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INTERNAL PARASITES OF THE SEBAGO SALMON

Front BULLETIN OF THE BUREAU OF FISHERIES, Volume XXVIfJ,. 1908

Proceedings of. the .Fourth International: Fishery: Congress..:~ -, Washington, 1908

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INTERNAL PARASITES OF THE SEBAGO SALMON

From BULLETIN OF THE BUREAU OF FISHERIES, Volume XXVIII, 1908

Proceedings of the Fourth International Fishery Congress : : Washington, 1908

LT
enna

WASHINGTON : : : : : : GOVERNMENT PRINTING OFFICE :::::: 1910

BUREAU OF FISHERIES DOCUMENT NO. 713
Issued April, 1910

INTERNAL PARASITES OF THE SEBAGO SALMON

a
By Henry B. Ward, Ph. D.

Professor of Zoology, University of Illinois

ad

Paper presented before the Fourth International Fishery Congress
held at Washington, U. S. A., September 22 to 26, 1908

1151

CONTENTS.

as
Page

Historical survey 22. 2= 22-3 2S se = so es a ae ee ee 1153
Parasites. of Atlantic salmon; withitabulated’summary=2=)-- =) see eee 1153
Parasites'of Pacific'salmon=- = 52: 28S) S22 2 ete: an 8 Sete ee ee ee ee 1172
Observations onthe Sebago:salmon us. 222 - =e" = fe an ee eee ee ee 1173
Specific’ relationships: _=--2 +1228 _2 2822 26ers 1173
Sourceof parasites: SS 2222 3-32 222 2) = Sa ee re a ee ee 1174
Ajnew: trematode|parasité_- 225 22e 2222 ose =e oe ee et ee ee ane eee 1176
Cestodes_ 2.222. 525 - en est eee tea ee 2 se ee ee ee 1184
Proteocephalus pusillus, nov. sp_------------ ee a 1186
Spargantim se bagoy mov Sp sate ate a ee ame ee ee sosseees 1187
Nematodes 25 2 ais Sa ata a a er 1188
Résumé and conclusions 2. = eae se aa acta ae se ee 1189
Bibliographys.— 2-252 --ace==— EAS ase Se a eae se oat Sone sa I1g2
Explanation(ofiplatese so-o == 5 22s eee ee ee se ne 1194

1152

INTERNAL PARASITES OF THE SEBAGO SALMON.

ed

By HENRY B. WARD, Ph. D.,
Professor of Zoology, University of [llinots.

a

In connection with other investigations of the United States Bureau of
Fisheries in Alaska in 1906, I had the privilege of spending two months in study
of the parasites of the Pacific salmon. The following year, for comparison of
the interesting results of this work with similar studies of Atlantic salmon, I
was designated to join a party engaged in a biological survey of Lake Sebago,
Maine. During six weeks in this region I examined for parasites a number of
the Sebago salmon and secured a series of parasites from other fish in the lake
and adjacent waters.

The large amount of valuable material obtained on these two trips has
engaged my entire attention during the interval since it was secured, and even
yet some questions have not been satisfactorily answered. It forms a most
interesting contribution to the parasitic fauna of these important fishes and at
the same time throws some light on the general relations between an animal
and its parasites, which I hope may be of interest to the scientist and of value
to the practical fish culturist. This report falls naturally into three parts—
first, a historical summary, which concerns chiefly the European or Atlantic
salmon, since this species is the only one that has been studied previous to
the present date; second, a report on the findings in the case of the Sebago
salmon, which is very closely related to the European species, together with a
discussion of the conclusions which may be drawn from these data; and third,
a similar report on the Pacific salmon, which is less closely related and rather
widely removed geographically from the other two forms. In the present paper
are included only the first and second sections of the entire report.

HISTORICAL SURVEY.
PARASITES OF ATLANTIC SALMON.

Rudolphi says that in 1726 Frisch observed a salmon parasite, later known
as Bothriocephalus solidus, and in 1735 published some record of its occurrence
in a paper entitled ‘‘ De teniis in pisiculo aculeato, qui in Marchia Brandenburgia
vocatur ‘Stecherling.’’’ This is the first account of a salmon parasite to which
I have found any reference, and I have been unable to ascertain more precisely

the data in this case or to verify the reference.
1153

1154 BULLETIN OF THE BUREAU OF FISHERIi&S.

The oldest record of a salmon parasite that I have been able to verify is
found in a paper by Sporing (1753), in which he defends the thesis that inhabit-
ants of fluviatile regions are more annoyed by tapeworms than those of other
places, no doubt because of the use of half-raw fish. Of weight for his argument
is the list of half a dozen fish, including Salmo salar, in which, according to his
observations, tapeworm? larve are present. The view that man was indebted
to the salmon for infection with fish tapeworms was generally current in early
times and, though supported by no scientific evidence, persisted until finally
thoroughly disproved by Zschokke (1890). Now it may be regarded as fully
established that man does not acquire a single parasite in any way by the use
of salmon as food.

O. F. Miiller (1776, 1777, 1780) was the first to describe and name accord-
ing to scientific principles some of the parasites from Salmo salar. He named
Fasciola varica, afterwards called Distoma varicum by Zeder; Echinorhynchus
salmonis, changed to E. inflatus by Rudolphi; E£. levis, later changed to E. nodu-
losus; Tenia solida, which later became Bothriocephalus solidus Rudolphi, and
Tenia salmonis, later called B. proboscideus Rudolphi.

Goeze (1782) gave the first description of Echinorhynchus quadrirostris,
later more correctly diagnosed and named Tetrarhynchus appendiculatus by
Rudolphi (1809). Goeze also gave a good description of the encapsulated nema-
tode larva common in salmon, which he referred to Cucullanus, though doubt-
fully. Rudolphi afterwards named this form Ascaris capsularia.

The first formal list of parasites from Salmo salar is that given by Rudolphi
in 1810, who lists as parasites already recorded for this host eight ° species, as

follows:
Bothriocephalus proboscideus.
Bothriocephalus solidus.
Tetrarhynchus appendiculatus.
Distoma varicum.
Ascaris capsularia.
Dub. (?Cucullanus).
Echinorhynchus inflatus.
Echinorhynchus (?) nodulosus.

It is of interest to note that Rudolphi records opposite every one of these
named from six to eight earlier references to the particular species. Five of
them were originally observed by O. F. Miiller, two by Goeze, and one is a doubt-
ful species.

@ Braun (1894), who cites the case, says Ligula larve, but as this genus has not been recorded for
Salmo salar I take it to apply only to certain of the host species listed. The original author of course
did not distinguish even genera in his observations.

b In the appendix (vol. 1, part 2, p. 376) Rudolphi lists another find under the name of Distoma
crenatum. This material was examined by Liihe (1901, 401) and pronounced not a hemiurid, but fur-
ther determination could not be made.

INTERNAL PARASITES OF THE SEBAGO SALMON. 1155

In a later paper (1819) Rudolphi added to the list no new parasite, Dis-
toma appendiculatum Rudolphi being merely another name for D. crenatum of
the appendix in the earlier work. In this list Echinorhynchus fusiformis Zeder
is only a change of name from E. inflatus of the earlier list; E. nodulosus is
omitted; Bothriocephalus solidus is interpreted as introduced by accident when
its proper hosts chance to be eaten by the salmon. Thus the true list of salmon
parasites is actually reduced, and numbers only seven in this later list of
Rudolphi.

In 1851, Diesing in his ‘‘Systema Helminthum” recorded for Salmo salar
ten parasites, as follows:

Distomum varicum.
Stenobothrium appendiculatum.
Schistocephalus dimorphus.
Dibothrium proboscideum.
Echinorhynchus pachysomus.

’ Echinorhynchus proteus.
Agamonema capsularia.
Ascaris capsularia.
Ascaris clavata.
Cucullanus elegans.

-

Although one notes at once the unfamiliar appearance of the list due to
numerous changes in the names employed, yet only the last two are actually
new forms. Thus, in spite of the frequent attention given to the salmon, the
list of its parasites had only increased from five to ten species in the seventy-
five years since O. F. Miiller first made scientific records of its parasitic fauna in
Denmark.

In 1878 von Linstow in the “Compendium der Helminthologie”’ listed 16
parasites for Salmo salar. New are:

Distomum ocreatum Rudolphi.
Distomum reflexum Creplin.
Bothriocephalus cordiceps Leidy.”
Tetrarhynchus grossus Rudolphi.
Tetrarhynchus solidus Drummond.

In his ‘“Nachtrag’’ (1889) the same author includes five new species of
parasites recorded for Salmo salar since the appearance of the earlier record,

namely :
Agamonema communis Diesing.
Distomum miescheri Zschokke.
Bothriocephalus sp.? Zschokke.
Leuckartia sp.? Moniez.?
Tetrabothrium minimum von Linstow.

a As indicated in the discussion (p. 1166), this is an error in citation.

b Moniez (1881) found three cestodes in the pyloric coeca of a salmon obtained in the fish market
at Lille (France), on which he based a new genus, Leuckartia. Except for the lack of a scolex, the
specimens agree well with Bothriocephalus infundibuliformis, better Abothrium crassum, to which they
may well belong.

1156 BULLETIN OF THE BUREAU OF FISHERIES.

Without tracing in detail the further progress of the record, it may
be said that at the present date the list includes 47 species, which are
enumerated later in this paper. It is of importance for a consideration of the
distribution of the salmon parasites, the especial object of this paper, to review
the later studies in this field in their geographic arrangement in order to com-
pare clearly the parasites found in one area with those which are present in
another. The salmon which have been most intensively studied are those of
the Rhine.

Our knowledge of these forms is due largely to a series of papers by the
distinguished Swiss helminthologist, Fr. Zschokke, of Basel, which cover the
work of many years. The first record of Zschokke (1889) included examina-
tions of 45 fish, of which 42 were found infected with parasites. All the fish
were caught in the Rhine in November, December, and January, and the
following parasitic species were listed:

Ratio of

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Parasite Organ infected infection.

Per cent.

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Rhynchobothrium paleaceum Rudolphi (larva)_________________

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Not a single parasite lay in the alimentary canal below the pyloric cceca.
Monticelli notes that most sharks lose their parasites after a long stay in an
aquarium, and Zschokke has observed that marine fish otherwise heavily
infested lose their intestinal parasites very rapidly when subjected to fasting
in captivity. The Rhine salmon behaves with regard to parasites just like
a fasting sea fish. Its parasitic fauna manifests an almost purely marine
aspect. Fresh-water elements are scanty and insignificant. Clearly, then, the
Rhine salmon takes little or no food during its fresh-water migration. Data
on individual species close the paper.

The parasitic fauna of the Atlantic salmon was discussed in extended
fashion later by Zschokke (1891) on the basis of his own previous studies and
those of earlier authors. In all he had examined the viscera of 129 fish caught
in the Rhine. The alimentary canal contained in all cases the thick yellowish
or yellow-brown mucus, but never any recognizable remnants of food mate-
rials, although once plant fibers and undigested remains of a Gammarus pulex
were found. As in similar previously reported cases, so here also the occur-
rence of these fragments should be regarded as purely accidental.

INTERNAL PARASITES OF THE SEBAGO SALMON, LS fi

Only four of the 129 salmon examined were free from parasites, and in
all 20 species of the latter were recorded from the infested fish. The list of
parasites recorded is as follows:

Ascaris adunca Rudolphi.
Ascaris angulata Rudolphi.
Ascaris clavata Rudolphi.
Ascaris (Agamonema) capsularia Diesing.
Ascaris (Agamonema) communis Diesing.
Echinorhynchus acus Rudolphi.
Echinorhynchus agilis Rudolphi.
Echinorhynchus proteus Westrumb.
Distomum varicum Zeder.
Distomum reflexum Creplin.
Distomum miescheri Zschokke.
Schistocephalus dimorphus Creplin.
Bothriocephalus infundibuliformis Rudolphi.
Bothriocephalus osmeri (larva) von Linstow.
Bothriocephalus sp. 1 (larva).¢
Bothriocephalus sp. 11 (larva).
Rhynchobothrium paleaceum (larva) Rudolphi.
Tetrarhynchus solidus Drummond.
Tetrarhynchus grossus Rudolphi.
Tetrarhynchus macrobothrius von Siebold (=Stenobothrium appendicula-
tum Diesing).

Five of these species (Ascaris capsularia, Distomum varicum, Bothriocephalus
infundibuliformis, Rhynchobothrium paleaceum, and Tetrarhynchus macrobo-
thrius) are abundant, almost regular in their occurrence, while the other forms
are relatively rare in the Rhine salmon. The common parasites were also
usually abundant in the individual host; thus 20 to 40 specimens of Ascaris
capsularia were often found in a single host. Of Distomum varicum, from 30
to 50 individuals were taken from the oesophagus of one fish. In some cases
Bothriocephalus infundibulijormis was present in large numbers, but usually
in one or a few weak, starved specimens. Rhynchobothrium paleaceum and
Tetrarhynchus macrobothrius occurred in from 20 to 25 individuals in a single
host. All other parasites were found in small numbers, often only a single
specimen of any one species.

Among the 129 Rhine salmon investigated 4 were free from parasites, 55
sheltered a single species of parasite, and 43 but two species, while 20 had
three species, 6 had four species, and 1 had five species of parasites.

@ The various bothriocephalid larve which occur in the salmon are discussed in a separate paper
by Zschokke (1890). On the basis of morphologic data he inclined in this paper to the view that five
different forms, indicating as many species, might be distinguished. Later studies showed the first to
belong to Bothriocephalus osmert yon Linstow. This is the form he listed at first (1889) as Bothrio-
cephalus sp. The second is sp. 1 of the table, the third and fourth are united as sp. of the table,
and the fifth becomes sp. 11 of the table (see p. 1168).

1158 BULLETIN OF THE BUREAU OF FISHERIES.

In not a single case was a parasite found in the alimentary canal below
the pyloric cceca. Indeed, parasites which in other hosts inhabit only the
intestine, were found in the Rhine salmon to infest stomach and cesophagus,
as if better protected there than in the vicinity of the anus. The Rhine salmon
loses its intestinal guests like any fasting fish, and through the exclusion of
food any new importation of worms is prevented. From the absence of para-
sites behind the pyloric coeca one may conclude indirectly that Salmo salar
really fasts in the Rhine. When this species enters the river it is richly laden
with parasites. It loses its intestinal guests and these are not replaced by
any new supply. There remain only the natural inhabitants of the anterior
regions of the canal and those which can withdraw thither. Even these pro-
tected species diminish in number of species and individuals as the salmon
remains longer in fresh water and climbs higher in the stream, until finally
there are left only encapsulated forms. The journey up the Rhine has proved
at the same time a means of eliminating the intestinal parasites. Some investi-
gators, although without knowledge of these facts, have yet endeavored to
explain the migration of many fish as due to the necessity of freeing them-
selves from parasites acquired in the ocean.

Salmon caught in Holland, in the lower reaches of the Rhine, are richly
infested with parasites. Several species were regularly found in large numbers
and the parasitic fauna recalls strikingly that of the ocean salmon. Distomum
varicum was very abundant in the cesophagus and Bothriocephalus infundi-
bulijormis in the pyloric cceca. But fish from the upper reaches of the Rhine
presented a radically different picture. The parasites in cesophagus and
stomach were very rare. Dzstomum varicum had disappeared and Bothrio-
cephalus infundibulijormis appeared only as single, weak, emaciated specimens.
Often the entire alimentary tract yielded no trace of a parasite.

The parasitic fauna of the Rhine salmon decreases in proportion as the fish
ascends the stream.

A study of the seasonal distribution of parasites in the Rhine salmon
evidences that the number of species present becomes reduced in the winter
months, and the number of individuals also falls off markedly. The minimum
is reached in November and December, the months of spawning, when the fish
has penetrated farthest upstream. It has lost its unbidden guests on the long
journey. The maximum of parasitic infection is found in the summer months,
May to July, when the schools of salmon enter the river. Naturally the journey
exerts no influence upon those parasites which inhabit closed organs.

The question next considered is the origin of the salmon’s parasites, whether
marine, limnetic, or indifferent in character. The analysis of the forms recorded
indicates that the Rhine salmon does not exhibit a single true limnetic parasite,

INTERNAL PARASITES OF THE SEBAGO SALMON. I159

and its most abundant guests are typically marine. In spite of a long and
repeated sojourn in the river it does not infect itself with a single fresh-water
parasite, a fact that indicates strongly the complete fasting of the salmon while
in the Rhine. In other migratory fish the marine elements become greatly
reduced or even disappear entirely. Yet tabular comparisons show that in
contrast with the Rhine salmon all other migratory fish infect themselves in
fresh water more or less strongly with parasites, thus indicating that whereas
the salmon fasts in the Rhine, its near relatives feed abundantly on wandering
from the ocean into the river.

It was possible to examine also 34 salmon from the Baltic Sea; all of them
were infected, and a total of 12 species of parasites were recorded from them,
as follows:

Ascaris adunca Rudolphi.

Ascaris (Agamonema) capsularis Diesing.
Ascaris (Agamonema) communis Diesing.
Ascaris aculeati von Linstow.
Echinorhynchus acus Rudolphi.
Echinorhynchus pachysomus Creplin.
Distomum varicum Zeder.

Distomum appendiculatum Rudolphi.
Bothriocephalus infundibuliformis Rudolphi.
Bothriocephalus sp. 11 (larva).
Bothriocephalus sp. mr (larva).
Trieanophorus nodulosus Rudolphi (larva).

The Baltic salmon is much more heavily parasitized than the salmon of
the Rhine. Seven parasites are common to both, and of these five are more
abundant in the Baltic salmon and two only more abundant in the Rhine
salmon, while six parasites of the former do not occur in the latter. The rela-
tive infestation of the two forms is shown in the accompanying synopsis:

Infested with parasites of given number of species.

a Number Not
ish. exam- | ;
aed infected.
is Ze Se 4. 5.
A Per cent. | Per cent. Per cent. Per cent. Per cent. Per cent.
eines salto ee a ee 129 Bex || 42.6 3255 16.5 4.6 0.77
Balticisa limonene see 34 ° 50 23.5 17.6 8.8 °

Of parasitic species found in the Baltic salmon, Bothriocephalus infundi-
bulijormis was present often in enormous numbers, and the same was true of
Distomum varicum. On the other hand Ascaris capsularis did not manifest
the frequence or the abundance already noted for the Rhine salmon. Every-
thing indicates a rich and uninterrupted consumption of food by the Baltic

1160 BULLETIN OF THE BUREAU OF FISHERIES.

type in contrast with the fasting Rhine fish.* Parasites are also found in the
intestine behind the pylorus, where the Rhine salmon remains free from para-
sites. Among the intestinal parasites of the Baltic salmon also are included no
true limnetic species. Such only lie encapsulated in various organs. This indicates
that the infection with the true fresh-water parasites, Cucullanus, Trienophorus,
Ascaris aculeati, actually occurs in the rivers. The Baltic salmon comes into
fresh water as richly laden with parasites as the fish caught in the lower stretches
of the Rhinein Holland. While the parasitic fauna of the Rhine salmon decreases
in proportion as it ascends the stream, that of the salmon in many other rivers
is enriched by numerous limnetic elements. The natural explanation lies in
the fasting of the Rhine salmon, whereas its relatives in other streams do not
cease taking food. The Baltic salmon, having returned to the ocean, loses the
limnetic parasites of the open intestine but retains those located in the closed
organs of the host.

The material is too scanty to determine a seasonal distribution, if any
exists, and in fact the food of the Baltic salmon undergoes little change through-
out the entire year, so that no general modification would be expected in the
parasitic fauna, variations being merely of an individual or casual type.

Upon a careful study of the individual species the parasitic fauna of the
Baltic salmon manifests a more varied aspect than that of its relative. There
are 2 pure marine forms, in contrast to 8 in the Rhine salmon, 2 pure limnetic
species as against not a single one in the other host, 6 parasites found in both
marine and fresh-water fishes, and 3 parasites found only in the Baltic salmon,
with a fourth which can not be assigned with certainty to either type of environ-
ment. It is very striking that the purely marine Tetrarhyncht so abundant in
the Rhine salmon have not yet been demonstrated in the Baltic fish. These
relations are indicated in the appended table of parasites from the European
salmon, collated from various authors.

The Rhine salmon shelters a purely marine parasitic fauna, while the Baltic
salmon reckons many limnetic forms among its parasitic guests. This remark-
able condition finds its explanation in the continued feeding of the latter type,

@ One should not forget in estimating this factor as presented by Zschokke that in one important
respect conditions are not identical. The Baltic salmon are still in salt water; not until they enter
some estuary and begin the ascent of some river do they meet the fresh water environment to which
the Rhine salmon investigated by Zschokke are subject. To secure an exact parallel one should
compare the Baltic salmon with such of the Rhine variety as may be captured in the North Sea.
Zschokke refers in a later paper to some taken from this body of water and notes in their case also that
the average degree of infection with parasites is greater than in the case of those fish taken from the
Rhine stream itself. This fact only emphasizes the immediateness and definiteness of the effect on
the parasitic fauna of the salmon which is produced by the fresh water environment and abstinence
from food.

INTERNAL PARASITES OF THE SEBAGO SALMON. II61

even in fresh water, and the resulting enrichment of its parasitic fauna with
limnetic forms when it returns to the sea.

The parasitic record reflects clearly the manner of life led by any host.

In all, 33 species have been recorded from this salmon, making the list of
its parasites one of the longest known for any fish. ‘The list of these is then
given, as follows:

Ascaris adunca Rudolphi.

Ascaris angulata Rudolphi.

Ascaris clavata Rudolphi.

Ascaris (Agamonema) capsularis Diesing.

Ascaris (Agamonema) communis Diesing.

Ascaris aculeati von Linstow.

Cucullanus elegans Zeder.

Echinorhynchus proteus Westrumb.

Echinorhynchus pachysomus Creplin.

Echinorhynchus acus Rudolphi.

Echinorhynchus agilis Rudolphi.

Distomum varicum Zeder.

Distomum reflexum Creplin.

Distomum miescheri Zschokke.

Distomum appendiculatum Rudolphi.

Distomum ocreatum Rudolphi.

Distomum tereticolle Rudolphi.

Distomum sp. McIntosh.

Bothriocephalus infundibuliformis Rudolphi.

Bothriocephalus cordiceps Leidy.

Bothriocephalus osmeri (larva) von Linstow.

Bothriocephalus sp. 1 (larva) Zschokke.

Bothriocephalus sp. 11 (larva) Zschokke.

Bothriocephalus sp. m1 (larva) Zschokke.

Schistocephalus dimorphus Creplin.

Triznophorus nodulosus (larva) Rudolphi.

Leuckartia sp. Moniez.

Tetrabothrium minimum von Linstow.

Rhynchobothrium paleaceum Rudolphi.

Tetrarhynchus solidus.

Tetrarhynchus grossus Rudolphi.

Tetrarhynchus macrobothrius von Siebold (=Stenobothrium appendicu-
latum Diesing).

Tetrarhynchus sp. McIntosh.

The paper of Zschokke closes with a detailed discussion of the biology and
relationships of the individual salmon parasites, including citations of the work
of previous investigators on these forms.

I162 BULLETIN OF THE BUREAU OF FISHERIES.

In a later paper Zschokke (1896) lists the parasites of salmon caught in the
Rhine at Basel, including the results of examinations extending over several
years and embracing 16 species, as follows:

Bothriocephalus infundibuliformis Diesing.
Tetrarhynchus solidus Drummond.
Tetrarhynchus sp.

Schistocephalus dimorphus.
Distomum varicum Zeder.

Distomum appendiculatum Rudolphi.
Distomum ocreatum Rudolphi.
Distomum reflexum Creplin.
Distomum miescheri Zschokke.
Ascaris clavata Rudolphi.

Ascaris capsularia Diesing.

Ascaris sp.

Ascaris sp.

Echinorhynchus claveceps Zeder.
Echinorhynchus acus Rudolphi.
Pisicola geometra Linneus.

Unreported previously are Echinorhynchus claveceps Zeder, Pisicola geom-
etra Linneus, and possibly also two undetermined species of Ascaris. Elimi-
nating forms which do not properly belong to the Rhine at Basel and adding
species recorded previously, the net result is 17 species of parasites in the salmon
at Basel, or one-third of the total known parasitic fauna of that region. Of
these 17, 13 are characteristic of the salmon and wanting in other fish there.
The large majority of the list are of purely marine character and a further
group is characteristic of migratory fish, leaving nothing of a limnetic type
save Pisicola geometra, a leech which is merely a temporary ectoparasite.

This paper records also the results of the examination of additional salmon
from the North Sea, the lower Rhine, and the middle and upper Rhine, making
the grand total of 179 Rhine salmon examined by this author. The only new
parasite recorded is Scolex polymorphus Rudolphi. Again, later, Zschokke
(1902, p. 128-130) discusses the records of his earlier work without adding any
new data.

In studies on the Rhine salmon Hoek (1899) records that he found in the
young fish an ascarid, according to Fritsch A. clavata, and repeatedly specimens
of a species of Echinorhynchus which Fritsch names E. pachysomus Creplin,
though he did not observe it in the young salmon. In Hoek’s opinion the forms
obtained, though not fully grown, agree better with the description of E. proteus
Westrumb, and indeed with the more limited concept of the name according to
Hammann. Hoek observed not infrequently that young salmon were infested
with a leech, Cystobranchus (Pisicola) respirans Troesch, which lived as an
ectoparasite on the skin.

INTERNAL PARASITES OF THE SEBAGO SALMON, 1163

Concerning the Baltic salmon, other fragmentary data are also on record.
Olsson (1867) reported Bothriocephalus proboscideus Rudolphi as frequent in
Salmo salar both from fresh and from salt water during April and August.
Later the same author (Olsson, 1876) listed Distomum appendiculatum Rudolphi
as frequent in Salmo salar during August. Again (1893) he reported Distoma
appendiculatum Rudolphi from the stomach as abundant in July. The material
came from the Baltic Sea and the Gulf of Bothnia.

Hausmann (1897) lists from Salmo salar Distomum appendiculatum, D. ocrea-
tum, D. reflexum, and D. varicum. Among 20 specimens examined 13 only
were infested with trematodes.

Mithling (1898) records from Salmo salar in East Prussia six species of para-
sites, as follows: Bothriotenia proboscidea, Apoblema appendiculatum, Echino-
rhynchus acus, Ech. fusijormis, Ech. proteus, and Ech. pachysomus. The first
two are very common, the others occasional. Ech. fusijormis is cited after
Neumann.

G. Schneider (1902) reports the following data concerning salmon parasites
in Finland: A salmon 1 m. long, caught November 6, 1900, in the mouth of the
river, was infested with several hundred individuals of Bothriotenia proboscidea
Batsch, which entirely filled the pylorus portion of the intestine and of the
pyloric cceca. Otherwise the intestine contained no parasites and no food. A
second salmon, investigated fresh July 2, 1902, had in the intestine the young
and adult Bothriotenia proboscidea Batsch and one Echinorhynchus larva, which,
however, evidently came froni fish that had been eaten. In the stomach of
this salmon he found Clupea sprattus Linneus [p. 18 the name is given as Clupea
harengus membras 1,.] and in the intestine remains of digested fishes, probably
also herring. The synchronus presence of herring remains and of very young
Bothriotenia in the intestine of this salmon confirms fully his formerly expressed
opinion that the salmon infects itself with tapeworms through eating the
herring.

According to Schneider (1902, p. 20), Kessler in a Russian paper 1eported
the occurrence of adult Bothriotenia proboscidea in the intestine of Salmo salar
from Lake Onega. This body of water is directly connected with the Baltic
Sea, where, according to Miihling, as just noted, this species is a very common
parasite of the salmon. Schneider has also found it abundant in salmon from
the Gulf of Finland.

No doubt some observations have been made on the parasites of salmon in
the Scandinavian peninsula, but they have thus far eluded my search.

Concerning the parasites in the British Isles many observations are on
record. But they concern individual investigations at particular locations, and
as a rule do not cover any continuous study of the problem. In consequence the
lists are not as complete as those already cited for the Rhine and the Baltic,

1164 BULLETIN OF THE BUREAU OF FISHERIES.

and it is somewhat difficult to draw a precise comparison with the data for the
latter regions. First may be placed such records as concern streams directly
connected with the North Sea, and hence with the body of water from which
the Rhine salmon come.

Concerning the parasites of salmon in the Tay, McIntosh (1863) has recorded
certain data. More than 100 fish were examined, few were entirely free from
parasites, many were richly infested. The parasitic species were both fre-
quent and abundant, although only ro species are definitely recorded, as against
14 in the Baltic and 20 in the Rhine salmon. The species from Tay salmon
McIntosh lists as follows:

Ascaris (Agamonema) capsularia Diesing.
Echinorhynchus proteus Westrumb.
Echinorhynchus pachysomus Creplin.
Distomum varicum Creplin.

Distomum tereticolle Rudolphi.

Distomum sp.

Bothriocephalus infundibuliformis Rudolphi.
Tetrabothrium minimum von Linstow.
Tetrarhynchus macrobothrius von Siebold.
Tetrarhynchus sp.

The examination of this list shows clearly that the Scotch salmon combines
elements from the parasitic fauna of both its relatives, the Rhine salmon and
the Baltic salmon. The strong and continued infestation of the intestine below
the pylorus goes to establish the fact that the taking of food is continuous.

No seasonal distribution of parasites could be noted, but the character of
the parasitic species was striking. “One pure marine species and two almost
equally such, together with five characteristic salmonid parasites, show that the
major portion of the parasitic fauna is of marine origin. On the other hand, the
intestinal parasites were in large part not marine, but limnetic forms or such as
are typical in the salmon. Asin the Rhine salmon, so also in the Tay, the marine
alimentary parasites are gradually lost without being renewed. They are replaced
by such as are of evident limnetic character. Hence the conclusion of McIn-
tosh, based on other evidence also, that the Tay salmon does from time to time
take nourishment during its stay in fresh water. A comparison of the parasitic
fauna of the three salmons gives, according to Zschokke, the following:

Besides in migratory fish also in—
Typical ane In other :
: Number of romitia other migratory == ;

aes ee particular salmon pee Marine Limnetic Both ma-

P F salmon. | and other Saar fish fish rine and

localities. : cs ar limnetic.
Rhine/salmon=s="5 - oe eee ee ee 20 2 2 2 8 I 5
Balticisalmon™= <== == =2ea eee ene 14 I 2 I 2 2 6
Tay salmon=>— ===: 25-2 pes eee Io 3 I ° I 2 3

|

INTERNAL PARASITES OF THE SEBAGO SALMON. 1165

Much later than the work just outlined is a paper by Tosh (1905) in which
he discusses his work on the internal parasites of the Tweed salmon. The mate-
rial was collected in 1895 at a single place. The author notes the distinctly
marine character of the parasitic fauna of this salmon, attributing it to the fact
that ‘salmon do not feed in the fresh water of a short river like the Tweed, except
under extraordinary conditions, when a prolonged stay is imposed upon them.”’
In all he lists 15 species, as follows:

Ascaris capsularia Rudolphi.

Ascaris acuta Muller.

Ascaris obtusocaudata Zeder.

Distoma varicum Rudolphi.

Distoma ocreatum Rudolphi.

Distoma miescheri Zschokke.
Echinorhynchus acus Rudolphi.
Echinorhynchus proteus Westrumb.
Echinorhynchus angustatus Rudolphi.
Bothriocephalus infundibuliformis Rudolphi.
Tetrarhynchus grossus Rudolphi.
Tetrarhynchus macrobothrius Rudolphi.
Tetrabothrium minimum (larva).
Tetrabothrium sp. (larva).

Tenia sp. (larva).

Details are given concerning the frequence, appearance, and biology of
each form. The most important is held to be Bothriocephalus infundibuliformis,
which, according to an appended table, occurs in 26.4 per cent of the 892 fish
examined. It does not seem, in the opinion of Tosh, to be seriously harmful to
the host and is found in the largest and best-fed fish in numbers ranging from
1 to 6 per host. The tremendous infestations noted by Zschokke apparently do
not occur in this region in the salmon, although observed in the sea trout.

The only notices from Ireland concerning salmon parasites are brief and
also of long standing. Drummond (1838), writing in Belfast, described Tetra-
rhynchus grossus from the abdominal cavity of the salmon, which he found only
once, and Tetrarhynchus solidus, new species, from the peritoneum and mesentery,
which he took from three salmon in July, 1838.

Somewhat later Bellingham (1844) listed among the entozoa indigenous to
Ireland the following taken from the salmon, namely:

Ascaris capsularia, on the peritoneum; also in 14 other species of fish,
all marine.

Ascaris clavata, from intestine and peritoneum; also in 9 other species of
fish, all marine.

Disioma varicum, from the stomach; common in some localities and seasons,
rare in others.

Tetrarhynchus grossus, from the abdominal cavity; entered in this list on
the authority of Drummond (1838).

1166 BULLETIN OF THE BUREAU OF FISHERIES.

Tetrarhynchus solidus, from the abdominal cavity; a single specimen loose
in peritoneal cavity.

Bothriocephalus proboscideus, from intestine and pyloric cceca; exceedingly
common and most so in largest and fattest salmon.

One should always recall the relative value of such comparisons as those in
the preceding pages. The fact that from Irish salmon only 6 species of para-
sites are recorded, from the Scotch form ro species, from the Baltic form 14 spe-
cies, and from the Rhine salmon 20 species, is partly accounted for by the amount
of attention directed to the various forms. Thus the first record concerning the
Rhine salmon (Zschokke, 1889) listed 11 species of parasites obtained in the
course of examining 45 specimens of the Rhine salmon. The second record by
the same author (Zschokke, 1891) included 20 species of parasites from 129
hosts, and the third record (Zschokke, 1896) gave 23 species of parasites from a
total of 179 hosts. Of these 136 came from the Rhine itself and 43 from the
sea. More extended study of any host will increase the list of the parasites
which it is known to support.

The same species of fish, Salmo salar, occurs in streams on the western or
American coast of the Atlantic Ocean. Thus far no one appears to have devoted
especial attention to the parasitic fauna of the American fish, but some scattered
references to species found in our American salmon are recorded by different
authors. No doubt the list can be extended considerably by longer search,
but so far as I can ascertain the following brief references include all records of
salmon parasites made on this continent and published up to the present time.

According to Zschokke (1891) Leidy reported Bothriocephalus cordiceps
from the intestine of Trutta salar Linneus. The reference, which is apparently
cited from von Linstow (1878), is incorrect both in location and content. Leidy
(1871) reported on the authority of Professor Hayden “the brook trout, Salmo
jontinalis, of the headwaters of the Yellowstone River, to be much infested
with a species of tapeworm * * * from the abdominal cavity, but not from
the intestinal canal * * *. It belongs to the old genus Bothriocephalus, and
to that section now named Dibothrium.’’ This new species was named Diboth-
rium cordiceps. The species was subsequently studied in detail by Linton. I
am unable to find any other reference to this parasite in the writings of Leidy
or any record of its occurrence in any other than the original host, which was in
reality Salmo mykiss, the Rocky Mountain trout; the adult parasite occurs in
the intestine of the American white pelican, Pelecanus erythrorhynchus. This
parasite accordingly seems to have no relation whatever to the salmon and
should be eliminated from the list of its parasites.

In the catalogue of parasites from various collections in the United States
by Stiles and Hassall (1894) there are listed from Salmo salar Bothriocephalus

INTERNAL PARASITES OF THE SEBAGO SALMON. 1167

proboscideus from Berlin in the Stiles collection and Bothriocephalus sp. from
England in the Hassall collection; no specimens whatever are noted as having
been taken from autochthonous fish.

In a list of trematodes from Canadian fishes Stafford (1904) records from
Salmo salar Linneus, Derogenes varicus O. F. Miiller, found in mouth, cesoph-
agus, and stomach; Hemiurus appendiculatus Rudolphi, found in cesophagus and
stomach; Lecithaster bothryophorus Olsson (=Apoblema mollissimum Levinsen),
and Sinistroporus simplex Rudolphi, from the intestine. The fish were appar-
ently purchased in the markets in Montreal and represent conditions during
the spring and autumn months of 1903.

I have found no further references to the parasitic fauna of Salmo salar on
this continent. The list contains two species not previously recorded for this
host, and yet it is insignificant in comparison with European records for the
same host.

Appended hereto is a tabular list of all parasites hitherto reported from
Salmo salar, arranged according to the place which the parasites hold in the
present accepted system. The taxonomy of these groups is at present in such
confusion that I have contented myself with entering the names employed by
the author cited and in making a few inevitable corrections. Any attempt to
adjust the nomenclature adequately would demand an amount of time beyond
my present command and an amount of space out of keeping with the rest of
this article. By the citation in the table of the authority, date, locality, and
location, the reader is enabled to form at a glance a general opinion regarding
the importance of any parasite yet reported from the salmon and to follow up
its record with the minimum delay.

BULLETIN OF THE BUREAU OF FISHERIES.

1168

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1169

INTERNAL PARASITES OF THE SEBAGO SALMON.

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BULLETIN OF THE BUREAU OF FISHERIES.

1170

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L172 BULLETIN OF THE BUREAU OF FISHERIES.

PARASITES OF PACIFIC SALMON.

The list of parasites for Atlantic salmon in America, though small, is much
more extended than the records concerning the Pacific salmon. While tremen-
dous numbers of the latter fish, which belong to several species of the genus Onco-
rhynchus, are taken every year for commercial purposes, apparently no one has
studied the parasitic fauna or done more than to record casually a few data
taken during a study of some other factor concerning the species. Even of such
notes I have found only a very few.

In a report on the life history of the Alaska salmon, Bean (1890, and also
1893) noted a few items concerning parasites. He mentions the presence in
1889 of numerous intestinal worms in the red salmon and finds that all species of
salmon [in fresh water?] are more or less covered with parasitic copepoda.

Much more extensive are the notes made by the brilliant young naturalist

-and student of the Pacific salmon, Cloudsley Rutter, who only a short time
back met such an untimely death.

In the course of investigations on the natural history of the quinnat salmon
in the Sacramento River, Rutter (1902) records some interesting items regarding
their parasites. A common pest in the adult of this species in fresh water is a
parasitic copepod which attaches itself to the gill filaments. Usually not
numerous on a single fish, they yet sometimes destroy the gill filaments almost
entirely. The intestine of the spawning salmon is frequently inhabited by
tapeworms extending into the cceca and at times filling them completely. They
do not occur in the stomach. In 1898 they were much more abundant than in
1900. Among 200 young salmon examined from fresh-water stations in the
Sacramento basin in May, 1898, and April, 1899, parasites were found in the
stomach contents of 31 fish. They were described as of two or three kinds, one
elongated [cestode?], the others short and grain-like [trematodes?]. Rutter
thinks that residence in fresh water is conducive to the growth of parasites in
the stomachs of young salmon. He gives the following tables of their occurrence
according to size of host and dates of capture.

OCCURRENCE OF PARASITES IN QUINNAT SALMON FROM SACRAMENTO RIVER.

According to dates of capture.

Month Number | Number with Percentage
5 . examined. | parasites, with parasites.

SATAY Sate ee Se ies ce ete ae oe ete 9 I II
February _ | 10 ° °
March---- 10 ° °
Aprily_ s.2 15 ° °
Mays <5 Us Ss a ne es re Se a en ne eee 50 | 4 8
Viuly cee 2 oe. Y os ee NN eee ee ete eee eee 21 | I 5
August_____ 20 | 3 15
September _ - 18 3 17
October ___~ 30 8 23
November __ 15 cK} 20
December. === 2-— --— 2 eee SSeS ee a ee | II 8 73

MS Cea AE so Ses a oe ee | 09 31 15

INTERNAL PARASITES OF THE SEBAGO SALMON. 1173

OCCURRENCE OF PARASITES IN QUINNAT SALMON FROM SACRAMENTO RIVER—Continued.

According to size of fish.

Sire Number Number with Percentage
examined. parasites. with parasites,
TACO W201 11 Ch CS See sei eee eee ee se Pa Se ek Se! 61 | 3 5
2.1 to 3 inches___ 57 3 5
3-1 to 4 inches___ 53 | 10 | 19
4.1 to 5 inches___ 3 30 | 12 40
ipstto 603) inches 2-2) — oe ee eas a So oe Soe aes ess aseseseea sce as | 8 3 | 38
BERG i ba a ee 209 | 31 | 15

It will be noted that the percentage of infestation increases rapidly with the
size and age of the fish, but this would naturally be associated with the more
extensive feeding of the older and larger fish, whether in fresh or salt water. In
the absence of comparative data for salt water forms to contrast with these of
summer residents in fresh water, it is not allowable to attribute this condition
to the delayed migration of these fish, as Rutter does. From brackish-water
stations 20 young salmon were examined and parasites found in 3 only. This
number is too small to be available for comparison with those fresh-water forms
noted above. Unfortunately no further data are available concerning the
varieties of parasites found either in the adult or in the young specimens. It is
probable that the adult parasites are the same as certain forms to be discussed
later from the Alaska salmon.

OBSERVATIONS ON THE SEBAGO SALMON.
SPECIFIC RELATIONSHIPS

The Sebago salmon is regarded by some as merely a landlocked variety of
the Atlantic salmon, Salmo salar, found both in European streams and in the
rivers of Maine and northward. By others it is viewed as a separate species,
Salmo sebago, but in any event closely related to the former. In their extensive
catalogue of North American fishes, Jordan and Evermann (1896) include all
these forms in the single species Salmo salar Linnzus, speaking of its range as
follows:

North Atlantic, ascending all suitable rivers in northern Europe and the region
north of Cape Cod to Hudson Bay; formerly abundant in the Hudson and occasional in
the Delaware, its northern limit in the Churchill, Albany, and Moose rivers, flowing into
Hudson Bay; sometimes perfectly landlocked in lakes in Maine and northward, where
its habits and coloration (but no tangible specific characters) change somewhat, when
it becomes (in America) vars. sebayo and ouananiche. Similar landlocked varieties
occur in Europe.

Of the Lake Sebago form which I had the opportunity of studying and
which these authors regard as a subspecies, Salmo salar sebago (Girard), they
write as follows:

Smaller in size, rather more plump in form, and nonmigratory; not otherwise evi-
dently different. Sebago Pond and northward; introduced into lakes in various parts
of the country; seldom entering streams; reaches a weight of 25 pounds.

1174 BULLETIN OF THE BUREAU OF FISHERIES.

It is important to notice that the same authors also recognize a second
subspecies, and this may be the form from which were obtained the parasites
reported by Stafford (1904) and already commented upon. Concerning this
subspecies, Jordan and Evermann write that Salmo salar is—

* 3 represented in Lake St. John, Saguenay River, and neighboring waters
of Quebee by the landlocked Salmo salar owananiche McCarthy MS., new subspecies.
Still smaller, rarely reaching a weight of 714 pounds and averaging 31%. An extremely
vigorous and active fish, smaller and more active than ordinary salmon, but so far as
known not structurally different. Saguenay River, Canada (outlet of Lake St. John),
and neighboring waters.

Were it possible to determine definitely whether the records of Stafford
concern the oceanic form caught during its migration or the landlocked form,
a more definite value could be placed upon his data. In the absence of such
information one can not venture to use these records at all in the discussion
of the biological problems concerned. What these problems are will be clearer
after a more detailed consideration of the case.

SOURCE OF PARASITES.

In view of the close specific connection of the two forms, the European sal-
mon just considered and the Sebago salmon, a comparative study of their para-
sitic fauna is of unusual interest, especially since the Atlantic salmon spends
the greater part of its life in salt water, and after its entrance into fresh-water
streams in the course of its migration does not in most cases partake of any food.
Consequently whatever parasitic guests it harbors must, as already explained, be
of marine origin. The exceptions to this statement are due to accidental infec-
tion, and are both small in numbers and insignificant in variety and relative
importance. On the other hand, the landlocked Sebago salmon never enters
salt water. Its period of active feeding and growth is passed in inland waters,
those of Sebago Lake in the case of the specimens we secured and examined.
Whatever parasites it harbors are hence obtained in that lake, and are either pure
fresh-water organisms or such as have been introduced with the host and subse-
quently acclimatized to a fresh-water existence. In the case of such parasitic
species as undergo direct development, like many nematodes, the introduction of
a marine parasite into fresh water involves the habituation of the free living stage,
either egg or larva, or both, to the limnetic environment, and this is the identical
process involved in the transfer of any free living organism from a marine exist-
ence to one in fresh water. In the case of parasites which manifest indirect
development with change of host the case is much more complicated. Such
parasités usually have one or more brief stages of free existence in the open
water as egg, embryo, or larva, like those just referred to. But they also employ
one or more intermediate hosts, in which certain parts of the development are
passed. Now, either the same marine animals which serve as intermediate
hosts in the sea must be found in fresh water also, or must be successfully

INTERNAL PARASITES OF THE SEBAGO SALMON, IGS

introduced at the same time with the primary host and its parasites to which
they are related, or, finally, there must be present in the fresh water other animals
which can serve successfully as intermediate hosts. The interrelation is thus very
complicated and the chance of achieving it so small that in most cases marine
forms do not bring the majority of their parasites with them in the transfer to
fresh-water existence. In other words, limnetic animals are less heavily para-
sitized than marine. For this reason the examination of so recent a migrant
into fresh water as the Sebago salmon is of great biological interest.

At Lake Sebago only 7 specimens of the Sebago salmon were obtained and
examined. These weighed, respectively, 2, 2, 2,3,5!2,8,and16pounds. While
the number examined was from one standpoint small, yet in view of the scarcity
of the species in the lake it was fortunately large. The series was also representa-
tive of different ages, ranging probably over several years in growth. It seems
likely that if marked variations in food materials were found such a range of
specimens would indicate the fact through differences in parasitic infestation.
Yet there was a striking uniformity in the records in the series. Furthermore,
the fish were all examined very soon after capture, and thus any post-mortem
wanderings, which certainly do influence the location of parasites collected
from market fish, were largely avoided. No doubt there are rare parasites of
this species which are not represented in this collection, but, all things being con-
sidered, it may be asserted with some confidence that the records give a true
picture of the number and location of the parasites infesting them.

The parasites found are recorded in the following table:

RECORD OF PARASITES FROM SALMO SEBAGO.

[x=many. xx=very many. §=more than in fish no. 14—not counted.]

Host. Parasites, number and location.
§ -
| = Ses) Pyloric coca and : : >
=, we phagus and . Intestine behind py- :
a | 2 3 stomach. adiscent pert of loric ceca. Body cavity.
a ia |e | a
In. | Lbs. ‘
14 | 16 2 3 | 7 Azygia sebago--_--_-_ 45 Abothrium cras- | 1 Proteocephalus pusil- | 1 Nematode A.
sum. lus.
(@yiziNematode Al == Eas nse ee 1 Azygia sebago________| (?) See also stomach.
I5 | 16 2 o | 13 Azygia sebago__-_-_- § Abothrium cras- | 1 Proteocephalus larva_
sum.
eS, |S aeel eeeer Be Se ea ee [beck scat le ee ae | 1 Bothriocephalid larva_
aoe e Pre) Sees ees oe ee eee oe | es Se oe aa ae Proteocephalus pusillus_
16 | 27 8 o | xx Azygia sebago @_____ 7o Abothrium cras- | Proteocephaluspusillus_| ; large Bothriocephalid
sum. | larva.
pe el eS Se) een eee = St en eel [ace ea ee | 1 Bothriocephalid larva_| small larval cestode.
aa x7 2 Gil neAzyeia sebapose= == 30-1 A bothrinm cras-1)- 2 ee ee eee
| sum.
ATA eS3h|exOns| lye |)xSeAzvela-sebaro.———|)8o\Albothrinm (cras-)|-" === ee 33 Nematode B.?
| sum,
Be See a Me a al (ea el | emg ne ee ee | x Bothriocephalid larva
encysted in spleen.
42 | 19 234 |) On i eCkeAzyela sebagos—.-.|| x Abothrium eras- |22l7=- 2-2-2 Se ee ee 3 Nematode A.
sum. |
106 | 22 5u4| o 19 Azygia sebago______| OPA DOLNTIMIN CTA S—5 [eet eee | Not examined.
sum.
Go) tor Nematode ds sae | eee ee ee (2) See also stomach.
| | |

@ Also in swimming bladder (?). See text. > Viscera a mass of adhesions; parasites difficult to pick out.

1176 BULLETIN OF THE BUREAU OF FISHERIES.
A NEW TREMATODE PARASITE.

Every one of the 7 fish examined contained specimens of a new trematode,
which I have named Azygia sebago. It is relatively insignificant in size and
difficult to detect amid the thick white mucus which lines the wall of stomach
and cesophagus. Nota single host was without this parasite, and several salmon
sheltered considerable numbers; yet in most cases they were not seen in life, but
only appeared after the stomach and its contents had been agitated in a pre-
serving fluid. Careful examination of the débris then never failed to disclose
some specimens of this worm. Moreover, it was the only species of trematode
that was found in the Sebago salmon. The description of the species may
properly precede a discussion of its biological characteristics.

The genus Azygia was established by Looss (1899, p. 569) to include a well-
known [European species, istomum tereticolle Rudolphi, which was made the type
of the new genus. It was also the only species in the genus; for, as Looss remarks,
he had not been successful in finding among the flukes that he knew any form
which could be included naturally with the old species, Distomum tereticolle.
‘There are at the disposal of the student several good descriptions and delinea-
tions of the old species, Azygia tereticollis Rudolphi, so that it is possible to
determine with precision its structural features; the best of these descriptions is
undoubtedly that by Looss (1894).

The new species, Azygia sebago,? is much smaller than the older form,
measuring 10 mm. in maximum length and averaging 5 to 6, or less often 8 mm.,
in well-developed specimens. Fortunately, I have a large range of sizes, from
such as are only barely, over 1 mm. in length to the maximum noted, so that it
was possible to follow the changes accompanying the assumption of the adult
form. Specimens 2.85 mm. long have not yet produced ova.

The general form of the body is cylindrical, bluntly rounded at the anterior
end, and tapering slightly toward the posterior end, which, however, is ulti-
mately rounded off. The body is regularly divided into two regions by a shal-
low furrow at which the direction of the long axis changes more or less (fig. 1),
giving the worm in lateral aspect much the appearance of a can-top tightener.
While the relation of the regions is very variable, at times forming almost a sin-
gle straight line and again standing at a considerable angle with each other, yet
one can make out these conditions even in specimens which are poorly killed and
badly distorted. The anterior region assumes the form of an ellipse surrounding
the two suckers. This region changes relatively little in size with growth. In
one of the smallest specimens measured (1.6 mm.) the distance between the

aDuring the spring of 1908 two of my students, Messrs. W. N. Anderson and H. B. Boyden, made
a study of this form and prepared a partial report on its structure, to which I am indebted for some
of the data in the following description, and also for two figures.

INTERNAL PARASITES OF THE SEBAGO SALMON. 09/7

centers of the two suckers was 0.5 mm. In one 10 mm. long this distance
measured 1 mm.

The posterior region is nearly a perfect cylinder until shortly before the
tip, where it tapers somewhat. In some specimens the posterior end is consid-
erably inflated and appears semitranslucent. This is undoubtedly due to the
distended condition of the excretory reservoir, which inhibits contraction of
the circular muscles in the portion of the skin adjacent to it.

The breadth of the body varies according to the degree of contraction, but
may be estimated in general as from 0.7 to 1 mm. An immature specimen
2.85 mm. long measured 0.65 mm. in breadth between the suckers, 0.6 mm.
behind the acetabulum, and 0.52 mm. behind the posterior testis. An imma-
ture specimen only 1.6 mm. in length measured 0.32, 0.28, and 0.21 mm. in
breadth at the same points. In cross section the body is round or very
slightly oval.

The oral sucker is subterminal and its opening looks almost directly ventrad.
It is rather conspicuous, and in an average specimen measured 0.68 mm. in
antero-posterior diameter and 0.67 mm. transversely. The depth in the same
specimen was 0.6 mm. The orifice is nearly circular, though often appearing
slightly flattened along the posterior margin. In an immature specimen 2.85
mm. long the oral sucker measured 0.35 mm. in antero-posterior diameter and
o.4 mm. laterally; the orifice measured 80 by 150 pz.

The ventral sucker or acetabulum is usually distinctly smaller than the
oral. In the extreme case it appears about equal in size or, on the other hand,
only about half aslarge. Ordinarily it is prominent, but in short, thick specimens
it is almost hidden, whereas in elongated, slender specimens it projects so far as
to appear almost pedunculate. It is also often slightly oval in a transverse
plane. Inanadult specimen it measured 0.57 mm. in antero-posterior diameter
and 0.69 mm. laterally. Ina specimen 2.65 mm. long the corresponding meas-
urements were 0.3 and 0.33 mm., and the orifice measured 52 by 80 p.

The alimentary canal opens in the oral sucker, close behind which lies the
pharynx without any prepharynx between the two. The pharynx measures
0.21 by 0.13 mm. It is often seen in the vertical position represented in the
figure of Messrs. Anderson and Boyden, which I have taken the liberty of copying
here. The cesophagus is very short and it often proceeds anteriad from the
upright pharynx, as shown in the drawing (fig. 3, pl. cxx1). Atits tip start the
two branches of the intestine, which also usually extend forward a short distance
and then turning posteriad continue almost to the extreme posterior tip of the
body. These crura being longer than the body in the usual specimen are thrown
into folds, which often appear as if the canal possessed irregular outpocketings,
such as one finds in Paragonimus. Observations both on the living material and

1178 BULLETIN OF THE BUREAU OF FISHERIES.

on serial sections show positively that such is not the case, but that the crura
are simple tubes. The number of folds, twists, and turns depends upon the
degree of contraction and usually appears greatest between the acetabulum and
the ovary.

The excretory system is very characteristic of the genus Azygia. An
elongate carrot-shaped collecting reservoir or bladder extends from the
excretory pore, which is located at the posterior tip, through the center of the
body anteriad to the posterior testis. The wall is heavy and is thrown into
folds which appear at intervals projecting slightly into the cavity. From the
anterior end of this reservoir two tubes pass off, right and left, which are
at the start dorsal to the posterior testis; they soon pass toward the ventral
surface, but cross the acetabulum on its dorsal aspect and dorsal to the oral
sucker and are reflected posteriad. During their entire course they lie within the
intestinal crura and usually ventrad to it. Their heavier walls indicate clearly
that these conspicuous tubes are more nearly analogous to the collecting reser-
voirs of other flukes than to the delicate excretory vessels which here also are
seen connecting with the tubes and the reservoir at various points.

The three germ glands, the ovary and two testes, lie close together in a longi-
tudinal row distant from the anterior end about two-thirds the length of the
worm. The ovary is most anterior and smallest of the group. An unusual
morphological feature is the inclusion of the shell gland, a small yolk reservoir,
the ends of the yolk ducts, and the first coils of the uterus within the same capsule
that incloses the gland proper (fig. 6, pl. cxx1). The relation of the ducts as
worked out by reconstruction is represented in figure 5 after the studies of Messrs.
Anderson and Boyden. This resembles closely conditions as shown by Looss
(1894) for A. tereticollis, although I do not find that he has noted the massing of
organs within a common capsule. The uterus extends forward in numerous short
coils which all lie within the intestinal crura until at the acetabulum it merges
into a short, heavy-walled metraterm. The latter passes dorsal to the acetabu-
lum and ventral to the cirrus pouch into the genital cloaca, with an inconspicu-
ous genital pore located just anteriad to the acetabulum.

The vitelline glands lie along either side of the worm exterior to the intestinal
crura. They begin a little behind the level of the acetabulum and extend to a
point about halfway from the posterior testis to the end of the body. This
constitutes perhaps the most striking morphological difference between this
species and Azygia tereticollis, in which the vitellaria do not pass posteriad of
the posterior testis. This conspicuous difference in the extent of the vitellaria
enables the student to differentiate the two forms at a glance.

Attention should be called to the fact that on account of this structural
feature a correction must be made in the generic description of Azygza, in which

INTERNAL PARASITES OF THE SEBAGO SALMON. 1179

stress was originally laid on the extent of the vitellaria. The condition of the
vitellaria in the older species has also been employed by Pratt (1902) as a char-
acteristic of the genus in elaborating his key for the determination of the flukes.
Although typically a member of the genus Azygza, the present form would fall
in another genus according to the terms of that synopsis. No one who sees a
specimen or reviews the structure of this form can doubt its relationship; the
precise extent of the vitellaria is evidently a subordinate feature, and as such
of specific rank only.

The follicles of the vitellaria are distinct, regularly oval bodies, lying in
two longitudinal rows on each side with a more or less conspicuous break oppo-
site the ovary between the anterior and posterior series. The follicles measure
from 0.06 to 0.07 by 0.03 to 0.04 mm. The symmetry of the rows is in places
interrupted by extra follicles, making at such points three rows of follicles
instead of two as usual. The ducts from the anterior and posterior series unite
opposite the ovary to form a common transverse duct which at the center of
the body joins its fellow from the opposite side. At the point of union there is a
small yolk reservoir. As already noted, this is included within the common
capsule which surrounds the ovary and is ordinarily not visible except in sec-
tions. Laurer’s canal is present and opens on the dorsal surface just posterior
to the ovary. It does not have the enlargement ordinarily called a seminal
receptacle, but is usually somewhat coiled and lies on the left side of the ovary.
This may be an adaptation to the extreme variations in length so character-
istic of this worm.

The eggs are small; an average of 50 measurements places their size at 48
by 27 #, which is slightly larger and broader than those of A. tereticollis, accord-
ing to the measurements given by Looss (1894).

The testes are oval bodies lying one directly behind the other and that
behind the ovary. The three organs are separated only very slightly from each
other. The outline of the testes is smooth and measures 0.42 to 0.46 by 0.59
to 0.6 mm. with the major axis transverse. One can usually distinguish that
the two are not equal in size. The coiled seminal vesicle and a poorly devel-
oped cirrus with prostate lie in a common connective tissue capsule, the cirrus
pouch, which stands immediately anterior to the acetabulum. The pouch
measures about 0.23 by 0.17 mm. in diameter. It opens anterior to the metra-
term into the genital sinus already mentioned.

One histological feature deserves consideration here because of its con-
spicuous character. In sections of Azygia sebago one notices certain muscle
elements which are so prominent and regular as to deserve almost the name of
a layer; they occur within the parenchyma, far removed from the usually rec-
ognized dermal layers and at a point where ordinarily one finds only scattered

1180 BULLETIN OF THE BUREAU OF FISHERIES.

dorso- ventral or oblique fibers which are not subject to any regularity in
arrangement. These are longitudinal fibers extending from the oral sucker -
throughout the entire length of the distome, as is clearly seen in a frontal section
(fig. 4, pl. cxx1). In position they lie one-fourth to one-fifth the radius of the
section distant from the external surface. The cross sections of these fibers
show them to be much heavier than the other muscle elements and to occupy
an oval zone parallel to the outer surface of the body. They divide the body
accordingly into a cortical anda medullary portion. ‘The vitellaria are the only
conspicuous organs which lie in the cortical layer. This muscle layer is
undoubtedly related to the marked contractions of the fluke which have already
been commented upon. Unfortunately I have no material available from
which to determine whether similar fibers also exist in A. tereticollis. Looss
(1904) does not mention them.

The relations of oral sucker, pharynx, and crura, the convolutions of the
intestinal branches, the coils of Laurer’s canal and of various ducts and the
sinuous course of the collecting tubes in the excretory system all point toward
the variable extensibility of the worm. Differences in caliber and in the dis-
tance between organs also indicate the same. Observations on the living
parasite serve to show that it is constantly extending and contracting the body
to such an extent as to double or halve the length within a few seconds of time.
In fact, I have never before observed a form which indulged in such energetic
twisting and contracting. This habit renders any observations on the living
worm very difficult.

Looss (1894, p. 7) comments on the active migration of A. tereticollis after
the death of the host, a feature previously recorded for D. cylindraceum by
Braun (1890, p. 568). A. sebago manifests the same tendency in the most
marked degree. ‘The normal seat of this parasite I feel sure is the stomach,
and perhaps the oesophagus also, but even a slight delay in the exanunation of
the host resulted in finding single specimens well down the intestine as well as
up in the pharynx and even among the gill filaments. In one case a salmon
caught late in the day was kept overnight to be photographed, as it was a
peculiarly fine specimen. When the viscera were examined, about twenty
hours after the capture of the fish, my field notes record that there were 36 dis-
tomes in the air bladder and that they were scen coming in through the ostium
with mucus from the cesophagus. Other specimens were found in the pharynx
and gill cavity and one even in the body cavity. The last can be attributed
no doubt to some tear in the alimentary lining which permitted the fluke to
make its way unhindered into what is ordinarily a closed cavity. In still
another salmon which had gorged itself on smelts my field notes contain com-

INTERNAL PARASITES OF THE SEBAGO SALMON. 1181

ments on the activity manifested by these distomes, which climbed about on
the smelts and in them as they lay half digested in the stomach of the
salmon.

This was so noticeable that I turned my attention at once to the smelt @ to
ascertain if perchance it played any part in the life history of the distome. In
all, I have records of 52 smelts examined, and in 46 of these were found speci-
mens of Azygia sebago. The parasite occurred in the stomach only and the
infestation was small, from 1 to 14 distomes being found in each host, with an
average of only 4 toa fish. In most cases the parasites which were taken from
the stomach of the smelt were immature, not having yet reached that size at
which the production of ova begins; they were on the average 3 to 4 mm. long,
or in some cases even smaller, running from 1.5 to 2.5 mm. in length. Single
specimens reached a length of 6, 7,and even 1omm. _ In one case, indeed, there
were none shorter than 6 mm., and the specimens varied from that to 10 mm.,
so that one can not fairly maintain that they never reach the size attained in
the salmon. Nevertheless, after the account is cast up the average shows dis-
tinctly that the distomes do not reach their full size in the smelt and, so far as
collections made during July and August can indicate, those taken from this
host are usually small in size and sexually immature. I did not obtain any
information as to the source from which the smelt acquires its infection, but in
view of the universality with which smelt form the food of the salmon in Sebago
Lake the latter undoubtedly owe to them the major portion of their infestation
with this parasite.

The host record of Azygia sebago is even yet unfinished. In the course of
my work numerous other fish from these same waters were examined. In
young specimens of Esox reticulatus 6 to 16 inches long I found this same para-
site reasonably abundant. To be sure, they seemed to average somewhat longer,
being 10 to 12 mm. in length in material from one host and ro to 14 or even 18

@ This fish I am compelled to designate under the name Osmerus mordax (Mitchill), as Jordan and
Evermann (1896) do not recognize the Sebago smelt as a separate form, saying of the species ‘Atlantic
coast of the United States from Virginia northward to Gulf of St. Lawrence, entering streams and
often landlocked.’”’ I am inclined to think that even in Sebago Lake there are two smelts. My atten-
tion was first directed to this possibility by Dr. W. C. Kendall, who, recalling our previous discussion,
writes as follows in a recent letter:

“You may recall that there seem to be two forms in the lake differing somewhat in size and habits.
The large form, which is the one that we caught with hook and line, is nearer to the marine smelt.
The small form is the one that we found in the salmons’ stomachs. You will doubtless recall that the
principal food, when any at all was found in their stomachs, of the large form was small fish, generally
young smelts. Our examinations of the stomach contents of the small form show Entomostraca almost
exclusively. This difference is indicated also by the gillrakers, which are more numerous in the small
form.”

These distomes occurred equally in both sorts of smelt and those from the smaller smelts were
larger than those from the larger fish. This is, of course, a mere accident, but it serves to show that
the two types of smelt conduct themselves alike toward the parasite.

118 BULLETIN OF THE BUREAU OF FISHERIES.

Ne

mm. long in that from another host. In the latter it was noticeable that the
suckers protruded very conspicuously and the body was much smaller in caliber
than in the specimens from the salmon and the smelt. Yet in the absence of
any structural differences I am forced to conclude that this contrast in size and
general external appearance is due to some slight difference in the technique
employed or in the condition of the parasites when they were preserved. This
is all the more probable when one considers that in one case the specimens from
Esox were identical in appearance with those from the salmon. This parasite
was found in all but one of the dozen specimens of Esox reticulatus examined,
being present in the stomach in numbers of 1 to 80 in each host. In two cases
a single specimen was found in the intestine, perhaps due to some post-mortem
wandering on the part of the parasites. In 4 specimens of Anguilla chrysypa
out of 9 examined I also found Azygza sebago in the stomach, but in small num-
bers only, averaging 3 to each host. Finally 2 of these distomes were found
in a single Perca flavescens, here also in the stomach.

In order to give a ready comparison, I append hereto a table of similar
measurements from a series of this distome taken from the various hosts men-
tioned. ‘The difference in length indicates in part age and in part method of
preservation. In fact, it is difficult to achieve any uniformity among speci-
mens so exceedingly active as this species.

MEASUREMENTS OF AZYGIA SEBAGO.

Dis- : |
A Dis- tance a ie
nte- =" e- 1s- ance |
| rior Dian axe Diam- Ante: | tween] tance | from Breadth Breadth
Seria tip to | tere tment eter | tip to | n- be- | poste- Breadth senind behind
No: Host. Length, cen- | o¢ oral] cen, of ace-| pecee | AKs of |tween| rior | between acetab-| Poste
a ae | ter of eet f tabu- | ter of | OVaTy| cen- testis | suckers. Titan |) erior
| oral jue (Se Se lum. | *€T ©! | and | ters of] to pos- D testis.
| isucker.| SuCe jOvary-| ante- | testes.| terior |
| ot | rior tip.
| | testis.
| Mm. | Mm. | Mm. | Mm. | Mm. Mm. | Mm. | Mm. | Mm. Mm. Mm. Mm.
16 | From Salmo_-_-| 8.75 | 0.31 |0.74 1.38 | 0.65 | 4.76 | 0.31 | 0.62 | 3.07 1.29 r.38 | ig)
74-79 | From Osmerus-_| 2.85 16 .4 62 330 || ale Ilia’ ra! |x 65 c 53
1.64 I 25 4 2 | .89] I I 55 .32 28 21
Yad eee 66. Fil Meese s se eel eee) Ie 28 31 2
| 12.6 cheb eee esl |ueseey| 55 | 7-88 9 290) (3225 75 77 74
4.08 29 |. 52 -78 35 2.69 | Is LO) 16 7 77 55
| |by-57 by .4 |
}

@ Much elongated; poor technique; preserved by helper.

The question naturally presents itself, Has this form been seen by others
previous to the present date? The records on the subject are scanty, but they
throw some light on the question.

INTERNAL PARASITES OF THE SEBAGO SALMON. 1183

Leidy has described (1851, p. 206) a form as Distomum terreticolle * Rudolphi,
which Pratt (1902, p. 957) lists as Azygia tereticollis (R.) Leidy. The original
description is as follows (Leidy, 1851, p. 206):

Distomum terreticolle, Rud. Entoz. Syn., p. 102; Dujardin, Hist. Nat. des Helm.;
Diesing, Syst. Helm., p. 358. .

Body subcylindrie, light flesh color, posteriorly rounded. Ventral acetabulum (34
line) 1.6 mm. behind the oral (% line) 0.7 mm. in diameter. Oral acetabulum (1% line)
0.5 mim.

: Length (8 lines) 16.8 mm.; breadth posteriorly (1% line) 1 mm., anteriorly (7% line)
Pe Bem ieation =-stemark of Esox reticulatus Lesueur.

Remark.—The generative aperture is placed immediately in advance of the ventral
acetabulum. When the animal contracts, the two acetabula are nearly brought into
contact.

The description is scanty, and yet one can say with some assurance that the
form before Leidy was not the European species named by Rudolphi and dis-
cussed by a long series of authors, of whom Looss (1894) has given the most
complete description with truly admirable figures. Leidy’s specimen is much
too small for average adults of Azygia tereticollis, which is, moreover, cylindrical
instead of broader posteriorly, as was Leidy’s worm. Again, Azygza tereticollis
has the oral sucker larger than the acetabulum, whereas in Leidy’s form the
reverse is true. Finally the suckers in Leidy’s form do not agree at all in size
with the suckers in Azygta tereticollis, as described by Dujardin and others.

It is somewhat more difficult to say whether the form before Leidy was the
same as that I collected in the Sebago salmon. In size the two are not very
different, although Leidy’s was larger. Other measurements do not agree at
all well. The sizes given for the suckers are just about reversed. The final
determination of this point, however, must await a reexamination of Leidy’s
original material.

The only other reference to the occurrence of Azygia on this continent, so far
as I know, is the brief note of Stafford (1904, p. 488), in which he records Azygza ®
tereticollis Rudolphi from mouth, pharynx, cesophagus, and stomach of Esox
lucius Linneeus, Lota maculosa Le Sueur, and Ameturus nigricans Le Sueur.
Absolutely the only data concerning the worm which Stafford records is the size,
12 by 1 mm. Now, this does not agree with adults of A. tereticollis, for Looss
(1894, p. 18) says of that species that the first eggs are not set free into the
uterus until the worm is 8 to 10 mm. or more in length, and these are uniformly
abnormal and defective. In another place he remarks (1894, p. 7) that in most
cases eggs are found in worms 12 mm. long, although in scanty numbers. I
am of the opinion that Stafford did not have before him the true A. fereticollis

@ The text by error contains terreticolle for the specific name instead of fereticolle.
b Unfortunately, Stafford spells the genus Azzgza and the species fereticolle.

1184 BULLETIN OF THE BUREAU OF FISHERIES.

and incline to the belief that the form which he observed may have been the
species under discussion.

The European species, \zygza tereticollis, has been reported from Esoxlucius,
Lucioperca sandra, Lota vulgaris, Truita variabilis, Salmo trutta, Salmo fario,
Salmo hucho, Salmo alpinus, and Salmo salar. All of these save Salmo salar are
fresh-water fish, and the parasite may be regarded as a characteristic of fresh-
water species. The American species, Azygia sebago, I found in Salmo sebago,
Esox reticulatus, Osmerus mordax, Anguilla chrysypa, and Perca flavescens.
Stafford recorded what may have been the same from Esox lucius, Lota maculosa,
and Ameiurus nigricans. ‘These include strictly fresh-water forms, landlocked
species, and one migratory fish, but inasmuch as the records have been taken in
fresh water even the last host does not constitute any evidence against the fresh-
water habitat of Azygia sebago. Its congener, Azygia tereticollis, found by
McIntosh in the salmon of the Tay, formed part of the evidence that this host
feeds during its fresh-water residence. Equally here we may regard A. sebago
as a fresh-water element acquired by its host since the latter became landlocked
in Lake Sebago. The presence of the parasite in several other characteristic
fish of the same water basin is clear evidence of the sources from which it might
have come.

CESTODES.

Cestodes constituted the most conspicuous element of the parasitic fauna.
Every salmon opened contained a mass of large worms in the pyloric region.
They lay with the head and anterior portion of the body in a pyloric coecum
usually at or near its tip. The worms were large and the body was thrown into
loops which occupied the initial coecum and folded through the intestinal canal
into other coeca, often crowding them full apparently to bursting. Viewed from
the body cavity, even before the viscera were opened, one could distinguish the
cceca which contained the parasites by their opaque, chalky appearance in distinct
contrast with the translucent character of those cceca in which there were no
tapeworms. When the intestine was opened it appeared full of the cestodes,
which protruded in loops hanging from the cceca into the cavity or crossing into
other cceca in a tangled mass, in several cases large enough to distend the wall
conspicuously. The anterior coeca were those primarily or chiefly occupied by
the worms and although often the entire cavity of the intestinal canal was
crowded full of parasites, it was noteworthy that they rarely if ever entered any
of the posterior coeca. When few worms were found they lay with the scolices
at least in the cceca of the most anterior region.

The species to which I have referred in the preceding paragraph is the well-
known Bothriocephalus infundibuliformis, according to Liihe (1899) more cor-
rectly designated Abothrium crassum, which is so common in the Atlantic salmon

INTERNAL PARASITES OF THE SEBAGO SALMON, 1185

from various parts of Europe. Of its occurrence in the Rhine salmon, where it
is found in 42 per cent of the specimens examined, in 91 per cent of the Baltic
salmon, in 26 per cent of the Tweed salmon, in most of the Tay salmon and of
the Irish salmon, enough has been said in the historical survey. It is a typical
salmonid parasite, and is found even in eight species of that family which inhabit
fresh water. Its presence in the landlocked Salmo sebago, which confines its
life cycle to fresh water, is hence not surprising. Evidently the life cycle of the
species permits of easy adaptation to a fresh-water existence, for I have to report
its occurrence not only in the host under discussion, but also in another promi-
nent American salmonid, the Great Lakes trout, Cristivomer namaycush (Wal-
baum). It was found abundantly in specimens of this host which I examined
in July and August, 1894, at Charlevoix, Mich. From 30 to 80 tapeworms of
this species were present in each Sebago salmon, and neither size nor age played
any evident part in determining the degree of infestation. Absolutely every
one of the salmon taken was infested. In considering the possible life history,
I naturally turned to the Sebago smelt as the host of the larval form, probably a
plerocercoid, and examined a number of these fish with great care, but was
unable to detect the larva, if indeed it was present. Nothing was discovered
which throws any light on the life cycle. It is worthy of note that all of these
parasites were full grown; not a single specimen was found which was not dis-
charging ripe proglottids. Consequently the infestation must have taken place
somewhat earlier in the year. It would take observations at other months to
determine when; and the food at that time would evidently be the source of
the parasite.

In addition to this dominant species some other cestodes were also recorded.
A few fragments of a small species of Proteocephalus were found in each of four
hosts, and a larval form, which probably belongs to the same Proteocephalus,
was obtained in each of two hosts. Two different bothriocephalid larve of
small size also occurred each ina single salmon. The four forms just mentioned
were all found in the intestine.

The insignificant size of a new species of Proteocephalus found and the small
number of individuals present in any one host resulted in its being overlooked
at first, and it may easily have been present in more hosts than shown by the
records. It was found in four out of the seven salmon examined, but in one
case only a few loose proglottids were discovered by accident among material
from the intestine. A careful examination in comparison with the descriptions
of known species leads me to the view that this is a new species to which the
name Proteocephalus pusillus may be given. ‘The salient points in the descrip-
tion of this new species are as follows:

Proteocephalus pusillus nov. spec.—Adult cestode with short strobila, meas-
uring only 30 to 50 mm. in length. Proglottids scanty, segmentation

1186 BULLETIN OF THE BUREAU OF FISHERIES.

distinct. Head much contracted. Neck 1 to 1.5 mm. long by 0.21 mm. broad.
First proglottids 0.09 mm. broad, changing gradually until in mature proglottids
the length greatly exceeds the breadth. Ripe proglottids measure 0.84 to 1.4
mm. long by 0.18 to 0.35 mm. broad. Terminal proglottids present and fertile.
Sexual organs typical for Proteocephalus; uterus median, with to to 14 lateral
outpocketings on either side. Testes numerous, within vitellaria. Genital pore
lateral, one-third to two-fifths of length of proglottid from anterior margin of
same. Ovaries bilobed, median isthmus indistinct, anteroposterior diameter
nearly equal to breadth of both lobes. Only a few specimens obtained from a
single host species, Salmo sebago.

This species approaches most nearly to P. ocellata and P. perce among
known species. Unlike the new species, however, both of these older forms have
a fifth sucker, fewer lateral uterine outpocketings, a longer neck, differently
shaped ovaries, and markedly different proglottids.

In specimens with developed proglottids the head was so much contracted
or distorted that any special description would be of little value. One could easily
observe the general features characteristic of the genus. There was no well
developed terminal or fifth sucker, and the end organ, which is known to replace
it in many forms of this genus, was inconspicuously developed, if present.
Personally, I incline to the view that on more careful examination this structure
will be found in all species, even those in which its absence has been made a
matter of record. Accordingly, not much weight can be put in its presence or
absence in any individual case.?

Three plerocercoid larve or young cestodes were found in company with
Proteocephalus pusillus, which I regard as young forms of this species. The
largest came from the salmon which was most heavily infected with this cestode
parasite. It was 3.15 mm. long and had begun to assume clearly the appear-
ance of an immature cestode. The head measured 0.3 mm. wide by 0.26 mm.
long, and the suckers 0.14 mm. in length by 0.11 mm. in width. The neck
was slightly narrower than the head, but was not clearly set off from the body,
which was very uniform in diameter and measured 0.25 mm. in average width.
The posterior end of the body was swollen into a rounded knob about 0.35 mm.
broad and of approximately the same length. This feature was evidently
produced by a powerful contraction of the terminal region of the body. In
and near it one could see very indistinct indications of proglottid formation.
In form, size, and general aspect this young cestode was in full agreement with
the anterior regions of the mature cestodes of this species with which it was

@¥or a more definite discussion of this peculiar structure so variable in development in the cestodes
of this genus, I would refer to a paper now in press by my student, Mr. George R. La Rue, to whom
I am indebted for a comparison of this material from Salmo sebago with preparations of other species
of Proteocephalus

INTERNAL PARASITES OF THE SEBAGO SALMON. 1187

associated. The head, which was not contracted, showed on careful study the
delicate outline of a rudimentary end organ. While such a structure was not
demonstrated in the mature individuals described above, one can say positively
that if present it could not have been seen owing to the greatly contracted
condition of the adult scolices. I believe that its presence will be demonstrated
in more favorable specimens. The complete agreement of this largest larva
with the mature specimens in all other features compels me to regard both as
different stages in the development of the same species.

The other larve were still in early stages of development, and probably
had been ingested by the salmon at a very recent date. Their relationship is
not so clear in all respects, and yet I do not hesitate to associate with the new
species of Proteocephalus a plerocercoid or young cestode obtained from the
same host as the adult worms and the older larva just described. The head is
broadly conical, without furrows, and measures 0.3 mm. in breadth. The
suckers measure 60 to 75min diameter. There is no rostellum or fifth sucker
to be found, while the end organ is so poorly developed as to be visible with
difficulty and only under the most favorable circumstances. The neck is
nearly as broad as the head. In general-appearance this larva resembles the
adult cestode and the older larva previously described. With some reserve one
may also assign to this species a single plerocercus taken from another specimen
of Salmo sebago. The head, which measures only 1504 in breadth, is shaped
like that of the young cestode and like it is without rostellum or fifth sucker,
while the end organ is difficult to demonstrate. Neither furrows nor ridges are
seen on the larva, which has a total length of 1.14 mm. The sucker measures
only 30 to 45 in diameter. The neck is slightly narrower than the head.
This form certainly belongs to the genus Proteocephalus and probably to the
species already described.

From the scantiness of the material obtained one might infer that the
Sebago salmon is only a casual host of the species. Yet I did not secure this
parasite from any other fish in Lake Sebago and adjacent waters, and I have
not met it in fish examined in other places. The presence of larve in different
stages of development with only a few adult specimens in any one host,
although some were found in the majority of the salmon examined, would
rather favor the view that the cestode was a regular though infrequent parasite
of this host.

Sparganum sebago, nov. spec.—In addition to the cestodes already men-
tioned, there are to be noted two specimens of bothriocephalid larvae which
deserve more extended mention.

The first was taken from the spleen of one salmon. It measured 25 mm.
in length and 1.8 mm. in maximum diameter. There is no neck, but the body

1188 BULLETIN OF THE BUREAU OF FISHERIES.

increases slightly in breadth for about one-quarter of the entire length and
then tapers gradually to the posterior end, which is rounded off. The body
is elliptical in cross section without any segmentation, but with numerous rather
prominent annular wrinkles. It seemed as if the margins of the body were
thicker than the center. The head was retracted. (Fig. 7 and 8, pl. cxx1.)

The second specimen (fig. 9g and 10, pl. cxx1) was found free in the body
cavity of another salmon. It was 36 mm. long and 0.86 mm. in breadth. The
body was somewhat thicker than in the other specimen, but less deeply wrinkled,
and the center was certainly thicker than the margins. In this, as in the color
and texture, it appeared different from the first specimen. There was no neck.
The head measured 0.31 mm. in transverse diameter and 0.43 mm. from the
apex to the base of the grooves, which were keyhole shaped. The groove
measured 0.25 mm. in transverse diameter at the anterior end and 0.09 near
its posterior end. In spite of the differences in appearance noted above it is
easily possible that the two specimens belong to the same species and I have
preferred to list them for the present under a single heading, naming the form
Sparganum sebago.

A word should be said with regard to other hosts for these cestodes.
Abothrium crassum was not found in any other fish examined at Sebago Lake.
Larve of Proteocephalus and of some bothriocephalid were found in a very few
cases in other fish taken from these waters. There were none, however, of
which it could be said with reasonable certainty that they were the same as the
forms collected from the Sebago salmon and mentioned above. The question
of the occurrence of such salmon parasites in other hosts of this region must be
left entirely open for the present at least.

NEMATODES.

Nematodes were not common. ‘They occurred only in half of the specimens
of salmon examined and were not abundant. In one salmon 33 of these worms
were obtained, but in the other three only a dozen all told. Accordingly they
seem to play only a minor part in the parasitic fauna of the Sebago salmon.
They belong to two or three separate species, which are radically distinct. Thus
far I have not been able to make a satisfactory determination for any of them,
owing to the scantiness of the material and to its unsatisfactory condition.
This much can be said: They do not belong to any of the species, or even to
the genera, heretofore recorded for the Atlantic salmon. A few notes may be
added here concerning these forms.

A small nematode was found in the stomach and in the body cavity of two
salmon. In all there were only six individuals of this species. I have not been
able to satisfy myself that the individuals recorded as from the stomach
really belong there, but incline to think that they were adherent to the external

INTERNAL PARASITES OF THE SEBAGO SALMON. 1189

surface of the stomach and passed unnoticed when that organ was opened and
shaken in a preserving fluid in order to collect the small specimens of Azygia
sebago concealed in the gastric mucus. Subsequently they were found in the
material obtained in this process. They are probably true parasites of the
body cavity. Since an approximate determination may easily be misleading I
forego all attempt to name this form and designate it for the present simply
as ‘Nematode A.”

The group of 33 nematodes obtained from the body cavity was a source of
great surprise. These worms are identical with a form found in very large num-
bers in the Alaska salmon. Since, however, this species is to be discussed at
length in the section of my report which deals with that host, it seems wise to omit
here any details and refer to the worm simply as ‘‘Nematode B.”’ It is a large
form belonging to the Filariadz, but so delicate that it is almost impossible to
obtain perfect specimens, and it has thus far proved beyond my skill to preserve
any in a complete condition. It has been an exceedingly interesting object of
study and will receive at an early date, in connection with the records of the
Alaska salmon and its parasites, that detailed consideration which its frequence
and its interest warrant. The six nematodes recorded from the stomach were
collected and preserved by an assistant. They are in very poor condition,
so that any determination can hardly be more than an impression, but the
only real reason why I hesitate torefer them to the same species is that in all the
thousands of specimens from nearly 200 hosts which I handled in the course of
my investigations on the Alaska salmon I never once found the species any-
where save in the body cavity. It is not impossible that these specimens were
reported from the stomach through some error. As repeated examination is
bringing me more and more firmly to accept the identity of this lot with those
which I collected personally from the body cavity of the Sebago salmon and
of the Alaska salmon, I am being forced to assume the existence of some error
in recording them as from the stomach.

In any event, it may be said that not more than three species of nematodes
are present in the Sebago salmon and that these species are only infrequently
and scantily represented in this host. None of the nematodes were found in
any other fish examined at Sebago Lake, nor are they known to me from fish
of any fresh-water locality in this country. Thus far also I have failed to find
any reference in the literature which could be construed as indicating either

of these forms. ‘ ;
RESUME AND CONCLUSIONS.

The first general conclusion to be drawn from this study of the parasitic
fauna of the Sebago salmon is that the total number of parasites recorded
from this host is small. In all, there have been listed only 1 trematode, 2
cestodes, 4 (?) cestode larvae, and 2 nematodes, or a total at most of 9 species

I190 BULLETIN OF THE BUREAU OF FISHERIES.

of parasites. To be sure, the number of hosts examined was small, and
this may account for the low total record. Two of these parasites, Azygia
sebago and Abothrium crassum, were found in every fish examined, and each of
six other parasites was found in two hosts. This may be compared with
Zschokke (1896, p. 824), who records the parasitic census of 10 salmon from the
North Sea. In these ro fish were found 10 species of parasites. A trematode
and a cestode occurred each in 9g of the fish examined. The cestode was
Abothrium crassum, the same species as that found in every Sebago salmon;
the trematode was Distomum ocreatum, a purely marine form, and hence in
sharp contrast with the abundant trematode in the Sebago salmon, which is
a member of a characteristic fresh-water genus. This contrast, as well as
several other details commented on in the previous pages, seem to indicate
the fresh-water aspect of the parasitic fauna in the Sebago salmon.

The conditions in the Sebago salmon are all the more striking when one
considers the forms which are not found among its parasites. Reverting first
to the trematodes, one notices that the only genus represented here, Azygza,
has been recorded from the Atlantic salmon in Europe only in a single case,
while here its representatives were found in every host examined. On the other
hand, Derogenes varicus, recorded from a good percentage of European salmon
in all localities, was not seen even once. ‘The other distomes recorded by
European observers in various regions, and often as fairly frequent parasites
of the salmon, are entirely wanting in Sebago salmon. Azygia is the only
purely fresh-water distome found in European salmon; it is the only distome
found in the Sebago salmon. The other distomes recorded in European salmon
are purely marine species, or very largely so, but none of them occur in the
Sebago salmon.

Among the cestodes conditions are identical. The common form, A bothrium
crassum, is confined to salmonids, without reference to their habitat, and is as
common in fresh-water species as in marine. On the other hand, those cestodes
which are typically marine, like Rhynchobothrium paleaceum, Scolex polymorphus,
and the several species of Tetrarhynchus, are absolutely wanting in the Sebago
salmon. ‘The various cestode larve are too little known to justify their con-
sideration in this connection. They are not referable, even indefinitely, to
either habitat. To this statement one must make two exceptions. Scolex
polymorphus, recorded from the salmon in Europe, is typically marine, occurring
in many sea fish, even though several species may be indicated under the single
name. On the other hand, the larva of Proteocephalus is equally typically
limnetic and it is recorded from the Sebago salmon only unless the single record
of Tenia sp. for a larva from the salmon in the Tweed should be referred to
this form. In this group again it appears clear that the marine parasites of the
European salmon are wanting in the Sebago species, that the only cestodes

INTERNAL PARASITES OF THE SEBAGO SALMON, 119i

identical in the two forms are such as are clearly fresh-water species, and that
the Sebago salmon contain at least one clearly fresh-water genus which is not
reported from the corresponding European host.

Among the nematodes the evidence is less conclusive, since the amount of
material is smaller; indeed, hardly enough to form a basis for any conclusions.
At the same time, all the species which give to the parasitic fauna of the European
salmon its marine aspect are entirely wanting here. Not a single specimen of
Agamonema was discovered, although two species are found in the European
salmon, and one of them, Agamonema capsularia, is very common. Both Ascaris
and Echinorhynchus are unrepresented in the parasitic fauna of the Sebago
salmon. Among the numerous species of each already recorded as parasitic in
the European salmon three out of four are purely marine. Here again one
notes that the marine elements in the parasitic fauna of the European salmon
are wanting in the Sebago salmon. Possibly the large filariad found abun-
dantly in the Alaska salmon, and reported also from one or two salmon taken in
Sebago Lake, forms an exception to the general rule. As I have already noted,
it appears to be marine in origin. This may be, however, a false argument,
and the species may actually be one limited to this host or to the salmonid
family, regardless of habitat. In this connection one naturally recalls at once
the case of Abothrium crassum, which, from the observations on salmon in the
North Sea and then in the Rhine, might be said to be a marine form, since it
gradually disappears on the journey up the Rhine. But it occurs in hosts of
purely fresh-water habitat, such as Salmo hucho in Europe and Cristivomer
namaycush in the Great Lakes of North America. Evidently further informa-
tion is needed before one can safely assign this nematode to a definite habitat.

Summing up all the evidence concerning the parasites of the Sebago salmon,
one finds that four species are unknown in character, one only is possibly marine,
‘one is a pure salmon parasite, and three are clearly fresh-water forms. The
latter are also its most frequent and numerous guests. Furthermore, the
Sebago salmon lacks every one of those parasites found in the European salmon
which must be regarded as purely or largely marine, and possesses in common
with its European congener only one characteristic salmon parasite and possibly
also two fresh-water forms, which, though abundant in its own parasitic fauna,
are very rare in that of its relative.

The parasitic fauna of the Sebago salmon manifests a striking fresh-water
aspect, all the more unexpected in view of the marine character of that in the
European salmon as demonstrated by Zschokke. One could hardly find a more
convincing demonstration of the fundamental biological relation between parasite
and host.

The parasitic fauna of any animal is primarily a function of its habitat.

11g2 BULLETIN OF THE BUREAU OF FISHERIES.

BIBLIOGRAPHY.
BEAN, T. H.

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and needs of the salmon fisheries. Bulletin U. S. Fish Commission, vol. x, p. 165-208.
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BELLINGHAM, O.
1840. Catalogue of the Entozoa indigenous to Ireland. Magazine of Natural History, n. s., vol.
4, P- 343-351.
1844. Catalogue of the Entozoa indigenous to Ireland. (Reprinted.) Annals and Magazine of
Natural History, vol. 14, p. 471-479.
1844. OnJrish Entozoa. Ibid., vol. 13, p. 167-174, 422-430; vol. 14, p. 162-165, 251-256.
Braun, M.
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kunde, bd. 7, p. 568.
1894. Vermes.—Trematodes. Bronn’s Klassen und Ordnungen des Thierreichs, bd. rv, abt. 1.
DIESING, C. M.
1851. Systema Helminthum, vol. u. Vindobonz.

DrummMonp, J. L.
1838. Notices of Irish Entozoa. Magazine of Natural History, n. s., vol. 2, p. 515-524, 571-577
655-662, 32 fig.
GoEzE, J. A. E.
1782. Versuch einer Naturgeschichte der Eingeweidewiirmer thierischer Kérper. 471 p., 35 pl.
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Hausmann, L.
1897. Ueber Trematoden der Siisswasserfische. Revue suisse de Zoologie, t. 5, p. 1-42, 1 pl.
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1899. Neuere Lachs- und Maifisch-Studien. Tijdschrift der Nederlandsche Dierkundige Vereeni-
ging, 2 de serie, deel vi, p 156-242, 5 pl.
Jorpan, D. §., and EveRMANN, B. W.
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vol. 5, p. 205-210.
1871. Notices of some worms, Dibothrium cordiceps, Hirudo, Gordius. Ibid., vol. 23, p. 305-307.

Linstow, O. von

1878. Compendium der Helminthologie. Hannover.
1889. Compendium der Helminthologie. Nachtrag. Hannover.

Looss, A.

1899. Weitere Beitrage zur Kenntniss der Trematoden-Fauna Aegyptens, zugleich Versuch einer
natiirlichen Gliederung des Genus Distomum Retzius. Zoologische Jahrbiticher, Syst.,
bd. 12, p. 521-784, 9 taf.

1894. Die Distomen unserer Fische und Frésche. Bibliotheca Zoologica, hft. 16.

1907. Beitrage zur Systematik der Distomen—Zur Kenntniss der Familie Hemiuride. Zoologische
Jahrbiicher, Systematik, bd. 26, p. 63-180, 9 taf.

INTERNAL PARASITES OF THE SEBAGO SALMON, 1193

Lune, M.
1899. Zur Anatomie und Systematik der Bothriocephaliden. Verhandlungen der deutschen
zoologischen Gesellschaft, 1899, p. 30-55.
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1863. Notes on the food and parasites of the Salmo salar of the Tay. Journal Linnean Society of
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Montez, R.
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1902. Ichthyologische Beitrage. 111. Ueber die in den Fischen des Finnischen Meerbusens vor-
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1194 BULLETIN OF THE BUREAU OF FISHERIES.

Stites, C. W., and Hassauu, A.

1894. A preliminary catalogue of the parasites contained in the collections of the United States
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Tos, Jas. R.

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ZSCHOKKE, FR.
1899. Erster Beitrag zur Parasitenfauna von Trutta salar. “Verhandlungen der Naturforschenden
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1891. Die Parasitenfauna von Trutta salar, Ibid., bd. 10, p. 694-699, 738-745, 792-801, 829-838,
8 tab.

1896. Zur Faunistik der parasitischen Wirmer von Siisswasserfischen. Ibid., bd. 19, p. 772-784,
815-825.

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schaft in Basel, bd. 16, p. 118-157.

EXPLANATION OF PLATE.

Fic. 1. Azygia sebago. Group of individuals from Salmo sebago, after preservation in corrosive sub-
limate and then alcohol. 2.

2. Azygia sebago. Specimen from salmon, stained and mounted in balsam. Dorsal view. 12%.

3. Azygia sebago. Anterior region of alimentary canal in lateral aspect. Reconstruction by
Messrs. W. M. Anderson and H. B. Boyden. 2, intestine; @, cesophagus; os, oral sucker;
ph, pharynx. Highly magnified.

4. Azygia sebago. Longisection showing relations of principal organs. exc, main excretory
vessels; /pm, longitudinal parenchym muscles, for explanation of which compare text; vz,
follicles of vitellarium. Camera drawing. 358.

5. Azygia sebago. Female reproductive system in dorsal aspect. Semidiagrammatic to show
relation of organs in ovarial complex. /c, Laurer’s canal; od, germ duct; ov, germarium,
sg, shell gland; ut, first coils of uterus; yd, transverse vitelline duct; yr, yolk reservoir.
After reconstruction by Messrs. Anderson and Boyden. Highly magnified.

6. Azygia sebago. ‘Transsection through ovarial complex, showing relations of organs to common
capsule (see text). 7%, intestinal crura; /pm, longitudinal parenchym muscles; ov, germ
gland; sg, shell gland; ut, first coil of uterus; wi, follicle of vitellarium; yd, common yolk duct
and part of yolk reservoir. Camera drawing 60.

7. Sparganum sebago, nov. sp. Bothriocephalid larva from spleen of Salmo sebago. Drawn from

alcoholic specimen. X2.

8. Head of larva, shownin fig.7 X25.

9. Sparganum sebago, nov. sp. Bothriocephalid larva from body cavity of Salmo sebago. Drawn
from alcoholic specimen. 2.

10. Head of larva, shown in fig. 9. X25.

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