of spines on proboscis in Bolbosoma bobrovoi (in mm)
Spines
II
III
Iv
V
Free part
1,g
1 th I width
Root
length I width
0.089
0.073
0.067
0.061
0.017
0.055
0.061
0.055
0.067
0.066
0.017
0.015
0.022
0.017
0.022
0.022
0.022
0.028
0.028
0.026
III. Northern sea-lion - Eumetopias jubatus Schreber
Three adult northern sea-lions were dissected. Four species of helminths (not
including anisakid larvae) were found in two animals. Two of the northern sealions were caught on Tyuleniy Is. in September, and the third one was taken in
Chaisky Bay in December.
Pyramicocephalus phocarum (Fabricius, 1780)
Two tapeworms of this species were found in the small intestine of one
northern sea-lion
Anophryocephalus sp.
One cestode was found in the small intestine of one animal (this was the first
time a cestode was recorded in a northern sea-lion).
Anisakidae sp. (larva)
Approximately 3000 larvae were found in the large intestine of one northern
seal-lion, and more than 2500 larvae in another one.
Bolbosoma bobrovoi n. sp.
Twenty-six of these acanthocephalans were found in the small intestine of one
northern sea-lion.
Basic measurements of T. decipiens (in mm)
Characteristics
Length of body
Maximum width
Length of esophagus
Length of stomach
Length of intestinal processs
Dorsal lip
Lateroventral lip
Distance from vulva to head end
Length of spines
Size of eggs
According to Mozgovoi (1948)
from Erienatus barbatus
male
I female
43-53
42-64
1.33-1.40
1.48-1.89
3.20-3.33
3.67-4.33
1.01-1.17
1.07-1.39
1.56-1.76
0.181-0.247x 0.181-0.256x
x0.119-0.241 x0.192-0.267
0.173-0.232x 0.181-0.245x
x0.180-0.229 x0.181-0.256
26.5
2.23-2.68
0.046-0.055
Our own data
from Phoca hispida
male I female
I
I
from Callorhinus ursinu
male
J female
45.0
50.0
1.35
1.65
3.20
3.37
1.00
1.22
1.49
2.56
0.250x0.259 0.257x0.276
57.0
88.0
1.65
2.80
3.69
5.88
1.64
1.80
2.02
2.21
0.221x0.202 0.278x0.278
0.230x0.230 0.202x0.221
0.220x0.190 0.278x0.250
24.0
2.41
3.80
2.704-2.912
0.048
0.055-0.060
10
Corynosoma strumosum (Rudolphi, 1802)
Thirty-five specimens of this parasite were found in one northern sea-lion.
IV. Okhotsk ringed seal Phoca hispida ochotensis Pallas
-
A total of 15 ringed seals was dissected; two of them were adults and 13 were
juveniles from one to three years of age (predominantly two-year-olds). Both of the
adults were highly infested with nematodes and cestodes. Four of the young seals
proved to be sterile, and the rest were infested mainly with acanthocephalans (C.
strumosum). A total of 8 species of helminths was recorded in the seals. Nine of the
seals were caught in Aniva Bay in December, and the rest in Chaisky Bay in
November.
Diphyllobothrium lanceolatum (Krabbe, 1865)
255 and 150 specimens of this species were found in the small intestine of two
ringed seals.
Pyramicocephalus phocarum (Fabricius, 1780)
620 and 805 specimens of this species were found in the small intestine of two
adult seals.
Trigonocotyle sp.
One specimen was found in the small intestine of a two-year-old ringed seal.
Contracaecum osculatum (Rudolphi, 1802) Baylis, 1920
357 and 3437 specimens of this helminth were recorded in adult ringed seals,
and six specimens were found in one two-year-old. The parasites were localized in
the stomach and esophagus. Our specimens are distinguished from the typical form
by a larger number of caudal papillae (11-18 pairs more).
•
,
,
11
Terra nova (Terranova) decipiens (Krabbe, 1878) Baylis, 1920
219 and 2 specimens of this parasite were found in two adult ringed seals. One
specimen was found in a two-year-old.
Anisakidae sp. (larva)
One larva was found in each of two young ringed seals.
Corynosoma strumosum (Rudolphi, 1802)
From 3 to 33 specimens of this helminth were found in the small intestine of
nine ringed seals.
Cor ynosoma sp.
33 and 10 specimens were found in two adult ringed seals.
Bolbosoma nipponicum Yamaguti, 1939
Two acanthocephalans were localized in the small intestine of one adult
ringed seal.
V. Bearded seal Erignathus barbatus nauticus Pallas
-
One animal caught in Chaisky Bay in December was dissected. Several
thousands of Terra nova (terranova) decipiens (Krabbe, 1879) Baylis, 1920 were found
in its stomach.
.
12
References
1. Afanasyev V.P. 1941. The parasite fauna of the commercial mammals of the Commander IsIs.
Uch. zap. Leningr. Gos. un-ta, ser. biol., 74, 13: 93-117.
2. Vasilkova Z.G. 1926. On the nematodes of gulls and terns of Kazakhstan. Tr. Gos. in-ta
eksper. veterinarii, 4, 1: 105-113.
3. Gushanskaya L.Kh. 1950. On the cancellation of the tribe Antennocarea and the genus
Antennocara. Tr. Gelm. laboratorii AN SSSR, IV: 53-54.
4. Markov G.S. 1941. Parasitic worms of Bezymyannaya Bay (Novaya Zemlya). DAN SSSR, 30,
6: 573-576.
5. Mozgovoi A.A. 1948. Contribution to the study of anisakids of cetaceans. Tr. Gelm. laboratorii
AN SSSR, II: 26-40.
6. Mozgovoi A.A. 1950. New anisakids of birds. Ibid., III: 90-101.
7. Oshmarin P.G. 1950. On the helminths of birds of the Far East. Ibid., III: 166-179.
8. Skryabin K.I. 1942. Paths of phylogenetic evolution in nematodes of the family Pseudaliidae,
parasites of the hearing organs, circulatory system and respiratory tract of marine mammals. DAN
SSSR, 37, 1: 41-46.
9. Skryabin KJ. 1948. Trematodes of Animals and Humans. Moscow-Leningrad, H: 129 158.
-
10. Meggit F. 1924. The Cestodes of Mammals. London, pp. 109-139.
11. Railliet A. et Henry. 1912. Helminthes recueillis par l'expedition antarctique francaise du
Pourquoi-pas? II. Cestodes de Phoques. Bull. Mus. Hist. Nat., pp. 153-159.
12. Stundard H.W. 1948. Pseudaphyllidean cestodes from Alaskan pinnipeds. J. Parasitol., 34 (3):
211-228.
13. Yarnaguti S. 1939. Studies on the helminth fauna of Japan. Part 29. Acanthocephala II. Jap. J.
Zool., 8: 317-352.