TOPIC:

J. Helminthol. Soc. Wash.
61(1), 1994, pp. 67-72
Parasites of Ale wives, Alosa pseudoharengus, from the Great Lakes
PATRICK M. MUZZALL
Department of Zoology, Natural Science Building, Michigan State University,
East Lansing, Michigan 48824
ABSTRACT: A total of 302 alewives, Alosa pseudoharengus (Clupeidae), were collected from 2 locations in Lake
Michigan and from Saginaw Bay, Lake Huron, between May 1990 and July 1992 and examined for parasites.
Ten parasite species (2 Trematoda, 4 Cestoda, 1 Nematoda, 1 Acanthocephala, 1 Copepoda, and 1 Protozoa)
infected alewives from Lake Michigan, with Echinorhynchus salmonis Miiller, 1784, being most common.
Diplostomum sp., Contracaecum sp., and Ergasilus luciopercarum Henderson, 1927, infrequently infected alewives
from Saginaw Bay. Alewives from Ludington, Michigan, had the highest mean parasite species richness
(0.7229). A summary and comparison of the parasites found in alewives from the Great Lakes are presented
with 22 parasite species reported. This information revealed that the alewife is an important intermediate and
transport host for helminths that mature in piscivorous fishes and birds in the Great Lakes area.
KEY WORDS: alewife, Alosa pseudoharengus, Clupeidae, parasites, survey, Michigan, Great Lakes.
The alewife, Alosa pseudoharengus (Wilson),
is an anadromous fish species of eastern North
America (Scott and Grossman, 1973). Its origin
in the Great Lakes has not been established with
certainty (R. R. Miller, 1957). The alewife was
first reported in Lake Huron in 1933 and in Lake
Michigan in 1949, and since then it has become
well established in many parts of these lakes. The
importance of the alewife as a food item for
salmonids (Jude et al., 1987; M. A. Miller and
Holey, 1992) and piscivorous birds (Ludwig,
1966; Fox et al., 1990) in the Great Lakes is well
known.
The objectives of the present study were (a) to
provide information on the occurrence and
abundance of parasites in alewives from 2 locations
in Lake Michigan and from the western
portion of Saginaw Bay, Lake Huron; (b) to summarize
and compare the known information
about parasites infecting this important forage
species in the Great Lakes; and (c) to examine
the role of alewives as intermediate and transport
hosts for parasites that mature in piscivorous
fishes and birds in the Great Lakes area.
Materials and Methods
Alewives were collected by beach seine and trawl
from 2 locations in Lake Michigan and from the western
portion of Saginaw Bay, Lake Huron. Fish data are
given below with information on location; month and
year of collection; number offish examined; total length,
with range in millimeters (followed by mean ± SD);
and 95% confidence intervals.
1. Southern Lake Michigan, Michigan City, Indiana;
August 1991; « = 75; 101-212(151 ±29.1); 144.1-
157.5.
2. Eastern Lake Michigan, Ludington, Michigan; MayAugust
1990, April-June 1991; rc = 166; 102-239
(160 ± 28.6); 155.8-164.6.
3. Western portion of Saginaw Bay, Lake Huron,
Michigan; May-July 1992; n = 61; 62-203 (141 ±
35.1); 132.1-150.1.
Ludington, Michigan, is approximately 247 km north
of Michigan City, Indiana. Alewives were frozen in the
field and measured and sexed at necropsy. The skin,
fins, gills, eyes, kidney, gonads, spleen, liver, gall bladder,
mesenteries, esophagus, gastrointestinal tract, heart,
and the left or right side of the musculature were examined.
Parasites were collected and processed using
routine procedures. Prevalence is the percentage offish
infected, and mean intensity is the mean number of
worms of a species per infected fish. Voucher specimens
have been deposited in the U.S. National Parasite
Collection, Beltsville, Maryland 20705: Diplostomum
sp. (83226), Tetracotyle sp. (83227), Cyathocephalus
truncatus (83228), Diphyllobothrium sp. (83229), Eubothrium
salvelini (83230), Proteocephalus sp. (83231),
Haplonema hamulatum (83233), and Echinorhynchus
salmonis (83232). Specimens of Ergasilus luciopercarum
are in the collection of L. Roberts. Specimens of
other helminth species were not retained by the author
and therefore were not deposited.
Information on the parasites of alewives was obtained
from examining published studies performed in
the Great Lakes. Species richness refers to the number
of parasite species infecting alewives from each Great
Lake. The Jaccard coefficient of community similarity
was calculated as
CC. = + S2 - Q,
where 5\d S2 are the number of parasite species in
communities 1 and 2, respectively, and Cis the number
of species common to both communities (Brower and
Zar, 1984). For calculations of the Jaccard coefficient
of community similarity and species richness, Diplostomum
(present study) and Diplostomulum in other
studies were considered to be a single genus.
67
Copyright © 2011, The Helminthological Society of Washington
68 JOURNAL OF THE HELMINTHOLOGICAL SOCIETY OF WASHINGTON, 61(1), JAN 1994
Results
Thirty (40%) alewives from Michigan City, Indiana,
91 (55%) from Ludington, Michigan, and
7 (11%) from Saginaw Bay, Michigan, were infected
with 1 or more parasites. A total of 10
parasite species (4 from Michigan City and 9
from Ludington) infected alewives from both locations
in Lake Michigan (Table 1). Echinorhynchus
salmonis had the highest prevalence and
mean intensity at each location. Correlation coefficients
between E. salmonis intensity and length
of infected alewife from Michigan City and Ludington
were 0.172 (P > 0.05) and 0.592 (P <
0.01), respectively. Of the helminth species found,
only Cyathocephalus truncatus (Pallus, 1781) and
E. salmonis were gravid. Diplostomum sp. was
more common in alewives from Michigan City
than from Ludington, whereas cestodes were
more common in alewives from Ludington than
from Michigan City. Three parasite species (Diplostomum
sp., Contracaecum sp., and Ergasilus
luciopercarum) infrequently infected alewives
from Saginaw Bay. There were no significant differences
in prevalence (chi-square analysis, P >
0.05) and intensity (Student's Mest, P > 0.05)
of parasitism between female and male alewives
at each location. The alewife is a new host record
for Haploncma hamulatum Moulton, 1931, and
E. luciopercarum.
Jaccard's coefficients of similarity for the parasite
faunas of alewives between locations are
0.30 for Michigan City-Ludington, 0.40 for
Michigan City-Saginaw Bay, and 0.09 for Ludington-Saginaw
Bay. When the data for uninfected
and infected fish were combined, mean
parasite species richness ± SD, range, and 95%
confidence intervals in alewives from Michigan
City (0.5333 ± 0.6830, 0-2, 0.3670-0.6997),
from Ludington (0.7229 ± 0.7991,0-4,0.6016-
0.8441), and from Saginaw Bay (0.1148 ±0.3214,
0-1, 0.0324-0.1971) were significantly different
(analysis of variance, F= 16.7, P < 0.001). However,
when data from infected fish only were used
in the analyses, mean parasite species richness
± SD, range, and 95% confidence intervals in
alewives from Michigan City (1.3333 ± 0.4795,
1-2, 1.1543-1.5124), from Ludington (1.3187 ±
0.5940, 1-4, 1.1949-1.4424) and from Saginaw
Bay (x = 1, range = 1) were not significantly
different (analysis of variance, F = 1.13, P >
0.05).
Discussion
Echinorhynchus salmonis was the most common
parasite species found in alewives from Lake
Michigan in the present study. Alewives in this
lake feed on the amphipod, Pontoporeia affinis,
which serves as an intermediate host for this parasite
(Amin, 1978). Morsell and Norden (1968)
reported that as alewives in western Lake Michigan
increased in length a greater proportion of
P. affinis was found in their diet. This could explain
the significant relationship between E. salmonis
intensity and length of infected alewives
from Ludington, Michigan. Webb and McComish
(1974) found that the largest percentage
of volume and percent frequency of occurrence
of P. affinis in alewives from southern Lake
Michigan occurred in August 1972; however, it
was of negligible importance in their diet in 19 71.
Rhodes and McComish (1975) reported that alewives
consumed the largest volume of P. affinis
in October in southern Lake Michigan.
Amin and Burrows (1977) found E. salmonis
infecting alewives in western Lake Michigan. A
mean intensity of 1.9 E. salmonis per infected
fish was calculated using their data in Table 1.
This value and prevalence are low compared to
the infection values of E. salmonis in the present
study. Fish length and time of collection do not
appear to play major roles in these infection differences,
because examined fish had similar
lengths and were collected during similar months.
Possible explanations for these infection differences
may involve the availability of the amphipod
intermediate host and its importance in
the diet of alewives from 1 year to the next or
E. salmonis may be more common in 1 location
than in another.
Muzzall (1989) hypothesized that the alewife
serves as an important transport host for E. salmonis
to salmonids in eastern Lake Michigan.
Hnath (1969) experimentally demonstrated the
transfer of E. salmonis between coho salmon,
Oncorhynchus kisutch, and brook trout, Salvelinus
fontinalis, from Lake Michigan. Jude et al.
(1987) reported that the alewife made up 78% of
the identifiable prey species eaten by salmonids
in Lake Michigan. The high infection values of
E. salmonis in alewives in the present study supports
this suggestion that alewives serve as important
transport hosts for E. salmonis to salmonids.
Seng (1975) estimated that approximately
one-eighth of E. salmonis flows through transport
hosts in the ecosystem of Cold Lake, Alberta.
Furthermore, it is known that as salmonids
become older (larger) they ingest a larger proportion
of alewives (Muzzall, 1989). Amin and
Burrows (1977) suggested that other species of
Copyright © 2011, The Helminthological Society of Washington
Table 1. Prevalence (P), mean intensity (MI), and maximu
m number of parasites (max.) found in Alosa pseudoharengus fro
m Lake Michigan (Michigan City, Indiana,
and Ludington, Michigan) and Sagina
w Bay, Lake Huron, 1990-1992.*
Parasite
Digenea
Diplostomum sp4
Tetracotyle sp.t
Cestoda
Cyathocephalus truncatus
Diphyllobothrium sp4
Eubothrium salvelini§
Proteocephalus sp.§
Nematoda
Contracaecum sp4
Michigan City Ludington
(n = 75)t (n= 166)
MI ± 1 S
D MI ± 1 S
D
P (max.) P (max.)
21 1.6 ± 1.0 0.6 1
(4)
- - 1 1
- - 1
2 1.6 ±0.9
(4)
- - 0.
6 1
- - 8 2.0 ± 1.5
(5)
1 1 1.8 1
_ _ _ _
Sagina
w Bay
(n = 61)
MI ± 1 SD
P (max.) Site
3 1 Lens
— — Encysted in mesenteries
— — Pyloric ceca
— — Encysted around pyloric cecu
m
— — Anterior intestine, pyloric ceca
— — Anterior intestine
5 3.7 ± 1.5 Encysted in mesenteries
(5)
2
c
yN
f
r
1>
?3
GO
mGO
/~\ hamulatum§ —
Acanthocephala
Echinorhynchus salmonis 29
Copepoda
Ergasilus luciopercarum 1
Protozoans
Trichodina sp. —
* Unless otherwise indicated, parasites were gravid.
f Number offish examined.
t Metacercariae or larvae.
§ Immature parasites.
4.0 ± 3.4
(13)
48 8.4 ± 11.3
(72)
0.6
Small intestine
Intestine
Gills
Gills
Copyright © 2011, The Helminthological Society of Washington
70 JOURNAL OF THE HELMINTHOLOGICAL SOCIETY OF WASHINGTON, 61(1), JAN 1994
Table 2. Parasites reported from Alosa pseudoharengus in the Great Lakes.
Lake Lake Lake Lake
Michigan Superior Huron Lake Erie Ontario
Parasite (n = 241)* (n = 12) (n = 297) (n = 14) (n = 61)
Monogenea
Octomacrum sp. — — — 10 —
Digenea
Diplostomum jlexicaudum — — 1 — —
Diplostomum spathaceum — 5 6,8 — 12
Diplostomum sp. 1,2 — 9 10
Posthodiplostomum minimum — — — — 12
Tetracotyle intermedia — — 6 — —
Tetracotyle sp. 2 — 8 — —
Metacercariae — — — 10 —
Cestoda
Cyathocephalus truncatus 2 — — — —
Diphyllobothrium sp. 2 — — — —
Eubothrium salvelini 2 — — — —
Proteocephahis sp. 1,2 — — — —
Nematoda
Camallanus oxycephalus — — — 11 —
Capillaria sp. — — — 10
Contracaecum sp. — — 9 — —
Haplonema hamulatum 2 — — — —
Acanthocephala
Acanthocephalus dirus 3 5 6,7, 8 — 12
Echinorhynchus salmonis 1,2,4 — 6,7 — —
Copepoda
Ergasilus luciopercarum 1 — 9 — —
Fungi
Saprolegnia sp. — 5 6,7,8 — 12
Protozoa
Trichodina sp. 2 — — — —
Acarina
Hydrachna sp. — — 6 — —
* Total number of fish examined. Entries are abbreviations for published investigations on the parasites of alewives from the
Great Lakes. 1 = present study, Michigan City, Indiana; 2 = present study, Ludington, Michigan; 3 = Amin (1977); 4 = Amin
and Burrows (1977); 5 = Dechtiar and Lawrie (1988); 6 = Collins and Dechtiar (1974); 7 = Dechtiar and Berst (1978); 8 = Dechtiar
etal. (1988); 9 = present study, Saginaw Bay, Michigan; 10 = Bangham(1972); 11 = StrombergandCrites(1975); 12 = Dechtiar
and Christie (1988).
forage fish in Lake Michigan serve as transport Michigan. Acanthocephalus dirus has been found
hosts for E. salmonis. in alewives from 4 Great Lakes. Although E.
This is the first published study to summarize salmonis infect fishes from Lake Huron, it was
the parasites of a fish species in the Great Lakes not found in alewives from Saginaw Bay. None
with a total of 22 parasite species being reported of the parasite species infecting alewives in the
from the alewife (Table 2). Taxonomically, larval Great Lakes is specific to this fish species,
digenean species are most common followed by Mean parasite species richness was significestode
and nematode species. No parasite spe- cantly higher in alewives from Ludington than
cies has been reported from alewives in all the from the other locations because more parasite
Great Lakes. Diplostomum is the only genus species were found and the high prevalence of
found in alewives from all the Great Lakes. Ces- E. salmonis. Parasite species richness (in parentodes
were reported from alewives only from Lake theses) in alewives from each lake are Lake MichCopyright
© 2011, The Helminthological Society of Washington
MUZZALL-PARASITES OF ALEWIVES OF THE GREAT LAKES 71
Table 3. Jaccard's index of community similarity based
on presence of parasite species reported from Alosa
pseudoharengus in each lake.*
Lakef 1
1 1.0
2
3
4
5
2
0.08
1.0
3
0.29
0.27
1.0
4
0.07
0.00
0.07
1.0
5
0.07
0.75
0.15
0.00
1.0
* See Table 2 for the parasite species used in these calculations
and specific investigations.
t 1 = Lake Michigan, 2 = Lake Superior, 3 = Lake Huron,
4 = Lake Erie, 5 = Lake Ontario.
igan (11), Lake Superior (3), Lake Huron (11),
Lake Erie (5), and Lake Ontario (4). Species richness
is highest in Lake Michigan and Lake Huron,
where the largest numbers of alewives were
examined. Jaccard's coefficients of similarity for
the parasite faunas in alewives between the Great
Lakes do not follow a specific pattern (Table 3).
Alewives from Lake Erie had the lowest coefficients
(<0.07), indicating that they shared the
fewest parasite species with alewives from the
other Great Lakes. Alewives from Lake Superior
and Lake Ontario had the highest coefficient
(0.75), indicating that they shared the most parasite
species of those species found in alewives
from each lake.
Several hypotheses have been proposed and
discussed by Wisniewski (1958), Chubb (1963,
1964, 1970), Esch (1971), Halvorsen (1971),
Kennedy (1978), Holmes and Price (1986), and
Marcogliese and Cone (1991) to explain the patterns
of distribution and abundance of metazoan
parasites in freshwater fishes. The present study
is the first to investigate the distribution of parasites
in 1 fish species in the Great Lakes. None
of these hypotheses, however, explains the distribution
and number of helminth species in alewives
from the Great Lakes. An explanation is
confounded by the small number of alewives examined
from Lake Superior and Lake Erie. It is
believed more parasite species will be found when
more alewives are examined from these 2 lakes.
Eight (7 larval digenean species and Diphyllobothrium
sp.) of the 18 helminth species reported
from alewives in the Great Lakes (Table
2) are allogenic, maturing in piscivorous birds.
Both Ludwig (1966) and Fox et al. (1990) have
reported that the alewife and rainbow smelt, Osmerus
mordax, accounted for at least 80% of the
fish eaten by herring gulls, Larus argcntatus, in
the Great Lakes. Eubothrium salvelini (Schrank,
1790), Proteocephalus sp., Capillaria sp., Contracaecum
sp., and Haplonema hamulatum, listed
in Table 2, mature in other fish species and
not in the alewife. It is believed that alewives
serve as transport hosts for these helminth species
and E. salmonis. Therefore, it is hypothesized
that the dominance of allogenic helminth
species in alewives and the occurrence of helminths
in alewives that mature in other fish species
is attributable to the position of alewives in
the food web as planktivores and macroinvertivores
that are prey species for piscivorous fishes
and birds in the Great Lakes area.
Acknowledgments
I thank Dan Brazo, Indiana Department of
Natural Resources, Michigan City, Indiana, and
Tom McComish, Ball State University, Muncie,
Indiana; Rob Elliott and Doug Peterson, Michigan
State University, East Lansing, Michigan;
and Bob Haas, Jack Hodge, and Larry Shubel,
Michigan Department of Natural Resources,
Mount Clemens, Michigan, for providing the alewives;
and Larry Roberts for confirming my
identification of Ergasilus luciopercarum.
Literature Cited
Amin, O. M. 1977. Helminth parasites of some
southwestern Lake Michigan fishes. Proceedings
of the Helminthological Society of Washington 44:
210-217.
. 1978. On the crustacean hosts of larval acanthocephalan
and cestode parasites in southwestern
Lake Michigan. Journal of Parasitology 64:842-
845.
-, and J. M. Burrows. 1977. Host and seasonal
associations of Echinorhynchus salmonis (Acanthocephala:
Echinorhynchidae) in Lake Michigan
fishes. Journal of the Fisheries Research Board of
Canada 34:325-331.
Bangham, R. V. 1972. A resurvey of the fish parasites
of western Lake Erie. Bulletin of the Ohio Biological
Survey 4:1-23.
Brower, J. E., and J. H. Zar. 1984. Field and Laboratory
Methods for General Ecology, 2nd ed.
William C. Brown Publishers, Dubuque, Iowa.
Chubb, J. C. 1963. On the characterization of the
parasite fauna of the fish of Llyn Tegid. Proceedings
of the Zoological Society of London 141:609-
621.
. 1964. A preliminary comparison of the specific
composition of the parasite fauna of the fish
of Llyn Padarn, Caenarvonshire, an oligotrophic
lake, and Llyn Tcgid (Bala Lake), Merionetshire,
a late oligotrophic or early [sic] mesotrophic lake.
Wiadomosci Parazytologiczne 10:499-516.
. 1970. The parasite fauna of British fresh-
,
Copyright © 2011, The Helminthological Society of Washington
72 JOURNAL OF THE HELMINTHOLOGICAL SOCIETY OF WASHINGTON, 61(1), JAN 1994
water fish. Symposia of the British Society for Parasitology
8:119-144.
Collins, J. J., and A. O. Dechtiar. 1974. Parasite
fauna of kokanee salmon (Oncorhynchus nerkd)
introduced into Lake Huron. Journal of the Fisheries
Research Board of Canada 31:1818-1821.
Dechtiar, A. O., and A. H.Berst. 1978. Parasite fauna
of splake (Salvelinus fontinalis x S. namaycush).
Proceedings of the Helminthological Society of
Washington 45:249-254.
, and W. J. Christie. 1988. Survey of the parasite
fauna of Lake Ontario fishes, 1961 to 1971.
Great Lakes Fisheries Commission, Technical Report
51:66-106.
, J. J. Collins, and J. A. Reckahn. 1988. Survey
of the parasite fauna of Lake Huron fishes,
1967 to 1971. Great Lakes Fisheries Commission,
Technical Report 51:19-48.
-, and A. H. Lawrie. 1988. Survey of the parasite
fauna of Lake Superior fishes, 1969 to 1975.
Great Lakes Fisheries Commission, Technical Report
51:1-18.
Esch, G. W. 1971. Impact of ecological succession
on the parasite fauna in centrarchids from oligotrophic
and eutrophic ecosystems. American Midland
Naturalist 86:160-168.
Fox, G. A., L. J. Allan, D. V. Weseloh, and P. Mineau.
1990. The diet of herring gulls during the nesting
period in Canadian waters of the Great Lakes.
Canadian Journal of Zoology 68:1075-1085.
Halvorsen, O. 1971. Studies of the helminth fauna
of Norway. XVIII. On the composition of the parasite
fauna of coarse fish in the River Glomma,
south-eastern Norway. Norwegian Journal of Zoology
19:181-192.
Hnath, J. G. 1969. Transfer of an adult acanthocephalan
from one fish to another. Transactions
of the American Fisheries Society 98:332.
Holmes, J. C., and P. W. Price. 1986. Communities
of parasites. Pages 187-213 in J. Kikkawa and D.
J. Anderson, eds. Community Ecology: Pattern
and Process. Blackwell Scientific Publication, Oxford.
Jude, D. J., F. J. Tesar, S. J. DeBoe, and T. J. Miller.
1987. Diet and selection of maj or prey species by
Lake Michigan salmonids, 1973-1982. Transactions
of the American Fisheries Society 116:677-
691.
Kennedy, C. R. 1978. An analysis of the metazoan
parasitocoenoses of brown trout Salmo trutta from
British Lakes. Journal of Fish Biology 13:255-263.
Ludwig, J. P. 1966. Herring and ring-billed gull populations
of the Great Lakes, 1960-1965. Publication
No. 15, Great Lakes Research Division,
University of Michigan, Ann Arbor. Pages 80-89.
Marcogliese, D. J., and D. K. Cone. 1991. Importance
of lake characteristics in structuring parasite
communities of salmonids from insular Newfoundland.
Canadian Journal of Zoology 69:2962-
2967.
Miller, M. A., and M. E. Holey. 1992. Diets of lake
trout inhabiting nearshore and offshore Lake
Michigan environments. Journal of Great Lakes
Research 18:51-60.
Miller, R. R. 1957. Origin and dispersal of the alewife,
Alosa pseudoharengus, and the gizzard shad,
Dorosoma cepedianum, in the Great Lakes. Transactions
of the American Fisheries Society 86:97-
111.
Morsell, J. W., and C. R. Norden. 1968. Food habits
of the alewife, Alosa pseudoharengus (Wilson), in
Lake Michigan. Proceedings of the Conference on
Great Lakes Research 11:96-102.
Muzzall, P. M. 1989. Endohelminths of salmonids
from two localities in Lake Michigan, with emphasis
on Echinorhynchus salmonis. Canadian
Journal of Zoology 67:1604-1607.
Rhodes, R. J., and T. S. McComish. 1975. Observations
on the adult alewive's food habits (Pisces:
Clupeidae: Alosa pseudoharengus) in Indiana's
waters of Lake Michigan in 1970. Ohio Journal
of Science 75:50-55.
Scott, W. B., and E. J. Crossman. 1973. Freshwater
fishes of Canada. Bulletin of the Fisheries Research
Board of Canada No. 184.
Seng, R. L. T. 1975. Metazoan parasites of fishes of
Cold Lake, Alberta: a community analysis. Ph.D.
Thesis, University of Alberta, Edmonton. 170 pp.
Stromberg, P. C., and J. L. Crites. 1975. An analysis
of the changes in the prevalence of Camallanus
oxycephalus (Nematoda: Camallanidae) in western
Lake Erie. Ohio Journal of Science 75:1-6.
Webb, D. A., and T. S. McComish. 1974. Food habits
of adult alewives in Lake Michigan near Michigan
City, Indiana, in 1971 and 1972. Proceedings of
the Indiana Academy of Science 83:179-184.
Wisniewski, W. L. 1958. Characterization of the parasitofauna
of an eutrophic lake (parasitofauna of
the biocoenosis of Druzno Lake. Part I). Acta Parasitologica
Polonica 6:1-64