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0090-3558-21 1 11 PDF
0090-3558-21 1 11 PDF
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ABSTRACT: Infective larvae of Dioctophyrna renale were found in the hvpaxial musculature of
pumpkinseed (Lepomis gibbosus L.) from three lakes in Algonquin Provincial Park, Ontario,
Canada. This represents the first report of D. renale in centrarchid fish. In the three lakes surveyed
prevalence and mean intensity ranged from 5 to 23% and one to two larvae respectively. Larvae
elicited a mild granulomatous reaction in pumpkinseed. Two ferrets were each given five larvae
from pumpkinseed. Adult D. renale were recovered from the right kidney capsule of ferrets 108
and 134 days post-infection. An opening in the ventral surface of the right kidne’ capsule ‘as
present in one ferret. Chronic peritonitis was associated with eggs of D. renale and cellular debris
which probably entered the abdominal cavity from the right kidney capsule.
11
cohol). Larvae were cleared by allowing the ver (Castor canadensis Kuhl) activity facilitat-
alcohol to evaporate. ed movement of these fish from Border Lake
Encapsulated larvae in muscle were fixed in to Ryan Lake. It is unknown how pumpkinseed
Gendre’s fluid (Humason, 1972) or in 10% buff- re-entered Billy Lake. Lake Sasajewun was cre-
ered formalin. Tissue was then prepared for ated by damming the North Madawaska River
histologic examination using standard proce- in the early 1900’s. Lake Sasajewun has not been
dures. Sections were cut at 6 gm and stained treated with toxicants or stocked with fish.
with hematoxylin and eosin. Mallory’s phos-
phomolybdic acid hematoxylin stain (Mallory, RESULTS
1942) was used to detect collagen in capsules.
Two male ferrets (A and B) were purchased Examination of fish
from Marshall Research Animals, Inc. (North Larval Dioctophyma renale were found
Rose, New York 14516, USA). At 14 wk of age
in pumpkinseed from Ryan Lake, Billy
each ferret was given five larvae of D. renale
encapsulated in muscle of pumpkinseed col- Lake and Lake Sasajewun. One specimen
lected from Billy Lake in October. Food was of D. renale was also found on the stom-
withheld from ferrets 10-12 hr prior to infec- ach wall in one of 16 brown bullheads
tion. Ferrets were kept in an outdoor enclosure from Lake Sasajewun. There was no dif-
and given water and Co-op Purrfect Catfood
ference in prevalence between male and
(United Co-operatives of Ontario, 151 Center
City Drive, Mississauga, Ontario L5A 3A4, female pumpkinseed in each lake sam-
Canada) ad lib. Diet was supplemented with pled (x2. P < 0.05, df = 1). Similarly there
lard, cooked liver and cooked fish. Patency was was no difference in prevalence between
determined by weekly examination of urine for male pumpkinseed in each lake and be-
eggs of D. renale. Ferrets were killed with an
tween female pumpkinseed in each lake
intracardiac injection of Somnotol (MTC Phar-
maceuticals Ltd., Hamilton, Ontario L4W 2S5, (x2 P <0.05, df = 2) (Table 1). Intensities
Canada) and examined for D. renale 108 and were similar in the three lakes studied.
134 days post-infection. Tissues were fixed in Mean total length of infected pumpkin-
10% buffered formalin and prepared for histo-
seed was 11.4 (9.4-14.5) cm in Lake Sa-
logic examination using standard procedures.
sajewun, 11.8 (11.0-12.9) cm in Ryan Lake
Sections were cut at 6 sm and stained with he-
matoxylin and eosin. and 14.0 (11.9-17.6) cm in Billy Lake. In-
Specimens of larvae of D. renale from ex- fected pumpkinseed were approximately
perimentally infected Lumbriculus variegatus Age Class III and IV based on total length
(USNM Helm. Coll. No. 73805) and Rana pip- (see Cone and Anderson, 1977).
lens (USNM Helm. Coll. No. 73806) deposited
Larvae of Dioctophyrna renale were
by Dr. T. Mace in the U.S. National Parasite
Collection, Beltsville, Maryland 20705, USA, within small (1 to 2 mm) oval, white cap-
were examined. sules situated predominantly in the hyp-
axial musculature (Table 2). The longitu-
Description of study areas
dinal axis of capsules was oriented parallel
Billy Lake (93 ha, maximum depth of 9 m)
to muscle fibers (Fig. 1). Capsules were
and Ryan Lake (50 ha, maximum depth of 10
m) are shallow, oligotrophic lakes. Lake Sasa- composed of layers of tough, opaque,
jewun (44 ha, maximum depth of 12 m, but white tissue. A cloudy, white exudate was
averaging less than 3 m) is a shallow, eutrophic released when larvae were dissected from
lake. These three lakes are situated in Algon- capsules. One larva was found free within
quin Provincial Park, Ontario. Billy Lake and
the hypaxial musculature.
Ryan Lake were treated in 1965 and 1962, re-
spectively, with toxaphene to remove undesir- Larval Dioctophyrna renale in capsules
able fish. One yr after treatment Billy Lake and situated in the hypaxial musculature of
Ryan Lake were stocked with hatchery-reared pumpkinseed elicited a mild granuloma-
brook trout (Salvelinus fontinalis Mitchill),
tous reaction (Fig. 1). Capsules were com-
rainbow trout (Salmo gairdneri Richardson),
and splake (Salvelinus namaycush Walbaum x posed of two layers. The outermost layer
Salvelinus fontinalis) (Fraser, pers. comm.). consisted of dense connective tissue with
Pumpkinseed re-entered Ryan Lake when bea- fibroblasts scattered between collagen fi-
TABLE 1. Prevalence and mean intensity of larval Dioctophyma renale in Lepomis gibbosus collected in
Algonquin Provincial Park, Ontario.
bers. The inner layer consisted primarily variegatus and frogs deposited by Dr.
of macrophages but some lymphocytes Thomas Mace in the U.S. National Para-
were present (Fig. 2). An occasional giant site Collection.
cell was observed in the inner layer. Ne- Specimens of larval D. renale from
crotic cells which contained nuclear de- pumpkinseed have been deposited in the
bris and pale vacuolated cytoplasm were U.S. National Parasite Collection, Belts-
present in the inner layer near apices (Fig. ville, Maryland (USNM Helm. Coll. No.
3). Connective tissue fibers proliferated 78096). Specimens of larval D. renale from
into some necrotic areas. Muscle tissue pumpkinseed have also been deposited in
surrounding capsules appeared normal the National Museum of Natural Sciences,
except for some mild compression. Ottawa, Ontario, Canada (NMCIC(P) No.
Specimens of Dioctophyma renale in 1984-0324).
pumpkinseed from the three lakes were
Transmission to ferrets
third-stage larvae. There was no signifi-
cant difference (Mann-Whitney test, P < Fifteen minutes post-infection Ferret A
0.05) between total length of male and given infected pumpkinseed muscle be-
female larvae (Table 3). The genital pri- came agitated. Vomition began 30 mm
mordium of female larvae was mono- post-infection, was violent and intermit-
delphic and opisthodelphic. The vagina tent and lasted for 45 mm. Ferret B given
was evident, but the vulva was not yet infected pum pkinseed muscle started
patent (Fig. 4). The vulva was located near vomiting 30 mm post-infection. Vomition
the esophageal-intestinal junction. From
the vulva the female genital tube extend-
TABLE 2. Location of larval Dioctophyma renale
ed posteriorly and the distal tip was en- in Lepomis gibbosus from Algonquin Provincial Park,
larged. The male genital primordium was Ontario.
diorchic and opisthorchic and the bifur-
cation of the male genital primordium was Nu mber of infected fish
6
FIGUREs 1-6. 1-3. Capsule containing larvae of Dioctophyrna renale within the hpaxial ntnscle of
Leponiis gth1x.sus. (Hematoxvlin and eosin.) 1. Encapsulated larval D. renale. Arrows denote outside la er
of dense connective tissue and area of necrotic cells at apex of capsule. 2. Inner layer of capsule containing
macrophages larro\vs) between cross-sections of larval 1). renale. :3. Area of capsule apex showing necrotic
cells (top arrow) and infiltration by collagen fibers (bottom arow). 4-6. Third stage larvae of Dioctophyrna
renale. 4. \‘ulvar printordiurn of female larva. Cuticle of larva is to the top of the photograph. 5. Posterior
extremity of male larva. Arrow denotes third-stage larval cuticle within the second-stage larval cuticle. 6.
Posterior extremity of female larva. Arrow denotes third-stage larval cuticle within the second-stage larval
cuticle.
TABLE 3. Dimensionsa of larval Dioctophyma renale from the muscle of Lepomis gibbosus collected in
Algonquin Provincial Park, Ontario.
Male Female
Number 10 10
Length 5.9 (4.1-7.4) mm 6.5 (5.1-8.6) mm
Nerve ring” 100 (70-130) 105 (90-120)
Esophageal length 2.3 (1.6-3.1) mm 2.4 (2.0-3.3) mm
% of total length 38 (34-42) 37 (33-40)
Width at esophageal-
intestinal junction 150 (110-190) 179 (160-200)
Vulvar primordium” - 3.2 (2.5-5.0) mm
% of total length - 49 (43-58)
Length of rectum 194 (150-250) 177 (110-230)
Width at anus 90 (70-130) 74 (50-90)
1?
‘P{
4h.
FIGURES 7-11. 7. Abdominal cavity of Ferret A experimentally infected with Dioctophyma renale. Note
enlarged infected right kidney capsule with ventral opening (arrow). 8-11. Tissue from Ferret B experi-
mentally infected with D. renale. (Hematoxylin and eosin.) 8. Extension of the peritoneum into the abdom-
inal cavity. 9. Fibrous proliferative lesion on the peritoneum. Note eggs of D. renale. 10. Eggs of D. renale
surrounded by macrophages. Note granules within macrophages (arrow). 11. A pedunculate mass of mono-
nuclear cells, fibrous connective tissue and eggs of D. renale attached to the liver.
body cavity of mink. In the present study Dr. J. R. Lichtenfels of the U.S. National Par-
asite Collection kindly provided specimens for
adult worms were found only within the
examination. This study was funded through a
right kidney capsule. There was an open-
University Research Support Fund grant from
ing in the right kidney capsule of Ferret the Canadian Wildlife Service and an operating
A which probably permitted eggs of D. grant from the National Science and Engineer-
renale and cellular debris to enter the ing Research Council of Canada to Dr. R. C.
Anderson. This project was made possible with
peritoneal cavity. No opening on the kid-
the co-operation of the Ontario Ministry of
ney capsule was observed in Ferret B al- Natural Resources.
though chronic peritonitis seen in this an-
imal was associated with the presence of LITERATURE CITED
eggs. Dark brown granules seen histolog-
BANGHAM, R. V., ANI) C. W. HUNTER. 1939. Stud-
ically were probably hemosiderin from ies on fish parasites of Lake Erie. Distribution
lysis of erythrocytes. studies. Zoologica 24: 385-448.
Mace and Anderson (1975) suggested BE.xvEn, P. C., AND J. H. THEI5. 1979. Dioctophy-
that frogs may be important paratenic matid larval nematode in a subcutaneous nodule
from man in California. Am. J. Trop. Med. Hyg.
hosts in some enzootic areas (Lake Sasa-
28: 206-212.
jewun, Washago) while fish such as bull-
CUIREA, J. 1921. Sur la source d’infestation par
heads may be important paratenic hosts l’eustrongyle g#{233}ant(Eustrongylus gigas Rud.).
in other enootic areas (Lake Sasajewun). C. R. Soc. Biol. 85: 532-534.
The present study indicated that centrar- CoNE, D. K., AND R. C. ANDERSON. 1977. Parasites
of pumpkinseed (Lepornis gibbosus L.) from
chids may be more important paratenic
Ryan Lake, Algonquin Park, Ontario. Can. J.
hosts than bullheads or frogs in some en-
Zool. 55: 1410-1423.
zootic areas (Lake Sasajewun, Ryan and FASTZKIE, J. S., AND J. L. CRITES. 1977. A rede-
Billy lakes). Fish, including centrarchids, scription of Eustrongylides tubifex (Nitzsch
are the predominant source of food of 1819) Jagerskiold 1909 (Nematoda: Dioctophy-
matidae) from mallards (Anas platyrhynchos).
mink especially in spring, fall and winter
J. Parasitol. 63: 707-712.
(Hamilton, 1940; Sealander, 1943; Wilson,
GERELL, R. 1967. Food selection in relation to hab-
1954; Gerell, 1967). itat in mink (Mustela vison Schreber) in Swe-
Dioctophyma renale can cause morbid- den. Oikos 18: 233-246.
ity in man if infective stages are ingested HAI.LBERG, C. W. 1953. Dioctophyrna renale
(Goeze, 1782). A study of the migration routes
(Mace, 1975; Beaver and Theis, 1979). The
to the kidneys of mammals and resultant pa-
present report of infective larvae of D.
thology. Trans. Am. Microsc. Soc. 72: 351-363.
renale in the musculature of pumpkin- HA,SIILTON, W. J. 1940. The summer food of mink
seed suggests a human health risk in en- and raccoons on the Montezuma marsh, New
zootic areas if pumpkinseed are poorly York. J. Wildl. Manage. 4: 80-84.
HUMASON, C. L. 1972. Animal Tissue Techniques.
cooked or eaten raw. Other centrarchids,
W. Freeman, San Francisco, California, 641 pp.
such as bass preferred by sportsmen, may
KARMANOVA, E. M. 1959. (The life-cycle of the
also be suitable hosts. nematode, Dioctophynie renale.) Dokl. Acad.
Nauk SSSR 127: 1317-1319. (In Russian.)
ACKNOWLEDGMENTS
1960. (The life-cycle of the nematode,
The kind co-operation, assistance and advice Dioctophyme renale (Goeze, 1782) parasitic in
of Jim Fraser, Greg Betteridge and staff of the the kidneys of carnivorous animals and man.)
Ministry of Natural Resources, Algonquin Pro- Doki. Acad. Nauk SSSR 132: 1219-1221. (In
vincial Park are gratefully acknowledged and Russian.)
appreciated. Ms. Cathy Laing provided invalu- 1961.(The first report of Dioctophyrne
able assistance during this study. Mrs. Uta Stre- renale larvae in fish of the U.S.S.R.) Tr.
live assisted in preparation of tissue for histo- Gel’mintol. Lab. 11: 118-121. (In Russian.)
logic examination. Drs. H. W. Ferguson and I. 1962. (The life-cycle of Dioctophyme re-
K. Barker of the Ontario Veterinary College nale in its intermediate and definitive hosts.) Tr.
provided useful advice on the histopathologv. Gel’mintol. Lab. 12: 27-36. (In Russian.)
LICI-ITENFELS, J. R., AND P. A. MADDEN. 1980. Ce- B. Saunders Co., Philadelphia, Pennsylvania, 156
phalic papillae of giant kidney nematode Dioc- pp.
tophyma renale (Goeze, 1782) and comparison SCOTT, W. B., AND E. J. CROSSMAN. 1973. Fresh-
with Eustrongylides spp. Proc. Helminthol. Soc. water Fishes of Canada. Fish. Res. Board Can.
Wash. 47: 55-62. Bull. 184. 966 pp.
MACE, T. F. 1975. Bibliography of giant kidney SEALANDER, J. A. 1943. Winter food habits of mink
worm Dioctophyma renale (Goeze, 1782). Wildl. in southern Michigan. J. Wildl. Manage. 7: 411-
Dis. 69, 36 pp. 417.
1976. Lesions in mink (Mustela vison) in- WILSON, K. A. 1954. The role of mink and otter
fected with giant kidney worm (Dioctophyma as muskrat predators in northeastern North Car-
renale). J. Wildl. Dis. 12: 88-92. olina. J. WildI. Manage. 18: 199-207.
AND R. C. ANDERSON. 1975.
Development WOODFIEAD, A. E. 1950. Life-history cycle of the
of the giant kidney worm, Dioctophyma renale giant kidney worm, Dioctophyma renale (Nem-
(Goeze, 1782) (Nematoda: Dioctophymatoidea). atoda), of man and many other mammals. Trans.
Can. J. Zool. 53: 1552-1568. Am. Microsc. Soc. 69: 21-46.
M.SLLORY, F. B. 1942. Pathological Technique. W.